The DOI matches its Crossref record; 57 of the 58 references it cites were found in a registry or an index.
Insights into Mechanisms Used by Staphylococcus aureus to Avoid Destruction by Human Neutrophils
Abstract
Polymorphonuclear leukocytes (PMNs, or neutrophils) are critical for human innate immunity and kill most invading bacteria. However, pathogens such as Staphylococcus aureus avoid destruction by PMNs to survive, thereby causing human infections. The molecular mechanisms used by pathogens to circumvent killing by the immune system remain largely undefined. To that end, we studied S. aureus pathogenesis and bacteria-PMN interactions using strains originally isolated from individuals with community-acquired (CA) and hospital-acquired infections. Compared with strains from hospital infections (COL and MRSA252), strain MW2 and a methicillin-susceptible relative, MnCop, were significantly more virulent in a mouse model of S. aureus infection, and caused the greatest level of pathology in major vital organs. Although phagocytosis of each strain triggered production of reactive oxygen species and granule-phagosome fusion, those from CA infections were significantly more resistant to killing by human PMNs and caused greater host cell lysis. Microarray analysis of the strains during neutrophil phagocytosis identified genes comprising a global S. aureus response to human innate host defense. Genes involved in capsule synthesis, gene regulation, oxidative stress, and virulence, were up-regulated following ingestion of the pathogen. Notably, phagocytosis of strains from CA infections induced changes in gene expression not observed in the other strains, including up-regulation of genes encoding virulence factors and hypothetical proteins. Our studies reveal a gene transcription program in a prominent human pathogen that likely contributes to evasion of innate host defense.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“which appears to have enhanced virulence as compared to the traditional hospital-associated MRSA strains [26], [27], [28].”
From Interactions of Methicillin Resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in Polymicrobial Wound Infection (2013) · cites this paper as [28]
Citations
Cites
Staphylococcus aureus Infections
Lowy, F. D. (1998) · New England Journal of Medicine · doi:10.1056/nejm199808203390806 · Cited by 6,018
Bodey, G. P., BUCKLEY, M., SATHE, Y. S., & FREIREICH, E. J. (1966) · Annals of Internal Medicine · doi:10.7326/0003-4819-64-2-328 · Cited by 2,465
Exotoxins of Staphylococcus aureus
Dinges, M. M., Orwin, P. M., & Schlievert, P. M. (2000) · Clinical Microbiology Reviews · doi:10.1128/cmr.13.1.16-34.2000 · Cited by 1,837
Vandenesch, F., Naimi, T. S., Enright, M. C., Lina, G., Nimmo, G. R., Heffernan, H., Liassine, N., Bes, M., Greenland, T., Reverdy, M. E., et al. (2003) · Emerging infectious diseases · doi:10.3201/eid0908.030089 · Cited by 1,718
Naimi, T. S. (2003) · JAMA · doi:10.1001/jama.290.22.2976 · Cited by 1,688
Gillet, Y., Issartel, B., Vanhems, P., Fournet, J.-C., Lina, G., Bes, M., Vandenesch, F., Piémont, Y., Brousse, N., Floret, D., et al. (2002) · The Lancet · doi:10.1016/s0140-6736(02)07877-7 · Cited by 1,514
Methicillin-Resistant Staphylococcus aureus Disease in Three Communities
Fridkin, S. K., Hageman, J. C., Morrison, M., Sanza, L. T., Como-Sabetti, K., Jernigan, J. A., Harriman, K., Harrison, L. H., Lynfield, R., & Farley, M. M. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa043252 · Cited by 1,493
Herold, B. C. (1998) · JAMA · doi:10.1001/jama.279.8.593 · Cited by 1,412
