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The biology of ergothioneine, an antioxidant nutraceutical

Irina Borodina, Louise C. Kenny, Cathal M. McCarthy and 5 more

Nutrition Research Reviews · 2020 · Review

doi:10.1017/s0954422419000301

Abstract

Ergothioneine (ERG) is an unusual thio-histidine betaine amino acid that has potent antioxidant activities. It is synthesised by a variety of microbes, especially fungi (including in mushroom fruiting bodies) and actinobacteria, but is not synthesised by plants and animals who acquire it via the soil and their diet, respectively. Animals have evolved a highly selective transporter for it, known as solute carrier family 22, member 4 (SLC22A4) in humans, signifying its importance, and ERG may even have the status of a vitamin. ERG accumulates differentially in various tissues, according to their expression of SLC22A4, favouring those such as erythrocytes that may be subject to oxidative stress. Mushroom or ERG consumption seems to provide significant prevention against oxidative stress in a large variety of systems. ERG seems to have strong cytoprotective status, and its concentration is lowered in a number of chronic inflammatory diseases. It has been passed as safe by regulatory agencies, and may have value as a nutraceutical and antioxidant more generally.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 20, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Most of the classical vitamins such as vitamins A, B1, B2, B3, C, D, etc., were discovered by means of the fact that an inadequacy in their supply led to overt forms of deficiency disease such as blindness, beri-beri, pellagra, scurvy, rickets and so on. Consequently, it was easy to establish those food sources that contained such vitamins, since they relieved or prevented the relevant syndromes. It is correspondingly hard, by these means, to detect the presence of a vitamin if it is present in virtually every foodstuff that an individual consumes. Recently, however, l-(+)-ergothioneine, hereafter ergothioneine (ERG), has emerged as an important nutrient, and indeed possible vitamin, that has precisely these properties of a very widespread occurrence coupled, commonly, to a functional undersupply.

A related class of nutrient, which has not been demonstrated as necessary or essential for life yet provides health benefits when added at levels greater than a normal diet generally provides, has come to be known as nutraceuticals, a coinage based on an amalgamation of ‘nutrition’ and ‘pharmaceutical’. Interest in such nutraceuticals, also known as ‘functional foods’, has increased enormously over the last few decades as our understanding of the important roles of diet in health has improved. However, the enthusiasm for such products has not always been matched by the extent or quality of the evidence for their efficacy.

Since ERG classes as a nutraceutical, it seems timely to bring together the extensive but widespread knowledge of its biology so that it may be made more widely available, and that is the purpose of this review.

Discovery and structure

ERG is a somewhat unusual betaine amino acid. It was discovered by Charles Tanret in 1909 while investigating the ergot fungus Claviceps purpurea. It is also known as 2-mercaptohistidine trimethylbetaine, and its formal International Union of Pure and Applied Chemistry (IUPAC) name is (2S)-3-(2-thioxo-2,3-dihydro-1H-imidazol-4-yl)-2-(trimethylammonio)propanoate. It is an l-histidine derivative that is Nα,Nα,Nα-trimethyl-l-histidine in which the hydrogen at position 2 on the imidazole ring is replaced by a mercapto group. Its structure, and those of some related molecules, is given in Fig. 1, indicating that is a tautomer that has both a thiol and a thione form. Although it is a thiol, and hence an antioxidant, the thione tautomer is predominant at physiological pH, and this makes it unusually resistant to autoxidation, i.e. simple oxidation by molecular O2. Its midpoint potential for a thiol is consequently unusually high, being +0·06 V v. −0·2 to −0·4 V for typical thiols including glutathione and mycothiol, and −0·193 V for the also somewhat oxidising thiol cofactor coenzyme M, which is 2-mercaptoethanesulfonate. Its reaction with hydroxyl radicals (OH•) is virtually instantaneous, while it reacts only more slowly with H2O2 and/or O2 •−. Its Se equivalent is known as selenoneine and also has strong antioxidant properties, but is not otherwise discussed here.

From a pharmaco-chemical point of view ERG is also unusual, since – using our standard substructure analysis in KNIME – we note that just two drugs marketed for human consumption (the anti-thyroxine-production drug methimazole and its pro-drug carbimazole, Fig. 1), and no endogenous genome-encoded metabolites from Recon2 contain the imidazole-2-thione substructure. This said, a good many fungicides do contain the benzimidazole substructure, and a variety of benzothiazoles are used as dyes.

Biosynthesis and phylogenetic distribution

A particular feature of ERG is that although it is more or less universally distributed among higher organisms, none of them – as is consistent with the idea that it may in fact be a vitamin requiring exogeneous sources – can in fact biosynthesise it. The chief organisms capable of its synthesis are fungi and certain yeasts, though actinobacteria and certain other micro-organisms, including the slime mould Physarum polycephalum, cyanobacteria and methylotrophs are also naturally capable of its production. The related mycothiol is typically ten times more concentrated in actinobacteria than is ERG, and its biosynthetic pathway might provide an antitubercular drug target. Other organisms acquire ERG through transporter-mediated uptake. Thus higher plants contain it but do not biosynthesise it; instead they and other organisms take it up from fungal production in the soil, and possibly via actinobacterial or fungal symbionts. Animals are also considered not to biosynthesise it, and accumulate it using a particular transporter, detailed below, via the plants and animals that they eat. Although not easy, it is possible to raise animals such as pigs on a diet such as casein, sucrose, lard, butter and salts that is considered to lack ERG; such animals are said to have undetectable levels of the compound, and rats treated similarly have reproduced. However, we do not know the minimum amount and its location that animals need, and these are old experiments that need to be repeated with modern techniques with lower detection limits. Only then might we have a definitive statement as to whether ERG is absolutely required as a true vitamin or not, and if so in what amounts for health. In a similar vein, ERG can be present in cell culture media and cells with organic cation transporter N1 (OCTN1)/solute carrier family 22, member 4 (SLC22A4) can accumulate it, a fact little considered to date in cell culture studies.

To the extent that ERG is a ‘secondary’ metabolite, defined as a molecule whose synthesis has a relatively restricted distribution in different organisms, the biosynthetic pathways diverge from primary metabolism via the amino acids histidine, cysteine and methionine. Thus (Fig. 2), histidine is trimethylated using S-adenosyl methionine to form trimethyl histidine, also known as hercynine. This reacts oxidatively with cysteine to form hercynylcysteine sulfoxide, which is converted to ERG. In some organisms, hercynine takes a more convoluted route via γ-glutamylhercynylcysteine sulfoxide (Fig. 2). Table 1 provides references for different organisms. An excellent phylogenetic analysis is given by Jones et al.. In more recent work, it has been suggested that ERG was probably first biosynthesised by anaerobes using a slightly different route that converts hercynine directly to ERG, and that was later repurposed.

Three-dimensional structures are known for a number of the relevant enzymes, including mycobacterial EgtB for example, PDB 4XBE, EgtC for example, PDB 4ZFJ, EgtD for example, PDB 4PIM, and Neurospora crassa early G1 transcript 2 (egt2) which is like egtE for example, PDB 5UTS. Very recently, EgtB from Candidatus Chloracidobacterium thermophilum was crystallised, and engineered towards Egt1 activity. Thumbnails are given in Fig. 2. Egt1 from N. crassa is 876 amino acids long, while egtD (from Mycobacterium tuberculosis) is just 321 amino acids long; since the N-terminal sequences are well conserved (Fig. 3), this implies an extra C-terminal domain catalysing the production of hercynylcysteine sulfoxide from hercynine.

In addition, enantiopure l-ERG has been synthesised chemically, and by fermentation of genetically engineered micro-organisms (Table 2). Initial efforts in ERG synthesis were carried out in Schizosaccahromyces pombe using egt1 overexpression under an inducible promoter. The N starvation and glucose starvation conditions causing long quiescence led to the maximum ERG production of 1606·3 µm while the wild-type strain produced 0·3 µm. Methylobacterium aquaticum strain 22A was engineered by expressing an additional copy of egtBD genes and by deleting the gene encoding histidine ammonia lyase, which degrades an ERG precursor l-histidine. The resulting strain produced up to 7·0 mg EGT/g dry cell weight and 100 μg EGT/5 ml per 7 d in test-tubes. The filamentous fungus Aspergillus oryzae has also been engineered to produce ERG by expression of egt1 and egt2 genes from N. crassa, resulting in 231 mg ERG per kg of solid media.

Expression of egtBCDE genes from Mycobacterium smegmatis in Escherichia coli and optimisation of medium composition has led to 24 mg/l or 104 μm of secreted ERG. The egtA gene from M. smegmatis was not expressed because E. coli contains a homologous glutamate–cysteine ligase encoded by gshA and involved in glutathione biosynthesis. In a follow-up study, the authors expressed egtA from M. smegmatis and it had a positive effect on ERG production. Furthermore, they enhanced cysteine and S-adenosine methionine biosynthesis and obtained 1·3 g/l or ERG in a fed-batch fermentation, achieving currently the highest titre reported for heterologous ERG production.

Recently, we reported the engineering of baker’s yeast Saccharomyces cerevisiae for the production of ERG. S. cerevisiae has a generally recognised as safe (GRAS) status and has been exploited for the commercial production of several nutraceutical compounds; it is thus a highly attractive host for the production of ERG. We have tested sixteen different pathway variants, nine containing only fungal genes, one with bacterial genes from M. smegmatis, and six hybrid pathway variants containing both fungal and bacterial transgenes. The best-performing strain contained egt1 from N. crassa and egt2 from C. purpurea. The composition of the medium was improved using a fractional factorial design. Fed-batch cultivation resulted in 598 (sd 18) mg/l ERG after an 84-h fermentation. Some 60 % of the measured ERG was extracellular and the rest accumulated in the cells. Table 2 summarises the various recombinant expression hosts that have been used.

The distribution of solute transporters between tissues in differentiated organisms is particularly heterogeneous, and it is to be expected that both SLC22A4 and ERG might also be distributed heterogeneously as well. This is indeed the case, their distribution being especially high in tissues that are considered to have the potential for oxidative stress, such as erythrocytes, bone marrow, liver and kidney, seminal fluid and the lens and cornea of the eyes. It may also be accumulated in the CNS.

Finally, here, we note – as with the activity of the ‘master Fe regulator’ hepcidin, that acts chiefly via the ferrous Fe transporter ferroportin – that the action of a transporter in concentrating a substance in one tissue will typically lead to its depletion from another. Consequently, it is necessary to measure all relevant compartments to assess whether a molecule such as ERG, whose distribution is strictly transporter-mediated, is protective against a particular disease/effect or otherwise in a particular place or case.

SLC22A4: the ergothioneine transporter

Although this view remains controversial, even hydrophobic molecules do not normally ‘float across’ whatever phospholipid bilayer portion of cells may be untrammelled by proteins. Xenobiotics in particular need to ‘hitchhike’ on protein transporters that have presumably evolved for ‘natural’ substrates but that are capable of their uptake. While transporters seem to have remained somewhat understudied, those transporters involved in uptake and encoded by the human genome are now catalogued formally as SLC for solute carriers, with efflux transporters mainly being classed as ABC families.

One solute carrier, previously known as organic cation transporter N1 (OCTN1), and now known as SLC22A4 (the human version is Uniprot Q9H015), a 551-amino-acid transporter with three glycosylation sites, is of special interest. It had been designated as a transporter of carnitine and of the (non-physiological) tetraethylammonium cation. However, in a really groundbreaking paper, Gründemann et al. recognised that the rates observed (using radioisotopes) were too small to be physiologically meaningful, and using a method that we would now refer to as ‘untargeted metabolomics’, they incubated two kinds of HEK293 cells in serum. The first were normal cells, that, as with many transporters, do not in fact express SLC22A4 at significant levels, while the second had been engineered to overexpress the transporter. They then simply looked for those molecules that were most differentially taken up, a molecule called stachydrine, also known as proline betaine, being the main one observed, Stachydrine is a constituent of citrus juices. Some elementary cheminformatics based on structure similarity searches indicated that ERG, as a betaine, was indeed similar to stachydrine. Incubating the cells just with ERG showed that it was taken up about 100 times more quickly than was tetraethylammonium, leading to the designation of SLC22A4 as ‘the’ ERG transporter. Subsequent work has confirmed and reinforced this view of SLC22A4 and its homologues as having significant specificity for ERG, and weak activity for various drugs. It is concentrative, coupled in humans to influx of 2 or 3 Na+ ions per ERG transported. Interestingly, it is up-regulated chronobiologically just before meal times. The rat and human orthologues are interchangeable. Tissue levels of ERG depend on an exogenous supply, but are then well correlated with the expression levels of SLC22A4. SLC22A4 expresses well even in microbial systems, and is widely tolerant of amino acid substitutions. As yet, no other transporter with significant activity for ERG in humans is known, making it a potentially interesting drug target.

