Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 17, 2026.

Intracellular staphylococcus aureus: Live-in and let die

Martin Fraunholz, Bhanu Sinha

Frontiers in Cellular and Infection Microbiology · 2012 · Review

doi:10.3389/fcimb.2012.00043

Abstract

Staphylococcus aureus uses a plethora of virulence factors to accommodate a diversity of niches in its human host. Aside from the classical manifestations of S. aureus-induced diseases, the pathogen also invades and survives within mammalian host cells.The survival strategies of the pathogen are as diverse as strains or host cell types used. S. aureus is able to replicate in the phagosome or freely in the cytoplasm of its host cells. It escapes the phagosome of professional and non-professional phagocytes, subverts autophagy, induces cell death mechanisms such as apoptosis and pyronecrosis, and even can induce anti-apoptotic programs in phagocytes. The focus of this review is to present a guide to recent research outlining the variety of intracellular fates of S. aureus.

Shown for reading. Its publisher allows quoting it, not republishing it.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 17, 2026. Paragraph numbers are ours, so an answer can point at one.

INTRODUCTION

Most manifestations of Staphylococcus aureus disease involve extracellular bacteria (furuncles, carbuncles, impetigo, abscesses, septicemia, necrotizing pneumonia) or biofilm formation (catheter-induced infective endocarditis, atherosclerosis). Aside from this S. aureus infections have a second face: there is accumulating evidence that S. aureus is able to survive within its hosts cells and thus might be termed a facultative intracellular pathogen. Intracellularity of S. aureus has been implied as immune-evasive strategy thereby escaping detection by professional phagocytes.

INTERNALIZATION OF S. aureus BY HOST CELLS

Invasion of non-professional phagocytes by S. aureus is mediated by a zipper-type mechanism. To date many bacterial adhesins have been identified with Fibronectin (Fn)-binding proteins A and B (FnBPA, FnBPB) constituting the major staphylococcal adhesins for non-professional phagocytes such as epithelial, endothelial cells, fibroblasts, osteoblasts, and keratinocytes (;;;;;;;;;; Figure 1, Map Item 1). Fibronectin-bridging between FnBPs and α5β1 integrins on the host cell surface is sufficient to induce zipper-type uptake of staphylococci. However, FnBPs also have been shown to directly bind to human heat shock protein 60 (Hsp60) exposed on the cellular surface. FnBP-independent invasion was observed in S. aureus Newman, which produces C-terminally truncated FnBPs that are not covalently anchored to the cell wall of S. aureus. It has been shown that strain Newman gets internalized by epithelial cells and fibroblasts mediated by extracellular adherence protein (Eap; ) with its cellular receptor still not identified to date. Recently, the staphylococcal autolysin (Atl) was identified to function as adhesin/invasin with heat shock cognate protein Hsc70 being the direct cellular receptor. Further, wall teichoic acids (WTA) seem to be important for establishment of nasal colonization and there is evidence that a scavenger receptor is involved in WTA binding. Clumping factor B (ClfB) has been shown to bind to cytokeratins in the extracellular matrix (ECM) of host cells, and staphylococcal protein A can directly interact with tumor necrosis factor α receptor 1 (TNFR1; ). To what extent the internalization of the pathogen is mediated by WTA, ClfB, protein A, and a body of other molecules interacting with the ECM of host cells is not known thus far.

Since FnBPs contribute to the adherence of S. aureus to intact endothelium in vivo, we can assume that staphylococcal invasion of epithelia or the endothelium is relevant in natural infections. The interaction of FnBP with ECM Fn is mediated by tandem β zipper structures via the binding of multiple fibronectin molecules by the repetitively arranged modules within a single FnBP. As a result FnBP/Fn sequester α5β1 integrins on the host cell surface. The resulting receptor clustering relays signals that result in cytoskeletal rearrangements. The rearrangements initiated at focal adhesions, which are remodeled to fibrillar adhesions by loss of focal adhesion kinase (FAK), paxillin, and vinculin. The rearrangement is accompanied by a centripetal movement of S. aureus on the host cell surface that were observed by videomicroscopy. The repeated generation of actin comet tails beneath adherent staphylococci or FnbA-coated beads and the formation of actin cups without internalization of staphylococci is interpreted by the authors as a delay of phagocytosis (; Figure 1, Map Item 2). Invasion signaling further involves src kinase. Extracellular signal-regulated kinases (ERK) and c-Jun N-terminal kinase (JNK) but not mitogen-activated protein kinase (MAPK) p38 are required in osteoblasts, whereas in HEp-2 cells p38 MAPK was found to be upregulated alongside ERK. Further, phosphorylation of transcription factor c-Jun, but not of Elk-1 or ATF-2 has been demonstrated during invasion of osteoblasts. The phosphoinositide-3-kinase (PI3K)-Akt pathway is active during S. aureus internalization by bovine endothelial cells.

Eventually, S. aureus gets endocytosed by professional as well as non-professional cells where the pathogen faces a variety of intracellular fates.

Staphylococcus aureus INTRACELLULAR PERSISTENCE AND GROWTH

The fates of the pathogen and the infected host cell depend on staphylococcal isolate and genotype as well as differential susceptibility of host cells to virulence factors, host cell gene expression, etc. For example, S. aureus produces different hemolysins. The majority of bovine mastitis strains were phenotypically positive for the sphingomyelinase β-toxin, whereas only a minority of human strains isolated from cases of septicemia or nasal carriage was positive for β-toxin. There seems to exist a selective pressure for S. aureus strains colonizing humans to acquire β-toxin converting phage. This is most likely due to staphylococcal complement inhibitor SCIn and the chemotaxis inhibitor protein CHIPS (and additional factors) that are usually found to be encoded by the respective phage genomes. Purified β-toxin, selectively kills monocytes and destroys platelets, but barely affects other cell types. Similarly, most human cell types are fairly insensitive to the pore-former α-toxin, whereas human leukocytes and cells from other mammalian species are highly susceptible. The metalloprotease ADAM10 has been recently identified as receptor of α-toxin monomers (;; Figure 1, Map Item 3). The differential specificities of α-toxin possibly reflect ADAM10 expression differences in the respective cells or might result from differential capability of host cells to remove α-toxin pores by endocytosis.

Staphylococcus aureus survival within host cells was highly dependent on multiplicity of infection (MOI; e.g.,;; ) and also the growth phase of the bacteria used for infection. Green-fluorescent protein (GFP)-expressing S. aureus displayed bleaching of the fluorescent protein, which indicated degradation of the bacteria in polymorphonuclear neutrophils (PMN; Figure 1, Map Item 4a). The loss of fluorescence was not strain-specific and was seen in each of several different strains of S. aureus, including nosocomial and community-associated methicillin-resistant strains. When rapidly growing S. aureus was used for infection, the bacteria were found to be more susceptible to GFP bleaching. This indicated that these bacteria were cleared more efficiently. Bacterial disinfection was mainly dependent on hypochlorous acid (HOCl; ). Phagosomal acidification and digestion of S. aureus within professional phagocytes is required for MyD88-dependent toll-like receptor (TLR) responses to infection.

