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Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease

Rebeca Martín, Sylvie Miquel, Jonathan Ulmer and 3 more

Microbial Cell Factories · 2013 · Review

doi:10.1186/1475-2859-12-71

Abstract

The human gut is one of the most complex ecosystems, composed of 10 13 -10 14 microorganisms which play an important role in human health. In addition, some food products contain live bacteria which transit through our gastrointestinal tract and could exert beneficial effects on our health (known as probiotic effect). Among the numerous proposed health benefits attributed to commensal and probiotic bacteria, their capacity to interact with the host immune system is now well demonstrated. Currently, the use of recombinant lactic acid bacteria to deliver compounds of health interest is gaining importance as an extension of the probiotic concept. This review summarizes some of the recent findings and perspectives in the study of the crosstalk of both commensal and probiotic bacteria with the human host as well as the latest studies in recombinant commensal and probiotic bacteria. Our aim is to highlight the potential roles of recombinant bacteria in this ecosystem.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.

Relationship humans-bacteria: a history of common benefits

The human gastrointestinal tract (GIT) is one of the most complex ecosystems known. Its microbiota consists of a large number of bacteria (10-fold more than the total number of human cells) that shapes many important physiological and metabolic processes as well as the development of the immune system. The advances of molecular techniques have shown that the collective adult human GIT microbiota is composed of up to 1000–1150 bacterial species. The most frequently found species are Gram-positive bacteria. The predominant species (46-58%) are those with low GC-content and the Clostridium group is the most abundant in this complex ecosystem. Physiological conditions differ widely in the human GIT leading to an individual gut microbiota. Some studies suggest that the faecal microbiota does not necessarily represent the bacteria inside the GIT. Additionally, the intestinal lumen microbiota differs significantly from the one in the mucus layer and near the epithelium due to the poor accessibility of the crypts covered by mucins.

Despite its complexity, the faecal microbiota of adult human individuals is unique and highly stable through time. Primocolonizing microorganisms appear in the gut immediately after birth in an organized and lifelong process. During the first year, after the initial establishment of the intestinal microbiota, its composition is relatively simple and varies between individuals. After that, the main dominant groups of the adult microbiota will be conserved between all individuals. These groups are stable in spite of the great number of factors that can affect them. In contrast, at the phylum level, the variation is higher between individuals although people who are related tend to have similar microbiota perhaps due to a shared environment and genetic similarities.

This microecosystem, which is a direct consequence of the mutualism between the host and its microbiota, is fundamental for the maintenance of the homeostasis of a healthy individual. Commensal bacteria provide the host with essential nutrients. They metabolize indigestible compounds, defend against colonization of opportunistic pathogens and contribute to the development of the intestinal architecture as well as stimulation of the immune system among others. Conversely, the host provides the bacteria with nutrients and a stable environment (Figure 1). Both host and indigenous microorganisms have then adapted to each other in a particular case of microevolution to maintain the benefits that this mutualism confers.

Probiotics: an additional bacterial advantage for humans

Probiotics are defined as “live microorganisms which when administered in adequate amounts confer a health benefit on the host”. This concept is based on the observations made by Élie Metchnikoff in 1907 in which the regular consumption of Lactic Acid Bacteria (LAB) in fermented dairy products, such as yogurt, was associated with enhanced health and longevity in many people living in Bulgarian villages.

Most probiotics belong to LAB, but new species and genera are being assessed for future use. Some other well-known probiotics are Bifidobacterium sp., one strain of the Gram-negative bacterium Escherichia coli Nissle 1917 and the yeast Saccharomyces boulardii.

However, not all microorganisms are beneficial and screenings in order to identify novel candidate probiotics with immunomodulatory properties are frequently performed. In fact, a Dutch trial using a probiotic preparation in patients with acute pancreatitis showed to be harmful. These negative results show how important it is to choose the right protocol (indeed, the main problem with this study was the bad idea to administer massive quantitites of probiotics in very vulnerable patients) and to make a careful selection when using probiotics in humans. Certainly, a supposed beneficial effect of a specific strain cannot be extrapolated to another strain even within to the same species.

Modulation of host immunity and promotion of host defense are the most commonly supported benefits of the consumption of probiotics. For a microorganism to be considered probiotic (i.e. bacteria or yeast), the following criteria need to be fulfilled: i) it should have a clear beneficial effect on the host, ii) it should be non-pathogenic, iii) it should be able to survive transit through the GIT and iv) a large number of viable bacteria must be able to survive prolonged periods (i.e. upon storage).

What happens if homeostasis is broken?

The term dysbiosis refers to microbial imbalances on or within the body. When homeostasis (balanced microbial ecosystem) is broken, different subdominant opportunistic bacteria can grow leading to a situation of illness. Additionally, when commensal bacteria are depleted, an abnormal health situation can be triggered due to a lack of the benefits these bacteria provide rather than the overgrowth of pathobionts.

a) Binomial dysbiosis – illness

The term dysbiosis has been related to many different kinds of pathologies although it is not clear whether the imbalance of microbiota is a cause or a consequence of the illness. The clearest correlation between dysbiosis and disease has been found with inflammatory bowel diseases (IBD) where the proportion of Firmicutes, in particular Faecalibacterium prausnitzii, was found to be low in patients that exhibited endoscopic recurrence 6 months after surgery. IBD, including Crohn’s disease (CD) and ulcerative colitis (UC), are characterized by an abnormal activation of the immune system associated with the gut, resulting in a chronic inflammation of the digestive system. However, some other factors also seem to be involved in IBD such as genetic components, immunological disorders, environmental factors, pathogens, and microbiota. Faecal analyses have shown a quantitative and qualitative reduction in the representation of the Firmicutes phylum, mostly the clostridial cluster IV members in CD patients while low numbers of total lactobacilli have been reported in UC members, although no correlation was found between F. prausnitzii abundance and the severity of CD.

