Host defense and pathogenesis in Staphylococcus aureus infections

DeLeo, Frank R.; Diep, Binh An; Otto, Michael

doi:10.1016/j.idc.2008.10.003

Cited by 270Antimicrobial Resistance in StaphylococcusNeutrophil, Myeloperoxidase and Oxidative MechanismsStreptococcal Infections and Treatments

Host defense and pathogenesis in Staphylococcus aureus infections

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DeLeo, Frank R., Diep, Binh An, Otto, Michael·2009·Infectious Disease Clinics of North America

DOI 10.1016/j.idc.2008.10.003PMC PMC2748223

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Abstract

Staphylococcus aureus is the most abundant cause of bacterial infections in the United States. As such, the pathogen has devised means to circumvent destruction by the innate immune system. Neutrophils are a critical component of innate immunity and the primary cellular defense against S aureus infections. This article reviews human neutrophil function in the context of S aureus virulence mechanisms and provides an overview of community-associated methicillin-resistant S aureus pathogenicity.

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Peptidoglycan recognition protein (PGRP) plays a role in the neutrophil killing of Gram-positive bacteria, inhibiting their growth.
“Peptidoglycan recognition protein (PGRP) plays a role in the neutrophil killing of Gram-positive bacteria [38], inhibiting their growth.”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [38]