Not all bacterial cells are disinfected by the phagolysosomes. S. aureus has been reported to persist inside phagocytes or endothelial cells for prolonged periods (;;;;;;;;; reviewed in ). Persistence is most often attributed to small colony variants (SCVs) of S. aureus. SCVs often present a metabolically quiescent, non-hemolytic, non-pigmented phenotype characterized by reversible auxotrophies in heme biosynthetic pathways or in oxidative phosphorylation as well as a defined transcriptome and proteome. Also, SCVs are generally found to be mutants in the accessory gene regulator locus (agr), thus failing to produce a variety of quorum sensing-controlled virulence factors. SCVs grow slowly and hence are more resistant to a variety of antibiotics (reviewed in ). Further, SCVs display a thick cell wall and an up-regulation of alternative sigma-factor σB, which enables S. aureus to cope with a variety of environmental stressors. There is increasing evidence that S. aureus can persist in vivo in human infections presumably owing to its extreme durability and resistance against a variety of environmental conditions and thus can serve as a potential source for recurrent infection (;;;; reviewed in; ). SCVs of S. aureus even have been shown to survive and grow within host cell phagosomes (; Figure 1, Map Item 4b). Also, the complementation of rsbU in laboratory strains restored activity of the alternative sigma-factor σB and led to intracellular growth of S. aureus within phagolysosomes of THP-1 phagocytes. Contrasting these reports, staphylococcal growth has been described after pathogen translo-cation to the host cell cytoplasm (Figure 1, Map Item 4c): S. aureus strain Newman is able to escape the phagosome and persists within human monocyte-derived macrophages (hMDM) which resulted in host cell lysis on day 5 after infection. The authors postulate that this survival within phagocytes might constitute a route for dissemination of staphylococcal infection. This is further corroborated by the identification of cytopro-tective effects on macrophages after phagocytosis of S. aureus. Thus, the up-regulation of anti-apoptotic factors upon staphy-lococcal infection is responsible for extended phagocyte lifetime. Both studies suggest that S. aureus might penetrate deeper into the tissue and even disseminate to different sites within “Trojan horse” phagocytes. Survival within PMN is reported to depend on the accessory regulator Sar1, which was crucial to S. aureus survival inside spacious vacuoles, whereas sar- strains were localizing to so-called “tight vacuoles”. Such different vacuoles can also be observed innon-professional phagocytes. The large vacuoles also are reminiscent of spacious Liste-ria-containing phagosomes, which were found to be non-acidified and non-degradative niches in macrophages. However, a more thorough characterization of the different vacuolar locations in intracellular S. aureus infections is lacking.

Staphylococcus aureus PHAGOSOMAL ESCAPE

Phagocytosed bacterial pathogens evade lysosomal killing, e.g., by disintegration of the organelle membrane in order to translocate into the host cell cytoplasm. Listeria monocytogenes co-opts the pore-forming toxin (PFT) listeriolysin O (LLO) and phos-pholipases (reviewed in; ), and Group A streptococci use the PFT strep-tolysin O. Phagosomal escape of S. aureus initially has been described by and the agr-dependency of this process has been demonstrated. The membrane destructive function of staphylococcal a-toxin thus suggested an involvement of the pore-former in phagosomal membrane disruption. The requirement for phago-somal escape and intracellular bacterial survival has been reported in CFT-1, a cystic fibrosis (CF) lung cell line as well as in macrophages (; Figure 1, Map Item 5a). In CFT-1, S. aureus translocates into the cytoplasm in an α-toxin-dependent manner and the bacteria replicate within the cytoplasm. However, in the LCSFN cell line complemented with the wild-type CF transmem-brane conductance regulator, CFTR, α-toxin has no effect. Further, it has been demonstrated that neither α-toxin overexpressing strains nor laboratory strains inducibly expressing α-toxin are capable of releasing staphylococci into the host cell cytoplasm. By expression of the amphiphilic 26 amino-acid (AA) peptide δ-toxin in the non-cytotoxic laboratory strain S. aureus RN4220 S. aureus was capable of escape in rates similar to that of heterolo-gously expressed LLO. δ-Toxin is encoded by the agr-effector RNAIII and is translated about 1 h after transcription of RNAIII. It is capable of lysing bacterial protoplasts, lysosomes, lipid spherules, mitochondria, and erythrocytes in vitro in a temperature-independent manner. Its activity and mode of action is comparable to that of non-ionic detergents (;;;; reviewed in ). δ-Toxin is encoded by RNAIII, the agr effector, and thus might constitute an immediate response to space limitation by phagosomal engulfment (Figure 1, Map Item 5b). However, membrane disruption by δ-toxin depended on the presence of the staphylococcal sphingomyelinase, β-toxin, which cleaves sph-ingomyelins (SM) to phosphorylcholine and ceramide moieties. δ-Toxin hardly binds to negatively charged phospholipids, binds strongly to liquid-disordered domains and poorly to cholesterol and sphingomyelin liquid-ordered raft domains. In one model, β-toxin thus may cleave SM to ceramides, which tend to accumulate in membrane microdomains. The hydrophobic nature of ceramide-rich domains thus might constitute regions of δ-toxin assembly, which eventually lead to target membrane permeabilization (Figure 2). S. aureus strain USA300 LAC, however, is escape proficient yet does not encode a functional β-toxin due to lysogeny of a β-converting phage. We thus have to hypothesize alternative factors that can act in phagosomal escape, such as a variety of lipases encoded by the staphylococcal genome or phenol-soluble modulins (PSMs; see below). Alternatively, prophages might be lost, e.g., during exposure to phagosomal reactive oxygen species, and then might contribute to phagosomal escape. A similar activation mechanism is used by Streptococcus pneumoniae, which produces hydrogen peroxide and thereby lyses S. aureus by a “remote control” prophage activation.

For complete hemolysis of erythrocytes in sheep blood agar plates either a shift to 4°C (hot-cold hemolysis), osmotic stress, or synergistic toxins are necessary. δ-Toxin belong to the class of PSMs, which initially had been shown to be present within a hot-phenol extraction of S. epidermidis extracts and only later had been identified in S. aureus by sequence homology. The major groups of PSMs are divided into two operons referred to as PSMα and PSMβ. The PSMα operon is comprised of four open reading frames (ORFs) with approximately 20 AA. PSMβ encodes two ORFs, which are about 40 AA in length. The expression of PSMβ has been demonstrated to result in phagosomal escape in a gain-of-function study. Just like δ-toxin, PSMα and PSMβ are agr-dependently expressed. It recently was shown that the staphylococcal agr system is confinement induced and thus comprises not only a quorum sensing system but also a diffusion sensing system active at the single cell level. δ-Toxin and PSMs are hence produced upon phagosomal confinement and thus also low numbers of endocytosed staphy-lococci should be able to mount a toxin response in order to avoid lysosomal killing. Whereas gain of function assays demonstrated PSMβ activity in phagosomal escape, in vivo studies suggests a prominent role of PSMα, with the third ORF of the operon, PSMα3, being the most virulent principle. Despite these incongruities a common theme emerges: amphiphilic PSMs are involved in phagosomal escape. One possibility to explain the observed differences is the postu-lation of alternative pathways of phagosomal escape mechanisms for S. aureus.

Molecular patterns of pathogens that reside in the cytoplasm of their hosts are detected by nucleotide-binding and oligomerization domain proteins NOD1 and NOD2, which detect γ-D-glutamyl-diaminopimelic acid and muramyl dipeptide, pep-tidoglycan components of Gram-negative and Gram-positive bacteria. Peptidoglycan binding leads to a conformation change in NOD proteins, which initiates the recruitment of ubiquitin lig-ases and kinases and ultimately results in nuclear translocation of NFκB and activator protein 1 and expression of inflammatory genes (reviewed in ). NOD2 signaling upon S. aureus infection has been found to induce cytokine production and thus might contribute to induction of inflammation, e.g., in the lung (; Figure 1; Map Item 6). NOD2-deficient mice exhibit a delayed inflammatory response and impaired bacterial clearance after infection with S. aureus. α-Toxin facilitates NOD2-dependent recognition of S. aureus muramyl dipeptide, possibly by interfering with phagosomal integrity.

The observation that S. aureus can translocate into the cytoplasm of host cells and grow without an immediately ensuing cell death (e.g., ) illustrates that phagosomal escape is not identical with cytotoxicity Thus, the link between phagosomal escape and host cell death still needs to be elucidated.