Even if the composition of the human microbiota is different in each individual, changes in phylogenic distribution have also been specifically found in obese and diabetic individuals versus normal ones (Table 1). The importance of the human microbiota has been demonstrated in the hygiene hypothesis, defined in 1989 by Strachan who postulated that low exposure to infectious agents in early life explains the increased numbers of people suffering from allergies and asthma in developed countries. This hypothesis suggests that a well-balanced human microbiota is a factor that protects from such pathologies.

Some microbial activities have shown relevance to health and disease. Following this line of thought, the production of short chain fatty acids (SCFA) such as butyrate has been proposed to protect against different illnesses (Table 2).

b) Probiotics to restore dysbiosis

As we have seen before, dysbiosis are involved in a great variety of different illnesses. Considering this fact, the administration of beneficial microorganisms to restore the normal ecosystem is a strategy to improve the health status of the patient and/or to prevent a normal healthy individual from acquiring dysbiosis in the future. Currently, there is evidence of the use of probiotics as therapeutics against traveler’s diarrhea, irritable bowel syndrome (IBS), IBD, lactose intolerance, peptic ulcers, allergy and autoimmune disorders among others. For instance, it has been suggested that colonization of the GIT with Bifidobacteria properly shapes gut microbiota, induces oral tolerance and decreases the frequency of allergic disorders. For lactobacilli, a clinical study demonstrates that perinatal administration of a probiotic strain of Lactobacillus rhamnosus GG (LGG) reduces the development of atopic eczema in children. This effect may be due to the anti-inflammatory properties of this probiotic bacterium. Consumption of LGG by children with atopic dermatitis has been reported to enhance the production of the anti-inflammatory cytokine IL-10. Other studies have demonstrated that oral administration of L. casei Shirota strain to mice inhibited specific IgE production while Abrahamsson et al. have observed in a double-blind, randomized, placebo-controlled trial that infants treated with L. reuteri ATCC 55730 strain had less IgE-associated eczema.

As mentioned above, when the equilibrium of the microbiota is disturbed, the bacterial ecosystem is thought to contribute to several intestinal diseases such as IBD. In fact, gut microbiota metabolize nutrients, produce vitamins and degrade toxic products (such as: carcinogens, food additives, bile salts, and cholesterol, among others), where the importance and interest in modulate microbiota with probiotic products. Results from animal models and human clinical trials have confirmed various therapeutic effects of selected strains of probiotics in IBD. For instance, L. casei BL23 strain has shown anti-inflammatory effects in a murine DSS-induced colitis model and some other probiotic strains (eg. VSL#3, LGG, BIFICO, E. coli Nissle) have shown effects in human patients with pouchitis, UC and CD. Additionally, the modulatory effect of Lactobacillus acidophilus in intestinal pain due to the induction of opioid and cannabinoid receptors has been reported in rats. This fact highlights the use of probiotics in other intestinal disorders such as such as IBS, characterized by chronic abdominal pain, discomfort, bloating and alteration of bowel habits. In this sense, in the last years, many studies confirm the overall positive results of probiotics in human IBS patients using different bacteria such as: Lactobacillus spp., Bifidobacterium and Streptococcus among others.

From this perspective, the use of probiotics has been expanded in the last few years, with a great number of probiotic products in our supermarkets and pharmacies. However, the knowledge of their mechanisms of action remains largely unknown.

New prospects of commensal and probiotic bacteria: genetically modified microorganisms

a) Strategies to deliver therapeutic molecules.

Since probiotic therapy is mainly focused on restoring the normal balance of the intestinal ecosystem, we can deduce that the use of commensal bacteria as probiotics is the natural way to get rid of dysbiosis within the GIT. Furthermore, they represent potential live delivery vectors for target compounds (Figure 2). The use of live delivery vectors, such as food-grade LAB, at the mucosal level has been widely described before. They are based on the use of recombinant bacteria producing the heterologous molecule of interest in vivo and their use is mainly related to vaccines. This is due to the fact that genetically engineered bacteria or viruses (used as carriers) producing heterologous antigens can increase the immunogenicity of otherwise weakly immunogenic antigens. In addition, such live bacterial vectors have the additional advantage (compared to viruses) of having a genome able to harbor many heterologous genes, in contrast to viruses where the capacity to encapsulate foreign DNA is limited. This research field comes from exploring novel effective strategies to deliver therapeutic molecules to the mucosal tissues in order to avoid degradation and promote uptake of the antigen in situ (ie. in the GIT), and stimulate adaptive immune responses rather than the tolerogenic immune responses that are observed in feeding studies with soluble antigens. Besides the enhancement of the potency and specificity of mucosal delivery of therapeutic molecules, the use of mucosal routes reduces potential side effects observed in systemic ones.

In principle, two types of bacterial vectors can be used to deliver compounds at the mucosal level: attenuated pathogens and non-pathogenic bacteria. Gram-positive commensal or food-grade bacteria constitute attractive good alternatives to pathogenic bacteria. Particularly, the food-grade LAB are attractive candidates because they have been used for centuries in the fermentation and preservation of food, and are considered to be safe organisms with a GRAS (Generally Recognized As Safe) status. One major advantage of LAB as delivery vectors for vaccines purposes is their potential to elicit both antigen-specific immune responses at mucosal surfaces and effective systemic immune responses. Indeed, some studies have successfully shown that candidate LAB vaccines elicited antigen-specific IgA responses in feces, saliva or bronchoalveolar and intestinal lavage fluids, as well as antigen-specific IgA-secreting cells in the lungs and mesenteric lymph nodes.