Expression patterns

SLC22A4 is known to express in the intestinal lumen, acting to take up ERG, as well as some xenobiotics including pyrilamine, quinidine and verapamil, and having multiple known but weak inhibitors.

Fig. 4 shows the expression of the transcript for SLC22A4 in fifty-six cell lines using previous data taken from the human protein atlas, indicating a range in expression levels between different cell lines of more than 4000-fold, a number not atypical for human transporters. Tissue expression data are given in Fig. S4 of O’Hagan et al..

The intracellular expression patterns are as yet uncertain, with early claims for a mitochondrial expression being based on very weak and contradictory evidence. However, while the cellular uptake of ERG does require plasma membrane expression, the latest version of the protein atlas indicates mitochondrial expression as well. However, as is well known, antibody specificities are rarely either known or absolute. Thus, relying on antibody evidence alone is rather hazardous, and, as mentioned before, mitochondrial transporters have an SLC25 family designation. Definitive measurements on the uptake or otherwise of ERG into isolated mitochondria, or indeed into other organisms that cannot make it, are eagerly awaited.

Evolution and phylogenetic distribution of SLC22A4

Phylogenetic analyses indicate that homologues of SLC22A4, a relative of the major facilitator superfamily 2, exist only in vertebrate animals, especially mammals, birds and fish, with occasional examples in reptiles (for example, Xenopus spp.).

In practice, it appears that the transporters responsible for the uptake of some 85 % of pharmaceutical drugs actually evolved to take up exogenous natural products. In the case of the cocaine transporter, a simple narrative can serve to explain how a cocaine-mediated ability to outrun a predator such as a sabre-tooth tiger can rather obviously be selected provided the bioactive substance is actually taken up by the host. More generally, the ability to transport exogenous natural products is likely to be selected for when these confer fitness benefits on the host, and this probably underpins the finding that successful, marketed drugs are indeed similar to (mainly ‘secondary’) natural products.

Oxidative stress

Oxidative stress is widespread to the point of ubiquity in chronic, inflammatory diseases, with over fifty papers having the words ‘oxidative’, ‘stress’ and ‘review’ in their titles at PubMed in 2018 alone! It can occur when oxygen tension is low and respiratory chains are over-reduced such that they reduce O2 with one electron to superoxide or two electrons to H2O2, instead of the four that are used during the reduction of dioxygen to water by cytochrome oxidase (Fig. 5). Peroxides are also produced in vivo by various oxidases and peroxidases, such as xanthine oxidase, by reduction of dioxygen (for example, Babior, Cave et al. and Bedard & Krause).

While H2O2 and superoxide are certainly capable of effecting unwanted oxidations, it is the hydroxyl radical that is the key. Thus an important reaction of H2O2 with (free or poorly liganded) Fe(II) is the Fenton reaction, leading to the very reactive and damaging hydroxyl radical (OH•):

which can react within nanoseconds with anything adjacent. The role of Fe is absolutely vital here. Superoxide can also react with ferric Fe in the Haber–Weiss reaction to produce Fe(II) again, thereby effecting redox cycling, and meaning the ‘iron’ is catalytic (Fig. 6):

In addition O2 •− can release ‘catalytic’ Fe from Fe-S clusters in certain proteins and from ferritin, another way in which it can promote the Fenton reaction. Note that other reactions can produce OH• anaerobically. Because OH• is so reactive it is not really observable in its free form; its action is detected via products of molecules with which it has reacted. These include 8-oxo-guanine derivatives, nitrotyrosine (itself formed from peroxynitrite, possibly formed more commonly via superoxide), 4-hydroxy-nonenal, and many others reviewed previously. In evaluating the antioxidant potency of ERG or anything else, it is molecules such as these that are normally assessed. Although the literature is somewhat scattered and heterogeneous, it seems clear that as well as hydroxyl radicals, ERG can also react with and detoxify, or prevent the formation of, singlet oxygen, ozone, superoxide, peroxide, hypochlorite and peroxynitrite. Consequently, it is a potent antioxidant.

Roles in the producer

Although it is not a priori certain that they would be the same in both producer and consumer organisms, it is of interest, before looking at higher organisms, to consider the roles of ERG in the producer organisms themselves. In the case of C. purpurea, the ERG serves as an antioxidant to neutralise a plant host defence response based on H2O2 that would otherwise inhibit the production of its conidia. In M. tuberculosis and other mycobacteria, and also in other actinobacteria and in fungi, it is clear that ERG can have a role as an antioxidant and also act as a buffer against reductive stress. In nature many organisms can be subjected to oxidative stress, and produce a variety of molecules to combat it. This also seems true of mushrooms, where ERG is typically the main antioxidant, and where it may also inhibit the oxidative enzyme tyrosinase. Given suggestions that the ‘purpose’ of secondary metabolite formation is to serve as a signalling molecule in different cells of the producer organism, i.e. as a pheromone, it is interesting to note that this may also involve crosstalk of ERG, due in part to the complex networks in which it may be embedded. The same is true of the imidazole thiol-containing ovothiol. In a similar vein, and although outwith our scope here, we note the potential of other antioxidant natural products such as curcumin.

Nutritional sources

Betaines are generally seen as nutritionally beneficial, and many are ‘compatible solutes’, defined as solutes whose accumulation assists the survival of the organism when undergoing various kinds of stress such as osmotic or thermal stress. However, of these, only ERG is seen as a major antioxidant. Although a variety of foodstuffs such as oats contain ERG because they take it up from exogenous sources, it is really mushrooms that are the prime sources for humans. Indeed, ERG has been proposed as a nutritional biomarker for mushroom consumption, albeit that different mushrooms typically contain different amounts, and these can vary with physiological or environmental conditions. Those with the highest amounts include oyster mushrooms (Pleurotus spp., up to 4 mg/g DM), the golden oyster Pleurotus citrinopileatus with 10·65 mg/g DM, and shiitake (Lentinula edodes, about 1 mg/g DM), while of those more common outside Asia, porcini or ceps (Boletus edulis, > 7 mg/g DM), stand out. However, even common field or ‘button’ mushrooms, Agaricus bisporus, contain some 0·4 mg/g DM. Note too that tempe(h), the result of a solid substrate Rhizopus oligosporus fermentation, also contains high levels of ERG. Mushrooms may also be a significant benefit to those seeking a meat-free diet as they can be made to share certain organoleptic features with meat. Notably, ‘the production of cultivated, edible mushrooms worldwide has increased more than 30-fold since 1978, whereas the population has only increased by about 1·7-fold during the same period’.

Some studies that have demonstrated nutritional/health benefits of mushrooms and their antioxidant activity) did not always seek to deconstruct these into their constituents such as ERG, but ERG is clearly the chief mushroom antioxidant. We note too that some effects may be dependent on the composition of the gut microflora, that are of course themselves likely to be changed by ERG, just as they are by many other non-antibiotic drugs.

Safety

Producer organisms such as mushrooms are well known to make many secondary metabolites, some of which can be highly toxic and by various mechanisms. Notwithstanding the highly variable intake between individuals, however, a number of high-dose studies have indicated that ERG is safe for mammalian consumption at levels far in excess of those likely to be encountered in foodstuffs, and it has been declared safe by relevant committees such as those of the European Food Standards Agency. It also lacks any detectable mutagenicity or genotoxicity in such assays, even at very high doses.

Analytics

Leaving aside early efforts such as the colorimetric methods of Hunter, of Melville and colleagues and of Carlsson et al., a variety of analytical methods have been proposed, mostly involving capillary electrophoresis or chromatography coupled to absorbance, fluorescence detection, electrochemical detection or MS. A useful feature is that ERG is unusually stable, in that anhydrous ERG decomposes only at 275–276°C, allowing its isolation at temperatures close to that of boiling water. As judged by the reversibility of its acid–base titration, it is also stable to extremes of pH.

Industrial purification of glycine betaine is done by extraction with water and subsequent ion exchange chromatography, which can be done in simulated moving bed fashion. Glycine betaine can then be crystallised. As glycine betaine is structurally similar to ERG, this straightforward industrial process could potentially be adapted for ERG.

Serum and other concentrations

While most ERG is inside erythrocytes in whole blood, there have been a number of measurements of ERG concentrations in serum. Unsurprisingly it varies with diet, starvation, age and other factors, including diseases of oxidative stress, with typical values of 20–100 µg/ml. A detailed list is provided by Cheah & Halliwell; a smaller listing is given in Table 3. Interestingly, ERG is also present in seminal fluid and human breast milk. Any possible correlation with male fertility seems not to have been established, though there were no negative effects, and ERG improved oocyte quality and maturation in cows and sheep. ERG is also present in eye lens, where its concentration is lower in individuals with cataracts.

Metabolism and excretion

ERG is metabolised and excreted only slowly. In a recent and detailed study, Cheah et al. administered 5–25 mg daily doses of ERG to human volunteers for 7 d. There was little urinary excretion (<4 %), and the main metabolites were hercynine, plus lesser amounts of S-methyl-ERG, whose concentrations were well correlated with the level of ERG and the dose of ERG given. Similar observations were made in mice. Various other biomarkers of oxidative stress (for example, 8-iso-PGF2α from lipid peroxidation) were lowered concomitantly in the human study, attesting to the antioxidant functions of ERG in vivo, although in this case the healthy young subjects were probably not suffering from oxidative stress. There was also quite some variation in uptake between individuals, presumably reflecting variation in their expression of SLC22A4. Agrobacterium radiobacter and other bacteria contain an ergothionase that degrades ERG to thiolurocanic acid (3-(1H-imidazol-5-yl)prop-2-enethioic S-acid) and trimethylamine, also implying that such cells possess one or more transporters for ERG. The thiolurocanic acid can be further degraded to glutamate.

Apparent fitness benefits and bioactivities of ERG and the role of SLC22A4

Given the great technical difficulties associated, because of its ubiquity, with withholding ergothoneine from a human or animal diet, one means of ‘removing’ ERG from a host is to remove the ERG transporter by genetic means. This has in fact been done in mice; such SCL22A4–/– mice had immeasurably low levels of ERG relative to controls, and were much more sensitive to oxidative stress than were the wild type. Similar effects were observed in Caenorhabditis elegans. Polymorphisms in SLC22A4, of which there can be many, under selection, have also been associated with ischaemic stroke, erythroid differentiation, hearing loss, rheumatoid arthritis, lupus, Crohn’s disease, hearing loss, type 1 diabetes and diabetic embryopathy. The expression of SLC22A4 can itself be modulated by other factors, including by PPAR-α activity. The very diversity of these diseases speaks naturally to a broad and common underlying cause, the easiest of which involves mechanisms of oxidative stress, inflammation and cell death.

Mechanisms of action

It has become common to discover a binding of a small molecule to another molecule such as a protein, and assume that this interaction, leading to activation or inhibition of the target, constitutes ‘the’ mechanism of action of the small molecule at a physiological level. Unfortunately this is rarely the case, and known drugs, despite often being selected for inhibiting potently a specific molecular target, have, on average, six known binding targets. When these interactions ramify through a complex and non-linear biochemical network it can be hard to apportion the effects of a small exogenous molecule between the various interactions.