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Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1
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“Protein A also has a more specific role in the pathogenesis of airway infections by interacting with the tumor necrosis factor a receptor on airway epithelia.(76)”
Background
Vaccine protection against Staphylococcus aureus pneumonia
Wardenburg, J. B., & Schneewind, O. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20072208 · Cited by 406 · cited 1× · see citing works
“Immunization with inactivated a-toxin or passive transfer of anti-a-toxin antibodies also protected mice from lethal pneumonia.(90) Taken together, these studies indicate that a-toxin plays an essential role in pneumonia.”
Background
Peptidoglycan Recognition Proteins
Liu, C., Xu, Z., Gupta, D., & Dziarski, R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105566200 · Cited by 398 · see citing works
Emergence of Multidrug-Resistant, Community-Associated, Methicillin-Resistant Staphylococcus aureus Clone USA300 in Men Who Have Sex with Men
Diep, B. A., Chambers, H. F. “., Graber, C. J., Szumowski, J. D., Miller, L. G., Han, L. L., Chen, J. H., Lin, F., Lin, J., Phan, T. H., et al. (2008) · Annals of Internal Medicine · doi:10.7326/0003-4819-148-4-200802190-00204 · Cited by 390 · see citing works
Self-citation
Epidemic community-associated methicillin-resistant Staphylococcus aureus : Recent clonal expansion and diversification
Kennedy, A. D., Otto, M. J., Braughton, K. R., Whitney, A. R., Chen, L., Mathema, B., Mediavilla, J. R., Byrne, K. A., Parkins, L. D., Tenover, F. C., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710217105 · Cited by 387 · cited 1× · see citing works
“The current CA-MRSA epidemic is due to clonal emergence of USA300 isolates that have enhanced virulence or a “hypervirulence” phenotype [14,15].”
BackgroundSelf-citation
Immunodeficiency Diseases Caused by Defects in Phagocytes
Lekstrom-Himes, J. A., & Gallin, J. I. (2000) · New England Journal of Medicine · doi:10.1056/nejm200012073432307 · Cited by 386 · cited 1× · see citing works
“have recurrent bacterial and fungal infections, especially infections caused by S aureus.(44)”
Background
Laboratory-based surveillance of current antimicrobial resistance patterns and trends among Staphylococcus aureus: 2005 status in the United States
Styers, D., Sheehan, D. J., Hogan, P. A., & Sahm, D. F. (2006) · Annals of Clinical Microbiology and Antimicrobials · doi:10.1186/1476-0711-5-2 · Cited by 384 · cited 5× · see citing works
“Menstrual TSS is caused by S aureus colonization of tampons.79 Nonmenstrual TSS also may be caused by enterotoxins, which, however have a more notorious role as the cause for S aureus food poisoning.80 COMMUNITY-ASSOCIATEDMETHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS VIRULENCE Hospital-Associated Versus Community-Associ…”
BackgroundInfluential
Selective Roles for Toll-Like Receptor (TLR)2 and TLR4 in the Regulation of Neutrophil Activation and Life Span
Sabroe, I., Prince, L. R., Jones, E. C., Horsburgh, M. J., Foster, S. J., Vogel, S. N., Dower, S., & Whyte, M. K. B. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.10.5268 · Cited by 352 · see citing works
Alpha-toxin of Staphylococcus aureus.
Bhakdi, S., & Tranum-Jensen, J. (1991) · Microbiological Reviews · doi:10.1128/mmbr.55.4.733-751.1991 · Cited by 351 · cited 1× · see citing works
“α-toxin (α-hemolysin, Hla)—α-toxin is a well-characterized pore forming cytolytic toxin that is similar in sequence and function to the leukocidins [95], albeit it does not lyse neutrophils [96].”
Background
DEGRANULATION OF POLYMORPHONUCLEAR LEUCOCYTES FOLLOWING PHAGOCYTOSIS OF MICROORGANISMS
Hirsch, J. G., & Cohn, Z. A. (1960) · The Journal of Experimental Medicine · doi:10.1084/jem.112.6.1005 · Cited by 335 · cited 2× · see citing works
“Concomitant with the production of ROS, neutrophil cytoplasmic granules fuse with bacteria-containing phagosomes, a process called degranulation.(45) Fusion of azuro-”
Background
Neutrophils exposed to bacterial lipopolysaccharide upregulate NADPH oxidase assembly.
DeLeo, F. R., Renee, J., McCormick, S. J., Nakamura, M., Apicella, M. A., Weiss, J. P., & Nauseef, W. M. (1998) · Journal of Clinical Investigation · doi:10.1172/jci949 · Cited by 312 · cited 1× · see citing works
“Priming includes mobilization of secretory vesicles (and thus up-regulation of specific cell surface receptors, eg, CD11b/CD18) and secretion of cytokines, but fails to trigger release of azurophilic granules or elicit production of superoxide.(29) Importantly, chemotactic/ priming agents ultimately promote efficient…”
BackgroundSelf-citation
The antimicrobial peptide‐sensing system aps of Staphylococcus aureus
Li, M., Cha, D. J., Lai, Y., Villaruz, A. E., Sturdevant, D. E., & Otto, M. J. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05986.x · Cited by 297 · cited 1× · see citing works
“anisms to interfere specifically with the activity of cationic AMPs, using a dedicated three-component AMP sensing system.(69,70) The regulated resistance mechanisms”
MethodSelf-citation
Gram-positive three-component antimicrobial peptide-sensing system
Li, M., Lai, Y., Villaruz, A. E., Cha, D. J., Sturdevant, D. E., & Otto, M. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702159104 · Cited by 288 · cited 2× · see citing works
“Furthermore, expression of the VraFG transporter is increased upon AMP exposure.(70) VraFG has a demonstrated role in AMP resistance(69) and the”
BackgroundMethodSelf-citation
Staphylococcus aureusSepsis and the Waterhouse–Friderichsen Syndrome in Children
Adem, P. V., Montgomery, C. P., Husain, A. N., Koogler, T. K., Arangelovich, V., Humilier, M., Boyle‐Vavra, S., & Daum, R. S. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa044194 · Cited by 277 · cited 1× · see citing works
“Although USA400 remained a significant cause of CA-MRSA infections through 2005 [11,12], it has been replaced almost completely by a genotype known as USA300 [6,13], which is now epidemic in the United States.”
Background
Modulation of phagocyte apoptosis by bacterial pathogens
DeLeo, F. R. (2004) · APOPTOSIS · doi:10.1023/b:appt.0000031448.64969.fa · Cited by 264 · cited 1× · see citing works
“Indeed, bacterial pathogens have devised mechanisms to alter apoptosis and promote pathogenesis.(55,56) For example, USA300 and USA400 cause rapid PMN lysis and/or accelerate bacteria-induced apoptosis to the point of secondary lysis.”
BackgroundSelf-citation
Formation of singlet oxygen by the myeloperoxidase-mediated antimicrobial system.
Rosen, H., & Klebanoff, S. J. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)40127-x · Cited by 263 · see citing works
Neutrophils in the innate immune response.
Kobayashi, S. D., Voyich, J. M., Burlak, C., & DeLeo, F. R. (2005) · PubMed · Cited by 260 · see citing works
Self-citation
Widespread Skin and Soft-Tissue Infections Due to Two Methicillin-Resistant Staphylococcus aureus Strains Harboring the Genes for Panton-Valentine Leucocidin
Diep, B. A., Sensabaugh, G. F., Somboona, N. S., Carleton, H. A., & Perdreau‐Remington, F. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.5.2080-2084.2004 · Cited by 254 · cited 1× · see citing works
“emergence of USA300 isolates that have enhanced virulence or a hypervirulence phenotype.(14,15) Hypervirulence, defined here as the ability of CA-MRSA to cause widespread infections in otherwise healthy individuals, likely is related in part to the ability”
BackgroundSelf-citation
Panton‐Valentine Leukocidin Is Not a Virulence Determinant in Murine Models of Community‐Associated Methicillin‐ResistantStaphylococcus aureusDisease
Wardenburg, J. B., Palazzolo‐Ballance, A. M., Otto, M., Schneewind, O., & DeLeo, F. R. (2008) · The Journal of Infectious Diseases · doi:10.1086/592053 · Cited by 236 · cited 1× · see citing works
“aureus strain Newman, no significant contribution of PVL to lethal pneumonia was found [88,89].”
BackgroundSelf-citation
Staphylococcal complement evasion by various convertase-blocking molecules
Jongerius, I., Köhl, J., Pandey, M. K., Ruyken, M., van Kessel, K. P. M., van Strijp, J. A. G., & Rooijakkers, S. H. M. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070818 · Cited by 233 · cited 1× · see citing works
“is an excellent example of the functional redundancy of S aureus molecules interfering with the same immune defense mechanism (see Table 1).(65)”
Background
Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: Cell fate is regulated at the level of gene expression
Kobayashi, S. D., Voyich, J. M., Buhl, C. L., Stahl, R. M., & DeLeo, F. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092148299 · Cited by 225 · cited 1× · see citing works
“On the other hand, neutrophil apoptosis is accelerated significantly following phagocytosis [53,54] and this phenomenon appears critical to the resolution of the inflammatory response (Fig.”
BackgroundSelf-citation
How do microbes evade neutrophil killing?
Urban, C. F., Lourido, S., & Zychlinsky, A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00792.x · Cited by 221 · cited 1× · see citing works
“Indeed, bacterial pathogens have devised mechanisms to alter apoptosis and promote pathogenesis [55,56].”
Background
The NADPH oxidase of human polymorphonuclear leukocytes. Evidence for regulation by multiple signals.
McPhail, L. C., Clayton, C. C., & D, R. S. M. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)91080-x · Cited by 217 · cited 1× · see citing works
“at substimulatory concentration, to enhance superoxide production elicited by a second stimulus.(27) Neutrophils can be primed for enhanced adhesion, phagocytosis, production of reactive oxygen species (ROS), cytokine secretion, leukotriene synthesis, degranulation, and bactericidal activity.”
Background
Comparison of Virulence in Community‐Associated Methicillin‐ResistantStaphylococcus aureusPulsotypes USA300 and USA400 in a Rat Model of Pneumonia
Montgomery, C. P., Boyle‐Vavra, S., Adem, P. V., Lee, J. C., Husain, A. N., Clasen, J., & Daum, R. S. (2008) · The Journal of Infectious Diseases · doi:10.1086/590157 · Cited by 208 · cited 1× · see citing works
“and there is strong expression of the agr regulatory molecule RNAIII in CA-MRSA strains, there may be a key role of this virulence regulator in CA-MRSA disease that remains to be investigated.(100)”
Background
Mammalian Peptidoglycan Recognition Protein Binds Peptidoglycan with High Affinity, Is Expressed in Neutrophils, and Inhibits Bacterial Growth
Liu, C., Gelius, E., Liu, G., Steiner, H., & Dziarski, R. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001239200 · Cited by 206 · cited 2× · see citing works
“Peptidoglycan recognition protein (PGRP) is a secreted host protein that contributes to intracellular killing of gram-positive bacteria by neutrophils.(35) There are four”
Background
National Trends in Staphylococcus aureus Infection Rates: Impact on Economic Burden and Mortality over a 6-Year Period (1998-2003)
Noskin, G. A., Rubin, R. J., Schentag, J. J., Kluytmans, J. A. J. W., Hedblom, E. C., Jacobson, C., Smulders, M., Gemmen, E., & Bharmal, M. F. (2007) · Clinical Infectious Diseases · doi:10.1086/522186 · Cited by 201 · cited 1× · see citing works
“5 billion in 2003.(3) A high percentage of hospital infections are caused by methicillin-resistant S aureus (MRSA).”
Background
Contribution of Panton-Valentine Leukocidin in Community-Associated Methicillin-Resistant Staphylococcus aureus Pathogenesis
