Home LiteratureArticle Details
PMID: 20829608 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

agr-Dependent interactions of Staphylococcus aureus USA300 with human polymorphonuclear neutrophils.

Journal of innate immunity ·Vol. 2 ·No. 6 ·2010-00-00 ·Pages 546-59

Pang YY, Schwartz J, Thoendel M, Ackermann LW, Horswill AR, Nauseef WM

Abstract

The emergence of serious infections due to community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) has fueled interest in the contributions of specific staphylococcal virulence factors to clinical disease. To assess the contributions of agr-dependent factors to the fate of organisms in polymorphonuclear neutrophils (PMN), we examined the consequences for organism and host cells of feeding PMN with wild-type CA-MRSA (LAC) or CA-MRSA (LAC agr KO) at different multiplicities of infection (MOIs). Phagocytosed organisms rapidly increased the transcription of RNAIII in a time- and MOI-dependent fashion; extracellular USA300 (LAC) did not increase RNAIII expression despite having the capacity to respond to autoinducing peptide-enriched culture medium. HOCl-mediated damage and intracellular survival were the same in the wild-type and USA300 (LAC agr KO). PMN lysis by ingested USA300 (LAC) was time- and MOI-dependent and, at MOIs >1, required α-hemolysin (hla) as USA300 (LAC agr KO) and USA300 (LAC hla KO) promoted PMN lysis only at high MOIs. Taken together, these data demonstrate activation of the agr operon in human PMN with the subsequent production of α-hemolysin and PMN lysis. The extent to which these events in the phagosomes of human PMN contribute to the increased morbidity and mortality of infections with USA300 (LAC) merits further study.