A standard view of systems or network biology (for example, Kell and Kell & Knowles) develops these ideas in four stages. In stages 1 and 2 we simply recognise the actors and the interactions between them at a qualitative level. Stages 3 and 4 then seek to describe the equations reflecting individual steps and the values of the parameters of those equations. Armed with these we can make an ordinary or, if spatial resolution within a compartment is required, a partial differential equation model of the system. This can then be run and the sensitivities of each step determined. We are very far from this last part, and so studies of the effects of ERG have in general been rather descriptive in nature. Many have been at the level of processes rather than mechanisms, and they have been reviewed in detail. Table 4 and Fig. 7 provide a selection of determinands that have been shown to change their concentrations or activities when ERG is added to the system of interest. In many cases it is not at all clear what the proximate mechanisms are. Note as just one example that the highly promiscuous transcription factor NF-κB, whose frequency-dependent activity directly affects the expression of hundreds of enzymes, is itself redox-sensitive, and is affected by ERG, while NF-κB increases the rates of SC22A4 transcription. Thus, deconstructing the many possible direct and consequential interactions of ERG with proteins, v. whether these are simply a consequence of its provision of a more reducing environment, is likely to be a formidable task. In a similar vein, the effects of ERG on the microbiomes of the hosts are likely to be significant, but do not yet seem to have been studied.

It seems clear that the chief role of ERG, via a variety of mechanisms, including directly, is to serve as an antioxidant and cellular protectant against various kinds of reactive oxygen and N species.

Cytoprotection

At a high level, ERG is seen as an excellent cytoprotectant against all kinds of cellular insults. We split some of the more detailed analyses into subdivisions in the following few sections.

Oxidative stress

Oxidative stress can be defined and measured in many ways, but is broadly taken to involve a dysregulation in the various redox systems of the organism of interest, coupled to the production of various ‘reactive oxygen species’, principally peroxide, superoxide, hydroxyl radical, and singlet oxygen. ERG has been shown to decrease oxidative stress in the liver and kidney of rats, rescued cells from β-amyloid-induced apoptotic death, protected against palmitic acid-induced cell death, mercuric chloride-induced cellular dysfunction, and prevented Cu-induced oxidative damage to DNA. It is protective against the oxidation of various kinds of molecule, including astaxanthin, and accumulates in a guinea-pig model of non-alcoholic fatty liver disease, massively so in mouse models of myocardial infarction and heart failure, and in a rat model of optic nerve crush. It serves to resist H2O2-induced cell death, pyrogallol-induced toxicity, cisplatin- or oxaliplatin-induced toxicity, glucose-induced senescence, as well as lipopolysaccharide-induced inflammation. In particular, it is protective against ischaemia–reperfusion injury, and may have uses in prolonging the lifetime of stored blood. Probably such antioxidant activities are at the core of its biological benefits.

Ergothioneine as a therapeutic for chronic inflammatory diseases?

Inflammation and oxidative stress go hand in hand, since reactive oxygen species (and materials such as bacterial cell wall components that can lead to their generation), lead to the production of inflammatory cytokines. Although a great many chronic, inflammatory diseases are recognised as having an oxidative stress component, the history of treating them with antioxidants such as ascorbate has largely been a litany of failure, with the treatment arm often even giving worse prognoses than the placebo. Arguably this is because nominally antioxidant molecules such as ascorbate have complex, multi-electron redox chemistry, and can in fact act as pro-oxidants, especially in the presence of free Fe or Cu. This is not an issue with ERG, however, partly because it can chelate them, and ERG levels are decreased, or ERG has been proposed as a useful antioxidant, in diseases such as acute respiratory distress syndrome, CVD, chronic obstructive pulmonary disease, pre-eclampsia (see also Turner et al.), overhydrated hereditary stomatocytosis, and is significantly lowered in others such as certain leukaemias. The evidence for this comes from a variety of sources, including metabolite measurements in human subjects, and intervention studies in both animals and cell lines. In particular, there is a notable relationship between ERG consumption and longevity (Fig. 6 in Beelman et al.), while in a 3236-participant Swedish study, ERG was the metabolite most strongly connected to a ‘health conscious food pattern’ and was associated with a lower risk of coronary disease (hazard ratio (HR) per 1 sd increment of ERG, HR = 0·85; P = 0·01), cardiovascular mortality (HR = 0·79; P = 0·002) and overall mortality (HR = 0·86; P = 4 × 10–5).

Neurological diseases and cognitive function

Mushrooms have been shown to have very substantial effects on cognitive function, and this is mainly ascribed to their ERG content, that also deceases with the age of the consumer. The kinds of evidence include both double-blind, placebo-controlled clinical trials and observational (cross-sectional) studies in both humans and rodents. Thus, consuming 1·5 mushroom servings per week was associated with a halving of the incidence of mild cognitive impairment (a precursor of Alzheimer’s dementia), while intake of nine servings per week was associated with a five-fold decrease. Note, however, that at least one mushroom trial indicated no measurable benefits in healthy young physical education students. Brain and serum ERG levels are also markedly different in Parkinson’s disease, reviewed in Hang et al., Shao & Le and Shah & Duda, and even in sudden infant death syndrome, and ERG has been shown to be protective against β-amyloid-induced neuronal injury and cytotoxicity. It can also act as an antidepressant. The evidence for this comes from direct studies and feeding experiments in mice, as well as via the reduction of β-amyloid peptide in a transgenic C. elegans model. As mentioned above, SLC22A4 polymorphisms are associated with ischaemic stroke.

Use of ergothioneine as an antioxidant in processed foodstuffs

Just as living beings exploit antioxidants, most foodstuffs can also be oxidised to produce taints, rancidity or other undesirable products, often via the Fenton reaction. ERG inhibits polyphenoloxidases, and thus ERG has been used in the feed of the shrimp Marsupenaeus japonicas to prevent melanosis during storage, while ERG-rich mushroom extract has also been used to prevent melanosis in post-harvest storage of the crab Chionoecetes japonicus. Thus, one can also envisage a role for ERG, whether natural or added, in extending shelf lives and commercial value. The thermostability of ERG is of particular importance here.

Use of ergothioneine in cosmetics

Just as processed foodstuffs ‘age’, so do tissues such as the skin, and although the same principles apply, it is common to refer to nutraceuticals that are also aimed at having cosmetic benefits as ‘cosmeceuticals’. Here too, ERG has been widely used, since much skin damage is caused by UV-mediated reactive oxygen species production; indeed, ERG is known as a skin protectant.

Role of ergothioneine as a cofactor?

Although it is possible that the role of ERG lies simply in being an antioxidant capable of mopping up hydroxyl radicals and other reactive oxygen species, especially in prokaryotes, the roles of most other vitamins involve interaction with proteins, often as cofactors. This is also true for mycothiol, though that molecule can also serve as a signal and nutrient resource. However, despite many hypotheses, the only example of ERG acting as a cofactor known to date is an involvement in the biosynthesis of lincomycin. An early paper implying an involvement of ERG in the maintenance of a reduced state of Fe in Hb, although apparently accurate, does not seem to have been followed up to date.

Conclusions

There is increasing awareness that health may be enhanced via the consumption of substances that either have no recommended daily intake or are taken at levels greater than normal, and such substances are commonly referred to as nutraceuticals. ERG, a potent and effective antioxidant, seems to be an important nutraceutical, and we rehearse a very broad literature, involving a great many cells, tissues and organisms, to that effect. The chief source of ERG in the human diet is mushrooms (usually the fruiting bodies of Basidiomycetes). The fact that a specific transporter known as SLC22A4 has evolved and been selected to effect ERG uptake in all known animals suggests strongly that ERG is of benefit to its consumers. While the evidence that ERG may be a useful nutraceutical as a preventive or palliative for various inflammatory diseases is extensive, it is mostly circumstantial rather than definitive, though many examples exist of the benefits of mushrooms in combating the results of oxidative stress.

Without mechanisms, finding that the concentration of a dietary metabolite X is low in disease Y does not mean that giving it might be of benefit in the prevention, delay or cure of that disease, although cases can clearly be made when X is a vitamin, or oxidative stress is known to be a damaging component of Y. Thus far, we lack examples in which ERG is found both to be low in individuals with a particular syndrome and where exogenous administration effects functional improvements, although – as reviewed above – we often have one or the other.

To assess definitively any health benefits of ERG, the ‘gold standard’ of randomised controlled trials may take time and money, but – as with mushrooms – are beginning. One trial with pure ERG has been registered.

Note added in proof

A recent paper indicates that ERG relieves the effects seen in a rat model of the pregnancy disorder pre-eclampsia.

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    Not in our library10.1080/09168451.2018.1527210

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    Not in our library10.3389/fbioe.2019.00262

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    O’Hagan S, Wright Muelas M, Day PJ, et al. (2018 ) GeneGini: assessment via the Gini coefficient of reference “housekeeping” genes and diverse human transporter expression profiles. Cell Syst 6, 230–244.

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    Chaleckis R, Ebe M, Pluskal T, et al. (2014 ) Unexpected similarities between the Schizosaccharomyces and human blood metabolomes, and novel human metabolites. Mol Biosyst 10, 2538–2551.

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    McMenamy RH, Lund CC & Wallach DF (1960 ) Unbound amino acid concentrations in plasma, erythrocytes, leukocytes and urine of patients with leukemia. J Clin Invest 39, 1688–1705.

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    Reglinski J, Smith WE, Wilson R, et al. (1991 ) Clinical analysis in intact erythrocytes using 1H spin echo NMR. Clin Chim Acta 201, 45–57.

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    Turner E, Brewster JA, Simpson NA, et al. (2009 ) Imidazole-based erythrocyte markers of oxidative stress in preeclampsia – an NMR investigation. Reprod Sci 16, 1040–1051.

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    Mitsuyama H & May JM (1999 ) Uptake and antioxidant effects of ergothioneine in human erythrocytes. Clin Sci (Lond) 97, 407–411.

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    Gründemann D, Harlfinger S, Golz S, et al. (2005 ) Discovery of the ergothioneine transporter. Proc Natl Acad Sci U S A 102, 5256–5261.

    Not in our library10.1073/pnas.0408624102

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    Nikodemus D, Lazic D, Bach M, et al. (2011 ) Paramount levels of ergothioneine transporter SLC22A4 mRNA in boar seminal vesicles and cross-species analysis of ergothioneine and glutathione in seminal plasma. J Physiol Pharmacol 62, 411–419.

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    Kaneko I, Takeuchi Y, Yamaoka Y, et al. (1980 ) Quantitative determination of ergothioneine in plasma and tissues by TLC-densitometry. Chem Pharm Bull (Tokyo) 28, 3093–3097.

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    Crossland J, Mitchell J & Woodruff GN (1966 ) The presence of ergothioneine in the central nervous system and its probable identity with the cerebellar factor. J Physiol 182, 427–438.

    Not in our library10.1113/jphysiol.1966.sp007830

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    Nakamichi N, Taguchi T, Hosotani H, et al. (2012 ) Functional expression of carnitine/organic cation transporter OCTN1 in mouse brain neurons: possible involvement in neuronal differentiation. Neurochem Int 61, 1121–1132.

    Not in our library10.1016/j.neuint.2012.08.004

  137. 137.

    Vermeulen E & Vermeersch P (2012 ) Hepcidin as a biomarker for the diagnosis of iron metabolism disorders: a review. Acta Clin Belg 67, 190–197.

    Not in our library10.2143/acb.67.3.2062654

  138. 138.

    Ganz T & Nemeth E (2011 ) The hepcidin–ferroportin system as a therapeutic target in anemias and iron overload disorders. Hematol Am Soc Hematol Educ Program 2011, 538–542.

    Not in our library10.1182/asheducation-2011.1.538

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    Ganz T & Nemeth E (2012 ) Hepcidin and iron homeostasis. Biochim Biophys Acta 1823, 1434–1443.

    Not in our library10.1016/j.bbamcr.2012.01.014

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    Nemeth E & Ganz T (2009 ) The role of hepcidin in iron metabolism. Acta Haematol 122, 78–86.

    Not in our library10.1159/000243791

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    Reichert CO, da Cunha J, Levy D, et al. (2017 ) Hepcidin: homeostasis and diseases related to iron metabolism. Acta Haematol 137, 220–236.

    Not in our library10.1159/000471838

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    Kell DB, Swainston N, Pir P, et al. (2015 ) Membrane transporter engineering in industrial biotechnology and whole-cell biocatalysis. Trends Biotechnol 33, 237–246.