McDougal, L. K., Steward, C. D., Killgore, G., Chaitram, J. M., McAllister, S. K., & Tenover, F. C. (2003) · Journal of Clinical Microbiology · doi:10.1128/jcm.41.11.5113-5120.2003 · Cited by 1,410
Genome and virulence determinants of high virulence community-acquired MRSA
Baba, T., Takeuchi, F., Kuroda, M., Yuzawa, H., Aoki, K.-I., Oguchi, A., Nagai, Y., Iwama, N., Asano, K., Naimi, T. S., et al. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08713-5 · Cited by 1,356
Research works printed but not linked: 56
- 1998, N. Engl. J. Med., 520
- 2003, Infect. Control Hosp. Epidemiol., 451
- 2000, Clin. Microbiol. Rev., 16
- 2004, Proc. Natl. Acad. Sci. USA, 12312
- 2002, Lancet, 1819
- 2001, Proc. Natl. Acad. Sci. USA, 8821
- 1999, J. Am. Med. Assoc., 1123
- 1989, Am. J. Dis. Child., 848
- 2005, N. Engl. J. Med., 1445
- 2005, N. Engl. J. Med., 468
- 2004, Clin. Infect. Dis., 1446
- 2005, Clin. Infect. Dis., 100
- 2004, Proc. Natl. Acad. Sci. USA, 9786
- 1979, Infect. Immun., 902
- 1998, J. Am. Med. Assoc., 593
- 2003, J. Clin. Microbiol., 5113
- 2003, Proc. Natl. Acad. Sci. USA, 10948
- 1999, J. Immunol., 6732
- 2003, Proc. Natl. Acad. Sci. USA, 1996
- 2002, Lancet, 753
- 2000, J. Immunol., 3713
- 2003, FEBS Lett., 54
- 2004, Clin. Microbiol. Rev., 218
- 2003, J. Bacteriol., 6686
- 2003, Mol. Microbiol., 1429
- 2003, Mol. Microbiol., 807
- 2004, FEMS Immunol. Med. Microbiol., 1
- 2004, J. Bacteriol., 3029
- 2000, J. Bacteriol., 4822
- 2000, Trends Microbiol., 274
- 2002, Proc. Natl. Acad. Sci. USA, 6901
- 2003, J. Leukocyte Biol., 315
- 2003, J. Immunol., 3357
- 2004, J. Immunol., 636
- 2004, Biochem. Soc. Trans., 474
- 2005, N. Engl. J. Med., 1485
- 2005, N. Engl. J. Med., 1436
- 2003, J. Am. Med. Assoc., 2976
- 2003, Emerg. Infect. Dis., 978
- 2001, Clin. Infect. Dis., 990
- 2004, J. Clin. Microbiol., 5673
- 2001, J. Am. Med. Assoc., 1201
- 1999, Clin. Infect. Dis., 797
- 2000, N. Engl. J. Med., 1703
- 1930, J. Am. Med. Assoc., 780
- 1966, Ann. Intern. Med., 328
- 1979, Medicine (Baltimore)., 128
- 1976, Am. J. Med., 849
- 2000, Infect. Immun., 6162
- 1997, Infect. Immun., 2517
- 2004, J. Immunol., 1194
- 2004, J. Clin. Invest., 1732
- 2004, J. Clin. Microbiol., 3752
- 2002, Clin. Infect. Dis., 819
- 2005, J. Clin. Microbiol., 3373
- 2004, Microbes. Infect., 1117
Cited by
Sorted by citations
Items 501–559 of 559
Host Defense against Staphylococcal Infection
Gresham, H. D., & Foster, T. J. (2009) · Wiley eBooks · doi:10.1002/9781444308464.ch7
Faroka, D., Rahayu, S., & Rifa’i, M. (2013) · The Journal of Experimental Life Sciences · doi:10.21776/ub.jels.2013.003.01.03
Insights into the SaeR/S-mediated pathogenesis of Staphylococcus aureus
Nygaard, T. K. (2011) · Montana State University ScholarWorks (Montana State University)
Schneider, J. E. T. (2015) · Scholarship@Western (Western University)
Inhibition of Virulence as Treatment Strategies for Staphylococcus aureus Infection
Daly, S. M. (2015) · UNM’s Digital Repository (University of New Mexico)
Gouveia, C. M. F. (2010) · Repositório da Universidade de Lisboa (University of Lisbon)
Pontier, S. (2007) · Revue des Maladies Respiratoires · doi:10.1016/s0761-8425(07)92813-2
Scott, S. (2006) · ACSMʼs Health & Fitness Journal · doi:10.1249/01.fit.0000252531.41939.0f
Bamberger, D. M., Goers, M., Quinn, T., & Herndon, B. (2012) · Advances in Infectious Diseases · doi:10.4236/aid.2012.22007
The importance of phenol-soluble modulins in Staphylococcus aureus infections
Altenburg, A. F. (2013) · Utrecht University Repository (Utrecht University)
Mead, J. S. (2013) · Montana State University ScholarWorks (Montana State University)