Staphylococcus aureus-INDUCED HOST CELL DEATH

The classical separation of host cell death into programed cell death (PCD; apoptosis) and accidental cell death or necrosis has long been superseded after the identifying a large variety of cell death mechanisms (for a reviews, see;; ). Many of which are defined by key factors that allow the assessment of death pathway activation following bacterial infection (e.g., reviewed in ), although the synchronous activity of virulence factors from the staphylococcal arsenal renders unequivocal correlations between toxin and associated mode of cell death a daunting task. When virulent S. aureus strains are added to host cells in tissue culture, host cell death occurs via mechanisms that have been mainly identified as apoptotic (;,;,;;;;;; Figure 1, Map Item 7). α-Toxin is both required and sufficient for induction of leukocyte cell death, either apoptotic or necrotic. Leukocytes are sensitive to staphylococcal α-toxin. Already low toxin doses induce apoptosis accompanied by a breakdown of the mitochondrial transmembrane potential. A recent study suggests that caspase-2 acts as an initiator caspase during cell death of non-professional phagocytes. Caspase 2 was induced by potassium efflux due to pore-forming toxins such as staphylococcal alpha-toxin and aerolysin. By contrast, high doses induce necrotic cell death. Human endothelial cells are virtually insensitive to the action of S. aureus α-toxin, however, comparatively low numbers of S. aureus cells with a combined invasive and strongly hemolytic phenotype readily induce apoptotic cell death in HUVEC. This suggests that cell death mechanisms are activated from within their intracellular location. The effect is highly specific, since fixed, non-hemolytic, rifampin-treated or weakly invasive staphylococci are not cytotoxic toward endothelial cells. Multiple other studies indicate that S. aureus might kill its other types of host cells from within. The virulence factors required for S. aureus-induced apoptosis in endothelial cells depend on agr and the alternative stress–response sigma-factor σB, but mainly seem to be independent of SarA - although there are contradicting results on the involvement of SarA.

Phage-encoded Panton-Valentine leukocidin (PVL) predominantly destroys leukocytes, although there also is some species specificity for human and rabbit PMN. In PMN, PVL induced a rapid caspase-9/3-dependent cell death in vitro. The authors further identified to a mitochondrial localization of the PVL toxin. Isolated mitochondria were permeabilized for pro-apoptotic factors such as cytochrome c (CytC) by PVL which suggested that PVL is able to create pores in the mitochondrial outer membrane and thus triggers a Bax-independent mitochondrial pathway of host cell apoptosis (; Figure 1, Map Item 8). During the intrinsic pathway of apoptosis release of CytC from injured mitochondria leads to activation of apoptosis-activating factor-1 (APAF-1). Oligomerizing CytC/APAF-1 recruits and subsequently activates pro-caspase 9. Caspase 9 then proteolytically activates effector caspases, which finally cleave their respective substrates resulting in membrane blebbing, and DNA fragmentation (reviewed in ). Similarly, α-toxin has been described to activate caspases via the intrinsic death pathway independently of death receptor signaling (CD95/Fas/APO-1). Bcl-2 overexpressing Jurkat cells were protected from α-toxin mediated cell death although recent result suggest that the function of Bcl-2 in autophagy might be responsible for the observed phenomena.

Interestingly, S. aureus also seems to be able to exert anti-apoptotic host cell responses. The pathogen was shown to suppress staurosporine-induced apoptosis in hMDM although early apoptotic features such as phosphatidylserine display at the outer plasma membrane leaflet, reduced mitochondrial membrane potential, CytC release, and caspase-3 activation are still observed. S. aureus infection strongly upregulated the expression of mitochondrial membrane potential stabilizing Bcl-2 and Mcl-1 gene products. Since also heat-killed S. aureus was able to suppress apoptosis in the host cells staphylococcal products such as lipoteichoic acid or peptidoglycan might activate the macrophages through intracellular pattern recognition sensors such as nucleotide oligomerization domain receptors (NOD;; ).

Aside from apoptosis S. aureus is also able to induce pyronecrosis (Figure 1; Map Item 9). There, caspase-1 is activated as part of an inflammasome, which further consists of NOD-like receptor protein 3 (NLRP3) and the adaptor protein, apoptosis-associated speck-like protein containing a caspase-associated recruitment domain (ASC). S. aureus can function as a stimulus for NLRP3, however, the molecular identity of the stimulating signal is not known thus far. Lysosomal permeabilization is one NLRP3-activating principle, wherein release of the lysosomal protease cathepsin B into the cytoplasm contributes to NLRP3 activation (reviewed in; ). Thus, it seems likely, that lysosomal rupture or permeabilization by S. aureus toxins releases cathepsin which then activates the inflammasome. Indeed staphylococcal α, β, and γ-hemolysins have been shown to be important activation of the NLRP3 inflammasome. The pore-forming α-and γ-toxins of S. aureus permeabilize membranes and thus might be involved in cathepsin release and subsequent inflammasome activation. α-Toxin further is known to permeabilize the plasma membrane for potassium ions. In turn, potassium efflux activates the inflammasome. β-Toxin has been shown to be involved in phagosomal escape and thus also might act in cathepsin release.

Staphylococcus aureus AND THE SUBVERSION OF AUTOPHAGY

Autophagy sequesters cytoplasmic contents via an isolation membrane. Engulfment of cargo by the so-called phagophore forms double membrane-bound autophagic vesicles that eventually fuse with lysosomes to yield autolysosomes. Autophagy serves for degradation of organelles or self-digestion during nutrient limiting conditions such as starvation and is generally thought to constitute a cellular survival mechanism. During bacterial infections autophagy disposes of leaky vesicles or intracellular bacteria, however, bacterial pathogens have found multiple ways to subvert autophagy (reviewed in;;;;; ).

Staphylococcus aureus was shown to interact with autophagosomes in a rather unique way when compared to autophagy-subvertive strategies of other bacterial pathogens. S. aureus inhibits fusion of phagosomes with lysosomes. It permeabilizes HeLa phagosomes by a mechanism dependent on Staphylococcus-secreted toxins. The leaky phagosomes are targeted by autophagy and within autophagosomes S. aureus replicates. Eventually the bacteria escape from their intracellular confinement into the host cell cytoplasm in an agr-dependent manner (; Figure 1, Map Item 9). Finally, host cell death is induced, which is independent of a caspase activation cascade but was blocked by overexpression of anti-autophagic Bcl-2. Induction of autophagy by rapamycin resulted in an increased number of recovered colony-forming units, whereas inhibition with wortmann in reduced the colonies recovered from the intracellular environment. S. aureus-induced autophagy resulted in a vacuolization of the host cell cytoplasm (“Swiss cheese phenotype”). agr-deficient S. aureus fail to induce autophagy, which results in maturation of bacteria-containing phagosomes followed by lysosomal degradation of the pathogens. α-Toxin is able to permeabilize membranes for Ca2+, an inducer of autophagy and autophagy targets phagosomes perforated by α-toxin in Chinese hamster ovary cells. Whereas latter observation is in line with the results obtained by it contrasts findings that α-toxin is not sufficient to permeabilize HeLa phagosomes.

CONCLUSION

With about 200–300 virulence factors, S. aureus is able to exert a multitude of effects upon its eukaryotic host cells. Although many details have emerged through ground-breaking and recent research, only a minority of pathogenicity factors of S. aureus has been functionally annotated to date. Particularly the assessment of intracellular staphylococcal virulence is often hampered by the difficulty to discriminate between toxin effects that result from extracellular or intracellular bacteria, although inducible toxin-expressing might provide valuable tools for molecular dissection of host–pathogen interactions.

With our advancing knowledge of cell death mechanisms ground-breaking experiments will have to be re-evaluated in order to understand the mechanisms of S. aureus-induced host cell killing. When comparing experimental research originating from different labs the influence of a body of factors should be taken into account that could lead to different infection outcomes:

Staphylococcus aureus strain used for infection, its growth phase at the time of infection (and hence the bacterial growth medium), as well as MOI are important, whereas on the host side the cell type and hence the protein profile will drastically influence infection outcome by altering host cell susceptibility to bacterial toxins, response to pathogen-associated molecular patterns, expression of receptors, caspases, and other host factors.