    Not in our library10.1016/j.tibtech.2015.02.001

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    Dobson PD & Kell DB (2008 ) Carrier-mediated cellular uptake of pharmaceutical drugs: an exception or the rule? Nat Rev Drug Disc 7, 205–220.

    Not in our library10.1038/nrd2438

  144. 144.

    Kell DB & Dobson PD (2009 ) The cellular uptake of pharmaceutical drugs is mainly carrier-mediated and is thus an issue not so much of biophysics but of systems biology In Proceedings of the International Beilstein Symposium on Systems Chemistry, pp. 149–168 [ MG Hicks and C Kettner, editors]. Berlin: Logos Verlag.

    Not in our library

  145. 145.

    Kell DB, Dobson PD & Oliver SG (2011 ) Pharmaceutical drug transport: the issues and the implications that it is essentially carrier-mediated only. Drug Disc Today 16, 704–714.

    Not in our library10.1016/j.drudis.2011.05.010

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    Kell DB, Dobson PD, Bilsland E, et al. (2013 ) The promiscuous binding of pharmaceutical drugs and their transporter-mediated uptake into cells: what we (need to) know and how we can do so. Drug Disc Today 18, 218–239.

    Not in our library10.1016/j.drudis.2012.11.008

  147. 147.

    Kell DB (2013 ) Finding novel pharmaceuticals in the systems biology era using multiple effective drug targets, phenotypic screening, and knowledge of transporters: where drug discovery went wrong and how to fix it. FEBS J 280, 5957–5980.

    Not in our library10.1111/febs.12268

  148. 148.
    How drugs get into cells: tested and testable predictions to help discriminate between transporter-mediated uptake and lipoidal bilayer diffusion · 2014
    No notice
  149. 149.

    Kell DB (2015 ) The transporter-mediated cellular uptake of pharmaceutical drugs is based on their metabolite-likeness and not on their bulk biophysical properties: towards a systems pharmacology. Perspect Sci 6, 66–83.

    Not in our library

  150. 150.

    Kell DB (2016 ) How drugs pass through biological cell membranes – a paradigm shift in our understanding? Beilstein Magazine 2, no. 5.

    Not in our library

  151. 151.

    Giacomini KM, Huang SM, Tweedie DJ, et al. (2010 ) Membrane transporters in drug development. Nat Rev Drug Discov 9, 215–236.

    Not in our library10.1038/nrd3028

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    Dickens D, Rädisch S, Chiduza GN, et al. (2018 ) Cellular uptake of the atypical antipsychotic clozapine is a carrier-mediated process. Mol Pharm 15, 3557–3572.

    Not in our library10.1021/acs.molpharmaceut.8b00547

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    César-Razquin A, Snijder B, Frappier-Brinton T, et al. (2015 ) A call for systematic research on solute carriers. Cell 162, 478–487.

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  154. 154.
    The ABCs of membrane transporters in health and disease (SLC series): Introduction · 2013
    No notice
  155. 155.

    Anonymous (2019 ) SLC Tables. http://www.bioparadigms.org/slc/intro.htm (accessed August 2019

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    Chen Z, Shi T, Zhang L, et al. (2016 ) Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: a review of the past decade. Cancer Lett 370, 153–164.

    Not in our library10.1016/j.canlet.2015.10.010

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    Koepsell H (2013 ) The SLC22 family with transporters of organic cations, anions and zwitterions. Mol Aspects Med 34, 413–435.

    Not in our library10.1016/j.mam.2012.10.010

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    Pochini L, Galluccio M, Scalise M, et al. (2019 ) OCTN: a small transporter subfamily with great relevance to human pathophysiology, drug discovery, and diagnostics. SLAS Discov 24, 89–110.

    Not in our library10.1177/2472555218812821

  159. 159.

    Garg N, Kapono C, Lim YW, et al. (2015 ) Mass spectral similarity for untargeted metabolomics data analysis of complex mixtures. Int J Mass Spectrom 377, 719–717.

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    Li XS, Wang Z, Cajka T, et al. (2018 ) Untargeted metabolomics identifies trimethyllysine, a TMAO-producing nutrient precursor, as a predictor of incident cardiovascular disease risk. JCI Insight 3, 99096.

    Not in our library10.1172/jci.insight.99096

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    Next‐generation metabolic screening: targeted and untargeted metabolomics for the diagnosis of inborn errors of metabolism in individual patients · 2018
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    Tautenhahn R, Cho K, Uritboonthai W, et al. (2012 ) An accelerated workflow for untargeted metabolomics using the METLIN database. Nature Biotechnol 30, 826–828.

    Not in our library10.1038/nbt.2348

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    Dunn WB, Broadhurst D, Begley P, et al. (2011 ) Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc 6, 1060–1083.

    Not in our library10.1038/nprot.2011.335

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    Dunn WB, Erban A, Weber RJM, et al. (2013 ) Mass appeal: metabolite identification in mass spectrometry-focused untargeted metabolomics. Metabolomics 9, Suppl. 1, S44–S66.

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    Heinzmann SS, Brown IJ, Chan Q, et al. (2010 ) Metabolic profiling strategy for discovery of nutritional biomarkers: proline betaine as a marker of citrus consumption. Am J Clin Nutr 92, 436–443.

    Not in our library10.3945/ajcn.2010.29672

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    Lang R, Lang T, Bader M, et al. (2017 ) High-throughput quantitation of proline betaine in foods and suitability as a valid biomarker for citrus consumption. J Agric Food Chem 65, 1613–1619.

    Not in our library10.1021/acs.jafc.6b05824

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    Lloyd AJ, Beckmann M, Favé G, et al. (2011 ) Proline betaine and its biotransformation products in fasting urine samples are potential biomarkers of habitual citrus fruit consumption. Br J Nutr 106, 812–824.

    Not in our library10.1017/s0007114511001164

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    Bacher P, Giersiefer S, Bach M, et al. (2009 ) Substrate discrimination by ergothioneine transporter SLC22A4 and carnitine transporter SLC22A5: gain-of-function by interchange of selected amino acids. Biochim Biophys Acta 1788, 2594–2602.

    Not in our library10.1016/j.bbamem.2009.09.019

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    Grigat S, Harlfinger S, Pal S, et al. (2007 ) Probing the substrate specificity of the ergothioneine transporter with methimazole, hercynine, and organic cations. Biochem Pharmacol 74, 309–316.

    Not in our library10.1016/j.bcp.2007.04.015

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    Gründemann D (2012 ) The ergothioneine transporter controls and indicates ergothioneine activity – a review. Prev Med 54, Suppl., S71–S74.

    Not in our library10.1016/j.ypmed.2011.12.001

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    Tschirka J, Kreisor M, Betz J, et al. (2018 ) Substrate selectivity check of the ergothioneine transporter. Drug Metab Dispos 46, 779–785.

    Not in our library10.1124/dmd.118.080440

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    Shimizu T, Masuo Y, Takahashi S, et al. (2015 ) Organic cation transporter OCTN1-mediated uptake of food-derived antioxidant ergothioneine into infiltrating macrophages during intestinal inflammation in mice. Drug Metab Pharmacokinet 30, 231–239.

    Not in our library10.1016/j.dmpk.2015.02.003

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    Yabuuchi H, Tamai I, Nezu J, et al. (1999 ) Novel membrane transporter OCTN1 mediates multispecific, bidirectional, and pH-dependent transport of organic cations. J Pharmacol Exp Ther 289, 768–773.

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    Akamine T, Koyanagi S, Kusunose N, et al. (2015 ) Dosing time-dependent changes in the analgesic effect of pregabalin on diabetic neuropathy in mice. J Pharmacol Exp Ther 354, 65–72.

    Not in our library10.1124/jpet.115.223891

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    Shimizu T, Kijima A, Masuo Y, et al. (2015 ) Gene ablation of carnitine/organic cation transporter 1 reduces gastrointestinal absorption of 5-aminosalicylate in mice. Biol Pharm Bull 38, 774–780.

    Not in our library10.1248/bpb.b15-00109

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    Tamai I (2013 ) Pharmacological and pathophysiological roles of carnitine/organic cation transporters (OCTNs: SLC22A4, SLC22A5 and Slc22a21). Biopharm Drug Dispos 34, 29–44.

    Not in our library10.1002/bdd.1816

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    Nakamura T, Yoshida K, Yabuuchi H, et al. (2008 ) Functional characterization of ergothioneine transport by rat organic cation/carnitine transporter OCTN1 (SLC22A4). Biol Pharm Bull 31, 1580–1584.

    Not in our library10.1248/bpb.31.1580

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    Darghouth D, Giarratana MC, Oliveira L, et al. (2016 ) Bio-engineered and native red blood cells from cord blood exhibit the same metabolomic profile. Haematologica 101, e220–e222.

    Not in our library10.3324/haematol.2015.141465

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    Taubert D, Lazar A, Grimberg G, et al. (2006 ) Association of rheumatoid arthritis with ergothioneine levels in red blood cells: a case control study. J Rheumatol 33, 2139–2145.

    Not in our library

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    Indiveri C, Galluccio M, Scalise M, et al. (2013 ) Strategies of bacterial over expression of membrane transporters relevant in human health: the successful case of the three members of OCTN subfamily. Mol Biotechnol 54, 724–736.

    Not in our library10.1007/s12033-012-9586-8

  182. 182.

    Frigeni M, Iacobazzi F, Yin X, et al. (2016 ) Wide tolerance to amino acids substitutions in the OCTN1 ergothioneine transporter. Biochim Biophys Acta 1860, 1334–1342.

    Not in our library10.1016/j.bbagen.2016.03.021

  183. 183.

    Nigam SK (2018 ) The SLC22 transporter family: a paradigm for the impact of drug transporters on metabolic pathways, signaling, and disease. Annu Rev Pharmacol Toxicol 58, 663–687.

    Not in our library10.1146/annurev-pharmtox-010617-052713

  184. 184.

    Pochini L, Scalise M, Galluccio M, et al. (2013 ) OCTN cation transporters in health and disease: role as drug targets and assay development. J Biomol Screen 18, 851–867.

    Not in our library10.1177/1087057113493006

  185. 185.

    Wolf KK & Paine MF (2018 ) Metabolic barrier of the gastrointestinal tract In Comprehensive Toxicology, 3rd ed, pp. 74–98 [ C McQueen, editor]. Amsterdam: Elsevier.

    Not in our library

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    Thul PJ, Åkesson L, Wiking M, et al. (2017 ) A subcellular map of the human proteome. Science 356, eaal3321.

    Not in our library10.1126/science.aal3321

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    Apostolova N & Victor VM (2015 ) Molecular strategies for targeting antioxidants to mitochondria: therapeutic implications. Antioxid Redox Signal 22, 686–729.

    Not in our library10.1089/ars.2014.5952

  188. 188.

    Lamhonwah AM & Tein I (2006 ) Novel localization of OCTN1, an organic cation/carnitine transporter, to mammalian mitochondria. Biochem Biophys Res Commun 345, 1315–1325.

    Not in our library10.1016/j.bbrc.2006.05.026

  189. 189.

    Lamhonwah AM, Hawkins CE, Tam C, et al. (2008 ) Expression patterns of the organic cation/carnitine transporter family in adult murine brain. Brain Dev 30, 31–42.

    Not in our library10.1016/j.braindev.2007.05.005

  190. 190.

    Xuan W, Lamhonwah AM, Librach C, et al. (2003 ) Characterization of organic cation/carnitine transporter family in human sperm. Biochem Biophys Res Commun 306, 121–128.

    Not in our library10.1016/s0006-291x(03)00930-6

  191. 191.

    Anonymous (2019 ) SLC22A4. https://www.proteinatlas.org/ENSG00000197208-SLC22A4/cell (accessed August 2019).

    Not in our library

  192. 192.

    Skogs M, Stadler C, Schutten R, et al. (2017 ) Antibody validation in bioimaging applications based on endogenous expression of tagged proteins. J Proteome Res 16, 147–155.

    Not in our library10.1021/acs.jproteome.6b00821

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    Edfors F, Hober A, Linderbäck K, et al. (2018 ) Enhanced validation of antibodies for research applications. Nat Commun 9, 4130.

    Not in our library10.1038/s41467-018-06642-y

  194. 194.