These studies with encouraging results confirm the potential use of LAB as live vectors for mucosal immunization and/or therapy. In this context, the model LAB species, Lactococcus lactis, has been used for the heterologous expression of therapeutic proteins such as: antigens, cytokines and enzymes. Thus, the resulting recombinant lactococci strains have been successfully tested for their prophylactic and therapeutic effects in many animal models such as: Human Papillomavirus type-16 (HPV-16)-induced tumors in mice, bovine β-lactoglobulin (BLG)-allergic reaction in mice and body weight and food consumption in obese mice.

b) Use of recombinant LAB and commensals in IBD.

Modulation of the mucosal immune system has been demonstrated in IBD. The currently used therapies to treat IBD are based on anti-inflammatory drugs combined with immunosuppressives. Immunomodulatory molecules have been efficient in the control of inflammation and in the remission of the episodes of the illness. The use of LAB to prevent and treat colitis was performed with a recombinant L. lactis strain producing and delivering IL-10, an anti-inflammatory cytokine, in situ in different mouse models. Daily mucosal administration of recombinant L. lactis secreting IL-10 led to a 50% decrease of the colitis induced by the administration of dextran sodium sulfate (DSS) in mice. This beneficial effect was dependent on the in situ secretion of IL-10 by the live lactococci. The rationale in using recombinant L. lactis for a local delivery of IL-10 in IBD is due to the large number of scientific studies proving that the topical treatment with this cytokine has clinic benefits although systemic IL-10 administration in Crohn’s disease patients has been associated with considerable side effects which are partly due to the fact that systemic IL-10 induces the pro-inflammatory cytokine IFN-γ. To address the safety issues in using genetically modified organisms in humans, the gene encoding the L. lactis thymidylate synthase (thyA) was replaced by the gene of the human IL-10 (hIL-10) to generate one L. lactis strain auxotrophic for thymidine or thymine. The viability and contention of this strain was validated in vivo in a swine model. Additionally, a small Phase I clinical study in patients with CD using the thyA-/hIL-10+ strain was recently conducted. This study not only showed that the contention strategy is effective, but also that the mucosal expression of IL-10 by L. lactis is feasible in humans. However, a phase IIA trial was performed which revealed that, although safety, tolerability, environmental containment and assessment of biomarkers associated with the strains have been achieved, no statistically significant difference has been found versus placebo in terms of beneficial effects (press release published in 2009). Due to these results, the necessity to optimize the LAB delivery strategy (new strains, different expression systems and different nature of the delivered molecules) is a requirement to reach a clear demonstration of their efficacy in human clinical trials, leading to their better acceptance. The delivery of immunosuppressive cytokines by other bacteria has also been tested. The probiotic potential of IL-10-expressing E. coli Nissle 1917 has been outlined in a mouse model of IBD. The use of LAB to produce Trefoil Factors (TFF) at the mucosal level to treat IBD has also been studied. TFF are a class of nonmitogenic peptides that play important roles in the protection and repair of the intestinal epithelium. These peptides are known because of their strong protective effects and for repairing the mucosa after damage. For this reason, they are interesting molecules to potentially treat IBD. However, when they are administered by an oral route, they adhere to the gut mucosa and are absorbed at the intestinal level. Interestingly, intragastric administration of recombinant L. lactis secreting TFF leads to the expression of the active peptides in the colon and prevents and repairs the damage due to the acute colitis induced by DSS. Another strategy to treat colitis was also based on the use of recombinant L. lactis secreting the LcrV antigen, an anti-inflammatory protein produced by Yersinia pseudotuberculosis to escape the immune response of the host. The therapeutic and protective potential of this strain was evaluated using two colitis murine models: DSS and trinitrobenzene sulfonic acid (TNBS). Still, another strategy to treat IBD is the use of antioxidant enzymes. It is well established that GIT inflammation is associated with an influx of neutrophils and macrophages and with the production of inflammatory mediators such as: proteases, cytokines and reactive oxygen species (ROS). ROS include the superoxide radical (O2°-), hydrogen peroxide (H2O2), and the hydroxyl radical (·OH). Their reactivity toward lipids, proteins and DNA causes both cytotoxic and mutagenic cellular damages. To detoxify ROS, cells have evolved protective mechanisms via antioxidant enzymes such as superoxide dismutases (SOD) and catalases (CAT) which degrade O2°- and H2O2 respectively, and thus prevent the formation of·OH. In this context, different studies have shown that recombinant strains of Lactobacillus spp. expressing either SOD or CAT can reduce inflammation in mouse models. In some cases, the anti-inflammatory mechanism of these recombinant strains has been elucidated and linked to the inhibition of neutrophil recruitment. The mucosal expression of elafin, a natural protease inhibitor expressed in healthy intestinal mucosa, is diminished in patients with IBD. Recently, LAB secreting elafin have been tested in chronic and acute colitis models and the inflamed epithelium was protected from increased intestinal permeability and from the release of cytokines and chemokines by LAB secreting elafin.