Long, D. R. (2012) · Montana State University ScholarWorks (Montana State University)
Molecular determinants involved during Staphylococcus aureus colonization and/or infection
Askarian, F. (2014) · NORA - Norwegian Open Research Archives
Study of in vivo interactions between penicillin-binding proteins of Staphylococcus aureus
Gonçalves, R. D. S. M. P. (2015) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Role of novel peptide, EP67, in controlling bacterial infection
Cavaco, C. K. (2012) · CSUN ScholarWorks (California State University, Northridge)
Estudo do gene ric de staphylococcus aureus
Godinho, C. S. C. (2012) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Neutrophil Responses to Mixed-Species Anaerobic Biofilms
Lockhart, J. (2015) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/27088
Microbial interactions with epithelial surfaces
Strandberg, K. L. (2009) · University of Minnesota Digital Conservancy (University of Minnesota)
DEVELOPMENT OF BACTERIAL STRAINS BY INDUCED MUTATIONS
Monajjemi, R. (2016) · International Journal of Plant Animal and Environmental Sciences
Neutrophil killing of Staphylococcus aureus In Sepsis
Nazari, S. (2017) · Otago University Research Archive (University of Otago)
Kyanya, C. K., Nyasinga, J., Matano, D., Oundo, V., Wacira, S., Sang, W., & Musila, L. A. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/390955
Yamada, K. J. (2019) · DigitalCommons@UNMC
Assessment of irradiated Staphylococcus aureus isolates as a vaccine
Gamal, I. M., El-Sonbaty, S. M., Mahmoud, H., Alam, H. A., & Abdelkhalek, N. S. (2018) · Benha Veterinary Medical Journal · doi:10.21608/bvmj.2018.48552
Yang, F., Liu, S., Xu, Y. S., Walker, S. G., Cho, W., Mironava, T., & Rafailovich, M. H. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3813471
Novel compounds inhibiting HIV infection, breast cancer metastasis, and bacterial growth
Shepard, J. B. (2012) · Montana State University ScholarWorks (Montana State University)
Kobayashi, S. D., & DeLeo, F. R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-801496-7.00005-8
Self-citationOethinger, M. D., & Campbell, S. M. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374419-7.00003-2
Mecsas, J. C. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.729805496.793562327
(2009) · Archives of Facial Plastic Surgery · doi:10.1001/archfaci.2008.537
Characterization of Staphylococcus aureus Lipase
Vijayakumaran, V. (2013) · Scholarship@Western (Western University)
Bolbot, Y. K., Бордий, Т. А., Алифанова, С. В., & Kalichevska, M. V. (2022) · CHILD`S HEALTH · doi:10.22141/2224-0551.17.3.2022.1510
Immune Evasion and Interaction Between Autophagy and Intracellular Staphylococcus aureus
Asano, K. (2024) · Springer eBooks · doi:10.1007/978-981-99-9428-1_6
A programmable, selection-free CRISPR interference system in Staphylococcus aureusPreprint
Miah, R., Johannessen, M., Kjos, M., & Lentz, C. S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.27.625599
Waigh, T. A. (2024) · Cambridge University Press eBooks · doi:10.1017/9781009313506.029
Interacting Bacteria and Biofilms
Waigh, T. A. (2024) · Cambridge University Press eBooks · doi:10.1017/9781009313506.024
Precipitated probe on aetiology of MRSA skin infections: a global concern
Rani, K. (2024) · Journal of Bacteriology & Mycology Open Access · doi:10.15406/jbmoa.2024.12.00387
Predtechenskaya, M., Arbizzani, C. J., Shomento, S. R., Borgogna, T. R., & Voyich, J. M. (2025) · Microbiology Spectrum · doi:10.1128/spectrum.01386-24
Self-citationStaphylococcus aureus Infections (Coagulase-Positive Staphylococci)