    Rabia LA, Desai AA, Jhajj HS, et al. (2018 ) Understanding and overcoming trade-offs between antibody affinity, specificity, stability and solubility. Biochem Eng J 137, 365–374.

    Not in our library10.1016/j.bej.2018.06.003

  195. 195.

    Jain D & Salunke DM (2019 ) Antibody specificity and promiscuity. Biochem J 476, 433–447.

    Not in our library10.1042/bcj20180670

  196. 196.

    Edwards BM, Barash SC, Main SH, et al. (2003 ) The remarkable flexibility of the human antibody repertoire; isolation of over one thousand different antibodies to a single protein, BLyS. J Mol Biol 334, 103–118.

    Not in our library10.1016/j.jmb.2003.09.054

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    Vaughan TJ, Osbourn JK & Tempest PR (1998 ) Human antibodies by design. Nat Biotechnol 16, 535–539.

    Not in our library10.1038/nbt0698-535

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    Michaud GA, Salcius M, Zhou F, et al. (2003 ) Analyzing antibody specificity with whole proteome microarrays. Nat Biotechnol 21, 1509–1512.

    Not in our library10.1038/nbt910

  199. 199.

    Palmieri F (2013 ) The mitochondrial transporter family SLC25: identification, properties and physiopathology. Mol Aspects Med 34, 465–484.

    Not in our library10.1016/j.mam.2012.05.005

  200. 200.

    Palmieri F (2014 ) Mitochondrial transporters of the SLC25 family and associated diseases: a review. J Inherit Metab Dis 37, 565–575.

    Not in our library10.1007/s10545-014-9708-5

  201. 201.

    Anonymous (2019 ) Q9H015 tree in phylome 533. http://phylomedb.org/?q=search_tree&seqid=Q9H015# (accessed August 2019).

    Not in our library

  202. 202.

    Anonymous (2019 ) GeneTree Image. http://www.ensembl.org/Multi/GeneTree/Image?gt=ENSGT00940000154155 (accessed August 2019).

    Not in our library

  203. 203.

    O’Hagan S & Kell DB (2017 ) Consensus rank orderings of molecular fingerprints illustrate the ‘most genuine’ similarities between marketed drugs and small endogenous human metabolites, but highlight exogenous natural products as the most important ‘natural’ drug transporter substrates. ADMET DMPK 5, 85–125.

    Not in our library

  204. 204.

    Chapy H, Smirnova M, Andre P, et al. (2014 ) Carrier-mediated cocaine transport at the blood–brain barrier as a putative mechanism in addiction liability. Int J Neuropsychopharmacol 18, pyu001.

    Not in our library10.1093/ijnp/pyu001

  205. 205.

    Danchin A (2018 ) Bacteria in the ageing gut: did the taming of fire promote a long human lifespan? Environ Microbiol 20, 1966–1987.

    Not in our library10.1111/1462-2920.14255

  206. 206.

    Kell DB & Pretorius E (2018 ) No effects without causes. The iron dysregulation and dormant microbes hypothesis for chronic, inflammatory diseases. Biol Rev 93, 1518–1557.

    Not in our library10.1111/brv.12407

  207. 207.

    Butterfield DA & Halliwell B (2019 ) Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease. Nat Rev Neurosci 20, 148–160.

    Not in our library10.1038/s41583-019-0132-6

  208. 208.
    Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases · 2009
    No notice
  209. 209.

    Babior BM (2000 ) Phagocytes and oxidative stress. Am J Med 109, 33–44.

    Not in our library10.1016/s0002-9343(00)00481-2

  210. 210.

    Cave AC, Brewer AC, Narayanapanicker A, et al. (2006 ) NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 8, 691–728.

    Not in our library10.1089/ars.2006.8.691

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    Bedard K & Krause KH (2007 ) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87, 245–313.

    Not in our library10.1152/physrev.00044.2005

  212. 212.

    Wardman P & Candeias LP (1996 ) Fenton chemistry: an introduction. Rad Res 145, 523–531.

    Not in our library

  213. 213.

    Kell DB (2010 ) Towards a unifying, systems biology understanding of large-scale cellular death and destruction caused by poorly liganded iron: Parkinson’s, Huntington’s, Alzheimer’s, prions, bactericides, chemical toxicology and others as examples. Arch Toxicol 577, 825–889.

    Not in our library10.1007/s00204-010-0577-x

  214. 214.

    Winston GW, Feierman DE & Cederbaum AI (1984 ) The role of iron chelates in hydroxyl radical production by rat liver microsomes, NADPH-cytochrome P-450 reductase and xanthine oxidase. Arch Biochem Biophys 232, 378–390.

    Not in our library10.1016/0003-9861(84)90553-8

  215. 215.

    Fong A & Hieftje GM (1995 ) Near-IR multiplex bandpass spectrometer utilizing liquid molecular filters. Appl Spectrosc 49, 493–498.

    Not in our library

  216. 216.

    Kehrer JP (2000 ) The Haber–Weiss reaction and mechanisms of toxicity. Toxicology 149, 43–50.

    Not in our library10.1016/s0300-483x(00)00231-6

  217. 217.

    Kell DB & Pretorius E (2014 ) Serum ferritin is an important disease marker, and is mainly a leakage product from damaged cells. Metallomics 6, 748–773.

    Not in our library10.1039/c3mt00347g

  218. 218.

    Valachová K, Mach M, Dubovický M, et al. (2019 ) The importance of ergothioneine synthesis in ancient time by organisms living in oxygen free atmosphere. Med Hypotheses 123, 72–73.

    Not in our library10.1016/j.mehy.2018.12.015

  219. 219.

    Migliore L, Fontana I, Colognato R, et al. (2005 ) Searching for the role and the most suitable biomarkers of oxidative stress in Alzheimer’s disease and in other neurodegenerative diseases. Neurobiol Aging 26, 587–595.

    Not in our library10.1016/j.neurobiolaging.2004.10.002

  220. 220.

    Ahsan H (2013 ) 3-Nitrotyrosine: a biomarker of nitrogen free radical species modified proteins in systemic autoimmunogenic conditions. Hum Immunol 74, 1392–1399.

    Not in our library10.1016/j.humimm.2013.06.009

  221. 221.
    Fundamentals on the biochemistry of peroxynitrite and protein tyrosine nitration · 2018
    Not checked
  222. 222.

    Ryberg H & Caidahl K (2007 ) Chromatographic and mass spectrometric methods for quantitative determination of 3-nitrotyrosine in biological samples and their application to human samples. J Chromatogr B 851, 160–171.

    Not in our library10.1016/j.jchromb.2007.02.001

  223. 223.

    Rahman I (2012 ) Pharmacological antioxidant strategies as therapeutic interventions for COPD. Biochim Biophys Acta 1822, 714–728.

    Not in our library10.1016/j.bbadis.2011.11.004

  224. 224.

    Aruoma OI, Whiteman M, England TG, et al. (1997 ) Antioxidant action of ergothioneine: assessment of its ability to scavenge peroxynitrite. Biochem Biophys Res Commun 231, 389–391.

    Not in our library10.1006/bbrc.1997.6109

  225. 225.

    Halliwell B (1997 ) What nitrates tyrosine? Is nitrotyrosine specific as a biomarker of peroxynitrite formation in vivo? FEBS Lett 411, 157–160.

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    Royse DJ, Baars J & Tan Q (2017 ) Current overview of mushroom production in the world In Edible and Medicinal Mushrooms: Technology and Applications, pp. 5–14 [ DC Zied and A Pardo-Giménez, editors]. New York: Wiley-Blackwell.

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    Khatun K, Mahtab H, Khanam PA, et al. (2007 ) Oyster mushroom reduced blood glucose and cholesterol in diabetic subjects. Mymensingh Med J 16, 94–99.

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    Guillamón E, García-Lafuente A, Lozano M, et al. (2010 ) Edible mushrooms: role in the prevention of cardiovascular diseases. Fitoterapia 81, 715–723.

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    Friedman M (2015 ) Chemistry, nutrition, and health-promoting properties of Hericium erinaceus (lion’s mane) mushroom fruiting bodies and mycelia and their bioactive compounds. J Agric Food Chem 63, 7108–7123.

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    Moon B & Lo YM (2014 ) Conventional and novel applications of edible mushrooms in today’s food industry. J Food Process Pres 38, 2146–2153.

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    Jayakumar T, Sakthivel M, Thomas PA, et al. (2008 ) Pleurotus ostreatus, an oyster mushroom, decreases the oxidative stress induced by carbon tetrachloride in rat kidneys, heart and brain. Chem-Biol Interact 176, 108–120.

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    Jayakumar T, Thomas PA, Sheu JR, et al. (2011 ) In vitro and in vivo antioxidant effects of the oyster mushroom Pleurotus ostreatus. Food Res Int 44, 851–861.

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    Jayakumar T, Thomas PA, Ramesh E, et al. (2010 ) An extract of the Pleurotus ostreatus mushroom bolsters the glutathione redox system in various organs of aged rats. J Med Food 13, 771–778.

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    Rahman MA, Abdullah N & Aminudin N (2017 ) Corroborative assessment of mushroom as the graceful ageing and lifespan promoting agent. Biointerface Res App 7, 2072–2083.

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    Rahman MA, Abdullah N & Aminudin N (2016 ) Interpretation of mushroom as a common therapeutic agent for Alzheimer’s disease and cardiovascular diseases. Crit Rev Biotechnol 36, 1131–1142.

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    Shukla Y, Kulshrestha OP & Khuteta KP (1981 ) Ergothioneine content in normal and senile human cataractous lenses. Indian J Med Res 73, 472–473.

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    Booth JS, Appleman MD (1963 ) Degradation of ergothioneine by cell-free extracts of Alcaligenes faecalis. II. Production of glutamic acid. J Bacteriol 85, 654–657.

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    Ben Said M, Grati M, Ishimoto T, et al. (2016 ) A mutation in SLC22A4 encoding an organic cation transporter expressed in the cochlea strial endothelium causes human recessive non-syndromic hearing loss DFNB60. Hum Genet 135, 513–524.

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    Urban TJ, Yang C, Lagpacan LL, et al. (2007 ) Functional effects of protein sequence polymorphisms in the organic cation/ergothioneine transporter OCTN1 (SLC22A4). Pharmacogenet Genomics 17, 773–782.

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    Toh DSL, Koo SH, Limenta LMG, et al. (2009 ) Genetic variations of the SLC22A4 gene in Chinese and Indian populations of Singapore. Drug Metab Pharmacokinet 24, 475–481.

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    Toh DSL, Cheung FSG, Murray M, et al. (2013 ) Functional analysis of novel variants in the organic cation/ergothioneine transporter 1 identified in Singapore populations. Mol Pharm 10, 2509–2516.

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    Not in our library10.1038/nature16152

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    Tokuhiro S, Yamada R, Chang X, et al. (2003 ) An intronic SNP in a RUNX1 binding site of SLC22A4, encoding an organic cation transporter, is associated with rheumatoid arthritis. Nat Genet 35, 341–348.

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    Barton A, Eyre S, Bowes J, et al. (2005 ) Investigation of the SLC22A4 gene (associated with rheumatoid arthritis in a Japanese population) in a United Kingdom population of rheumatoid arthritis patients. Arthritis Rheum 52, 752–758.

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    Taubert D, Grimberg G, Jung N, et al. (2005 ) Functional role of the 503F variant of the organic cation transporter OCTN1 in Crohn’s disease. Gut 54, 1505–1506.

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    Lai Y, Xue J, Liu CW, et al. (2019 ) Serum metabolomics identifies altered bioenergetics, signaling cascades in parallel with exposome markers in Crohn’s disease. Molecules 24, 449.

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    Not in our library10.1093/molbev/msr151

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    Peltekova VD, Wintle RF, Rubin LA, et al. (2004 ) Functional variants of OCTN cation transporter genes are associated with Crohn disease. Nat Genet 36, 471–475.

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    Newman B, Gu X, Wintle R, et al. (2005 ) A risk haplotype in the solute carrier family 22A4/22A5 gene cluster influences phenotypic expression of Crohn’s disease. Gastroenterology 128, 260–269.