In order to identify activities of single toxins or virulence factors gain-of-function studies can be useful, e.g., using the a pathogenic S. carnosus as toxin delivery vehicle. However, such strategies will not easily identify pathways during which an orchestrated interplay of multiple virulence factors is required. However, novel high-throughput sequencing technologies of transposon insertions open up new possibilities for analysis of genome-wide mutant libraries of clinically relevant strains. Using such novel tools we will be able to address a lot of open questions with regard to intracellular staphylococcal infections: do different adhesins result in employment of different uptake mechanisms into non-professional phagocytes as these would subsequently result in different infection outcomes? What is the nature of tight and spacious vacuoles that are occupied by, for example, sarA- and sarA+ S. aureus, respectively? Which alternative pathways for phagosomal escape do exist? Which modes of cell death are activated by a single strain in different host cell types or different strains in a single host cell line? There is still a lot to learn about the versatile facultative intracellular pathogen, Staphylococcus aureus.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References 135

  1. 1.

    Aarestrup F. M. Larsen H. D. Eriksen N. H. Elsberg C. S. Jensen N. E. (1999 ). Frequency of alpha- and beta-haemolysin in Staphylococcus aureus of bovine and human origin. A comparison between pheno- and genotype and variation in phenotypic expression. APMIS 107 425–430

    Not in our library

  2. 2.

    Abdelzaher A. M. Wright M. E. Ortega C. Solo-Gabriele H. M. Miller G. Elmir S. Newman X. Shih P. Bonilla J. A. Bonilla T. D. Palmer C. J. Scott T. Lukasik J. Harwood V. J. Mcquaig S. Sinigalliano C, Gidley, M. Plano L. R. Zhu X. Wang J. D. Fleming L. E. (2010 ). Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach. Appl. Environ. Microbiol. 76 724–732

    Not in our library10.1128/aem.02127-09

  3. 3.

    Agerer F. Lux S. Michel A. Rohde M. Ohlsen K. Hauck C. R. (2005 ). Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J. Cell Sci. 118 2189–2200

    Not in our library10.1242/jcs.02328

  4. 4.

    Agerer F. Michel A. Ohlsen K. Hauck C. R. (2003 ). Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J. Biol. Chem. 278 42524–42531

    Not in our library10.1074/jbc.m302096200

  5. 5.

    Ahmed S. Meghji S. Williams R. J. Henderson B. Brock J. H. Nair S. P. (2001 ). Staphylococcus aureus fibronectin binding proteins are essential for internalization by osteoblasts but do not account for differences in intracellular levels of bacteria. Infect Immun. 69 2872–2877

    Not in our library10.1128/iai.69.5.2872-2877.2001

  6. 6.

    Balaban N. Novick R. P. (1995 ). Translation of RNAIII, the Staphylococcus aureus agr regulatory RNA molecule, can be activated by a 3′-end deletion. FEMS Microbiol Lett. 133 155–161

    Not in our library10.1111/j.1574-6968.1995.tb07877.x

  7. 7.

    Bantel H. Sinha B. Domschke W. Peters G. Schulze-Osthoff K. Janicke R. U. (2001 ). alpha-Toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J. Cell Biol. 155 637–648

    Not in our library10.1083/jcb.200105081

  8. 8.

    Bayles K. W. Wesson C. A. Liou L. E. Fox L. K. Bohach G. A. Trumble W. R. (1998 ). Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect. Immun. 66 336–342

    Not in our library10.1128/iai.66.1.336-342.1998

  9. 9.

    Bergsbaken T. Fink S. L. Cookson B. T. (2009 ). Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7 99–109

    Not in our library10.1038/nrmicro2070

  10. 10.

    Bhakdi S. Bayley H. Valeva A. Walev I. Walker B. Kehoe M. Palmer M. (1996 ). Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch. Microbiol. 165 73–79

    Not in our library10.1007/s002030050300

  11. 11.

    Bhakdi S. Tranum-Jensen J. (1991 ). Alpha-toxin of Staphylococcus aureus. Microbiol. Rev. 55 733–751

    Not in our library10.1128/mr.55.4.733-751.1991

  12. 12.

    Bingham R. J. Rudino-Pinera E. Meenan N. A. Schwarz-Linek U. Turkenburg J. P. Hook M. Garman E. F. Potts J. R. (2008 ). Crystal structures of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains. Proc. Natl. Acad. Sci. U.S.A. 105 12254–12258

    Not in our library10.1073/pnas.0803556105

  13. 13.

    Birmingham C. L. Canadien V. Kaniuk N. A. Steinberg B. E. Higgins D. E. Brumell J. H. (2008 ). Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 451 350–354

    Not in our library10.1038/nature06479

  14. 14.

    Brady N. R. Hamacher-Brady A. Yuan H. Gottlieb R. A. (2007 ). The autophagic response to nutrient deprivation in the hl-1 cardiac myocyte is modulated by Bcl-2 and sarco/endoplasmic reticulum calcium stores. FEBS J. 274 3184–3197

    Not in our library10.1111/j.1742-4658.2007.05849.x

  15. 15.

    Buisman H. P. Buys L. F. Langermans J. A. Van Den Broek P. J. Van Furth R. (1991 ). Effect of probenecid on phagocytosis and intracellular killing of Staphylococcus aureus and Escherichia coli by human monocytes and granulocytes. Immunology 74 338–341

    Not in our library

  16. 16.

    Bulger R. J. Bulger R. E. (1967 ). Ultra structure of small colony variants of a methicillin-resistant Staphylococcus aureus. J. Bacteriol. 94 1244–1246

    Not in our library10.1128/jb.94.4.1244-1246.1967

  17. 17.

    Campoy E. Colombo M. I. (2009 ). Autophagy in intracellular bacterial infection. Biochim. Biophys. Acta 1793 1465–1477

    Not in our library10.1016/j.bbamcr.2009.03.003

  18. 18.

    Carnes E. C. Lopez D. M. Donegan N. P. Cheung A. Gresham H. Timmins G. S. Brinker C. J. (2009 ). Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat. Chem. Biol. 6 41–45

    Not in our library10.1038/nchembio.264

  19. 19.

    Chatterjee I. Kriegeskorte A. Fischer A. Deiwick S. Theimann N. Proctor R. A. Peters G. Herrmann M. Kahl B. C. (2008 ). In vivo mutations of thymidylate synthase (encoded by thyA) are responsible for thymidine dependency in clinical small-colony variants of Staphylococcus aureus. J. Bacteriol. 190 834–842

    Not in our library10.1128/jb.00912-07

  20. 20.
    Staphylococcus aureus Protein A Binds to Osteoblasts and Triggers Signals That Weaken Bone in Osteomyelitis · 2011
    No notice
  21. 21.
    Staphylococcus aureus α-Hemolysin Activates the NLRP3-Inflammasome in Human and Mouse Monocytic Cells · 2009
    No notice
  22. 22.

    Diep B. A. Gill S. R. Chang R. F. Phan T. H. Chen J. H. Davidson M. G. Lin F. Lin J. Carleton H. A. Mongodin E. F. Sensabaugh G. F. Perdreau-Remington F. (2006 ). Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367 731–739

    Not in our library10.1016/s0140-6736(06)68231-7

  23. 23.

    Dorn B. R. Dunn W. A. Jr. Progulske-Fox A. (2002 ). Bacterial interactions with the autophagic pathway. Cell. Microbiol. 4 1–10

    Not in our library10.1046/j.1462-5822.2002.00164.x

  24. 24.

    Dramsi S. Cossart P. (2002 ). Listeriolysin O: a genuine cytolysin optimized for an intracellular parasite. J. Cell Biol. 156 943–946

    Not in our library10.1083/jcb.200202121

  25. 25.

    Dziewanowska K. Carson A. R. Patti J. M. Deobald C. F. Bayles K. W. Bohach G. A. (2000 ). Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins: role in internalization by epithelial cells. Infect. Immun. 68 6321–6328

    Not in our library10.1128/iai.68.11.6321-6328.2000

  26. 26.