MeSH Terms
Bacterial Proteins/genetics,metabolism Bacterial Toxins/genetics,metabolism Cell Death/genetics Cells, Cultured Community-Acquired Infections/immunology,microbiology Gene Expression Regulation, Bacterial Gene Knockout Techniques Hemolysin Proteins/genetics,metabolism Host-Pathogen Interactions Humans Methicillin-Resistant Staphylococcus aureus/pathogenicity,physiology Neutrophils/immunology,metabolism,microbiology,pathology Phagocytosis/genetics RNA, Bacterial/biosynthesis,genetics Staphylococcal Infections/immunology,microbiology Trans-Activators/genetics,metabolism Virulence Factors
Chemicals
Agr protein, Staphylococcus aureus Bacterial Proteins Bacterial Toxins Hemolysin Proteins RNA, Bacterial RNAIII, Staphylococcus aureus Trans-Activators Virulence Factors staphylococcal alpha-toxin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Pang Yun Yun
Department of Medicine, Roy J and Lucille A Carver College of Medicine, University of Iowa, Iowa City, Iowa 52241, USA.
Schwartz Jamie
Thoendel Matthew
Ackermann Laynez W
Horswill Alexander R
Nauseef William M
References (44)
44 references, click to expand
  1. Autoinduction and signal transduction in the regulation of staphylococcal virulence.
    Mol Microbiol. 2003 Jun;48(6):1429-49 PMID: 12791129
  2. Biofilm dispersal of community-associated methicillin-resistant Staphylococcus aureus on orthopedic implant material.
    J Orthop Res. 2010 Jan;28(1):55-61 PMID: 19610092
  3. Methicillin-resistant Staphylococcus aureus disease in three communities.
    N Engl J Med. 2005 Apr 7;352(14):1436-44 PMID: 15814879
  4. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils.
    J Immunol. 2005 Sep 15;175(6):3907-19 PMID: 16148137
  5. Genetic systems in staphylococci.
    Methods Enzymol. 1991;204:587-636 PMID: 1658572
  6. Staphylococcus aureus RN6390 replicates and induces apoptosis in a pulmonary epithelial cell line.
    Infect Immun. 2000 Sep;68(9):5385-92 PMID: 10948168
  7. Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002.
    J Infect Dis. 2006 Jan 15;193(2):172-9 PMID: 16362880
  8. Quorum sensing in staphylococci.
    Annu Rev Genet. 2008;42:541-64 PMID: 18713030
  9. Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification.
    Proc Natl Acad Sci U S A. 2008 Jan 29;105(4):1327-32 PMID: 18216255
  10. Common methodology is inadequate for studies on the microbicidal activity of neutrophils.
    J Leukoc Biol. 2006 Jan;79(1):87-94 PMID: 16244110
  11. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era.
    J Clin Invest. 2009 Sep;119(9):2464-74 PMID: 19729844
  12. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule.
    EMBO J. 1993 Oct;12(10):3967-75 PMID: 7691599
  13. Toxicity of staphylococcal alpha toxin for rabbit alveolar macrophages.
    Infect Immun. 1983 Jan;39(1):439-44 PMID: 6822424
  14. Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation.
    Infect Immun. 2009 Apr;77(4):1623-35 PMID: 19188357
  15. Isolation of human neutrophils from venous blood.
    Methods Mol Biol. 2007;412:15-20 PMID: 18453102
  16. Global analysis of community-associated methicillin-resistant Staphylococcus aureus exoproteins reveals molecules produced in vitro and during infection.
    Cell Microbiol. 2007 May;9(5):1172-90 PMID: 17217429
  17. Myeloperoxidase: friend and foe.
    J Leukoc Biol. 2005 May;77(5):598-625 PMID: 15689384
  18. Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria.
    Nat Chem Biol. 2010 Jan;6(1):41-5 PMID: 19935660
  19. Transmembrane beta-barrel of staphylococcal alpha-toxin forms in sensitive but not in resistant cells.
    Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11607-11 PMID: 9326657
  20. How human neutrophils kill and degrade microbes: an integrated view.
    Immunol Rev. 2007 Oct;219:88-102 PMID: 17850484
  21. Regulation of exoprotein gene expression in Staphylococcus aureus by agar.
    Mol Gen Genet. 1986 Jan;202(1):58-61 PMID: 3007938
  22. Rapid neutrophil destruction following phagocytosis of Staphylococcus aureus.
    J Innate Immun. 2010;2(6):560-75 PMID: 20587998
  23. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia.
    Nat Med. 2007 Dec;13(12):1405-6 PMID: 18064027
  24. Biphasic intracellular expression of Staphylococcus aureus virulence factors and evidence for Agr-mediated diffusion sensing.
    Mol Microbiol. 2003 Aug;49(4):919-27 PMID: 12890018
  25. PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40(phox).
    Nat Cell Biol. 2001 Jul;3(7):679-82 PMID: 11433301
  26. Neutrophil bleaching of GFP-expressing staphylococci: probing the intraphagosomal fate of individual bacteria.
    J Immunol. 2009 Aug 15;183(4):2632-41 PMID: 19620311
  27. agr expression precedes escape of internalized Staphylococcus aureus from the host endosome.
    Infect Immun. 2001 Nov;69(11):7074-82 PMID: 11598083
  28. Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome: implications for microbial killing.
    J Biol Chem. 2006 Dec 29;281(52):39860-9 PMID: 17074761
  29. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12055-9 PMID: 8618843
  30. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore.
    Science. 1996 Dec 13;274(5294):1859-66 PMID: 8943190
  31. Direct real-time evaluation of nitration with green fluorescent protein in solution and within human cells reveals the impact of nitrogen dioxide vs. peroxynitrite mechanisms.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3481-6 PMID: 11904413
  32. The survival of staphylococci within human leukocytes.
    J Exp Med. 1952 Feb;95(2):209-30 PMID: 14907971
  33. Neutrophil microbicides induce a pathogen survival response in community-associated methicillin-resistant Staphylococcus aureus.
    J Immunol. 2008 Jan 1;180(1):500-9 PMID: 18097052
  34. Cinemicrophotographic observations on granule lysis in polymorphonuclear leucocytes during phagocytosis.
    J Exp Med. 1962 Dec 1;116:827-34 PMID: 13961191
  35. Kinetics of fusion of the cytoplasmic granules with phagocytic vacuoles in human polymorphonuclear leukocytes. Biochemical and morphological studies.
    J Cell Biol. 1980 Apr;85(1):42-59 PMID: 7364874
  36. Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003.
    Clin Infect Dis. 2006 Feb 1;42(3):389-91 PMID: 16392087
  37. Is quorum sensing a side effect of diffusion sensing?
    Trends Microbiol. 2002 Aug;10(8):365-70 PMID: 12160634
  38. Selective activation of sar promoters with the use of green fluorescent protein transcriptional fusions as the detection system in the rabbit endocarditis model.
    Infect Immun. 1998 Dec;66(12):5988-93 PMID: 9826382
  39. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA.
    Nat Med. 2007 Dec;13(12):1510-4 PMID: 17994102
  40. Inactivation of a bacterial virulence pheromone by phagocyte-derived oxidants: new role for the NADPH oxidase in host defense.
    Proc Natl Acad Sci U S A. 2004 Sep 21;101(38):13867-72 PMID: 15353593
  41. Differential recognition of Staphylococcus aureus quorum-sensing signals depends on both extracellular loops 1 and 2 of the transmembrane sensor AgrC.
    J Mol Biol. 2008 Aug 29;381(2):300-9 PMID: 18582472
  42. Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus.
    Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5883-8 PMID: 19293374
  43. Fluorescent reporters for Staphylococcus aureus.
    J Microbiol Methods. 2009 Jun;77(3):251-60 PMID: 19264102
  44. Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia.
    Infect Immun. 2007 Feb;75(2):1040-4 PMID: 17101657
Article Info
Journal
Journal of innate immunity
Abbr.
J Innate Immun
ISSN
1662-8128
Published
2010-00-00
Epub
2010-00-10
Pages
546-59
Language
English
Region
Switzerland
NLM ID
101469471
PMCID
PMC2982852
Subset
IM
Grants
BLRD VA · I01 BX000513 · United States
NIAID NIH HHS · R01 AI07958 · United States
NIAID NIH HHS · T32 AI 7511 · United States
NIAID NIH HHS · R01 AI078921 · United States
NIAID NIH HHS · T32 AI007511 · United States
NIGMS NIH HHS · T32 GM007337 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]