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    Leung E, Hong J, Fraser AG, et al. (2006 ) Polymorphisms in the organic cation transporter genes SLC22A4 and SLC22A5 and Crohn’s disease in a New Zealand Caucasian cohort. Immunol Cell Biol 84, 233–236.

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    Santiago JL, Martinez A, de la Calle H, et al. (2006 ) Evidence for the association of the SLC22A4 and SLC22A5 genes with type 1 diabetes: a case control study. BMC Med Genet 7, 54.

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    Zhao Z, Reece EA (2013 ) New concepts in diabetic embryopathy. Clin Lab Med 33, 207–233.

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    Mestres J, Gregori-Puigjané E, Valverde S, et al. (2009 ) The topology of drug-target interaction networks: implicit dependence on drug properties and target families. Mol Biosyst 5, 1051–1057.

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    Kell DB (2006 ) Metabolomics, modelling and machine learning in systems biology: towards an understanding of the languages of cells. The 2005 Theodor Bücher lecture. FEBS J 273, 873–894.

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    Palsson BØ (2015 ) Systems Biology: Constraint-Based Reconstruction and Analysis. Cambridge: Cambridge University Press.

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    The Escherichia coli transcriptome mostly consists of independently regulated modules · 2019
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    Kell DB (2005 ) Metabolomics, machine learning and modelling: towards an understanding of the language of cells. Biochem Soc Trans 33, 520–524.

    Not in our library10.1042/bst0330520

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    Kell DB & Knowles JD (2006 ) The role of modeling in systems biology In System Modeling in Cellular Biology: From Concepts to Nuts and Bolts, pp. 3–18 [ Z Szallasi, J Stelling and V Periwal, editors]. Cambridge, MA: MIT Press.

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    Ihekwaba AEC, Broomhead DS, Grimley R, et al. (2004 ) Sensitivity analysis of parameters controlling oscillatory signalling in the NF-kB pathway: the roles of IKK and IkBa. Systems Biol 1, 93–103.

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    Saltelli A, Tarantola S, Campolongo F, et al. (2004 ) Sensitivity Analysis in Practice: A Guide to Assessing Scientific Models. New York: Wiley.

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    Rand DA (2008 ) Mapping global sensitivity of cellular network dynamics: sensitivity heat maps and a global summation law. J R Soc Interface 5, Suppl. 1, S59–S69.

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  449. 449.

    Kell DB & Oliver SG (2004 ) Here is the evidence, now what is the hypothesis? The complementary roles of inductive and hypothesis-driven science in the post-genomic era. Bioessays 26, 99–105.

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    Ledoux AC & Perkins ND (2014 ) NF-κB and the cell cycle. Biochem Soc Trans 42, 76–81.

    Not in our library10.1042/bst20130156

  451. 451.

    Perkins ND (2012 ) The diverse and complex roles of NF-κB subunits in cancer. Nat Rev Cancer 12, 121–132.

    Not in our library10.1038/nrc3204

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    NF-kappaB Signaling Pathways in Neurological Inflammation: A Mini Review · 2015
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    Nelson DE, Ihekwaba AEC, Elliott M, et al. (2004 ) Oscillations in NF-kB signalling control the dynamics of gene expression. Science 306, 704–708.

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    Ashall L, Horton CA, Nelson DE, et al. (2009 ) Pulsatile stimulation determines timing and specificity of NFκ-B-dependent transcription. Science 324, 242–246.

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    Buelna-Chontal M & Zazueta C (2013 ) Redox activation of Nrf2 & NF-κB: a double end sword? Cell Signal 25, 2548–2557.

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    Kaur U, Banerjee P, Bir A, et al. (2015 ) Reactive oxygen species, redox signaling and neuroinflammation in Alzheimer’s disease: the NF-κB connection. Curr Top Med Chem 15, 446–457.

    Not in our library10.2174/1568026615666150114160543

  457. 457.

    Lepetsos P, Papavassiliou KA & Papavassiliou AG (2019 ) Redox and NF-κB signaling in osteoarthritis. Free Radic Biol Med 132, 90–100.

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  458. 458.

    Gao G & Dudley SC Jr (2009 ) Redox regulation, NF-κB, and atrial fibrillation. Antioxid Redox Signal 11, 2265–2277.

    Not in our library10.1089/ars.2009.2595

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    Xiao L, Zhao L, Li T, et al. (2006 ) Activity of the dietary antioxidant ergothioneine in a virus gene-based assay for inhibitors of HIV transcription. Biofactors 27, 157–165.

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    Rahman I, Gilmour PS, Jimenez LA, et al. (2003 ) Ergothioneine inhibits oxidative stress- and TNF-α-induced NF-κ B activation and interleukin-8 release in alveolar epithelial cells. Biochem Biophys Res Commun 302, 860–864.

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  461. 461.
    The effects of oxidative stress on female reproduction: a review · 2012
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  462. 462.
    Oxidative Stress in Preeclampsia and Placental Diseases · 2018
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    Wang J, Schipper HM, Velly AM, et al. (2015 ) Salivary biomarkers of oxidative stress: a critical review. Free Radic Biol Med 85, 95–104.

    Not in our library10.1016/j.freeradbiomed.2015.04.005

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    Schrag M, Mueller C, Zabel M, et al. (2013 ) Oxidative stress in blood in Alzheimer’s disease and mild cognitive impairment: a meta-analysis. Neurobiol Dis 59, 100–110.

    Not in our library10.1016/j.nbd.2013.07.005

  465. 465.

    Jones DP (2006 ) Redefining oxidative stress. Antioxid Redox Signal 8, 1865–1879.

    Not in our library10.1089/ars.2006.8.1865

  466. 466.

    Rice-Evans CA & Packer L (editors) (2003 ) Flavonoids in Health and Disease, 2nd ed New York: Marcel Dekker.

    Not in our library

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    Halliwell B & Gutteridge JMC (2006 ) Free Radicals in Biology and Medicine, 4th ed Oxford: Oxford University Press.

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    Halliwell B & Gutteridge JMC (2015 ) Free Radicals in Biology and Medicine, 5th ed Oxford: Oxford University Press.

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    Deiana M, Rosa A, Casu V, et al. (2004 ) l-Ergothioneine modulates oxidative damage in the kidney and liver of rats in vivo: studies upon the profile of polyunsaturated fatty acids. Clin Nutr 23, 183–193.

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  470. 470.

    Laurenza I, Colognato R, Migliore L, et al. (2008 ) Modulation of palmitic acid-induced cell death by ergothioneine: evidence of an anti-inflammatory action. Biofactors 33, 237–247.

    Not in our library10.1002/biof.5520330401

  471. 471.

    Gökçe G, Arun MZ & Ertuna E (2018 ) Ergothioneine prevents endothelial dysfunction induced by mercury chloride. Exp Ther Med 15, 4697–4702.

    Not in our library10.3892/etm.2018.6079

  472. 472.

    Rai RK, Chalana A, Karri R, et al. (2019 ) Role of hydrogen bonding by thiones in protecting biomolecules from copper(I)-mediated oxidative damage. Inorg Chem 58, 6628–6638

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    Zhu BZ, Mao L, Fan RM, et al. (2011 ) Ergothioneine prevents copper-induced oxidative damage to DNA and protein by forming a redox-inactive ergothioneine–copper complex. Chem Res Toxicol 24, 30–34.

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    Gokce G & Arun MZ (2014 ) Ergothioneine produces relaxation in isolated rat aorta by inactivating superoxide anion. Eur Rev Med Pharmacol Sci 18, 3339–3345.

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  475. 475.

    Pahila J, Ishikawa Y & Ohshima T (2019 ) Effects of ergothioneine-rich mushroom extract on the oxidative stability of astaxanthin in liposomes. J Agric Food Chem 67, 3491–3501.

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    Cheah IK, Tang R, Ye P, et al. (2016 ) Liver ergothioneine accumulation in a guinea pig model of non-alcoholic fatty liver disease. A possible mechanism of defence? Free Radic Res 50, 14–25.

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    Sansbury BE, DeMartino AM, Xie Z, et al. (2014 ) Metabolomic analysis of pressure-overloaded and infarcted mouse hearts. Circ Heart Fail 7, 634–642.

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    Agudo-Barriuso M, Lahoz A, Nadal-Nicolás FM, et al. (2013 ) Metabolomic changes in the rat retina after optic nerve crush. Invest Ophthalmol Vis Sci 54, 4249–4259.

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    Colognato R, Laurenza I, Fontana I, et al. (2006 ) Modulation of hydrogen peroxide-induced DNA damage, MAPKs activation and cell death in PC12 by ergothioneine. Clin Nutr 25, 135–145.

    Not in our library10.1016/j.clnu.2005.10.005

  480. 480.

    Song TY, Chen CL, Liao JW, et al. (2010 ) Ergothioneine protects against neuronal injury induced by cisplatin both in vitro and in vivo. Food Chem Toxicol 48, 3492–3499.

    Not in our library10.1016/j.fct.2010.09.030

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    Nishida K, Takeuchi K, Hosoda A, et al. (2018 ) Ergothioneine ameliorates oxaliplatin-induced peripheral neuropathy in rats. Life Sci 207, 516–524.

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    D’Onofrio N, Servillo L, Giovane A, et al. (2016 ) Ergothioneine oxidation in the protection against high-glucose induced endothelial senescence: involvement of SIRT1 and SIRT6. Free Radic Biol Med 96, 211–222.

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    Gunawardena D, Bennett L, Shanmugam K, et al. (2014 ) Anti-inflammatory effects of five commercially available mushroom species determined in lipopolysaccharide and interferon-γ activated murine macrophages. Food Chem 148, 92–96.

    Not in our library10.1016/j.foodchem.2013.10.015

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    Sakrak O, Kerem M, Bedirli A, et al. (2008 ) Ergothioneine modulates proinflammatory cytokines and heat shock protein 70 in mesenteric ischemia and reperfusion injury. J Surg Res 144, 36–42.

    Not in our library10.1016/j.jss.2007.04.020

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    Bedirli A, Sakrak O, Muhtaroglu S, et al. (2004 ) Ergothioneine pretreatment protects the liver from ischemia–reperfusion injury caused by increasing hepatic heat shock protein 70. J Surg Res 122, 96–102.

    Not in our library10.1016/j.jss.2004.06.016

  486. 486.

    Arduini A, Eddy L & Hochstein P (1990 ) The reduction of ferryl myoglobin by ergothioneine: a novel function for ergothioneine. Arch Biochem Biophys 281, 41–43.

    Not in our library10.1016/0003-9861(90)90410-z

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    Zimring JC, Smith N, Stowell SR, et al. (2014 ) Strain-specific red blood cell storage, metabolism, and eicosanoid generation in a mouse model. Transfusion 54, 137–148.

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    Kell DB & Pretorius E (2015 ) On the translocation of bacteria and their lipopolysaccharides between blood and peripheral locations in chronic, inflammatory diseases: the central roles of LPS and LPS-induced cell death. Integr Biol 7, 1339–1377.

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    Goodman M, Bostick RM, Kucuk O, et al. (2011 ) Clinical trials of antioxidants as cancer prevention agents: past, present, and future. Free Radic Biol Med 51, 1068–1084.

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    Oldham KM & Bowen PE (1998 ) Oxidative stress in critical care: is antioxidant supplementation beneficial? J Am Diet Assoc 98, 1001–1008.

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    Cuzzocrea S, Riley DP, Caputi AP, et al. (2001 ) Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol Rev 53, 135–159.

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    Miller ER 3rd, Pastor-Barriuso R, Dalal D, et al. (2005 ) Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 142, 37–46.

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    Vaziri ND & Rodriguez-Iturbe B (2006 ) Mechanisms of disease: oxidative stress and inflammation in the pathogenesis of hypertension. Nat Clin Pract Nephrol 2, 582–593.

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    Rodrigo R, Guichard C & Charles R (2007 ) Clinical pharmacology and therapeutic use of antioxidant vitamins. Fund Clin Pharmacol 21, 111–127.

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    Bjelakovic G, Nikolova D, Gluud LL, et al. (2007 ) Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 297, 842–857.

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    Bjelakovic G, Nikolova D, Gluud LL, et al. (2008 ) Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases. Cochrane Database Syst Rev, issue 2, CD007176.