In addition to these recombinant probiotic strains, mutants in specific genes encoding potential probiotic functions (mucal adhesion factors, resistance to acid, specific cell wall components, etc.) have been engineered to compare their biological effects with that of their wild-type counterparts. In 2005, Grangette et al. has provided an illustration of this approach by constructing a mutant of Lactobacillus plantarum impaired in its capacity to incorporate D-alanine in teichoic acids (Dlt- mutant). Strikingly, when tested in vivo, the Dlt- mutant proved to be more protective in a mouse model of colitis than the wild-type strain. Furthermore, the use of lipoteichoic acid (LTA)-deficient L. acidophilus in in vitro analysis enhances IL-10 production by dendritic cells and macrophages and downregulates IL-12 and TNF-α. This strain is also able to significantly protect dextran sulfate sodium and CD4+CD45RBhigh T cell-induced colitis in mice and to normalize innate and adaptative pathogenic immune responses in established colonic polyps causing cancer regression. However, no protective effects have been found in LTA-induced pro-inflammatory signals and subsequent colitis. Altogether, with the possibility to express different factors such as ScFv antibodies, host targeting molecules and immunomodulators in LAB, more applications and progress towards studies in humans should be performed in a next future.

The next step in this field seems to choose new delivery bacteria. As mentioned above, L. lactis is the most widely used LAB in the production of heterologous proteins and is considered as the model LAB and live delivery vector model. Despite all the advantages mentioned above, this bacterium has a short survival time (~24 hours) in the human GIT leading thus to a reduced time of action. In contrast, other probiotic bacteria which could be natural colonizers of the GIT, could combine their intrinsic probiotic effects to the probiotic effects conferred by the heterologous delivered protein. The most achieved project in this field is the one based on the use of the commensal Bacteroides ovatus Indeed, Hamady et al. chose this bacterium for the in vivo delivery of proteins for its ability to colonize the colon and its xylan utilisation properties. They were able to develop a xylan-regulated delivery of i) human keratynocyte growth factor-2 to the inflamed colon and ii) the human TGF-b1 to treat colitis in mice. These promising results confirm the potential of the use of recombinant commensal for in vivo delivery.

Conclusions and future research

We can conclude that current probiotic research encourages the search and characterization of gut bacteria as a model for finding new natural or engineered probiotic strains to be used to restore the normal balance of the human gut ecosystem.

The fact that commensal and probiotic bacteria interact with the host immune system is now well accepted and illustrated by in vitro and in vivo experiments. However, the current knowledge of the molecular mechanisms involved in this cross-talk remain poorly understood. Although some mechanisms and active compounds have been identified in a few commensal or probiotic strains, and taking into account that the human GIT is composed of 1013-1014 microorganisms, it is necessary to explore profoundly this research area and in particular to elucidate the exact role of bacterial compounds in homeostasis and immune response.

As for the use of genetically modified commensal and probiotic bacteria in humans, it is certain that most of the studies being done are Proof-of-Concept. However, although some researchers have claimed that genetically modified probiotics should be banned, the data obtained in the phase I clinical trial with the recombinant strain of L. lactis secreting IL-10 (see above in the text) showed that the containment strategy (ie. release of such genetically modified organisms into nature) used to construct the strain was not only safe and effective but also that mucosal delivery of IL-10 by a genetically modified LAB is feasible in humans.

In conclusion, it is clear that the analysis of the impact of commensals and probiotics on the host immune system has entered a new and fascinating phase of research. This new area offers us new knowledge that can be exploited to develop new approaches to modulate host immunity for protection against infectious diseases or for immunotherapy.

Abbreviations

BLG: β-lactoglobulin; CAT: Catalases; CD: Crohn’s disease; DSS: Dextran sodium sulfate; GIT: Gastrointestinal tract; GMO: Genetically modified organisms; GRAS: Generally recognized as safe; HPV-16: Human Papillomavirus type-16; IBD: Inflammatory bowel disease; IBS: Irritable bowel syndrome; LAB: Lactic acid bacteria; LGG: Lactobacillus rhamnosus GG; ROS: Reactive oxygen species; SCFA: Short chain fatty acids; SOD: Superoxide dismutases; TFF: Treefoil factors; TNBS: Trinitrobenzene sulfonic acid; UC: Ulcerative colitis

Competing interests

The authors declare that they have no competing interests.

Authors’ contribution

RM and LBH wrote the main text, figures and tables. SM, NK, JU, PL corrected and helped to draft the manuscript. All authors have read and approved the final manuscript.

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    Zhang HS DiBaise JK Zuccolo A Kudrna D Braidotti M Yu YS Parameswaran P Crowell MD Wing R Rittmann BE Krajmalnik-Brown R Human gut microbiota in obesity and after gastric bypassProc Natl Acad Sci USA2009 10623652370

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  44. 44.

    Wen L Ley RE Volchkov PY Stranges PB Avanesyan L Stonebraker AC Hu CY Wong FS Szot GL Bluestone JA Innate immunity and intestinal microbiota in the development of Type 1 diabetesNature2008 4551109U1110

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  45. 45.
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  46. 46.

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  49. 49.

    Bocker U Nebe T Herweck F Holt L Panja A Jobin C Rossol S BS R Singer MV Butyrate modulates intestinal epithelial cell-mediated neutrophil migrationClin Exp Immunol2003 1315360

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  50. 50.

    Luhrs H Gerke T Muller JG Melcher R Schauber J Boxberger F Scheppach W Menzel T Butyrate inhibits NF-kappa B activation in lamina propria macrophages of patients with ulcerative colitisScand J Gastroenterol2002 37458466

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  51. 51.