Diep, B. A., Palazzolo‐Ballance, A. M., Tattevin, P., Basuino, L., Braughton, K. R., Whitney, A. R., Chen, L., Kreiswirth, B. N., Otto, M. J., DeLeo, F. R., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003198 · Cited by 188 · cited 1× · see citing works
“cently, the failure to replicate the regulatory effects of PVL in USA300 and USA400 indicated that PVL does not contribute to CA-MRSA virulence by means of a gene regulatory mechanism.(92)”
BackgroundSelf-citation
The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction
Quinn, M. T., Ammons, M. C. B., & DeLeo, F. R. (2006) · Clinical Science · doi:10.1042/cs20060059 · Cited by 175 · cited 1× · see citing works
“dase that generates high levels of superoxide, a process traditionally called respiratory burst.(39) Superoxide anion is short-lived and dismutates rapidly to hydrogen peroxide and forms other secondary reactive products.”
BackgroundSelf-citation
From the Centers for Disease Control and Prevention. Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus--Minnesota and North Dakota, 1997-1999.
(1999) · PubMed · Cited by 170 · see citing works
The Emergence and Importation of Diverse Genotypes of Methicillin-Resistant Staphylococcus aureus (MRSA) Harboring the Panton-Valentine Leukocidin Gene ( pvl ) Reveal that pvl Is a Poor Marker for Community-Acquired MRSA Strains in Ireland
Rossney, A. S., Shore, A. C., Morgan, P. M., Fitzgibbon, M. M., O'Connell, B. C., & Coleman, D. C. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.00245-07 · Cited by 164 · cited 1× · see citing works
“Epidemiological data alone, however, is insufficient to establish whether PVL directly contributes to widespread dissemination of CA-MRSA clones [84,85].”
Background
Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2
Lotz, S., Aga, E., Wilde, I., van Zandbergen, G., Härtung, T., Solbach, W., & Laskay, T. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0803360 · Cited by 152 · cited 1× · see citing works
“Neutrophil TLRs activate signal transduction pathways that prolong cell survival [31], promote and/or enhance adhesion, phagocytosis, release of cytokines, chemokines and ROS [31,32], and trigger granule exocytosis [33], thereby contributing to microbicidal activity.”
Background
Neutrophil Microbicides Induce a Pathogen Survival Response in Community-Associated Methicillin-Resistant Staphylococcus aureus
Palazzolo-Ballance, A. M., Reniere, M. L., Braughton, K. R., Sturdevant, D. E., Otto, M., Kreiswirth, B. N., Skaar, E. P., & DeLeo, F. R. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.1.500 · Cited by 142 · cited 1× · see citing works
“aureus to circumvent innate host defense mechanisms, which includes production of many toxins and mechanisms involved in the uptake of iron [66].”
BackgroundSelf-citation
Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides
Tzianabos, A. O., Wang, J. Y., & Lee, J. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.161175598 · Cited by 133 · cited 1× · see citing works
“studies have demonstrated that stimulation of CD41 T-cells by S aureus capsular polysaccharide leads to production of chemokines that recruit neutrophils to the site of infection.(23,24) Further, S aureus cell surface components, primarily peptidoglycan (PGN), long have been known to elicit production of C5a,(25) a po…”
Background
Lipoteichoic acid induces secretion of interleukin-8 from human blood monocytes: a cellular and molecular analysis
Standiford, T. J., Arenberg, D. A., Danforth, J. M., Kunkel, S. L., VanOtteren, G. M., & Strieter, R. M. (1994) · Infection and Immunity · doi:10.1128/iai.62.1.119-125.1994 · Cited by 123 · see citing works
C hemotactic S ignaling P athways in N eutrophils: from R eceptor to A ctin A ssembly
Cicchetti, G., Allen, P. G., & Glogauer, M. (2002) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/154411130201300302 · Cited by 122 · cited 1× · see citing works
“A first step in the eradication of invading microorganisms is active recruitment of PMNs to the site of infection by chemotaxis.(18) This is a multistep process whereby neutrophils are mobilized from peripheral blood or bone marrow in response to”
Background
Transmembrane β-barrel of staphylococcal α-toxin forms in sensitive but not in resistant cells
Valeva, A., Walev, I., Pinkernell, M., Walker, B. W., Bayley, H., Palmer, M., & Bhakdi, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.21.11607 · Cited by 113 · cited 1× · see citing works
“a-toxin is a well-characterized pore forming cytolytic toxin that is similar in sequence and function to the leukocidins,(97) albeit it does not lyse neutrophils.(98) Recently, it was shown to be an essential virulence factor during S aureus pneumonia.”
Background
CD4 + T cells and CXC chemokines modulate the pathogenesis of Staphylococcus aureus wound infections
McLoughlin, R. M., Solinga, R. M., Rich, J., Zaleski, K. J., Cocchiaro, J. L., Risley, A., Tzianabos, A. O., & Lee, J. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508961103 · Cited by 111 · cited 1× · see citing works
“studies have demonstrated that stimulation of CD41 T-cells by S aureus capsular polysaccharide leads to production of chemokines that recruit neutrophils to the site of infection.(23,24) Further, S aureus cell surface components, primarily peptidoglycan (PGN), long have been known to elicit production of C5a,(25) a po…”
Background
Neutrophil chloramines: missing links between innate and acquired immunity
Marcinkiewicz, J. (1997) · Immunology Today · doi:10.1016/s0167-5699(97)01161-4 · Cited by 106 · cited 1× · see citing works
“These secondarily-derived products, including hypochlorous acid, hydroxyl radical, chloramines, and singlet oxygen, are effective microbicidal compounds [40-43].”
Background
Epidemiologic Distribution of the Arginine Catabolic Mobile Element among Selected Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus Isolates
Goering, R. V., McDougal, L. K., Fosheim, G. E., Bonnstetter, K. K., Wolter, D. J., & Tenover, F. C. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.00273-07 · Cited by 104 · cited 2× · see citing works
“From 1997 to 1999, S aureus was reported as the most abundant cause of bloodstream, skin and soft tissue, and lower respiratory tract infections in the United States, Canada, Europe, Latin America, and the Western Pacific.1 The pathogen is the leading cause of hospital-associated infections in the United States,2 and…”
BackgroundInfluential
Capsular polysaccharide types 5 and 8 of Staphylococcus aureus bind specifically to human epithelial (KB) cells, endothelial cells, and monocytes and induce release of cytokines
Soell, M., Diab, M., Archipoff, G., Beretz, A., Herbelin, C. J., Poutrel, B., & Klein, J. P. (1995) · Infection and Immunity · doi:10.1128/iai.63.4.1380-1386.1995 · Cited by 101 · cited 1× · see citing works
“aureus lipoteichoic acid (LTA) and capsular polysaccharide induce production of IL-8 by peripheral blood monocytes [19] and epithelial and endothelial cells [20], respectively.”
Background
Distribution of the ACME-arcA gene among methicillin-resistant Staphylococcus aureus from England and Wales
Ellington, M. J., Yearwood, L. M., Ganner, M., East, C., & Kearns, A. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm422 · Cited by 80 · cited 2× · see citing works
“From 1997 to 1999, S aureus was reported as the most abundant cause of bloodstream, skin and soft tissue, and lower respiratory tract infections in the United States, Canada, Europe, Latin America, and the Western Pacific.1 The pathogen is the leading cause of hospital-associated infections in the United States,2 and…”
BackgroundInfluential
PROTEIN A FROM STAPHYLOCOCCUS AUREUS: THE BIOLOGICAL SIGNIFICANCE OF ITS REACTION WITH IgG
Forsgren, A., & Nordström, K. (1974) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1974.tb41496.x · Cited by 58 · cited 1× · see citing works
“sequester nonspecific antibodies on its surface, which protects efficiently from attacks by the innate and acquired immune systems.(75) Protein A also has a more specific role in the pathogenesis of airway infections by interacting with the tumor necrosis factor a receptor on airway epithelia.”
Background
Interleukin-8 gene expression in Staphylococcus aureus-infected endothelial cells
Yao, L., Lowy, F. D., & Berman, J. W. (1996) · Infection and Immunity · doi:10.1128/iai.64.8.3407-3409.1996 · Cited by 53 · cited 1× · see citing works
“S aureus-activated endothelial cells produce IL-8 that promotes transmigration of neutrophils.(21) Freely secreted virulence molecules of S aureus, including toxic shock syndrome toxin-1 (TSST1), enterotoxin A (SEA), or enterotoxin B (SEB), also elicit production of IL-8 by human monocytic cells.”
Background
Synergy between Extracellular Group IIA Phospholipase A2 and Phagocyte NADPH Oxidase in Digestion of Phospholipids of Staphylococcus aureus Ingested by Human Neutrophils
Femling, J., Nauseef, W. M., & Weiss, J. P. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.7.4653 · Cited by 43 · cited 1× · see citing works
“For instance, group IIA phospholipase A2 (gIIA-PLA2), a small (approximately 14 kDa) cationic antimicrobial protein found in extracellular fluids, synergizes with the neutrophil NADPH oxidase to promote digestion of S aureus phospholipids.(49) More recently, studies by Corbin and colleagues(50) found that neutrophil c…”
Background
Chemotaxigenesis by cell surface components of Staphylococcus aureus
Schmeling, D. J., Peterson, P. K., Hammerschmidt, D. E., Kim, Y., Verhoef, J., Wilkinson, B. J., & Quie, P. G. (1979) · Infection and Immunity · doi:10.1128/iai.26.1.57-63.1979 · Cited by 35 · cited 4× · see citing works
“There is Table 1 Staphylococcus aureus molecules that contribute to immune evasion or alter host immune function Gene(s) Protein orMolecule Function/Effect on Immune System mprF Multiple peptide resistance factor, MprF Promotes resistance to cationic AMPs psm Phenol-soluble modulinlike peptides, PSMs Cause leukocyte l…”
BackgroundInfluential
STAPHYLOCOCCAL LEUKOCIDIN
Woodin, A. M. (1965) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1965.tb11636.x · Cited by 24 · cited 1× · see citing works
“Woodin to conclude that PVL alone is not a very toxic substance [86], as intravenous injection of PVL in rabbits resulted in granulocytopenia followed by a marked granulocytosis, and was not lethal.”
Background
Mayhem in the Lung
Kahl, B. C., & Peters, G. (2007) · Science · doi:10.1126/science.1139628 · Cited by 23 · see citing works
Distinction between Pore Assembly by Staphylococcal α -Toxin versus Leukotoxins
Joubert, O., Voegelin, J., Guillet, V., Tranier, S., Werner, S., Colin, D. A., Serra, M. D., Keller, D., Monteil, H., Mourey, L., et al. (2007) · BioMed Research International · doi:10.1155/2007/25935 · Cited by 17 · cited 1× · see citing works
“The b-barrel structured leukocidins form pores almost exclusively in leukocytes, by means of a mechanism similar to that used by a-toxin.(73) Although the biochemical function of leukocidins—that is, lysis of leukocytes—has been clearly established, their role in S aureus virulence and the biological reason for the pr…”
Background
Interleukin-8 Production by Human Monocytic Cells in Response to Staphylococcal Exotoxins Is Direct and Independent of Interleukin-1 and Tumor Necrosis Factor-
Krakauer, T. (1998) · The Journal of Infectious Diseases · doi:10.1086/517477 · Cited by 17 · cited 1× · see citing works
“aureus, including toxic shock syndrome toxin-1 (TSST1), enterotoxin A (SEA), or enterotoxin B (SEB), also elicit production of IL-8 by human monocytic cells [22].”
Background

