Host Defense and Pathogenesis in Staphylococcus aureus Infections

Infectious Disease Clinics of North America

Volumn 23, Issue 1, 2009, Pages 17-34

  DeLeo, Frank R ^a   Diep, Binh An ^b   Otto, Michael ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Innate immunity; Neutrophil; Staphylococcus; Virulence

Indexed keywords

ALPHA HEMOLYSIN; ARGININE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PANTON VALENTINE LEUKOCIDIN; REACTIVE OXYGEN METABOLITE;

ANTIBIOTIC RESISTANCE; APOPTOSIS; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CANADA; CATABOLISM; CELL DESTRUCTION; CELL FUNCTION; CELLULAR IMMUNITY; CHEMOTAXIS; DEGRANULATION; DELETION MUTANT; ENZYME SYNTHESIS; EPIDEMIC; EUROPE; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENOTYPE; GRANULOCYTE; HEALTH CARE COST; HEALTH STATUS; HOSPITAL INFECTION; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPROMISED PATIENT; INFECTION RISK; INFLAMMATION; INNATE IMMUNITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR RECOGNITION; MORTALITY; NEUTROPHIL; PATHOGENESIS; PHAGOCYTOSIS; PHENOTYPE; PULSED FIELD GEL ELECTROPHORESIS; REVIEW; SEPTICEMIA; SOUTH AND CENTRAL AMERICA; STAPHYLOCOCCUS INFECTION; SURGICAL PATIENT; UNITED STATES; VIRULENCE;

HUMANS; NEUTROPHILS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE; VIRULENCE FACTORS;

EID: 58149178679     PISSN: 08915520     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.idc.2008.10.003     Document Type: Review

References (100)