Kaplan, S. L., & Hultén, K. G. (2025) · Elsevier eBooks · doi:10.1016/b978-0-323-82763-8.00080-7
Cui, X., Qi, J., Yi, C., Liu, J., Yuan, X., Deng, W., & Xu, H. (2025) · Frontiers in Ophthalmology · doi:10.3389/fopht.2025.1719090
Larm, A. L. (2014) · Loyola eCommons (Loyola University of Chicago)
Edet, U. O., Nwaokorie, F. O., Mbim, E. N., Asanga, E. E., Ogar, A. Y., Okoroiwu, H. U., Edet, B. O., Umoafia, N., & Nkang, A. E. (2022) · Figshare · doi:10.6084/m9.figshare.20342357
Gökalsın, B. (2026) · Journal of Anatolian Environmental and Animal Sciences · doi:10.35229/jaes.1858655
Extracellular vesicles in S. aureus pathogenesis in a mastitis context
Tartaglia, N. R. (2018) · theses.fr (ABES) · doi:10.70675/2a1a6c5bz3e8cz412dz99cez5f04fe3a0b62
da Luz, B. S. R. (2022) · theses.fr (ABES) · doi:10.70675/2e2fa4bfz4a44z4eb8za456z56828affa1d9
Bacterial kinase in ESKAPE pathogen: regulators of virulence and novel therapeutic targets
Sharma, S., & Tiwari, V. (2026) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2026.2655678
Maji, S., Dam, S., Kumari, A., Sharma, H., Sharma, N., Rana, N. K., Samadder, A., & Bhattacharyya, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.16.732695
Vogl, C., Mikula, L. C., Marbach, H., Mayer-Weihrauch, K., Herndler, S., Breitschopf, L., Pickering, A. C., Jobson, M.-E., Rosel, A. C., Dinhopl, N., et al. (2026) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2026.1930
Askarian, F., Sun, D., Tat, J., Sorrentino, J. T., Kousha, A., Sauceda, C., Yendluri, S., Yan, Y., Yau, K. P. S., Masson, H. O., et al. (2026) · Science Advances · doi:10.1126/sciadv.aeh4023
Staphylococcal Leukocidin Receptor Identification: Hiding in Plain Sight
Spaan, A. N. (2015) · Utrecht University Repository (Utrecht University)
The Role of Reactive Chlorine Species in Bacterial Killing by Neutrophils
Coker, M. S. A. (2011) · Otago University Research Archive (University of Otago)
Burns, E. M. (2009) · Cardinal Scholar (Ball State University)
Metadata
- Authors
- Voyich, J. M., Braughton, K. R., Sturdevant, D. E., Whitney, A. R., Saïd-Salim, B., Porcella, S. F., Long, R. D., Dorward, D. W., Gardner, D. J., Kreiswirth, B. N., Musser, J. M., & DeLeo, F. R.
- Affiliations
- National Institutes of Health (US)
- Public Health Research Institute Tuberculosis Center, International Center for Public Health , Newark, NJ 07103
- International Center for Public Health (US)
- Baylor College of Medicine (US)
- ORCID
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2005-09
- Volume
- 175
- Issue
- 6
- Pages
- 3907-3919
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W1848320945
- Cited by
- 563
- References
- 58
- Citations by year
- 2026: 5 · 2025: 17 · 2024: 25 · 2023: 10 · 2022: 20 · 2021: 16 · 2020: 17 · 2019: 23 · 2018: 29 · 2017: 34 · 2016: 29 · 2015: 31 · 2014: 33 · 2013: 49 · 2012: 43
- FWCI
- 12.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Health Sciences › Medicine › Infectious Diseases › Streptococcal Infections and Treatments
- Keywords
- Staphylococcus aureus, polymorphonuclear leukocytes, innate immunity, phagocytosis, community-acquired infections, nosocomial infections, virulence, capsule synthesis, oxidative stress, gene expression response, virulence factors, methicillin-resistant Staphylococcus aureus, host-pathogen interaction
- MeSH terms
- Genes, Bacterial, Humans, Immunity, Innate, Neutrophils, Phagocytosis, Staphylococcal Infections, Staphylococcus aureus, Gene Expression Regulation, Bacterial, Gene Expression Profiling, Virulence Factors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review