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    Mendes-da-Silva RF, Lopes-de-Morais AA, Bandim-da-Silva ME, et al. (2014 ) Prooxidant versus antioxidant brain action of ascorbic acid in well-nourished and malnourished rats as a function of dose: a cortical spreading depression and malondialdehyde analysis. Neuropharmacology 86, 155–160.

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    Zhang P & Omaye ST (2001 ) Antioxidant and prooxidant roles for β-carotene, α-tocopherol and ascorbic acid in human lung cells. Toxicol In Vitro 15, 13–24.

    Not in our library10.1016/s0887-2333(00)00054-0

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    Ullah MF, Khan HY, Zubair H, et al. (2011 ) The antioxidant ascorbic acid mobilizes nuclear copper leading to a prooxidant breakage of cellular DNA: implications for chemotherapeutic action against cancer. Cancer Chemother Pharmacol 67, 103–110.

    Not in our library10.1007/s00280-010-1290-4

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    Repine JE & Elkins ND (2012 ) Effect of ergothioneine on acute lung injury and inflammation in cytokine insufflated rats. Prev Med 54, Suppl., S79–S82.

    Not in our library10.1016/j.ypmed.2011.12.006

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    Martin KR (2010 ) The bioactive agent ergothioneine, a key component of dietary mushrooms, inhibits monocyte binding to endothelial cells characteristic of early cardiovascular disease. J Med Food 13, 1340–1346.

    Not in our library10.1089/jmf.2009.0194

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    Servillo L, D’Onofrio N & Balestrieri ML (2017 ) Ergothioneine antioxidant function: from chemistry to cardiovascular therapeutic potential. J Cardiovasc Pharmacol 69, 183–191.

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    Darghouth D, Koehl B, Heilier JF, et al. (2011 ) Alterations of red blood cell metabolome in overhydrated hereditary stomatocytosis. Haematologica 96, 1861–1865.

    Not in our library10.3324/haematol.2011.045179

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    Smith E, Ottosson F, Hellstrand S, et al. (2019 ) Ergothioneine is associated with reduced mortality and decreased risk of cardiovascular disease. Heart 2019, heartjnl-2019-315485 (epublication ahead of print version 31 October 2019).

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    Nurk E, Refsum H, Drevon CA, et al. (2010 ) Cognitive performance among the elderly in relation to the intake of plant foods. The Hordaland Health Study. Br J Nutr 104, 1190–1201.

    Not in our library10.1017/s0007114510001807

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    Zhang S, Tomata Y, Sugiyama K, et al. (2017 ) Mushroom consumption and incident dementia in elderly Japanese: the Ohsaki Cohort 2006 Study. J Am Geriatr Soc 65, 1462–1469.

    Not in our library10.1111/jgs.14812

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    Phan CW, David P & Sabaratnam V (2017 ) Edible and medicinal mushrooms: emerging brain food for the mitigation of neurodegenerative diseases. J Med Food 20, 1–10.

    Not in our library10.1089/jmf.2016.3740

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    Thangthaeng N, Miller MG, Gomes SM, et al. (2015 ) Daily supplementation with mushroom (Agaricus bisporus) improves balance and working memory in aged rats. Nutr Res 35, 1079–1084.

    Not in our library10.1016/j.nutres.2015.09.012

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    Tsuk S, Lev YH, Rotstein A, et al. (2017 ) Clinical effects of a commercial supplement of Ophiocordyceps sinensis and Ganoderma lucidum on cognitive function of healthy young volunteers. Int J Med Mushrooms 19, 667–673.

    Not in our library10.1615/intjmedmushrooms.2017021202

  515. 515.

    Hatano T, Saiki S, Okuzumi A, et al. (2016 ) Identification of novel biomarkers for Parkinson’s disease by metabolomic technologies. J Neurol Neurosurg Psychiatry 87, 295–301.

    Not in our library10.1136/jnnp-2014-309676

  516. 516.

    Hang L, Basil AH & Lim KL (2016 ) Nutraceuticals in Parkinson’s disease. Neuromolecular Med 18, 306–321.

    Not in our library10.1007/s12017-016-8398-6

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    Recent advances and perspectives of metabolomics-based investigations in Parkinson’s disease · 2019
    No notice
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    Shah SP & Duda JE (2015 ) Dietary modifications in Parkinson’s disease: a neuroprotective intervention? Med Hypotheses 85, 1002–1005.

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    Graham SF, Chevallier OP, Kumar P, et al. (2017 ) Metabolomic profiling of brain from infants who died from sudden infant death syndrome reveals novel predictive biomarkers. J Perinatol 37, 91–97.

    Not in our library10.1038/jp.2016.139

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    Yang NC, Lin HC, Wu JH, et al. (2012 ) Ergothioneine protects against neuronal injury induced by β-amyloid in mice. Food Chem Toxicol 50, 3902–3911.

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    Cheah IK, Ng LT, Ng LF, et al. (2019 ) Inhibition of amyloid-induced toxicity by ergothioneine in a transgenic Caenorhabditis elegans model. FEBS Lett 593, 2139–2150.

    Not in our library10.1002/1873-3468.13497

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    Nakamichi N, Nakayama K, Ishimoto T, et al. (2016 ) Food-derived hydrophilic antioxidant ergothioneine is distributed to the brain and exerts antidepressant effect in mice. Brain Behav 6, e00477.

    Not in our library10.1002/brb3.477

  523. 523.

    Logan AS, Nienaber U & Pan XS (editors) (2013 ) Lipid Oxidation: Challenges in Food Systems. Urbana, IL: AOCS Press.

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    Gray JI, Gomaa EA & Buckley DJ (1996 ) Oxidative quality and shelf life of meats. Meat Sci 43, S111–S123.

    Not in our library10.1016/0309-1740(96)00059-9

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    Gülçin I (2012 ) Antioxidant activity of food constituents: an overview. Arch Toxicol 86, 345–391.

    Not in our library10.1007/s00204-011-0774-2

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    Perron NR & Brumaghim JL (2009 ) A review of the antioxidant mechanisms of polyphenol compounds related to iron binding. Cell Biochem Biophys 53, 75–100.

    Not in our library10.1007/s12013-009-9043-x

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    Hanlon DP (1971 ) Interaction of ergothioneine with metal ions and metalloenzymes. J Med Chem 14, 1084–1087.

    Not in our library10.1021/jm00293a017

  528. 528.

    Encarnacion AB, Fagutao F, Hirono I, et al. (2010 ) Effects of ergothioneine from mushrooms (Flammulina velutipes) on melanosis and lipid oxidation of kuruma shrimp (Marsupenaeus japonicus). J Agric Food Chem 58, 2577–2585.

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    Encarnacion AB, Fagutao F, Hirayama J, et al. (2011 ) Edible mushroom (Flammulina velutipes) extract inhibits melanosis in Kuruma shrimp (Marsupenaeus japonicus). J Food Sci 76, C52–C58.

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  530. 530.

    Bao HND, Ushio H & Ohshima T (2009 ) Antioxidative activities of mushroom (Flammulina velutipes) extract added to bigeye tuna meat: dose-dependent efficacy and comparison with other biological antioxidants. J Food Sci 74, C162–C169.

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    Encarnacion AB, Fagutao F, Jintasataporn O, et al. (2012 ) Application of ergothioneine-rich extract from an edible mushroom Flammulina velutipes for melanosis prevention in shrimp, Penaeus monodon and Litopenaeus vannamei. Food Res Int 45, 232–237.

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    Cai LY, Li XP, Wu XS, et al. (2014 ) Effect of chitosan coating enriched with ergothioneine on quality changes of Japanese sea bass (Lateolabrax japonicas). Food Bioproc Technol 7, 2281–2290.

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    Pahila J, Kaneda H, Nagasaka R, et al. (2017 ) Effects of ergothioneine-rich mushroom extracts on lipid oxidation and discoloration in salmon muscle stored at low temperatures. Food Chem 233, 273–281.

    Not in our library10.1016/j.foodchem.2017.04.130

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    Bao HND, Ushio H & Ohshima T (2008 ) Antioxidative activity and antidiscoloration efficacy of ergothioneine in mushroom (Flammulina velutipes) extract added to beef and fish meats. J Agric Food Chem 56, 10032–10040.

    Not in our library10.1021/jf8017063

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    Bao HND, Osako K & Ohshima T (2010 ) Value-added use of mushroom ergothioneine as a colour stabilizer in processed fish meats. J Sci Food Agric 90, 1634–1641.

    Not in our library10.1002/jsfa.3992

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    Muszyńska B & Sułkowska-Ziaja K (2015 ) Impact of food processing on non-hallucinogenic indole derivatives in edible mushrooms In Processing and Impact on Active Components in Food, pp. 55–62 [ V Preedy, editor]. San Diego, CA: Academic Press.

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    Cremades O, Diaz-Herrero MM, Carbonero-Aguilar P, et al. (2015 ) White button mushroom ergothione in eaqueous extracts obtained by the application of enzymes and membrane technology. Food Biosci 10, 42–47.

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    Sánchez C (2017 ) Reactive oxygen species and antioxidant properties from mushrooms. Synth Syst Biotechnol 2, 13–22.

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    Duy Bao HN & Ohshima T (2013 ) Strategies to minimize oxidative deterioration in aquatic food products: application of natural antioxidants from edible mushrooms In Lipid Oxidation, pp. 345–380 [ U Nienaber and X Pan, editors]. Urbana, IL: AOCS Press.

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    Lee CM (2016 ) Fifty years of research and development of cosmeceuticals: a contemporary review. J Cosmet Dermatol 15, 527–539.

    Not in our library10.1111/jocd.12261

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    Epstein H (2009 ) Cosmeceuticals and polyphenols. Clin Dermatol 27, 475–478.

    Not in our library10.1016/j.clindermatol.2009.05.011

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    Taofiq O, González-Paramás AM, Martins A, et al. (2016 ) Mushrooms extracts and compounds in cosmetics, cosmeceuticals and nutricosmetics – a review. Industrial Crops Products 90, 38–48.

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    Linder J (2012 ) Cosmeceutical treatment of the aging face In Aesthetic Medicine, pp. 69–84 [ PM Prendergast and MA Shiffman, editors]. Berlin: Springer.

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    Cronin H, Draelos ZD (2010 ) Top 10 botanical ingredients in 2010 anti-aging creams. J Cosmet Dermatol 9, 218–225.

    Not in our library10.1111/j.1473-2165.2010.00516.x

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    Souyoul SA, Saussy KP & Lupo MP (2018 ) Nutraceuticals: a review. Dermatol Ther (Heidelb) 8, 5–16.

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    Norins AL (1962 ) Free radical formation in the skin following exposure to ultraviolet light. J Invest Dermatol 39, 445–448.

    Not in our library10.1038/jid.1962.137

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    Hseu YC, Lo HW, Korivi M, et al. (2015 ) Dermato-protective properties of ergothioneine through induction of Nrf2/ARE-mediated antioxidant genes in UVA-irradiated human keratinocytes. Free Radic Biol Med 86, 102–117.

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  550. 550.

    Botta C, Di Giorgio C, Sabatier AS, et al. (2008 ) Genotoxicity of visible light (400–800 nm) and photoprotection assessment of ectoin, l-ergothioneine and mannitol and four sunscreens. J Photochem Photobiol B 91, 24–34.

    Not in our library10.1016/j.jphotobiol.2008.01.008

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    Bazela K, Solyga-Zurek A, Debowska R, et al. (2014 ) l-Ergothioneine protects skin cells against UV-induced damage – a preliminary study. Cosmetics 1, 51–60.

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    Sao Emani C, Williams MJ, Van Helden PD, et al. (2018 ) γ-Glutamylcysteine protects ergothioneine-deficient Mycobacterium tuberculosis mutants against oxidative and nitrosative stress. Biochem Biophys Res Commun 495, 174–178.

    Not in our library10.1016/j.bbrc.2017.10.163

  553. 553.

    Sao Emani C, Williams MJ, Van Helden PD, et al. (2018 ) Generation and characterization of thiol-deficient Mycobacterium tuberculosis mutants. Sci Data 5, 180184.

    Not in our library10.1038/sdata.2018.184

  554. 554.