1. Diekema D.J., Pfaller M.A., Schmitz F.J., et al. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis 32 Suppl 2 (2001) S114-S132
2. Styers D., Sheehan D.J., Hogan P., et al. Laboratory-based surveillance of current antimicrobial resistance patterns and trends among Staphylococcus aureus: 2005 status in the United States. Ann Clin Microbiol Antimicrob 5 (2006) 2
3. Noskin G.A., Rubin R.J., Schentag J.J., et al. National trends in Staphylococcus aureus infection rates: impact on economic burden and mortality over a 6-year period (1998-2003). Clin Infect Dis 45 9 (2007) 1132-1140
4. Chambers H.F. The changing epidemiology of Staphylococcus aureus?. Emerg Infect Dis 7 2 (2001) 178-182
5. Klevens R.M., Morrison M.A., Nadle J., et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298 15 (2007) 1763-1771
6. Moran G.J., Krishnadasan A., Gorwitz R.J., et al. Methicillin-resistant S aureus infections among patients in the emergency department. N Engl J Med 355 7 (2006) 666-674
7. Herold B.C., Immergluck L.C., Maranan M.C., et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 279 8 (1998) 593-598
8. From the Centers for Disease Control and Prevention. Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus-Minnesota and North Dakota, 1997-1999. JAMA 282 12 (1999) 1123-1125
9. McDougal L.K., Steward C.D., Killgore G.E., et al. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 41 11 (2003) 5113-5120
10. Baba T., Takeuchi F., Kuroda M., et al. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359 9320 (2002) 1819-1827
11. Adem P.V., Montgomery C.P., Husain A.N., et al. Staphylococcus aureus sepsis and the Waterhouse-Friderichsen syndrome in children. N Engl J Med 353 12 (2005) 1245-1251
12. King M.D., Humphrey B.J., Wang Y.F., et al. Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann Intern Med 144 5 (2006) 309-317
13. Diep B.A., Gill S.R., Chang R.F., et al. Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet 367 9512 (2006) 731-739
14. Kennedy A.D., Otto M., Braughton K.R., et al. Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc Natl Acad Sci U S A 105 4 (2008) 1327-1332
15. Diep B.A., Sensabaugh G.F., Somboona N.S., et al. Widespread skin and soft-tissue infections due to two methicillin-resistant Staphylococcus aureus strains harboring the genes for Panton-Valentine leucocidin. J Clin Microbiol 42 5 (2004) 2080-2084
16. Voyich J.M., Otto M., Mathema B., et al. Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease?. J Infect Dis 194 12 (2006) 1761-1770
17. Voyich J.M., Braughton K.R., Sturdevant D.E., et al. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175 6 (2005) 3907-3919
18. Cicchetti G., Allen P.G., and Glogauer M. Chemotactic signaling pathways in neutrophils: from receptor to actin assembly. Crit Rev Oral Biol Med 13 3 (2002) 220-228
19. Standiford T.J., Arenberg D.A., Danforth J.M., et al. Lipoteichoic acid induces secretion of interleukin-8 from human blood monocytes: a cellular and molecular analysis. Infect Immun 62 1 (1994) 119-125
20. Soell M. 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. Infect Immun 63 4 (1995) 1380-1386
21. Yao L., Lowy F.D., and Berman J.W. Interleukin-8 gene expression in Staphylococcus aureus-infected endothelial cells. Infect Immun 64 8 (1996) 3407-3409
22. Krakauer T. Interleukin-8 production by human monocytic cells in response to staphylococcal exotoxins is direct and independent of interleukin-1 and tumor necrosis factor-alpha. J Infect Dis 178 2 (1998) 573-577
23. McLoughlin R.M., Solinga R.M., Rich J., et al. CD4+ T cells and CXC chemokines modulate the pathogenesis of Staphylococcus aureus wound infections. Proc Natl Acad Sci U S A 103 27 (2006) 10408-10413
24. Tzianabos A.O., Wang J.Y., and Lee J.C. Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides. Proc Natl Acad Sci U S A 98 16 (2001) 9365-9370
25. Schmeling D.J., Peterson P.K., Hammerschmidt D.E., et al. Chemotaxigenesis by cell surface components of Staphylococcus aureus. Infect Immun 26 1 (1979) 57-63
26. Wang R., Braughton K.R., Kretschmer D., et al. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13 12 (2007) 1510-1514
27. McPhail L.C., Clayton C.C., and Snyderman R. The NADPH oxidase of human polymorphonuclear leukocytes. Evidence for regulation by multiple signals. J Biol Chem 259 9 (1984) 5768-5775
28. Kobayashi S.D., Voyich J.M., Burlak C., et al. Neutrophils in the innate immune response. Arch Immunol Ther Exp (Warsz) 53 6 (2005) 505-517
29. DeLeo F.R., Renee J., Mccormick S., et al. Neutrophils exposed to bacterial lipopolysaccharide up-regulate NADPH oxidase assembly. J Clin Invest 101 2 (1998) 455-463
30. Akira S., and Takeda K. Toll-like receptor signalling. Nat Rev Immunol 4 7 (2004) 499-511