    Dziewanowska K. Patti J. M. Deobald C. F. Bayles K. W. Trumble W. R. Bohach G. A. (1999 ). Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect. Immun. 67 4673–4678

    Not in our library10.1128/iai.67.9.4673-4678.1999

  27. 27.

    Edwards A. M. Potter U. Meenan N. A. Potts J. R. Massey R. C. (2011 ). Staphylococcus aureus keratinocyte invasionisdependent upon multiple high-affinity fibronectin-binding repeats within FnBPA. PLoS ONE 6 e18899

    Not in our library

  28. 28.
    Staphylococcus aureus Host Cell Invasion and Virulence in Sepsis Is Facilitated by the Multiple Repeats within FnBPA · 2010
    No notice
  29. 29.

    Ellington J. K. Elhofy A. Bost K. L. Hudson M. C. (2001 ). Involvement of mitogen-activated protein kinase pathways in Staphylococcus aureus invasion of normal osteoblasts. Infect. Immun. 69 5235–5242

    Not in our library10.1128/iai.69.9.5235-5242.2001

  30. 30.

    Essmann F. Bantel H. Totzke G. Engels I. H. Sinha B. Schulze-Osthoff K. Janicke R. U. (2003 ). Staphylococcus aureus alpha-toxin-induced cell death: predominant necrosis despite apoptotic caspase activation. Cell Death Differ. 10 1260–1272

    Not in our library10.1038/sj.cdd.4401301

  31. 31.

    Fowler T. Wann E. R. Joh D. Johansson S. Foster T. J. Hook M. (2000 ). Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur. J. Cell Biol. 79 672–679

    Not in our library10.1078/0171-9335-00104

  32. 32.
    A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells · 2007
    No notice
  33. 33.

    Garzoni C. Kelley W. L. (2009 ). Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol. 17 59–65

    Not in our library10.1016/j.tim.2008.11.005

  34. 34.

    Gawronski J. D. Wong S. M. Giannoukos G. Ward D. V. Akerley B. J. (2009 ). Tracking insertion mutants within libraries by deep sequencing and a genome-wide screen for Haemophilus genes required in the lung. Proc. Natl. Acad. Sci. U.S.A. 106 16422–16427

    Not in our library10.1073/pnas.0906627106

  35. 35.

    Genestier A. L. Michallet M. C. Prévost G. Bellot G. Chalabreysse L. Peyrol S. Thivolet F. Etienne J. Lina G. Vallette F. M. Vandenesch F. Genestier L. (2005 ). Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J. Clin. Invest. 115 3117–3127

    Not in our library10.1172/jci22684

  36. 36.

    Giese B. Dittmann S. Paprotka K. Levin K. Weltrowski A. Biehler D. Lam T. T. Sinha B. Fraunholz M. J. (2009 ). Staphylococcal alpha-toxin is not sufficient to mediate escape from phagolysosomes in upper-airway epithelial cells. Infect. Immun. 77 3611–3625

    Not in our library10.1128/iai.01478-08

  37. 37.

    Giese B. Glowinski F. Paprotka K. Dittmann S. Steiner T. Sinha B. Fraunholz M. J. (2011 ). Expression of delta-toxin by Staphylococcus aureus mediates escape from phago-endosomes of human epithelial and endothelial cells in the presence of beta-toxin. Cell. Microbiol. 13 316–329

    Not in our library10.1111/j.1462-5822.2010.01538.x

  38. 38.

    Goerke C. Pantucek R. Holtfreter S. Schulte B. Zink M. Grumann D. Broker B. M. Doskar J. Wolz C. (2009 ). Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J. Bacteriol. 191 3462–3468

    Not in our library10.1128/jb.01804-08

  39. 39.

    Gomez M. I. Prince A. (2008 ). Airway epithelial cell signaling in response to bacterial pathogens. Pediatr. Pulmonol. 43 11–19

    Not in our library10.1002/ppul.20735

  40. 40.

    Gresham H. D. Lowrance J. H. Caver T. E. Wilson B. S. Cheung A. L. Lindberg F. P. (2000 ). Survival of Staphylococcus aureus inside neutrophils contributes to infection 1. J. Immunol. 164 3713–3722

    Not in our library10.4049/jimmunol.164.7.3713

  41. 41.

    Haim M. Trost A. Maier C. J. Achatz G. Feichtner S. Hintner H. Bauer J. W. Onder K. (2010 ). Cytokeratin 8 interacts with clumping factor B: a new possible virulence factor target. Microbiology 156 3710–3721

    Not in our library10.1099/mic.0.034413-0

  42. 42.

    Hakansson A. Bentley C. C. Shakhnovic E. A. Wessels M. R. (2005 ). Cytolysin-dependent evasion of lysosomal killing. Proc. Natl. Acad. Sci. U.S.A. 102 5192–5197

    Not in our library10.1073/pnas.0408721102

  43. 43.

    Hamill R. J. Vann J. M. Proctor R. A. (1986 ). Phagocytosis of Staphylococcus aureus by cultured bovine aortic endothelial cells: model for postadherence events in endovascular infections. Infect. Immun. 54 833–836

    Not in our library10.1128/iai.54.3.833-836.1986

  44. 44.

    Harraghy N. Hussain M. Haggar A. Chavakis T. Sinha B. Herrmann M. Flock J. I. (2003 ). The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology 149 2701–2707

    Not in our library10.1099/mic.0.26465-0

  45. 45.

    Haslinger-Löffler B. Kahl B. C. Grundmeier M. Strangfeld K. Wagner B. Fischer U. Cheung A. L. Peters G. Schulze-Osthoff K. Sinha B. (2005 ). Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell. Microbiol. 7 1087–1097

    Not in our library10.1111/j.1462-5822.2005.00533.x

  46. 46.

    Haslinger B. Strangfeld K. Peters G. Schulze-Osthoff K. Sinha B. (2003 ). Staphylococcus aureus alpha-toxin induces apoptosis in peripheral blood mononuclear cells: role of endogenous tumour necrosis factor-alpha and the mitochondrial death pathway. Cell. Microbiol. 5 729–741

    Not in our library10.1046/j.1462-5822.2003.00317.x

  47. 47.

    Hiemstra P. S. Annema A. Schippers E. F. Van Furth R. (1992 ). Pertussis toxin partially inhibits phagocytosis of immunoglobulin G-opsonized Staphylococcus aureus by human granulocytes but does not affect intracellular killing. Infect. Immun. 60 202–205

    Not in our library10.1128/iai.60.1.202-205.1992

  48. 48.

    Hirschhausen N. Schlesier T. Schmidt M. A. Gotz F. Peters G. Heilmann C. (2010 ). A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell. Microbiol. 12 1746–1764

    Not in our library10.1111/j.1462-5822.2010.01506.x

  49. 49.

    Horsburgh M. J. Aish J. L. White I. J. Shaw L. Lithgow J. K. Foster S. J. (2002 ). sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184 5457–5467

    Not in our library10.1128/jb.184.19.5457-5467.2002

  50. 50.

    Hruz P. Zinkernagel A. S. Jenikova G. Botwin G. J. Hugot J. P. Karin M. Nizet V. Eckmann L. (2009 ). NOD2 contributes to cutaneous defense against Staphylococcus aureus through alpha-toxin-dependent innate immune activation. Proc. Natl. Acad. Sci. U.S.A. 106 12873–12878

    Not in our library10.1073/pnas.0904958106

  51. 51.

    Husmann M. Beckmann E. Boller K. Kloft N. Tenzer S. Bobkiewicz W. Neukirch C. Bayley H. Bhakdi S. (2009 ). Elimination of a bacterial pore-forming toxin by sequential endocytosis and exocytosis. FEBS Lett. 583 337–344

    Not in our library10.1016/j.febslet.2008.12.028

  52. 52.

    Inoshima I. Inoshima N. Wilke G. A. Powers M. E. Frank K. M. Wang Y. Bubeck Wardenburg J. (2011 ). A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat. Med. 17 1310–1314

    Not in our library10.1038/nm.2451

  53. 53.