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Sorted by citations

Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management.
Tong, S. Y. C., Davis, J. S., Eichenberger, E., Holland, T. L., & Fowler, V. G. (2015) · Clinical Microbiology Reviews · doi:10.1128/cmr.00134-14 · Cited by 5,192 · see citing works
Waves of resistance: Staphylococcus aureus in the antibiotic era
Chambers, H. F., & DeLeo, F. R. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2200 · Cited by 2,718 · see citing works
“aureus produces many other molecules that promote host colonization, facilitate evasion of the innate immune system and alter immune response”
BackgroundSelf-citation
Community-associated meticillin-resistant Staphylococcus aureus
DeLeo, F. R., Otto, M. J., Kreiswirth, B. N., & Chambers, H. F. “. (2010) · The Lancet · doi:10.1016/s0140-6736(09)61999-1 · Cited by 1,502 · see citing works
Self-citation
Staphylococcus aureus Panton-Valentine Leukocidin Is a Very Potent Cytotoxic Factor for Human Neutrophils
Löffler, B., Hussain, M. S., Grundmeier, M., Brück, M., Holzinger, D., Varga, G., Roth, J., Kahl, B. C., Proctor, R. A., & Peters, G. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000715 · Cited by 440 · see citing works
“Further on, it has been shown that phagocytosis significantly accelerates neutrophils apoptosis, which appears to contribute to the resolution of the inflammatory response [21,22].”
Background
Role of Pore-Forming Toxins in Bacterial Infectious Diseases
Los, F. C. O., Randis, T. M., Aroian, R. V., & Ratner, A. J. (2013) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00052-12 · Cited by 401 · see citing works
Neutrophils in innate host defense against Staphylococcus aureus infections
Rigby, K. M., & DeLeo, F. R. (2012) · Seminars in Immunopathology · doi:10.1007/s00281-011-0295-3 · Cited by 400 · see citing works
“produced within the phagosome following ingestion [13].”
BackgroundSelf-citation
Targeting of Alpha‐Hemolysin by Active or Passive Immunization Decreases Severity of USA300 Skin Infection in a Mouse Model
Kennedy, A. D., Wardenburg, J. B., Gardner, D. J., Long, D., Whitney, A. R., Braughton, K. R., Schneewind, O., & DeLeo, F. R. (2010) · The Journal of Infectious Diseases · doi:10.1086/656043 · Cited by 335 · see citing works
“There has been an intense effort to better understand the mechanisms of USA300 virulence and transmission [29–32].”
BackgroundSelf-citation
Are bloodstream leukocytes Trojan Horses for the metastasis of Staphylococcus aureus?
Thwaites, G. E., & Gant, V. A. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2508 · Cited by 319 · see citing works
“aureus tissue invasion provokes rapid migration of both host cell types to the site of infection in order to phagocytose and kill the bacteri”
Role of the Accessory Gene Regulator agr in Community-Associated Methicillin-Resistant Staphylococcus aureus Pathogenesis
Cheung, G. Y. C., Wang, R., Khan, B. A., Sturdevant, D. E., & Otto, M. J. (2011) · Infection and Immunity · doi:10.1128/iai.00046-11 · Cited by 317 · see citing works
“aureus may secrete toxins that lyse human neutrophils and other immune cells, such as alpha-toxin, phenol-soluble modulins (PSMs), and members of the leukocidin family, which include Panton-Valentine leukocidin (PVL) (12, 18).”
BackgroundInfluentialSelf-citation
Staphylococcus colonization of the skin and antimicrobial peptides
Otto, M. J. (2010) · Expert Review of Dermatology · doi:10.1586/edm.10.6 · Cited by 261 · see citing works
“The reader is referred to other reviews that focus on the molecular basis of virulence in staphylococci [15,30,31].”
BackgroundSelf-citation
Identification of a Novel Staphylococcus aureus Two-Component Leukotoxin Using Cell Surface Proteomics
Ventura, C. L., Małachowa, N., Hammer, C. H., Nardone, G. A., Robinson, M. A., Kobayashi, S. D., & DeLeo, F. R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011634 · Cited by 206 · see citing works
“aureus produces many molecules that can potentially contribute to immune evasion and virulence [8].”
BackgroundSelf-citation
Immune Evasion byStaphylococcus aureus
de Jong, N. W. M., van Kessel, K. P. M., & van Strijp, J. A. G. (2019) · Microbiology Spectrum · doi:10.1128/microbiolspec.gpp3-0061-2019 · Cited by 200 · see citing works
Hiding in Plain Sight: Interplay between Staphylococcal Biofilms and Host Immunity
Scherr, T. D., Heim, C. E., Morrison, J. M., & Kielian, T. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00037 · Cited by 179 · see citing works
Comparative Analysis of Virulence and Toxin Expression of Global Community‐Associated Methicillin‐ResistantStaphylococcus aureusStrains
Li, M., Cheung, G. Y. C., Hu, J., Wang, D., Joo, H., DeLeo, F. R., & Otto, M. (2010) · The Journal of Infectious Diseases · doi:10.1086/657419 · Cited by 175 · see citing works
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An update on recent developments in the prevention and treatment of Staphylococcus aureus biofilms
Suresh, M. K., Biswas, R., & Biswas, L. (2018) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2018.11.002 · Cited by 164 · see citing works
Regulation of Hemolysin Expression and Virulence of Staphylococcus aureus by a Serine/Threonine Kinase and Phosphatase
Burnside, K. L., Lembo, A., Reyes, M. D. L., Iliuk, A. B., BinhTran, N.-T., Connelly, J. E., Lin, W.-J., Schmidt, B. Z., Richardson, A. R., Fang, F. C., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011071 · Cited by 163 · see citing works
“aureus to overcome host defenses (for recent reviews, see [6,7]).”
Background
Bacterial resistance mechanisms against host defense peptides
Koprivnjak, T., & Peschel, A. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0716-4 · Cited by 158 · see citing works
“Innate immunity is the first line of defense against the invading microbial pathogens [1, 2].”
Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity
Cassat, J. E., & Skaar, E. P. (2012) · Seminars in Immunopathology · doi:10.1007/s00281-011-0294-4 · Cited by 155 · see citing works
“aureus produces an arsenal of factors that subvert neutrophil function, including pore-forming toxins, phenol soluble modulins, proteases, and molecules that inhibit chemotaxis [185].”
Background
Rapid Neutrophil Destruction following Phagocytosis of Staphylococcus aureus
Kobayashi, S. D., Braughton, K. R., Palazzolo‐Ballance, A. M., Kennedy, A. D., Sampaio, E. P., Kristosturyan, E., Whitney, A. R., Sturdevant, D. E., Dorward, D. W., Holland, S. M., et al. (2010) · Journal of Innate Immunity · doi:10.1159/000317134 · Cited by 154 · see citing works
“Collectively, these antimicrobial processes are highly effective at eliminating most invading bacteria. On the other hand, pathogens such as Staphylococcus aureus moderate and/or circumvent these processes and ultimately cause disease [reviewed in [”
BackgroundSelf-citation
Vaccine review: “Staphyloccocus aureus vaccines: Problems and prospects”
Jansen, K. U., Girgenti, D., Scully, I. L., & Anderson, A. S. (2013) · Vaccine · doi:10.1016/j.vaccine.2013.04.002 · Cited by 151 · see citing works
Lower Antibody Levels to Staphylococcus aureus Exotoxins Are Associated With Sepsis in Hospitalized Adults With Invasive S. aureus Infections
Adhikari, R. P., Ajao, A. O., Aman, M. J., Karaüzüm, H., Sarwar, J., Lydecker, A. D., Johnson, J. K., Nguyen, C., Chen, W. H., & Roghmann, M. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis462 · Cited by 144 · see citing works
“Some of these toxins, such as α-hemolysin (Hla) or Panton Valentine leukocidin (PVL), cause cytolysis of innate immune cells and erythrocytes, while others, such as superantigens, activate T-lymphocytes and lead to massive release of inflammatory cytokines, culminating in septic shock [5].”
Background
Five birds, one stone: Neutralization of α-hemolysin and 4 bi-component leukocidins of Staphylococcus aureus with a single human monoclonal antibody
Rouha, H., Badarau, A., Visram, Z., Battles, M. B., Prinz, B., Magyarics, Z., Nagy, G., Mirkina, I. I., Stulik, L., Zerbs, M., et al. (2014) · mAbs · doi:10.4161/19420862.2014.985132 · Cited by 143 · see citing works
“aureus pathogenesis.(12-15) In addition, HlgAB is a potent toxin for human red blood cells(12) and LukED has recently been reported to target human T cells.”
Background
Staphylococcus aureusbacteraemia and endocarditis – epidemiology and outcome: a review
Ásgeirsson, H., Thalme, A., & Weiland, O. (2017) · Scandinavian Journal of Infectious Diseases · doi:10.1080/23744235.2017.1392039 · Cited by 142 · see citing works
The Role of Reactive Species on Innate Immunity
Andrés, C., Pérez de la Lastra, J., Juan, C., Plou, F., & Pérez-Lebeña, E. (2022) · Vaccines · doi:10.3390/vaccines10101735 · Cited by 142 · see citing works
“Peptidoglycan recognition protein (PGRP) plays a role in the neutrophil killing of Gram-positive bacteria [38], inhibiting their growth.”
Background
Effectiveness of Measures to Eradicate Staphylococcus aureus Carriage in Patients with Community-Associated Skin and Soft-Tissue Infections: A Randomized Trial
Fritz, S. A., Camins, B. C., Eisenstein, K. A., Fritz, J. M., Epplin, E. K., Burnham, C. D., Dukes, J. L., & Storch, G. A. (2011) · Infection Control and Hospital Epidemiology · doi:10.1086/661285 · Cited by 137 · see citing works
“002 At 4 months 15/58 (26) 12/50 (24) NS 18/59 (30) NS 9/56 (16) NS”
Phage-based platforms for the clinical detection of human bacterial pathogens
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“aureus is a Gram-positive, coagulase positive, non-motile, nonsporulating bacterium that has been a prominent cause of human infections throughout history.(131) In the pre-antibiotic era, mortality rates for S.”