31. Sabroe I., Prince L.R., Jones E.C., et al. Selective roles for toll-like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. J Immunol 170 10 (2003) 5268-5275
32. Hayashi F., Means T.K., and Luster A.D. Toll-like receptors stimulate human neutrophil function. Blood 102 7 (2003) 2660-2669
33. Lotz S., Aga E., Wilde I., et al. Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. J Leukoc Biol 75 3 (2004) 467-477
34. Takeuchi O., Hoshino K., and Akira S. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol 165 10 (2000) 5392-5396
35. Liu C., Gelius E., Liu G., et al. Mammalian peptidoglycan recognition protein binds peptidoglycan with high affinity, is expressed in neutrophils, and inhibits bacterial growth. J Biol Chem 275 32 (2000) 24490-24499
36. Liu C., Xu Z., Gupta D., et al. Peptidoglycan recognition proteins: a novel family of four human innate immunity pattern recognition molecules. J Biol Chem 276 37 (2001) 34686-34694
37. Kanneganti T.D., Lamkanfi M., and Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 27 4 (2007) 549-559
38. Fujita T., Matsushita M., and Endo Y. The lectin-complement pathway-its role in innate immunity and evolution. Immunol Rev 198 (2004) 185-202
39. Quinn M.T., Ammons M.C., and DeLeo F.R. The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction. Clin Sci (Lond) 111 1 (2006) 1-20
40. Klebanoff S.J. Myeloperoxidase-halide-hydrogen peroxide antibacterial system. J Bacteriol 95 6 (1968) 2131-2138
41. Rosen H., and Klebanoff S.J. Formation of singlet oxygen by the myeloperoxidase-mediated antimicrobial system. J Biol Chem 252 14 (1977) 4803-4810
42. Marcinkiewicz J. Neutrophil chloramines: missing links between innate and acquired immunity. Immunol Today 18 12 (1997) 577-580
43. Klebanoff S.J. Myeloperoxidase: friend and foe. J Leukoc Biol 77 5 (2005) 598-625
44. Lekstrom-Himes J.A., and Gallin J.I. Immunodeficiency diseases caused by defects in phagocytes. N Engl J Med 343 23 (2000) 1703-1714
45. Hirsch J.G., and Cohn Z.A. Degranulation of polymorphonuclear leucocytes following phagocytosis of microorganisms. J Exp Med 112 (1960) 1005-1014
46. Faurschou M., and Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 5 14 (2003) 1317-1327
47. Ganz T., Selsted M.E., Szklarek D., et al. Defensins. Natural peptide antibiotics of human neutrophils. J Clin Invest 76 4 (1985) 1427-1435
48. Bellamy W., Takase M., Yamauchi K., et al. Identification of the bactericidal domain of lactoferrin. Biochim Biophys Acta 1121 1-2 (1992) 130-136
49. Femling J.K., Nauseef W.M., and Weiss J.P. Synergy between extracellular group IIA phospholipase A2 and phagocyte NADPH oxidase in digestion of phospholipids of Staphylococcus aureus ingested by human neutrophils. J Immunol 175 7 (2005) 4653-4661
50. Corbin B.D., Seeley E.H., Raab A., et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319 5865 (2008) 962-965
51. Brinkmann V., Reichard U., Goosmann C., et al. Neutrophil extracellular traps kill bacteria. Science 303 5663 (2004) 1532-1535
52. Savill J.S., Wyllie A.H., Henson J.E., et al. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 83 3 (1989) 865-875
53. Coxon A., Rieu P., Barkalow F.J., et al. A novel role for the β2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 5 6 (1996) 653-666
54. Kobayashi S.D., Voyich J.M., Buhl C.L., et al. Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression. Proc Natl Acad Sci U S A 99 10 (2002) 6901-6906
55. Urban C.F., Lourido S., and Zychlinsky A. How do microbes evade neutrophil killing?. Cell Microbiol 8 (2006) 1687-1696
56. DeLeo F.R. Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis 9 4 (2004) 399-413
57. Foster T.J. Immune evasion by staphylococci. Nat Rev Microbiol 3 12 (2005) 948-958
58. Gresham H.D., Lowrance J.H., Caver T.E., et al. Survival of Staphylococcus aureus inside neutrophils contributes to infection. J Immunol 164 7 (2000) 3713-3722
59. O'Riordan K., and Lee J.C. Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev 17 1 (2004) 218-234
60. Mack D., Fischer W., Krokotsch A., et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178 1 (1996) 175-183
61. Vuong C., Kocianova S., Voyich J.M., et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279 52 (2004) 54881-54886
62. Vuong C., Voyich J.M., Fischer E.R., et al. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 6 3 (2004) 269-275
63. de Haas C.J., Veldkamp K.E., Peschel A., et al. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial anti-inflammatory agent. J Exp Med 199 5 (2004) 687-695
64. Rooijakkers S.H., Ruyken M., Roos A., et al. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat Immunol 6 9 (2005) 920-927