    Harig JM Soergel KH Komorowski RA Wood CM Treatment of diversion colitis with short-chain-fatty acid irrigationN Engl J Med1989 3202328

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  52. 52.

    Jan G Belzacq AS Haouzi D Rouault A Metivier D Kroemer G Brenner C Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondriaCell Death Differ2002 9179188

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  53. 53.

    Li CJ Elsasser TH Butyrate-induced apoptosis and cell cycle arrest in bovine kidney epithelial cells: Involvement of caspase and proteasome pathwaysJ Anim Sci2005 838997

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  54. 54.

    Fukuda S Toh H Hase K Oshima K Nakanishi Y Yoshimura K Tobe T Clarke JM Topping DL Suzuki T Bifidobacteria can protect from enteropathogenic infection through production of acetateNature2011 469543U791

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  55. 55.

    Masood MI Qadir MI Shirazi JH Khan IU Beneficial effects of lactic acid bacteria on human beingsCrit Rev Microbiol2011 379198

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  56. 56.

    Gionchetti P Amadini C Rizzello F Venturi A Poggioli G Campieri M Probiotics for the treatment of postoperative complications following intestinal surgeryBest Pract Res Clin Gastroenterol2003 17821831

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    McCarthy J O’Mahony L O’Callaghan L Sheil B Vaughan EE Fitzsimons N Fitzgibbon J O’Sullivan GC Kiely B Collins JK Shanahan F Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balanceGut2003 52975980

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    Savilahti E Kuitunen M Vaarala O Pre and probiotics in the prevention and treatment of food allergyCurrent Opinion in Allergy and Clinical Immunology2008 8243248

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  59. 59.

    Vliagoftis H Kouranos VD Betsi GI Falagas ME Probiotics for the treatment of allergic rhinitis and asthma: systematic review of randomized controlled trialsAnn Allergy Asthma Immunol2008 101570579

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  60. 60.

    Weston S Halbert A Richmond P Prescott SL Effects of probiotics on atopic dermatitis: a randomised controlled trialArch Dis Child2005 90892897

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  61. 61.

    Isolauri E Rautava S Salminen S Probiotics in the development and treatment of allergic diseaseGastroenterol Clin North Am2012 41747762

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    Nermes M Kantele JM Atosuo TJ Salminen S Isolauri E Interaction of orally administered Lactobacillus rhamnosus GG with skin and gut microbiota and humoral immunity in infants with atopic dermatitisClinical and Experimental Allergy2011 41370377

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    Kuitunen M Probiotics and prebiotics in preventing food allergy and eczemaCurr Opin Allergy Clin Immunol2013 13280286

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    Foolad N Brezinski EA Chase EP Armstrong AW Effect of nutrient supplementation on atopic dermatitis in children: a systematic review of probiotics, prebiotics, formula, and fatty acidsJAMA Dermatol2013 149350355

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    Pessi T Sutas Y Hurme H Isolauri E Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GGClinical and Experimental Allergy2000 3018041808

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    Lim LH Li HY Huang CH Lee BW Lee YK Chua KY The Effects of Heat-Killed Wild-Type Lactobacillus casei Shirota on Allergic Immune Responses in an Allergy Mouse ModelInternational Archives of Allergy and Immunology2009 148297304

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    Abrahamsson TR Jakobsson T Bottcher MF Fredrikson M Jenmalm MC Bjorksten B Oldaeus G Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trialJ Allergy Clin Immunol2007 11911741180

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  68. 68.

    Knight DJ Girling KJ Gut flora in health and diseaseLancet1831 2003361

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  69. 69.

    Heselmans M Reid G Akkermans LM Savelkoul H Timmerman H Rombouts FM Gut flora in health and disease: potential role of probioticsCurr Issues Intest Microbiol2005 617

    Not in our library

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    Kruis W Review article: antibiotics and probiotics in inflammatory bowel diseaseAliment Pharmacol Ther2004 207578

    Not in our library10.1111/j.1365-2036.2004.02051.x

  71. 71.

    Rochat T Bermudez-Humaran L Gratadoux JJ Fourage C Hoebler C Corthier G Langella P Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in miceMicrob Cell Fact2007 622

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  72. 72.

    Hormannsperger G Haller D Molecular crosstalk of probiotic bacteria with the intestinal immune system: clinical relevance in the context of inflammatory bowel diseaseInt J Med Microbiol2010 3006373

    Not in our library10.1016/j.ijmm.2009.08.006

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    Rousseaux C Thuru X Gelot A Barnich N Neut C Dubuquoy L Dubuquoy C Merour E Geboes K Chamaillard M Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptorsNature Medicine2007 133537

    Not in our library10.1038/nm1521

  74. 74.

    Haller D Antoine JM Bengmark S Enck P Rijkers GT Lenoir-Wijnkoop I Guidance for substantiating the evidence for beneficial effects of probiotics: probiotics in chronic inflammatory bowel disease and the functional disorder irritable bowel syndromeJ Nutr2010 140690S697S

    Not in our library10.3945/jn.109.113746

  75. 75.

    Bermudez-Humaran LG Lactococcus lactis as a live vector for mucosal delivery of therapeutic proteinsHum Vaccin2009 5264267

    Not in our library10.4161/hv.5.4.7553

  76. 76.
    Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines · 2011
    No notice
  77. 77.

    Bermúdez-Humarán LG Aubry C Motta JP Deraison C Steidler L Vergnolle N Chatel JM Langella P Engineering lactococci and lactobacilli for human healthCurr Opin Microbiol2013 S1369-527413000763[Epub ahead of print] PubMed PMID: 23850097

    Not in our library10.1016/j.mib.2013.06.002

  78. 78.