    Imre G. Heering J. Takeda A. N. Husmann M. Thiede B. zu Heringdorf D. M. Green D. R. der Goot F. G. Sinha B. Dötsch V. Rajalingam K. (2012 ). Caspase-2 is an initiator caspase responsible for pore-forming toxin-mediated apoptosis. EMBO J. (in press)

    Not in our library10.1038/emboj.2012.93

  54. 54.

    Jarry T. M. Cheung A. L. (2006 ). Staphylococcus aureus escapes more efficiently from the phagosome of a cystic fibrosis bronchial epithelial cell line than from its normal counterpart. Infect. Immun. 74 2568–2577

    Not in our library10.1128/iai.74.5.2568-2577.2006

  55. 55.

    Jarry T. M. Memmi G. Cheung A. L. (2008 ). The expression of alpha-haemolysin is required for Staphylococcus aureus phagosomal escape after internalization in CFT-1 cells. Cell. Microbiol. 10 1801–1814

    Not in our library10.1111/j.1462-5822.2008.01166.x

  56. 56.

    Jevon M. Guo C. Ma B. Mordan N. Nair S. P. Harris M. Henderson B. Bentley G. Meghji S. (1999 ). Mechanisms of internalization of Staphylococcus aureus by cultured human osteoblasts. Infect. Immun. 67 2677–2681

    Not in our library10.1128/iai.67.5.2677-2681.1999

  57. 57.

    Kahl B. C. Goulian M. Van Wamel W. Herrmann M. Simon S. M. Kaplan G. Peters G. Cheung A. L. (2000 ). Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line. Infect. Immun. 68 5385–5392

    Not in our library10.1128/iai.68.9.5385-5392.2000

  58. 58.

    Kapetanovic R. Nahori M. A. Balloy V. Fitting C. Philpott D. J. Cavaillon J. M. Adib-Conquy M. (2007 ). Contribution of phagocytosis and intracellular sensing for cytokine production by Staphylococcus aureus-activated macrophages. Infect. Immun. 75 830–837

    Not in our library10.1128/iai.01199-06

  59. 59.

    Kapral F. A. (1976 ). Effect of fatty acids on Staphylococcus aureus delta-toxin hemolytic activity. Infect. Immun. 13 114–119

    Not in our library10.1128/iai.13.1.114-119.1976

  60. 60.

    Kebaier C. Chamberland R. R. Allen I. C. Gao X. Broglie P. M. Hall J. D. Jania C. Doerschuk C. M. Tilley S. L. Duncan J. A. (2012 ). Staphylococcus aureus alpha-hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J. Infect. Dis. 205 807–817

    Not in our library10.1093/infdis/jir846

  61. 61.

    Kerdudou S. Laschke M. W. Sinha B. Preissner K. T. Menger M. D. Herrmann M. (2006 ). Fibronectin binding proteins contribute to the adherence of Staphylococcus aureus to intact endothelium in vivo. Thromb. Haemost. 96 183–189

    Not in our library

  62. 62.

    Kintarak S. Whawell S. A. Speight P. M. Packer S. Nair S. P. (2004 ). Internalization of Staphylococcus aureus by human keratinocytes. Infect. Immun. 72 5668–5675

    Not in our library10.1128/iai.72.10.5668-5675.2004

  63. 63.

    Kipp F. Ziebuhr W. Becker K. Krimmer V. Hobeta N. Peters G. von Eiff C. (2003 ). Detection of Staphylococcus aureus by 16S rRNA directed in situ hybridisation in a patient with a brain abscess caused by small colony variants. J. Neurol. Neurosurg. Psychiatry 74 1000–1002

    Not in our library10.1136/jnnp.74.7.1000

  64. 64.

    Kirkegaard K. Taylor M. P. Jackson W. T. (2004 ). Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat. Rev. Microbiol. 2 301–314

    Not in our library10.1038/nrmicro865

  65. 65.
    Phagocytosis of Staphylococcus aureus by Macrophages Exerts Cytoprotective Effects Manifested by the Upregulation of Antiapoptotic Factors · 2009
    No notice
  66. 66.

    Kreger A. S. Bernheimer A. W. (1971 ). Disruption of bacterial protoplasts and spheroplasts by staphylococcal delta hemolysin. Infect. Immun. 3 603–605

    Not in our library10.1128/iai.3.4.603-605.1971

  67. 67.

    Kreger A. S. Kim K. S. Zaboretzky F. Bernheimer A. W. (1971 ). Purification and properties of staphylococcal delta hemolysin. Infect. Immun. 3 449–465

    Not in our library10.1128/iai.3.3.449-465.1971

  68. 68.

    Kriegeskorte A. Konig S. Sander G. Pirkl A. Mahabir E. Proctor R. A. von Eiff C. Peters G. Becker K. (2011 ). Small colony variants of Staphylococcus aureus reveal distinct protein profiles. Proteomics 11 2476–2490

    Not in our library10.1002/pmic.201000796

  69. 69.

    Krut O. Utermohlen O. Schlossherr X. Kronke M. (2003 ). Strain-specific association of cytotoxic activity and virulence of clinical Staphylococcus aureus isolates. Infect. Immun. 71 2716–2723

    Not in our library10.1128/iai.71.5.2716-2723.2003

  70. 70.
    A Potential New Pathway for Staphylococcus aureus Dissemination: The Silent Survival of S. aureus Phagocytosed by Human Monocyte-Derived Macrophages · 2008
    No notice
  71. 71.

    Lám T. T. Giese B. Chikkaballi D. Kuhn A. Wolber W. Pané-Farré J. Schäfer D. Engelmann S. Fraunholz M. Sinha B. (2010 ). Phagolysosomal integrity is generally maintained after Staphylococcus aureus invasion of nonprofessional phagocytes but is modulated by strain 6850. Infect. Immun. 78 3392–3403

    Not in our library10.1128/iai.00012-10

  72. 72.

    Lammers A. Nuijten P. J. M. Smith H. E. (1999 ). The fibronectin binding proteins of Staphylococcus aureus are required for adhesion to and invasion of bovine mammary gland cells. FEMS Microbiol. Lett. 180 103–109

    Not in our library10.1111/j.1574-6968.1999.tb08783.x

  73. 73.

    Laschke M. W. Kerdudou S. Herrmann M. Menger M. D. (2005 ). Intravital fluorescence microscopy: a novel tool for the study of the interaction of Staphylococcus aureus with the microvascular endothelium in vivo. J. Infect. Dis. 191 435–443

    Not in our library10.1086/427193

  74. 74.

    Levine B. (2005 ). Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120 159–162

    Not in our library10.1016/j.cell.2005.01.005

  75. 75.

    Li M. Rigby K. Lai Y. Nair V. Peschel A. Schittek B. Otto M. (2009 ). Staphylococcus aureus mutant screen reveals interaction of the human antimicrobial peptide dermcidin with membrane phospholipids. Antimicrob. Agents Chemother. 53 4200–4210

    Not in our library10.1128/aac.00428-09

  76. 76.
    Staphylococcus aureus Panton-Valentine Leukocidin Is a Very Potent Cytotoxic Factor for Human Neutrophils · 2010
    No notice
  77. 77.

    Lowy F. D. Fant J. Higgins L. L. Ogawa S. K. Hatcher V. B. (1988 ). Staphylococcus aureus – human endothelial cell interactions. J. Ultrastruct. Mol. Struct. Res. 98 137–146

    Not in our library10.1016/s0889-1605(88)80906-6

  78. 78.

    Mariathasan S. Weiss D. S. Newton K. Mcbride J. O’Rourke K. Roose-Girma M. Lee W. P. Weinrauch Y. Monack D. M. Dixit V. M. (2006 ). Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440 228–232

    Not in our library10.1038/nature04515

  79. 79.

    Menzies B. E. Kourteva I. (1998 ). Internalization of Staphylococcus aureus by endothelial cells induces apoptosis. Infect. Immun. 66 5994–5998

    Not in our library10.1128/iai.66.12.5994-5998.1998

  80. 80.