Background
Staphylococcal Superantigens: Pyrogenic Toxins Induce Toxic Shock
Krakauer, T. (2019) · Toxins · doi:10.3390/toxins11030178 · Cited by 123 · see citing works
“Virulence factors such as leukocidins and α-hemolysin are cytotoxic to host cells [9].”
Background
Limitations of antibiotic options for invasive infections caused by methicillin-resistant Staphylococcus aureus: is combination therapy the answer?
Nguyen, H. M., & Graber, C. J. (2009) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkp377 · Cited by 121 · see citing works
In Vivo Assessment of Phage and Linezolid Based Implant Coatings for Treatment of Methicillin Resistant S. aureus (MRSA) Mediated Orthopaedic Device Related Infections
Kaur, S., Harjai, K., & Chhibber, S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157626 · Cited by 116 · see citing works
Staphylococcus aureus Targets the Duffy Antigen Receptor for Chemokines (DARC) to Lyse Erythrocytes
Spaan, A. N., Reyes-Robles, T., Badiou, C., Cochet, S., Boguslawski, K. M., Yoong, P., Day, C. J., de Haas, C. J. C., van Kessel, K. P. M., Vandenesch, F., et al. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2015.08.001 · Cited by 114 · see citing works
“The pathogenesis of this bacterium is multifactorial, and is exacerbated by the combination of resistance to many antibiotics and the production of an arsenal of virulence (DeLeo et al., 2009).”
Background
Vaccine development inStaphylococcus aureus: taking the biofilm phenotype into consideration
Harro, J. M., Peters, B. M., O’May, G. A., Archer, N. K., Kerns, P. W., Prabhakara, R., & Shirtliff, M. E. (2010) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2010.00708.x · Cited by 109 · see citing works
“This microbial species has dozens of known toxins, multiple immunoavoidance, and adherence factors, most of which demonstrate transient, timed, and disease-specific expression (DeLeo et al., 2009).”
Background
Staphylococcal Skin and Soft Tissue Infections
Hatlen, T. J., & Miller, L. G. (2020) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2020.10.003 · Cited by 111 · see citing works
Neutrophil Recruitment to Lymph Nodes Limits Local Humoral Response to Staphylococcus aureus
Kamenyeva, O., Boularan, C., Kabát, J., Cheung, G. Y. C., Cicala, C., Yeh, A. J., Chan, J. L., Periasamy, S., Otto, M. J., & Kehrl, J. H. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004827 · Cited by 107 · see citing works
“aureus (MRSA) strain USA300 (known as Los-Angeles County clone) that compromises severely both innate and adaptive immunity of the host [34].”
BackgroundSelf-citation
Development of a multicomponentStaphylococcus aureusvaccine designed to counter multiple bacterial virulence factors
Anderson, A. S., Miller, A. A., Donald, R. G. K., Scully, I. L., Nanra, J. S., Cooper, D., & Jansen, K. U. (2012) · Human Vaccines & Immunotherapeutics · doi:10.4161/hv.21872 · Cited by 107 · see citing works
Host Immune Transcriptional Profiles Reflect the Variability in Clinical Disease Manifestations in Patients with Staphylococcus aureus Infections
Banchereau, R., Jordán-Villegas, A., Ardura, M. I., Mejías, A., Baldwin, N. E., Xu, H., Saye, E. J., Rosselló-Urgell, J., Nguyen, P., Blankenship, D., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034390 · Cited by 106 · see citing works
“The neutrophil depletion from PBMC may result in the loss of key information in the systemic characterization of bacterial infections [15].”
Background
Resistance Evolution Against Antimicrobial Peptides in Staphylococcus aureus Alters Pharmacodynamics Beyond the MIC
Shazely, B. E., Yu, G., Johnston, P. R., & Rolff, J. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00103 · Cited by 100 · see citing works
“In summary, such mutations facilitate acquisition of drug resistance, contribute to immune evasion or alter host immune function (DeLeo et al., 2009).”
Background
Staphylococcus aureus biofilms decrease osteoblast viability, inhibits osteogenic differentiation, and increases bone resorption in vitro
Sánchez, C. J., Ward, C. L., Romano, D. R., Hurtgen, B. J., Hardy, S. K., Woodbury, R. L., Trevino, A. V., Rathbone, C. R., & Wenke, J. C. (2013) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-14-187 · Cited by 100 · see citing works
“aureus include a family of four membrane-damaging hemolysins (alpha-, beta-, gamma-, and delta-hemolysin) of which αhemolysin (Hla) plays an important role in the pathogenesis [46].”
Background
Prevention of Recurrent Staphylococcal Skin Infections
Creech, C. B., Al-Zubeidi, D. N., & Fritz, S. A. (2015) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2015.05.007 · Cited by 99 · see citing works
Staphylococcus aureus Leukotoxin GH Promotes Inflammation
Małachowa, N., Kobayashi, S. D., Braughton, K. R., Whitney, A. R., Parnell, M. J., Gardner, D. J., & DeLeo, F. R. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis495 · Cited by 91 · see citing works
“The pathogen produces a variety of molecules that presumably facilitate survival in or on the human host (reviewed in [1]).”
BackgroundSelf-citation
Role of Lipase from Community-Associated Methicillin-Resistant Staphylococcus aureus Strain USA300 in Hydrolyzing Triglycerides into Growth-Inhibitory Free Fatty Acids
Cadieux, B., Vijayakumaran, V., Bernards, M. A., Mcgavin, M. J., & Heinrichs, D. E. (2014) · Journal of Bacteriology · doi:10.1128/jb.02044-14 · Cited by 84 · see citing works
“aureus produces a large repertoire of virulence factors, including surface-associated proteins and polysaccharides, and numerous toxins, exoenzymes, and immune evasion factors which collectively contribute to the success of this bacterium as a pathogen (1, 3, 4).”
Background
Peritoneal Dialysis-Related Peritonitis Due to Staphylococcus aureus: A Single-Center Experience over 15 Years
Barretti, P., de Moraes, T. M. C., Camargo, C. H., Caramori, J. C. T., Mondelli, A. L., Montelli, A. C., & Cunha, M. D. L. R. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031780 · Cited by 81 · see citing works
“are the staphylococcal enterotoxins and the related toxic shock syndrome toxin-1 (TSST-1) that act as superantigens [8].”
Background
Inducible Expression of a Resistance-Nodulation-Division-Type Efflux Pump in Staphylococcus aureus Provides Resistance to Linoleic and Arachidonic Acids
Alnaseri, H., Arsic, B., Schneider, J. E. T., Kaiser, J. C., Scinocca, Z. C., Heinrichs, D. E., & Mcgavin, M. J. (2015) · Journal of Bacteriology · doi:10.1128/jb.02607-14 · Cited by 78 · see citing works
Evasion of Neutrophil Killing by Staphylococcus aureus
McGuinness, W., Kobayashi, S. D., & DeLeo, F. R. (2016) · Pathogens · doi:10.3390/pathogens5010032 · Cited by 78 · see citing works
“In vitro, these molecules have been shown to inhibit neutrophil recruitment, bacterial binding and phagocytosis, and killing by ROS and antimicrobial peptides (AMPs) (reviewed in [41,42]) (Figure 3).”
BackgroundSelf-citation
An update on community-associated MRSA virulence
Kobayashi, S. D., & DeLeo, F. R. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.07.009 · Cited by 78 · see citing works
Self-citation
Staphylococcus aureus Stimulates Neutrophil Targeting Chemokine Expression in Keratinocytes through an Autocrine IL-1α Signaling Loop
Olaru, F., & Jensen, L. E. (2010) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.37 · Cited by 78 · see citing works
“It is well established that neutrophils have an important role in eliminating S. aureus from the host in general (Verdrengh and Tarkowski, 1997; DeLeo et al., 2009 and references therein) and from the skin specifically (Mölne et al., 2000).”
A natural human monoclonal antibody targeting Staphylococcus Protein A protects against Staphylococcus aureus bacteremia
Varshney, A. K., Kuzmicheva, G. A., Lin, J., Sunley, K. M., Bowling, R. A., Kwan, T.-Y., Mays, H. R., Rambhadran, A., Zhang, Y., Martin, R. L., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0190537 · Cited by 76 · see citing works
Community-associated methicillin-resistant Staphylococcus aureus immune evasion and virulence
Graves, S. F., Kobayashi, S. D., & DeLeo, F. R. (2010) · Journal of Molecular Medicine · doi:10.1007/s00109-009-0573-x · Cited by 76 · see citing works
“aureus produces numerous surface molecules and freely secreted toxins that have potential to alter or inhibit function of innate immune cells (reviewed in [29]).”
BackgroundSelf-citation
Early ICU Energy Deficit Is a Risk Factor for Staphylococcus aureus Ventilator-Associated Pneumonia
Faisy, C., Llerena, M. C., Savalle, M., Mainardi, J., & Fagon, J.-Y. (2011) · CHEST Journal · doi:10.1378/chest.11-1499 · Cited by 76 · see citing works
Pharmacokinetic and Pharmacodynamic Considerations for the Use of Monoclonal Antibodies in the Treatment of Bacterial Infections
Lin, S. X. W., & Balthasar, J. P. (2018) · Antibodies · doi:10.3390/antib7010005 · Cited by 68 · see citing works
Staphylococcus aureus Biofilms and their Impact on the Medical Field
Reffuveille, F., Josse, J., Vallé, Q., Mongaret, C., & Gangloff, S. C. (2017) · InTech eBooks · doi:10.5772/66380 · Cited by 66 · see citing works
“These cells can phagocyte planktonic bacteria and release bactericidal components such as reactive oxygen species or enzymes [82].”
Background
Drivers of methicillin-resistant Staphylococcus aureus (MRSA) lineage replacement in China
Chen, H., Yin, Y., van Dorp, L., Shaw, L. P., Gao, H., Acman, M., Yuan, J., Chen, F., Sun, S., Wang, X., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00992-x · Cited by 65 · see citing works