    Wells JM Mercenier A Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteriaNat Rev Microbiol2008 6349362

    Not in our library10.1038/nrmicro1840

  79. 79.

    Seegers JFML Lactobacilli as live vaccine delivery vectors: progress and prospectsTrends Biotechnol2002 20508515

    Not in our library10.1016/s0167-7799(02)02075-9

  80. 80.

    Neutra MR Kozlowski PA Mucosal vaccines: the promise and the challengeNat Rev Immunol2006 6148158

    Not in our library10.1038/nri1777

  81. 81.

    Lee SF Oral colonization and immune responses to Streptococcus gordonii: potential use as a vector to induce antibodies against respiratory pathogensCurr Opin Infect Dis2003 16231235

    Not in our library10.1097/00001432-200306000-00008

  82. 82.

    Bermudez-Humaran LG Cortes-Perez NG Le Loir Y Alcocer-Gonzalez JM Tamez-Guerra RS de Oca-Luna RM Langella P An inducible surface presentation system improves cellular immunity against human papillomavirus type 16 E7 antigen in mice after nasal administration with recombinant lactococciJ Med Microbiol2004 53427433

    Not in our library10.1099/jmm.0.05472-0

  83. 83.

    Bermudez-Humaran LG Cortes-Perez NG Lefevre F Guimaraes V Rabot S Alcocer-Gonzalez JM Gratadoux JJ Rodriguez-Padilla C Tamez-Guerra RS Corthier G A novel mucosal vaccine based on live Lactococci expressing E7 antigen and IL-12 induces systemic and mucosal immune responses and protects mice against human papillomavirus type 16-induced tumorsJ Immunol2005 17572977302

    Not in our library10.4049/jimmunol.175.11.7297

  84. 84.

    Bermudez-Humaran LG Langella P Cortes-Perez NG Gruss A Tamez-Guerra RS Oliveira SC Saucedo-Cardenas O Montes de Oca-Luna R Le Loir Y Intranasal immunization with recombinant Lactococcus lactis secreting murine interleukin-12 enhances antigen-specific Th1 cytokine productionInfect Immun2003 7118871896

    Not in our library10.1128/iai.71.4.1887-1896.2003

  85. 85.

    Bermudez-Humaran LG Nouaille S Zilberfarb V Corthier G Gruss A Langella P Issad T Effects of intranasal administration of a leptin-secreting Lactococcus lactis recombinant on food intake, body weight, and immune response of miceAppl Environ Microbiol2007 7353005307

    Not in our library10.1128/aem.00295-07

  86. 86.

    Cauchard S Bermudez-Humaran LG Blugeon S Laugier C Langella P Cauchard J Mucosal co-immunization of mice with recombinant lactococci secreting VapA antigen and leptin elicits a protective immune response against Rhodococcus equi infectionVaccine2011 3095102

    Not in our library10.1016/j.vaccine.2011.10.026

  87. 87.

    Cortes-Perez NG Bermudez-Humaran LG Le Loir Y Rodriguez-Padilla C Gruss A Saucedo-Cardenas O Langella P Montes-de-Oca-Luna R Mice immunization with live lactococci displaying a surface anchored HPV-16 E7 oncoproteinFEMS Microbiol Lett2003 2293742

    Not in our library10.1016/s0378-1097(03)00778-x

  88. 88.

    Cortes-Perez NG Lefevre F Corthier G Adel-Patient K Langella P Bermudez-Humaran LG Influence of the route of immunization and the nature of the bacterial vector on immunogenicity of mucosal vaccines based on lactic acid bacteriaVaccine2007 2565816588

    Not in our library10.1016/j.vaccine.2007.06.062

  89. 89.

    Corthesy B Boris S Isler P Grangette C Mercenier A Oral immunization of mice with lactic acid bacteria producing Helicobacter pylori urease B subunit partially protects against challenge with Helicobacter felisJ Infect Dis2005 19214411449

    Not in our library10.1086/444425

  90. 90.

    Grangette C Muller-Alouf H Hols P Goudercourt D Delcour J Turneer M Mercenier A Enhanced mucosal delivery of antigen with cell wall mutants of lactic acid bacteriaInfect Immun2004 7227312737

    Not in our library10.1128/iai.72.5.2731-2737.2004

  91. 91.

    Grangette C Muller-Alouf H Geoffroy M Goudercourt D Turneer M Mercenier A Protection against tetanus toxin after intragastric administration of two recombinant lactic acid bacteria: impact of strain viability and in vivo persistenceVaccine2002 2033043309

    Not in our library10.1016/s0264-410x(02)00301-8

  92. 92.

    Grangette C Muller-Alouf H Goudercourt D Geoffroy MC Turneer M Mercenier A Mucosal immune responses and protection against tetanus toxin after intranasal immunization with recombinant Lactobacillus plantarumInfect Immun2001 6915471553

    Not in our library10.1128/iai.69.3.1547-1553.2001

  93. 93.

    Wells JM Wilson PW Norton PM Gasson MJ Le Page RW Lactococcus lactis: high-level expression of tetanus toxin fragment C and protection against lethal challengeMol Microbiol1993 811551162

    Not in our library10.1111/j.1365-2958.1993.tb01660.x

  94. 94.

    Robinson K Chamberlain LM Schofield KM Wells JM Le Page RW Oral vaccination of mice against tetanus with recombinant Lactococcus lactisNat Biotechnol1997 15653657

    Not in our library10.1038/nbt0797-653

  95. 95.