    Jothivasan VK & Hamilton CJ (2008 ) Mycothiol: synthesis, biosynthesis and biological functions of the major low molecular weight thiol in actinomycetes. Nat Prod Rep 25, 1091–1117.

    Not in our library10.1039/b616489g

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    Feng J, Che Y, Milse J, et al. (2006 ) The gene ncgl2918 encodes a novel maleylpyruvate isomerase that needs mycothiol as cofactor and links mycothiol biosynthesis and gentisate assimilation in Corynebacterium glutamicum. J Biol Chem 281, 10778–10785.

    Not in our library10.1074/jbc.m513192200

  556. 556.

    Newton GL, Buchmeier N & Fahey RC (2008 ) Biosynthesis and functions of mycothiol, the unique protective thiol of Actinobacteria. Microbiol Mol Biol Rev 72, 471–494.

    Not in our library10.1128/mmbr.00008-08

  557. 557.

    Bzymek KP, Newton GL, Ta P, et al. (2007 ) Mycothiol import by Mycobacterium smegmatis and function as a resource for metabolic precursors and energy production. J Bacteriol 189, 6796–6805.

    Not in our library10.1128/jb.00644-07

  558. 558.

    Brummel MC (1985 ) In search of a physiological function for l-ergothioneine. Med Hypotheses 18, 351–370.

    Not in our library10.1016/0306-9877(85)90103-3

  559. 559.

    Brummel MC (1989 ) In search of a physiological function for l-ergothioneine – II. Med Hypotheses 30, 39–48.

    Not in our library10.1016/0306-9877(89)90123-0

  560. 560.

    Wang M, Zhao Q & Liu W (2015 ) The versatile low-molecular-weight thiols: beyond cell protection. Bioessays 37, 1262–1267.

    Not in our library10.1002/bies.201500067

  561. 561.

    Zhao Q, Wang M, Xu D, et al. (2015 ) Metabolic coupling of two small-molecule thiols programs the biosynthesis of lincomycin A. Nature 518, 115–119.

    Not in our library10.1038/nature14137

  562. 562.

    Goldberg A (1959 ) The enzymic formation of haem by the incorporation of iron into protoporphyrin; importance of ascorbic acid, ergothioneine and glutathione. Br J Haematol 5, 150–157.

    Not in our library10.1111/j.1365-2141.1959.tb04020.x

  563. 563.

    Anonymous (2019 ) Clinical trials with mushrooms. https://clinicaltrials.gov/ct2/results?cond=&term=mushrooms&cntry=&state=&city=&dist= (accessed January 2020).

    Not in our library

  564. 564.

    Cheah IK (2018 ) Investigating the efficacy of ergothioneine to delay cognitive decline. https://clinicaltrials.gov/ct2/show/NCT03641404 (accessed August 2019).

    Not in our library10.1177/13872877241291253

  565. 565.

    Gamage AM, Liao C, Cheah IK, et al. (2018 ) The proteobacterial species Burkholderia pseudomallei produces ergothioneine, which enhances virulence in mammalian infection. FASEB J 2018, fj201800716.

    Not in our library10.1096/fj.201800716

  566. 566.

    Heath H & Wildy J (1956 ) Biosynthesis of ergothioneine and histidine by claviceps-purpurea. 1. Incorporation of [2-14C]acetate. Biochem J 64, 612–620.

    Not in our library10.1042/bj0640612

  567. 567.

    Heath H & Wildy J (1957 ) Biosynthesis of ergothioneine. Nature 179, 196–197.

    Not in our library10.1038/179196a0

  568. 568.

    Pan L, Yu J, Ren D, et al. (2019 ) Metabolomic analysis of significant changes in Lactobacillus casei Zhang during culturing to generation 4,000 under conditions of glucose restriction. J Dairy Sci 102, 3851–3867)

    Not in our library10.3168/jds.2018-15702

  569. 569.

    Pluskal T, Nakamura T, Villar-Briones A, et al. (2010 ) Metabolic profiling of the fission yeast S. pombe: quantification of compounds under different temperatures and genetic perturbation. Mol Biosyst 6, 182–198.

    Not in our library10.1039/b908784b

  570. 570.

    van der Hoek SA, Darbani B, Zugaj K, et al. (2019 ) Engineering the yeast Saccharomyces cerevisiae for the production of l-(+)-ergothioneine. bioRxiv, 2019, 667592.

    Not in our library10.3389/fbioe.2019.00262

  571. 571.

    Sotgia S, Zinellu A, Mangoni AA, et al. (2014 ) Clinical and biochemical correlates of serum l-ergothioneine concentrations in community-dwelling middle-aged and older adults. PLOS ONE 9, e84918.

    Not in our library10.1371/journal.pone.0084918

  572. 572.

    Nishigori H, Hayashi R, Lee JW, et al. (1984 ) Effect of MPG on glucocorticoid-induced cataract formation in developing chick embryo. Invest Ophthalmol Vis Sci 25, 1051–1055.

    Not in our library

  573. 573.

    Song TY, Yang NC, Chen CL, et al. (2017 ) Protective effects and possible mechanisms of ergothioneine and hispidin against methylglyoxal-induced injuries in rat pheochromocytoma cells. Oxid Med Cell Longev 2017, 4824371.

    Not in our library10.1155/2017/4824371

  574. 574.

    Guijarro MV, Indart A, Aruoma OI, et al. (2002 ) Effects of ergothioneine on diabetic embryopathy in pregnant rats. Food Chem Toxicol 40, 1751–1755.

    Not in our library10.1016/s0278-6915(02)00177-1

  575. 575.

    Öztürkler Y, Yildiz S, Güngör O, et al. (2010 ) The effects of l-ergothioneine and l-ascorbic acid on the in vitro maturation (IVM) and embryonic development (IVC) of sheep oocytes. Kafkas Universitesi Veteriner Fakultesi Dergisi 16, 757–763.

    Not in our library

  576. 576.

    Zullo G, Albero G, Neglia G, et al. (2016 ) l-Ergothioneine supplementation during culture improves quality of bovine in vitro-produced embryos. Theriogenology 85, 688–697.

    Not in our library10.1016/j.theriogenology.2015.10.008

  577. 577.

    Moncaster JA, Walsh DT, Gentleman SM, et al. (2002 ) Ergothioneine treatment protects neurons against N-methyl-d-aspartate excitotoxicity in an in vivo rat retinal model. Neurosci Lett 328, 55–59.

    Not in our library10.1016/s0304-3940(02)00427-5

  578. 578.

    Kawano H, Higuchi F, Mayumi T, et al. (1982 ) Studies on ergothioneine. VII. Some effects on ergothioneine on glycolytic metabolism in red blood cells from rats. Chem Pharm Bull (Tokyo) 30, 2611–2613.

    Not in our library10.1248/cpb.30.2611

  579. 579.

    Kimura C, Nukina M, Igarashi K, et al. (2005 ) β-Hydroxyergothioneine, a new ergothioneine derivative from the mushroom Lyophyllum connatum, and its protective activity against carbon tetrachloride-induced injury in primary culture hepatocytes. Biosci Biotechnol Biochem 69, 357–363.

    Not in our library10.1271/bbb.69.357

  580. 580.

    Yoshida S, Shime H, Funami K, et al. (2017 ) The anti-oxidant ergothioneine augments the immunomodulatory function of TLR agonists by direct action on macrophages. PLOS ONE 12, e0169360.

    Not in our library10.1371/journal.pone.0169360

  581. 581.

    Yoshida S, Shime H, Matsumoto M, et al. (2019 ) Anti-oxidative amino acid l-ergothioneine modulates the tumor microenvironment to facilitate adjuvant vaccine immunotherapy. Front Immunol 10, 671.

    Not in our library10.3389/fimmu.2019.00671

  582. 582.

    Shinozaki Y, Furuichi K, Toyama T, et al. (2017 ) Impairment of the carnitine/organic cation transporter l-ergothioneine axis is mediated by intestinal transporter dysfunction in chronic kidney disease. Kidney Int 92, 1356–1369.

    Not in our library10.1016/j.kint.2017.04.032

  583. 583.

    Menna P, Salvatorelli E, Giampietro R, et al. (2002 ) Doxorubicin-dependent reduction of ferrylmyoglobin and inhibition of lipid peroxidation: implications for cardiotoxicity of anticancer anthracyclines. Chem Res Toxicol 15, 1179–1189.

    Not in our library10.1021/tx020055+

  584. 584.

    Song TY, Lin HC, Chen CL, et al. (2014 ) Ergothioneine and melatonin attenuate oxidative stress and protect against learning and memory deficits in C57BL/6J mice treated with d-galactose. Free Radic Res 48, 1049–1060.

    Not in our library10.3109/10715762.2014.920954

  585. 585.

    Motohashi N, Mori I, Sugiura Y, et al. (1974 ) Metal complexes of ergothioneine. Chem Pharmaceut Bull 22, 654–657.

    Not in our library

  586. 586.

    Motohashi N, Mori I & Sugiura Y (1976 ) Complexing of copper-ion by ergothioneine. Chem Pharmaceut Bull 24, 2364–2368.

    Not in our library10.1248/cpb.24.2364

  587. 587.

    Rabenstein DL & Isab AA (1982 ) A proton nuclear magnetic resonance study of the interaction of mercury with intact human erythrocytes. Biochim Biophys Acta 721, 374–384.

    Not in our library10.1016/0167-4889(82)90092-1

  588. 588.

    Hartman PE & Citardi MJ (1986 ) Protection afforded by carnosine and by ergothioneine against bacteriophage-P22 inactivation by gamma-irradiation. Environ Mol Mutagen 8, 35–35.

    Not in our library

  589. 589.

    Hartman Z, Hartman PE & Owens RA (1986 ) Ergothioneine (2-thiol-l-histidine betaine = Et) as an antimutagen – interception of direct-acting mutagens formed from nitrosation of spermidine. Environ Mol Mutagen 8, 36–36.

    Not in our library

  590. 590.

    Hartman Z & Hartman PE (1987 ) Interception of some direct-acting mutagens by ergothioneine. Environ Mol Mutagen 10, 3–15.

    Not in our library10.1002/em.2850100103

  591. 591.

    Hartman PE, Hartman Z & Citardi MJ (1988 ) Ergothioneine, histidine, and two naturally occurring histidine dipeptides as radioprotectors against γ-irradiation inactivation of bacteriophages T4 and P22. Radiat Res 114, 319–330.

    Not in our library

  592. 592.

    Ishimoto T, Nakamichi N, Hosotani H, et al. (2014 ) Organic cation transporter-mediated ergothioneine uptake in mouse neural progenitor cells suppresses proliferation and promotes differentiation into neurons. PLOS ONE 9, e89434.

    Not in our library10.1371/journal.pone.0089434

  593. 593.

    Misiti F, Castagnola M, Zuppi C, et al. (2001 ) Role of ergothioneine on S-nitrosoglutathione catabolism. Biochem J 356, 799–804.

    Not in our library10.1042/0264-6021:3560799

  594. 594.

    Ishimoto T, Masuo Y, Kato Y, et al. (2019 ) Ergothioneine-induced neuronal differentiation is mediated through activation of S6K1 and neurotrophin 4/5-TrkB signaling in murine neural stem cells. Cell Signal 53, 269–280.

    Not in our library10.1016/j.cellsig.2018.10.012

  595. 595.

    Chaves NA, Alegria TGP, Dantas LS, et al. (2019 ) Impaired antioxidant capacity causes a disruption of metabolic homeostasis in sickle erythrocytes. Free Radic Biol Med 141, 34–46.

    Not in our library10.1016/j.freeradbiomed.2019.05.034

  596. 596.

    Mann T & Leone E (1953 ) Studies on the metabolism of semen. 8. Ergothioneine as a normal constituent of boar seminal plasma. Purification and crystallization. Site of formation and function. Biochem J 53, 140–148.

    Not in our library10.1042/bj0530140

  597. 597.

    Williamson RD, McCarthy FP, Manna S, et al. (2020 ) l-(+)-Ergothioneine significantly improves the clinical characteristics of preeclampsia in the reduced uterine perfusion pressure rat model. Hypertension 75, 561–568.

    Not in our library10.1161/hypertensionaha.119.13929

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