“Virulence as a measurable trait ultimately requires evaluation using in vivo models though cytolytic activity, which can be readily measured using lysis of erythrocyte assays, offers a good proxy given hemolysins are wellestablished virulence factors [81].”
Background
Methicillin-resistant Staphylococcus aureus in HIV-infected patients
Hidrón, A., Moanna, A., Kempker, R. R., & Rimland, D. (2010) · Infection and Drug Resistance · doi:10.2147/idr.s7641 · Cited by 66 · see citing works
“Proper neutrophil function requires the coordination of many steps, including chemotaxis, phagocytosis, intracellular killing, and subsequent apoptosis.(25) Although not as well studied as cellular or adaptive immunity, the innate immune response in persons with HIV have revealed significant neutrophil dysfunction tha…”
Toll‐like Receptor 2 Ligand–Induced Protection against Bacterial Endophthalmitis
Kumar, A., Singh, C. N., Glybina, I. V., Mahmoud, T. H., & Yu, F. X. (2009) · The Journal of Infectious Diseases · doi:10.1086/649589 · Cited by 66 · see citing works
“Activation of the innate immune response is the first line of defense after tissue injury and infection [29, 30].”
Staphylococcus aureus: An Old Pathogen with New Weapons
Tang, Y., & Stratton, C. W. (2010) · Clinics in Laboratory Medicine · doi:10.1016/j.cll.2010.01.005 · Cited by 65 · see citing works
“pathogen is well equipped to evade the innate host defenses due to several virulence factors.(156,157) Virulence factors include biofilm, capsule, coagulase, lipase, hyaluronidase, protein A, fibronectin-binding protein, and multiple toxins.”
Synthesis, characterization and antimicrobial property of Fe3O4-Cys-HNQ nanocomplex, with l-cysteine molecule as a linker
Sangeetha, J., & Philip, J. (2013) · RSC Advances · doi:10.1039/c3ra00005b · Cited by 62 · see citing works
Staphylococcal superantigens interact with multiple host receptors to cause serious diseases
Stach, C. S., Herrera, A., & Schlievert, P. M. (2014) · Immunologic Research · doi:10.1007/s12026-014-8539-7 · Cited by 61 · see citing works
“Additionally, PSMs have pro-inflammatory and chemotactic activities [32].”
The bacteriology of chronic rhinosinusitis and the pre‐eminence of Staphylococcus aureus in revision patients
Cleland, E. J., Bassiouni, A., & Wormald, P. (2013) · International Forum of Allergy & Rhinology · doi:10.1002/alr.21159 · Cited by 59 · see citing works
A regulatory role for Staphylococcus aureus toxin–antitoxin system PemIKSa
Bukowski, M., Łyżeń, R., Helbin, W. M., Bonar, E., Szalewska-Pałasz, A., Węgrzyn, G., Dubin, G., Dubin, A., & Władyka, B. (2013) · Nature Communications · doi:10.1038/ncomms3012 · Cited by 58 · see citing works
Characterisation of virulence genes in methicillin susceptible and resistant Staphylococcus aureus isolates from a paediatric population in a university hospital of Medellín, Colombia
Jiménez, J. N., Ocampo, A. M., Vanegas, J. M., Rodríguez, E. A., Garcés, C., Patiño, L. A., Ospina, S., & Correa, M. M. (2011) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762011000800013 · Cited by 58 · see citing works
“Although there is controversy about the role of PVL in the spread and severity of S. aureus infections (Oliveira et al. 2002, Chambers & Deleo 2009, DeLeo et al. 2009, Otto 2010), the results of this study show the importance of this virulence factor among resistant strains and in different…”
BackgroundResult
Activation of heme biosynthesis by a small molecule that is toxic to fermenting Staphylococcus aureus
Mike, L. A., Dutter, B. F., Stauff, D. L., Moore, J. L., Vitko, N. P., Aranmolate, O., Kehl-Fie, T. E., Sullivan, S., Reid, P. R., DuBois, J. L., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303674110 · Cited by 50 · see citing works
“As part of the innate defense program, they secrete noxious chemicals to kill invading pathogens (18).”
Background
The potential use of toxin antibodies as a strategy for controlling acuteStaphylococcus aureusinfections
Cheung, G. Y. C., & Otto, M. J. (2012) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2012.682573 · Cited by 49 · see citing works
“aureus produces a large variety of virulence factors that inhibit neutrophil function [22], allowing S.”
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Staphylococcus aureus versus neutrophil: Scrutiny of ancient combat
Nasser, A., Moradi, M., Jazireian, P., Safari, H., Sani, M. A., Pourmand, M. R., & Azimi, T. (2019) · Microbial Pathogenesis · doi:10.1016/j.micpath.2019.04.026 · Cited by 49 · see citing works
Lack of a Major Role of Staphylococcus aureus Panton-Valentine Leukocidin in Lower Respiratory Tract Infection in Nonhuman Primates
Olsen, R. J., Kobayashi, S. D., Ayeras, A. A., Ashraf, M., Graves, S. F., Ragasa, W., Humbird, T. L., Greaver, J. L., Cantu, C., Swain, J. L., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090960 · Cited by 48 · see citing works
“aureus resists intracellular killing by host PMNs after phagocytosis,(49) new vaccine strategies that enhance the beneficial local immune function of IBALT may be important to study in this model.(50)”
BackgroundSelf-citation
Regulation of Staphylococcus aureus Virulence and Application of Nanotherapeutics to Eradicate S. aureus Infection
Arunachalam, K., Pandurangan, P., Shi, C., & Lagoa, R. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15020310 · Cited by 48 · see citing works
“In parallel, PMNs also activate phagocytosis to eradicate the free-living planktonic cells by reactive oxygen species (ROS) generation [26], and has a significant role in reducing the biofilms of S.”
Background
Covering all the Bases: Preclinical Development of an Effective Staphylococcus aureus Vaccine
Scully, I. L., Liberator, P., Jansen, K. U., & Anderson, A. S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00109 · Cited by 47 · see citing works
“Proc Natl Acad Sci U S A (1989) 86(22):8941–5.”
Background
Clinical utility of procalcitonin and its association with pathogenic microorganisms
Xu, H., Tian, M., & Pan, S. (2021) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408363.2021.1988047 · Cited by 47 · see citing works
“These cytokines ultimately promote the release of PCT [56,96].”
Background
Epicutaneous Model of Community-Acquired Staphylococcus aureus Skin Infections
Prabhakara, R., Foreman, O., Pascalis, R. D., Lee, G. M., Plaut, R. D., Kim, S. Y., Stibitz, S., Elkins, K. L., & Merkel, T. J. (2013) · Infection and Immunity · doi:10.1128/iai.01304-12 · Cited by 48 · see citing works
Significance of Four Methionine Sulfoxide Reductases in Staphylococcus aureus
Singh, V. K., Vaish, M., Johansson, T. R., Baum, K. R., Ring, R. P., Singh, S., Shukla, S. K., & Moskovitz, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117594 · Cited by 47 · see citing works
“to defend itself from the ROS [7].”
Flipping the switch: tools for detecting small molecule inhibitors of staphylococcal virulence
Quave, C. L., & Horswill, A. R. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00706 · Cited by 45 · see citing works
Concentration-dependent effects of antimicrobials on Staphylococcus aureus toxin-mediated cytokine production from peripheral blood mononuclear cells
Pichereau, S., Moran, J. J. M., Hayney, M. S., Shukla, S. K., Sakoulas, G., & Rose, W. E. (2011) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkr417 · Cited by 46 · see citing works
Membrane Damage Elicits an Immunomodulatory Program in Staphylococcus aureus
Attia, A. S., Benson, M. A., Stauff, D. L., Torres, V. J., & Skaar, E. P. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000802 · Cited by 44 · see citing works
“employs an arsenal of virulence factors including proteins that contribute to immune evasion and alter immune system function”
Background
Methicillin-Resistant Staphylococcus aureus: Docking-Based Virtual Screening and Molecular Dynamics Simulations to Identify Potential Penicillin-Binding Protein 2a Inhibitors from Natural Flavonoids
Masumi, M., Noormohammadi, F., Kianisaba, F., Nouri, F., Taheri‬, M., & Taherkhani, A. (2022) · International Journal of Microbiology · doi:10.1155/2022/9130700 · Cited by 44 · see citing works
Host Defence against Bacterial Biofilms: “Mission Impossible”?
Hänsch, G. M. (2012) · ISRN Immunology · doi:10.5402/2012/853123 · Cited by 44 · see citing works
“Staphylococci have developed numerous active and passive means to evade host defence mechanisms (reviewed in [127, 194–196]), and biofilm formation is just one of those.”
Background
Photodynamic therapy using intra‐articular photofrin for murine MRSA arthritis: Biphasic light dose response for neutrophil‐mediated antibacterial effect
Tanaka, M., Kinoshita, M., Yoshihara, Y., Shinomiya, N., Seki, S., Nemoto, K., Hamblin, M. R., & Morimoto, Y. (2011) · Lasers in Surgery and Medicine · doi:10.1002/lsm.21037 · Cited by 44 · see citing works
“In the case of bacterial infection, neutrophils are crucial for host defense against bacterial invasion and proliferation [18–20].”
Background
The staphylococcal surface-glycopolymer wall teichoic acid (WTA) is crucial for complement activation and immunological defense against Staphylococcus aureus infection
Kurokawa, K., Takahashi, K., & Lee, B. L. (2016) · Immunobiology · doi:10.1016/j.imbio.2016.06.003 · Cited by 40 · see citing works
Wall teichoic acids prevent antibody binding to epitopes within the cell wall of Staphylococcus aureus
Gautam, S., Kim, T., Lester, E., Deep, D., & Spiegel, D. A. (2015) · ACS Chemical Biology · doi:10.1021/acschembio.5b00439 · Cited by 40 · see citing works