    Cortes-Perez NG Ah-Leung S Bermudez-Humaran LG Corthier G Wal JM Langella P Adel-Patient K Intranasal coadministration of live lactococci producing interleukin-12 and a major cow’s milk allergen inhibits allergic reaction in miceClin Vaccine Immunol2007 14226233

    Not in our library10.1128/cvi.00299-06

  96. 96.

    Cortes-Perez NG Ah-Leung S Bermudez-Humaran LG Corthier G Langella P Wal JM Adel-Patient K Allergy therapy by intranasal administration with recombinant Lactococcus lactis Producing bovine beta-lactoglobulinInt Arch Allergy Immunol2009 1502531

    Not in our library10.1159/000210377

  97. 97.

    Amar J Chabo C Waget A Klopp P Vachoux C Bermudez-Humaran LG Smirnova N Berge M Sulpice T Lahtinen S Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatmentEMBO Mol Med2011 3559572

    Not in our library10.1002/emmm.201100159

  98. 98.

    Kuhbacher T Folsch UR Practical guidelines for the treatment of inflammatory bowel diseaseWorld J Gastroenterol2007 1311491155

    Not in our library10.3748/wjg.v13.i8.1149

  99. 99.

    Steidler L Hans W Schotte L Neirynck S Obermeier F Falk W Fiers W Remaut E Treatment of murine colitis by Lactococcus lactis secreting interleukin-10Science2000 28913521355

    Not in our library10.1126/science.289.5483.1352

  100. 100.

    Dumot JA Conwell DL Zuccaro G Vargo JJ Shay SS Easley KA Ponsky JL A randomized, double blind study of interleukin 10 for the prevention of ERCP-induced pancreatitisAm J Gastroenterol2001 9620982102

    Not in our library10.1111/j.1572-0241.2001.04092.x

  101. 101.

    Fedorak RN Gangl A Elson CO Rutgeerts P Schreiber S Wild G Hanauer SB Kilian A Cohard M LeBeaut A Feagan B Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn’s disease. The Interleukin 10 Inflammatory Bowel Disease Cooperative Study GroupGastroenterology2000 11914731482

    Not in our library10.1053/gast.2000.20229

  102. 102.

    Targan SR Hanauer SB van Deventer SJH Mayer L Present DH Braakman T DeWoody KL Schaible TF Rutgeerts PJ A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor alpha for Crohn’s diseaseN Engl J Med1997 33710291035

    Not in our library10.1056/nejm199710093371502

  103. 103.

    Tilg H van Montfrans C van den Ende A Kaser A van Deventer SJ Schreiber S Gregor M Ludwiczek O Rutgeerts P Gasche C Treatment of Crohn’s disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon gammaGut2002 50191195

    Not in our library10.1136/gut.50.2.191

  104. 104.

    Steidler L Neirynck S Huyghebaert N Snoeck V Vermeire A Goddeeris B Cox E Remon JP Remaut E Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10Nat Biotechnol2003 21785789

    Not in our library10.1038/nbt840

  105. 105.

    Braat H Rottiers P Hommes DW Huyghebaert N Remaut E Remon JP van Deventer SJ Neirynck S Peppelenbosch MP Steidler L A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s diseaseClin Gastroenterol Hepatol2006 4754759

    Not in our library10.1016/j.cgh.2006.03.028

  106. 106.

    Ross JJ Boucher PE Bhattacharyya SP Kopecko DJ Sutkowski EM Rohan PJ Chandler DKF Vaillancourt J Considerations in the development of live biotherapeutic products for clinical useCurrent Issues in Molecular Biology2008 101316

    Not in our library

  107. 107.

    Wells J Mucosal vaccination and therapy with genetically modified lactic acid bacteriaAnnu Rev Food Sci Technol2011 2423445

    Not in our library10.1146/annurev-food-022510-133640

  108. 108.

    Steidler L Rottiers P Coulie B Actobiotics (TM) as a novel method for cytokine delivery the interleukin-10 caseCytokine Therapies: Novel Approaches for Clinical Indications2009 1182135145

    Not in our library

  109. 109.

    Leblanc JG Aubry C Cortes-Perez NG de Moreno de Leblanc A Vergnolle N Langella P Azevedo V Chatel JM Miyoshi A Bermudez-Humaran LG Mucosal targeting of therapeutic molecules using genetically modified lactic acid bacteria: an updateFEMS Microbiol Lett2013 34419

    Not in our library10.1111/1574-6968.12159

  110. 110.

    Gardlik R Palffy R Celec P Recombinant probiotic therapy in experimental colitis in miceFolia Biol (Praha)2012 58238245

    Not in our library10.14712/fb2012058060238

  111. 111.

    Playford RJ Marchbank T Chinery R Evison R Pignatelli M Boulton RA Thim L Hanby AM Human spasmolytic polypeptide is a cytoprotective agent that stimulates cell-migrationGastroenterology1995 108108116

    Not in our library10.1016/0016-5085(95)90014-4

  112. 112.

    Vandenbroucke K Hans W Van Huysse J Neirynck S Demetter P Remaut E Rottiers P Steidler L Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in miceGastroenterology2004 127502513

    Not in our library10.1053/j.gastro.2004.05.020

  113. 113.

    Foligne B Dessein R Marceau M Poiret S Chamaillard M Pot B Simonet M Daniel C Prevention and treatment of colitis with Lactococcus lactis secreting the immunomodulatory Yersinia LcrV proteinGastroenterology2007 133862874

    Not in our library10.1053/j.gastro.2007.06.018

  114. 114.