    Menzies B. E. Kourteva I. (2000 ). Staphylococcus aureus alpha-toxin induces apoptosis in endothelial cells. FEMS Immunol. Med. Microbiol. 29 39–45

    Not in our library10.1111/j.1574-695x.2000.tb01503.x

  81. 81.

    Mestre M. B. Fader C. M. Sola C. Colombo M. I. (2010 ). Alpha-hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus-infected cells. Autophagy 6 110–125

    Not in our library10.4161/auto.6.1.10698

  82. 82.

    Mohammed K. A. Nasreen N. Antony V. B. (2007 ). Bacterial induction of early response genes and activation of proapoptotic factors in pleural mesothelial cells. Lung 185 355–365

    Not in our library10.1007/s00408-007-9046-6

  83. 83.

    Moisan H. Brouillette E. Jacob C. L. Langlois-Begin P. Michaud S. Malouin F. (2006 ). Transcription of virulence factors in Staphylococcus aureus small-colony variants isolated from cystic fibrosis patients is influenced by SigB. J. Bacteriol. 188 64–76

    Not in our library10.1128/jb.188.1.64-76.2006

  84. 84.

    Munoz-Planillo R. Franchi L. Miller L. S. Nunez G. (2009 ). A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome. J. Immunol. 183 3942–3948

    Not in our library10.4049/jimmunol.0900729

  85. 85.

    Nuzzo I. Sanges M. R. Folgore A. Carratelli C. R. (2000 ). Apoptosis of human keratinocytes after bacterial invasion. FEMS Immunol. Med. Microbiol. 27 235–240

    Not in our library10.1111/j.1574-695x.2000.tb01435.x

  86. 86.

    O’Brien L. M. Walsh E. J. Massey R. C. Peacock S. J. Foster T. J. (2002 ). Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell. Microbiol. 4 759–770

    Not in our library10.1046/j.1462-5822.2002.00231.x

  87. 87.

    Ogawa M. Mimuro H. Yoshikawa Y. Ashida H. Sasakawa C. (2011 ). Manipulation of autophagy by bacteria for their own benefit. Microbiol. Immunol. 55 459–471

    Not in our library10.1111/j.1348-0421.2011.00343.x

  88. 88.

    Olivier A. C. Lemaire S. Van Bambeke F. Tulkens P. M. Oldfield E. (2009 ). Role of rsbU and staphyloxanthin in phagocytosis and intracellular growth of Staphylococcus aureus in human macrophages and endothelial cells. J. Infect. Dis. 200 1367–1370

    Not in our library10.1086/606012

  89. 89.

    Orvedahl A. Levine B. (2009 ). Eating the enemy within: autophagy in infectious diseases. Cell Death Differ. 16 57–69

    Not in our library10.1038/cdd.2008.130

  90. 90.

    Otto M. O’Mahoney D. S. Guina T. Klebanoff S. J. (2004 ). Activity of Staphylococcus epidermidis phenol-soluble modulin peptides expressed in Staphylococcus carnosus. J. Infect. Dis. 190 748–755

    Not in our library10.1086/422157

  91. 91.

    Oviedo-Boyso J. Cortes-Vieyra R. Huante-Mendoza A. Yu H. B. Valdez-Alarcon J. J. Bravo-Patino A. Cajero-Juarez M. Finlay B. B. Baizabal-Aguirre V. M. (2011 ). The phosphoinositide-3-kinase-Akt signaling pathway is important for Staphylococcus aureus internalization by endothelial cells. Infect. Immun. 79 4569–4577

    Not in our library10.1128/iai.05303-11

  92. 92.

    Pang Y. Y. Schwartz J. Thoendel M. Ackermann L. W. Horswill A. R. Nauseef W. M. (2010 ). agr-Dependent interactions of Staphylococcus aureus USA300 with human polymorphonuclear neutrophils. J. Innate Immun. 2 546–559

    Not in our library10.1159/000319855

  93. 93.

    Peacock S. J. Foster T. J. Cameron B. J. Berendt A. R. (1999 ). Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology 145(Pt. 12) 3477–3486

    Not in our library10.1099/00221287-145-12-3477

  94. 94.

    Petrilli V. Papin S. Dostert C. Mayor A. Martinon F. Tschopp J. (2007 ). Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 14 1583–1589

    Not in our library10.1038/sj.cdd.4402195

  95. 95.

    Pokorny A. Yandek L. E. Elegbede A. I. Hinderliter A. Almeida P. F. (2006 ). Temperature and composition dependence of the interaction of delta-lysin with ternary mixtures of sphingomyelin/cholesterol/POPC. Biophys. J. 91 2184–2197

    Not in our library10.1529/biophysj.106.085027

  96. 96.

    Proctor R. A. Balwit J. M. Vesga O. (1994 ). Variant subpopulations of Staphylococcus aureus as cause of persistent and recurrent infections. Infect. Agents Dis. 3 302–312

    Not in our library

  97. 97.

    Proctor R. A. Van Langevelde P. Kristjansson M. Maslow J. N. Arbeit R. D. (1995 ). Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin. Infect. Dis. 20 95–102

    Not in our library10.1093/clinids/20.1.95

  98. 98.

    Qazi S. N. A. Counil E. Morrissey J. Rees C. E. D. Cockayne A. Winzer K. Chan W. C. Williams P. Hill P. J. (2001 ). agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect. Immun. 69 7074–7082

    Not in our library10.1128/iai.69.11.7074-7082.2001

  99. 99.

    Rahal J. J. Jr. (1972 ). Comparative effects of purified staphylococcal alpha and delta toxins on mitochondrial metabolism. J. Infect. Dis. 126 96–103

    Not in our library10.1093/infdis/126.1.96

  100. 100.

    Rudel T. Kepp O. Kozjak-Pavlovic V. (2010 ). Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat. Rev. Microbiol. 8 693–705

    Not in our library10.1038/nrmicro2421

  101. 101.

    Rudino-Pinera E. Schwarz-Linek U. Potts J. R. Garman E. F. (2004 ). Twinned or not twinned, that is the question: crystallization and preliminary crystallographic analysis of the 2F1(3)F1 module pair of human fibronectin. Acta Crystallogr. D Biol. Crystallogr. 60 1341–1345

    Not in our library10.1107/s0907444904011473

  102. 102.

    Schnaith A. Kashkar H. Leggio S. A. Addicks K. Krönke M. Krut O. (2007 ). Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J. Biol. Chem. 282 2695–2706

    Not in our library10.1074/jbc.m609784200

  103. 103.

    Schnupf P. Portnoy D. A. (2007 ). Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 9 1176–1187

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

  104. 104.

    Schröder A. Kland R. Peschel A. von Eiff C. Aepfelbacher M. (2006a ). Live cell imaging of phagosome maturation in Staphylococcus aureus infected human endothelial cells: small colony variants are able to survive in lysosomes. Med. Microbiol. Immunol. 195 185–194

    Not in our library10.1007/s00430-006-0015-0

  105. 105.

    Schröder A. Schröder B. Roppenser B. Linder S. Sinha B. Fassler R. Aepfelbacher M. (2006b ). Staphylococcus aureus fibronectin binding protein-A induces motile attachment sites and complex actin remodeling in living endothelial cells. Mol. Biol. Cell 17 5198–5210

    Not in our library10.1091/mbc.e06-05-0463

  106. 106.

    Schwartz J. Leidal K. G. Femling J. K. Weiss J. P. Nauseef W. M. (2009 ). Neutrophil bleaching of GFP-expressing staphylococci: probing the intraphagosomal fate of individual bacteria. J. Immunol. 183 2632–2641

    Not in our library10.4049/jimmunol.0804110

  107. 107.

    Schwarz-Linek U. Werner J. M. Pickford A. R. Gurusiddappa S. Kim J. H. Pilka E. S. Briggs J. A. Gough T. S. Hook M. Campbell I. D. Potts J. R. (2003 ). Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423 177–181

    Not in our library10.1038/nature01589

  108. 108.