Staphylococcus aureus and Host Immunity in Recurrent Furunculosis
Nowicka, D., & Grywalska, E. (2019) · Dermatology · doi:10.1159/000499184 · Cited by 39 · see citing works
Reactive Oxygen Species-Dependent Innate Immune Mechanisms Control Methicillin-Resistant Staphylococcus aureus Virulence in the Drosophila Larval Model
Ramond, E. J., Jamet, A., Ding, X., Euphrasie, D., Bouvier, C., Lallemant, L., He, X., Arbibe, L., Coureuil, M., & Charbit, A. (2021) · mBio · doi:10.1128/mbio.00276-21 · Cited by 39 · see citing works
“, phagocyte-mediated elimination via oxidative stress (by macrophages and neutrophils) and antimicrobial peptides secretion (7).”
Background
Chemical Probes Reveal an Extraseptal Mode of Cross-Linking in Staphylococcus aureus
Gautam, S., Kim, T., & Spiegel, D. A. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b02972 · Cited by 38 · see citing works
Structure-Based Identification of a Potent Inhibitor Targeting Stp1-Mediated Virulence Regulation in Staphylococcus aureus
Zheng, W., Cai, X., Xie, M., Liang, Y., Wang, T., & Li, Z. (2016) · Cell chemical biology · doi:10.1016/j.chembiol.2016.06.014 · Cited by 37 · see citing works
“…the virulence factors, including a-hemolysin (hla), leukocidin (lukD), exotoxins (lukF and lukS), and capsular polysaccharide synthesis enzymes (capA and capI), which contribute to immune evasion or alter host immune function, facilitating staphylococcal infection (DeLeo et al., 2009).”
Background
Surface Glycopolymers Are Crucial for In Vitro Anti-Wall Teichoic Acid IgG-Mediated Complement Activation and Opsonophagocytosis of Staphylococcus aureus
Lee, J.-H., Kim, N.-H., Winstel, V., Kurokawa, K., Larsen, J., An, J.-H., Khan, A., Seong, M.-Y., Lee, M. J., Andersen, P. S., et al. (2015) · Infection and Immunity · doi:10.1128/iai.00767-15 · Cited by 37 · see citing works
“aureus deploys a variety of survival and immune evasion strategies, such as the acquisition of essential nutrients and expression of adhesins, which promote colonization and survival, and the production of virulence factors, such as capsules and toxins, which aid host immune evasion (2, 3).”
Background
Deciphering agr quorum sensing in Staphylococcus aureus: insights and therapeutic prospects
Vinodhini, V., & Kavitha, M. (2024) · Molecular Biology Reports · doi:10.1007/s11033-023-08930-3 · Cited by 34 · see citing works
Activation of the SOS response increases the frequency of small colony variants
Vestergaard, M. R., Paulander, W., & Ingmer, H. (2015) · BMC Research Notes · doi:10.1186/s13104-015-1735-2 · Cited by 34 · see citing works
“As part of the host defense mechanism against infections, neutrophils generate reactive oxygen species, such as hydrogen peroxide and superoxide [22] that can damage DNA and trigger expression of the SOS regulon [21].”
Background
Staphylococcus aureus in Inflammation and Pain: Update on Pathologic Mechanisms
Rasquel-Oliveira, F. S., Ribeiro, J. M., Martelossi-Cebinelli, G., Costa, F., Nakazato, G., Casagrande, R., & Verri, W. A., Jr. (2025) · Pathogens · doi:10.3390/pathogens14020185 · Cited by 36 · see citing works
Molecular Characterization, Antibiotic Resistance, and Virulence Factors of Methicillin-Resistant Staphylococcus aureus Strains Isolated from Imported and Domestic Meat in Korea
Kim, Y. J., Oh, D. H., Song, B. R., Heo, E. J., Lim, J. S., Moon, J., Park, H. J., Wee, S. H., & Sung, K. (2015) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2014.1885 · Cited by 34 · see citing works
“It has been implicated in a number of diseases from minor skin infections to life-threatening infections, such as toxic shock syndrome, endocarditis, osteomyelitis, pneumonia, and bacteremia (Lowy, 1998; DeLeo et al. , 2009).”
Interactions of Staphylococci with Osteoblasts and Phagocytes in the Pathogenesis of Implant-Associated Osteomyelitis
Arciola, C. R., Hänsch, G. M., Visai, L., Testoni, F., Maurer, S., Campoccia, D., Selan, L., & Montanaro, L. (2012) · The International Journal of Artificial Organs · doi:10.5301/ijao.5000158 · Cited by 34 · see citing works
YpdA, a putative bacillithiol disulfide reductase, contributes to cellular redox homeostasis and virulence in Staphylococcus aureus
Mikheyeva, I. V., Thomas, J. M., Kolar, S. L., Corvaglia, A., Gaïa, N., Léo, S., François, P., Liu, G. Y., Rawat, M., & Cheung, A. L. (2019) · Molecular Microbiology · doi:10.1111/mmi.14207 · Cited by 34 · see citing works
“Bacterial cells use LMW thiols to maintain cellular redox potential and confer protection against ROS.”
BackgroundInfluential
Control of methicillin resistant Staphylococcus aureus infection utilizing a novel immunostimulatory peptide
Sheen, T. R., Cavaco, C. K., Ebrahimi, C. M., Thoman, M. L., Sanderson, S. D., Morgan, E. L., & Doran, K. S. (2011) · Vaccine · doi:10.1016/j.vaccine.2011.10.054 · Cited by 33 · see citing works
“Our results demonstrating that PMNs play an important role in defense against CA-MRSA dermal infection are consistent with previous findings [21] as neutrophils are a critical component of the innate immune response during MRSA infection [22].”
Result
Clinical and molecular epidemiology of invasive Staphylococcus aureus infection in Utah children; continued dominance of MSSA over MRSA
Crandall, H., Kapusta, A., Killpack, J., Heyrend, C., Nilsson, K., Dickey, M., Daly, J. A., Ampofo, K., Pavia, A. T., Mulvey, M. A., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0238991 · Cited by 33 · see citing works
Identification of a potent small-molecule inhibitor of bacterial DNA repair that potentiates quinolone antibiotic activity in methicillin-resistant Staphylococcus aureus
Lim, C. S. Q., Ha, K. P., Clarke, R. S., Gavin, L.-A., Cook, D. T., Hutton, J. A., Sutherell, C. L., Edwards, A. M., Evans, L. E., Tate, E. W., et al. (2019) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2019.06.025 · Cited by 33 · see citing works
Understanding the host inflammatory response to wound infection: An in vivo study of K lebsiella pneumoniae in a rabbit ear wound model
Seth, A. K., Geringer, M. R., Gurjala, A. N., Abercrombie, J. J., Chen, P., You, T., Hong, S. J., Galiano, R. D., Mustoe, T. A., & Leung, K. P. (2012) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2012.00764.x · Cited by 31 · see citing works
“To date, the majority of research aimed at defining the interaction between bacteria and their host has involved more common wound pathogens such as Staphylococcus aureus and Pseudomonas aeruginosa.(14,16,17,29) Klebsiella pneumoniae, classically an opportunistic, respiratory pathogen, triggers a destructive pneumonia…”
Background
Phenol-Soluble Modulins: Novel Virulence-Associated Peptides of Staphylococci
Li, S., Huang, H., Rao, X., Chen, W., Wang, Z., & Hu, X. (2013) · Future Microbiology · doi:10.2217/fmb.13.153 · Cited by 33 · see citing works
Intravenous curcumin efficacy on healing and scar formation in rabbit ear wounds under nonischemic, ischemic, and ischemia–reperfusion conditions
Jia, S., Xie, P., Hong, S. J., Galiano, R. D., Singer, A. J., Clark, R. A. F., & Mustoe, T. A. (2014) · Wound Repair and Regeneration · doi:10.1111/wrr.12231 · Cited by 29 · see citing works
The Staphylococcus aureus ABC-Type Manganese Transporter MntABC Is Critical for Reinitiation of Bacterial Replication Following Exposure to Phagocytic Oxidative Burst
Coady, A. M., Xu, M. J., Phung, Q. T., Cheung, T. K., Bakalarski, C. E., Alexander, M. K., Lehar, S. M., Kim, J., Park, S., Tan, M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138350 · Cited by 29 · see citing works
“During the oxidative burst (or respiratory burst) of phagocytic cells, a significant amount of reactive oxygen species (ROS) is released [18, 19].”
Background
Advanced Alcalase-Coated Clindamycin-Loaded Carbopol Nanogels for Removal of Persistent Bacterial Biofilms
Weldrick, P. J., San, S., & Paunov, V. N. (2021) · ACS Applied Nano Materials · doi:10.1021/acsanm.0c02810 · Cited by 29 · see citing works
Structure and host specificity of Staphylococcus epidermidis bacteriophage Andhra
Hawkins, N. C., Kizziah, J. L., Hatoum-Aslan, A., & Dokland, T. (2022) · Science Advances · doi:10.1126/sciadv.ade0459 · Cited by 25 · see citing works
Synergistic combinations of antimicrobial peptides against biofilms of methicillin-resistant Staphylococcus aureus (MRSA) on polystyrene and medical devices
Ciandrini, E., Morroni, G., Cirioni, O., Kamysz, W., Kamysz, E., Brescini, L., Baffone, W., & Campana, R. (2019) · Journal of Global Antimicrobial Resistance · doi:10.1016/j.jgar.2019.10.022 · Cited by 28 · see citing works
Epidemiology and Virulence of Community-Associated MRSA
Kennedy, A. D., & DeLeo, F. R. (2009) · Clinical Microbiology Newsletter · doi:10.1016/j.clinmicnews.2009.09.004 · Cited by 26 · see citing works
Self-citation
The AirSR two-component system contributes to Staphylococcus aureus survival in human blood and transcriptionally regulates sspABC operon
Hall, J. W., Yang, J., Guo, H., & Ji, Y. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00682 · Cited by 25 · see citing works
“The circulating neutrophils and monocytes are key innate cellular components to combat infection by S. aureus (Kapral and Shayegani, 1959; Mandell, 1974; Fournier and Philpott, 2005; DeLeo et al., 2009; Rigby and DeLeo, 2012; Spaan et al., 2013).”
Background
Injectable Platelet-Rich Fibrin as a Drug Carrier Increases the Antibacterial Susceptibility of Antibiotic—Clindamycin Phosphate
Egle, K., Skadiņš, I., Grava, A., Micko, L., Dubniks, V., Šalma, I., & Dubņika, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137407 · Cited by 24 · see citing works