    Segui J Gil F Gironella M Alvarez M Gimeno M Coronel P Closa D Pique JM Panes J Down-regulation of endothelial adhesion molecules and leukocyte adhesion by treatment with superoxide dismutase is beneficial in chronic immune experimental colitisInflamm Bowel Dis2005 11872882

    Not in our library10.1097/01.mib.0000183420.25186.7a

  115. 115.

    Grisham MB Gaginella TS von Ritter C Tamai H Be RM Granger DN Effects of neutrophil-derived oxidants on intestinal permeability, electrolyte transport, and epithelial cell viabilityInflammation1990 14531542

    Not in our library10.1007/bf00914274

  116. 116.

    Wardman P Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospectsFree Radic Biol Med2007 439951022

    Not in our library10.1016/j.freeradbiomed.2007.06.026

  117. 117.

    Carroll IM Andrus JM Bruno-Barcena JM Klaenhammer TR Hassan HM Threadgill DS Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitisAm J Physiol Gastrointest Liver Physiol2007 293G729G738

    Not in our library10.1152/ajpgi.00132.2007

  118. 118.

    Han W Mercenier A Ait-Belgnaoui A Pavan S Lamine F van S II Kleerebezem M Salvador-Cartier C Hisbergues M Bueno L Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutaseInflamm Bowel Dis2006 1210441052

    Not in our library10.1097/01.mib.0000235101.09231.9e

  119. 119.

    Watterlot L Rochat T Sokol H Cherbuy C Bouloufa I Lefevre F Gratadoux JJ Honvo-Hueto E Chilmonczyk S Blugeon S Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in miceInt J Food Microbiol2010 1443541

    Not in our library10.1016/j.ijfoodmicro.2010.03.037

  120. 120.

    Motta JP Bermudez-Humaran LG Deraison C Martin L Rolland C Rousset P Boue J Dietrich G Chapman K Kharrat P Food-grade bacteria expressing elafin protect against inflammation and restore colon homeostasisSci Transl Med2012 4158ra144

    Not in our library10.1126/scitranslmed.3004212

  121. 121.

    Grangette C Nutten S Palumbo E Morath S Hermann C Dewulf J Pot B Hartung T Hols P Mercenier A Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acidsProc Natl Acad Sci USA2005 1021032110326

    Not in our library10.1073/pnas.0504084102

  122. 122.

    Khan MW Zadeh M Bere P Gounaris E Owen J Klaenhammer T Mohamadzadeh M Modulating intestinal immune responses by lipoteichoic acid-deficient Lactobacillus acidophilusImmunotherapy2012 4151161

    Not in our library10.2217/imt.11.163

  123. 123.

    Mohamadzadeh M Pfeiler EA Brown JB Zadeh M Gramarossa M Managlia E Bere P Sarraj B Khan MW Pakanati KC Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acidProc Natl Acad Sci USA2011 10846234630

    Not in our library10.1073/pnas.1005066107

  124. 124.

    Khazaie K Zadeh M Khan MW Bere P Gounari F Dennis K Blatner NR Owen JL Klaenhammer TR Mohamadzadeh M Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acidProc Natl Acad Sci U S A2012 1091046210467

    Not in our library10.1073/pnas.1207230109

  125. 125.

    Zadeh M Khan MW Goh YJ Selle K Owen JL Klaenhammer T Mohamadzadeh M Induction of intestinal pro-inflammatory immune responses by lipoteichoic acidJ Inflamm (Lond)2012 97PubMed PMID: 22423982; PubMed Central PMCID: PMC3325164

    Not in our library10.1186/1476-9255-9-7

  126. 126.

    Hamady ZZ Novel xylan-controlled delivery of therapeutic proteins to inflamed colon by the human anaerobic commensal bacteriumAnn R Coll Surg Engl2013 95423540PubMed PMID: 23676805

    Not in our library10.1308/003588413x13511609958217

  127. 127.

    Hamady ZZ Farrar MD Whitehead TR Holland KT Lodge JP Carding SR Identification and use of the putative Bacteroides ovatus xylanase promoter for the inducible production of recombinant human proteinsMicrobiology2008 154Pt 10316574PubMed PMID: 18832322

    Not in our library10.1099/mic.0.2008/019109-0

  128. 128.

    Hamady ZZ Scott N Farrar MD Lodge JP Holland KT Whitehead T Carding SR Xylan-regulated delivery of human keratinocyte growth factor-2 to the inflamed colon by the human anaerobic commensal bacterium Bacteroides ovatusGut2010 5944619Epub 2009 Sep 7. PubMed PMID:19736360

    Not in our library10.1136/gut.2008.176131

  129. 129.

    Hamady ZZ Scott N Farrar MD Wadhwa M Dilger P Whitehead TR Thorpe R Holland KT Lodge JP Carding SR Treatment of colitis with a commensal gut bacterium engineered to secrete human TGF-beta1 under the control of dietary xylan 1Inflamm Bowel Dis2011 1719251935

    Not in our library10.1002/ibd.21565

  130. 130.

    Bron PA van Baarlen P Kleerebezem M Emerging molecular insights into the interaction between probiotics and the host intestinal mucosaNat Rev Microbiol2012 1066U90

    Not in our library10.1038/nrmicro2690

  131. 131.

    Cummins J MW H Genetically modified probiotics should be bannedMicrob Ecol Heal Dis2005 176668

    Not in our library10.1080/08910600510044480

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