    Selva L. Viana D. Regev-Yochay G. Trzcinski K. Corpa J. M. Lasa I. Novick R. P. Penades J. R. (2009 ). Killing niche competitors by remote-control bacteriophage induction. Proc. Natl. Acad. Sci. U.S.A. 106 1234–1238

    Not in our library10.1073/pnas.0809600106

  109. 109.

    Sendi P. Proctor R. A. (2009 ). Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends Microbiol. 17 54–58

    Not in our library10.1016/j.tim.2008.11.004

  110. 110.

    Shompole S. Henon K. T. Liou L. E. Dziewanowska K. Bohach G. A. Bayles K. W. (2003 ). Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agr-mediated diffusion sensing. Mol. Microbiol. 49 919–927

    Not in our library10.1046/j.1365-2958.2003.03618.x

  111. 111.

    Sinha B. Francois P. Que Y. A. Hussain M. Heilmann C. Moreillon P. Lew D. Krause K. H. Peters G. Herrmann M. (2000 ). Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect. Immun. 68 6871–6878

    Not in our library10.1128/iai.68.12.6871-6878.2000

  112. 112.

    Sinha B. François P. P. Nüße O. Foti M. Hartford O. M. Vaudaux P. Foster T. J. Lew D. P. Herrmann M. Krause K.-H. (1999 ). Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin a5β1. Cell. Microbiol. 1 101–117

    Not in our library10.1046/j.1462-5822.1999.00011.x

  113. 113.

    Sinha B. Fraunholz M. (2010 ). Staphylococcus aureus host cell invasion and post-invasion events. Int. J. Med. Microbiol. 300 170–175

    Not in our library10.1016/j.ijmm.2009.08.019

  114. 114.

    Strober W. Murray P. J. Kitani A. Watanabe T. (2006 ). Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6 9–20

    Not in our library10.1038/nri1747

  115. 115.

    Taylor R. C. Cullen S. P. Martin S. J. (2008 ). Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9 231–241

    Not in our library10.1038/nrm2312

  116. 116.

    Ting J. P. Lovering R. C. Alnemri E. S. Bertin J. Boss J. M. Davis B. K. Flavell R. A. Girardin S. E. Godzik A. Harton J. A. Hoffman H. M. Hugot J. P. Inohara N. Mackenzie A. Maltais L. J. Nunez G. Ogura Y. Otten L. A. Philpott D. Reed J. C. Reith W. Schreiber S. Steimle V. Ward P. A. (2008a ). The NLR gene family: a standard nomenclature. Immunity 28 285–287

    Not in our library10.1016/j.immuni.2008.02.005

  117. 117.

    Ting J. P. Willingham S. B. Bergstralh D. T. (2008b ). NLRs at the intersection of cell death and immunity. Nat. Rev. Immunol. 8 372–379

    Not in our library10.1038/nri2296

  118. 118.

    Tuchscherr L. Medina E. Hussain M. Volker W. Heitmann V. Niemann S. Holzinger D. Roth J. Proctor R. A. Becker K. Peters G. Loffler B. (2011 ). Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol. Med. 3 129–141

    Not in our library10.1002/emmm.201000115

  119. 119.

    Tucker K. A. Reilly S. S. Leslie C. S. Hudson M. C. (2000 ). Intracellular Staphylococcus aureus induces apoptosis in mouse osteoblasts. FEMS Microbiol. Lett. 186 151–156

    Not in our library10.1111/j.1574-6968.2000.tb09096.x

  120. 120.

    Vann J. M. Proctor R. A. (1988 ). Cytotoxic effects of ingested Staphylococcus aureus on bovine endothelial cells: role of S. aureus a-hemolysin. Microb. Pathog. 4 443–453

    Not in our library10.1016/0882-4010(88)90029-0

  121. 121.

    van Opijnen T. Bodi K. L. Camilli A. (2009 ). Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nat. Methods 6 767–772

    Not in our library10.1038/nmeth.1377

  122. 122.

    Verdon J. Girardin N. Lacombe C. Berjeaud J. M. Hechard Y. (2009 ). delta-hemolysin, an update on a membrane-interacting peptide. Peptides 30 817–823

    Not in our library10.1016/j.peptides.2008.12.017

  123. 123.

    von Eiff C. Peters G. Proctor R. A. (2001 ). “Small colony variants of Staphylococcus aureus: mechanisms for production, biology of infection, and clinical significance,” in Staphylococcus aureus Infection and Disease, eds Honeyman A. L. Friedman H. Bendinelli M. (New York, NY: Kluwer Academic/Plenum),17–33

    Not in our library

  124. 124.

    Wadstrom T. Mollby R. (1972 ). Some biological properties of purified staphylococcal haemolysins. Tox -icon 10 511–519

    Not in our library10.1016/0041-0101(72)90177-8

  125. 125.

    Walev I. Martin E. Jonas D. Mohamadzadeh M. Muller-Klieser W. Kunz L. Bhakdi S. (1993 ). Staphylococcal alpha-toxin kills human keratinocytes by permeabilizing the plasma membrane for monovalent ions. Infect. Immun. 61 4972–4979

    Not in our library10.1128/iai.61.12.4972-4979.1993

  126. 126.

    Wang R. Braughton K. R. Kretschmer D. Bach T. H. Queck S. Y. Li M. Kennedy A. D. Dorward D. W. Klebanoff S. J. Peschel A. Deleo F. R. Otto M. (2007 ). Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat. Med. 13 1510–1514

    Not in our library10.1038/nm1656

  127. 127.

    Weidenmaier C. Kokai-Kun J. F. Kristian S. A. Chanturiya T. Kalbacher H. Gross M. Nicholson G. Neumeister B. Mond J. J. Peschel A. (2004 ). Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10 243–245

    Not in our library10.1038/nm991

  128. 128.

    Weidenmaier C. Kokai-Kun J. F. Kulauzovic E. Kohler T. Thumm G. Stoll H. Gotz F. Peschel A. (2008 ). Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int. J. Med. Microbiol. 298 505–513

    Not in our library10.1016/j.ijmm.2007.11.006

  129. 129.

    Weidenmaier C. Peschel A. Xiong Y. Q. Kristian S. A. Dietz K. Yeaman M. R. Bayer A. S. (2005 ). Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J. Infect. Dis. 191 1771–1777

    Not in our library10.1086/429692

  130. 130.
    Key Role for Clumping Factor B in Staphylococcus aureus Nasal Colonization of Humans · 2008
    No notice
  131. 131.

    Wesson C. A. Deringer J. Liou L. E. Bayles K. W. Bohach G. A. Trumble W. R. (2000 ). Apoptosis induced by Staphylococcus aureus in epithelial cells utilizes a mechanism involving caspases 8 and 3. Infect. Immun. 68 2998–3001

    Not in our library10.1128/iai.68.5.2998-3001.2000

  132. 132.

    Wesson C. A. Liou L. E. Todd K. M. Bohach G. A. Trumble W. R. Bayles K. W. (1998 ). Staphylococcus aureus Agr and Sar global regulators influence internalization and induction of apoptosis. Infect. Immun. 66 5238–5243

    Not in our library10.1128/iai.66.11.5238-5243.1998

  133. 133.

    Wilke G. A. Bubeck Wardenburg J. (2010 ). Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc. Natl. Acad. Sci. U.S.A. 107 13473–13478

    Not in our library10.1073/pnas.1001815107

  134. 134.

    Willingham S. B. Ting J. P. (2008 ). NLRs and the dangers of pollution and aging. Nat. Immunol. 9 831–833

    Not in our library10.1038/ni0808-831

  135. 135.

    Wright J. A. Nair S. P. (2010 ). Interaction of staphylococci with bone. Int. J. Med. Microbiol. 300 193–204

    Not in our library10.1016/j.ijmm.2009.10.003

Cited by papers we hold 6

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.