Immunopathology of Saphylococcal Infections [34:3].
Rigby, K. M., & DeLeo, F. R. (2011)
Self-citation
Neutrophils in innate host defense against Staphylococcus aureus infections
Rigby, K. M., & DeLeo, F. R. (2012) · Seminars in Immunopathology · doi:10.1007/s00281-011-0295-3 · Cited by 400 · see citing works
Self-citation
Evasion of Neutrophil Killing by Staphylococcus aureus
McGuinness, W., Kobayashi, S. D., & DeLeo, F. R. (2016) · Pathogens · doi:10.3390/pathogens5010032 · Cited by 78 · see citing works
Self-citation
How methicillin-resistant Staphylococcus aureus evade neutrophil killing
Greenlee‐Wacker, M. C., DeLeo, F. R., & Nauseef, W. M. (2014) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000096 · Cited by 47 · see citing works
Self-citation
Evasion of Innate Host Defense by Staphylococcus aureus
DeLeo, F. R. (2008) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2008.05.122
Self-citation

Authors: DeLeo, F. R., Diep, B. A., & Otto, M.
Affiliations: National Institutes of Health (US)
University of California, San Francisco (US)
Corresponding author: DeLeo, Frank R.
ORCID: DeLeo, Frank R.
Diep, Binh An
Otto, Michael
Venue: Infectious Disease Clinics of North America
Publisher: Elsevier BV
Published: 2009-03
Volume: 23
Issue: 1
Pages: 17-34
ISSN: 0891-5520 (ISSN-L)
DOI: 10.1016/j.idc.2008.10.003
PMC: PMC2748223
OpenAlex: W2084838489
Cited by: 269
References: 103
Citations by year: 2026: 6 · 2025: 7 · 2024: 13 · 2023: 16 · 2022: 16 · 2021: 17 · 2020: 15 · 2019: 21 · 2018: 13 · 2017: 10 · 2016: 10 · 2015: 20 · 2014: 18 · 2013: 21 · 2012: 21
FWCI: 2.58
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Infectious Disease Clinics of North America (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute of Allergy and Infectious Diseases (Z01AI000900)
Topics: Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Streptococcal Infections and Treatments
Keywords: Staphylococcus aureus, host defense, innate immunity, neutrophils, virulence mechanisms, community-associated methicillin-resistant Staphylococcus aureus, pathogenesis, bacterial infection
MeSH terms: Humans, Neutrophils, Staphylococcal Infections, Staphylococcus aureus, Virulence, Virulence Factors

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Host defense and pathogenesis in Staphylococcus aureus infections

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