65. Jongerius I., Kohl J., Pandey M.K., et al. Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med 204 10 (2007) 2461-2471
66. Palazzolo-Ballance A.M., Reniere M.L., Braughton K.R., et al. Neutrophil microbicides induce a pathogen survival response in community-associated methicillin-resistant Staphylococcus aureus. J Immunol 180 1 (2008) 500-509
67. Liu G.Y., Essex A., Buchanan J.T., et al. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med 202 2 (2005) 209-215
68. Sieprawska-Lupa M., Mydel P., Krawczyk K., et al. Degradation of human antimicrobial peptide LL-37 by Staphylococcus aureus-derived proteinases. Antimicrobial Agents Chemother 48 12 (2004) 4673-4679
69. Li M., Cha D.J., Lai Y., et al. The antimicrobial peptide-sensing system aps of Staphylococcus aureus. Mol Microbiol 66 5 (2007) 1136-1147
70. Li M., Lai Y., Villaruz A.E., et al. Gram-positive three-component antimicrobial peptide-sensing system. Proc Natl Acad Sci U S A 104 22 (2007) 9469-9474
71. Peschel A., Jack R.W., Otto M., et al. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J Exp Med 193 9 (2001) 1067-1076
72. Peschel A., Otto M., Jack R.W., et al. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274 13 (1999) 8405-8410
73. Joubert O., Voegelin J., Guillet V., et al. Distinction between pore assembly by staphylococcal alpha-toxin versus leukotoxins. J Biomed Biotechnol 2007 (2007) 25935
74. Langone J.J. Protein A of Staphylococcus aureus and related immunoglobulin receptors produced by streptococci and pneumonococci. Adv Immunol 32 (1982) 157-252
75. Forsgren A., and Nordstrom K. Protein A from Staphylococcus aureus: the biological significance of its reaction with IgG. Ann N Y Acad Sci 236 (1974) 252-266
76. Gomez M.I., Lee A., Reddy B., et al. Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 10 8 (2004) 842-848
77. McCormick J.K., Yarwood J.M., and Schlievert P.M. Toxic shock syndrome and bacterial superantigens: an update. Annu Rev Microbiol 55 (2001) 77-104
78. Dinges M.M., Orwin P.M., and Schlievert P.M. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13 1 (2000) 16-34
79. Bohach G.A., Fast D.J., Nelson R.D., et al. Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit Rev Microbiol 17 4 (1990) 251-272
80. Le L.Y., Baron F., and Gautier M. Staphylococcus aureus and food poisoning. Genet Mol Res 2 1 (2003) 63-76
81. Holden M.T., Feil E.J., Lindsay J.A., et al. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A 101 26 (2004) 9786-9791
82. Diep B.A., Stone G.G., Basuino L., et al. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197 1 (2008) 1523-1530
83. Gillet Y., Issartel B., Vanhems P., et al. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359 9308 (2002) 753-759
84. Chambers H.F. Community-associated MRSA-resistance and virulence converge. N Engl J Med 352 14 (2005) 1485-1487
85. Rossney A.S., Shore A.C., Morgan P.M., et al. 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. J Clin Microbiol 45 8 (2007) 2554-2563
86. Woodin A.M. Staphylococcal leukocidin. In: Montje T., Kadis S., and Ajl S. (Eds). Microbial toxins (Bacterial protein toxins) vol. 3 (1970), Academic Press, Incorporated, New York and London 327-355
87. Labandeira-Rey M., Couzon F., Boisset S., et al. Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315 5815 (2007) 1130-1133
88. Bubeck Wardenburg J., Bae T., Otto M., et al. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13 12 (2007) 1405-1406
89. Bubeck Wardenburg J., Palazzolo-Ballance A.M., Otto M., et al. Panton-Valentine leukocidin is not a virulence determinant in murine models of community-associated methicillin-resistant Staphylococcus aureus disease. J Infect Dis 198 8 (2008) 1166-1170
90. Bubeck Wardenburg J., and Schneewind O. Vaccine protection against Staphylococcus aureus pneumonia. J Exp Med 205 2 (2008) 287-294
91. Kahl B.C., and Peters G. Microbiology. Mayhem in the lung. Science 315 5815 (2007) 1082-1083
92. Diep B.A., Palazzolo-Ballance A.M., Tattevin P., et al. Contribution of Panton-Valentine leukocidin in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. PLoS ONE 3 9 (2008) e3198
93. Goering R.V., McDougal L.K., Fosheim G.E., et al. Epidemiologic distribution of the arginine catabolic mobile element among selected methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates. J Clin Microbiol 45 6 (2007) 1981-1984
94. Ellington M.J., Yearwood L., Ganner M., et al. Distribution of the ACME-arcA gene among methicillin-resistant Staphylococcus aureus from England and Wales. J Antimicrob Chemother 61 1 (2008) 73-77
95. Stevens D.L., Ma Y., Salmi D.B., et al. Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillin-resistantStaphylococcus aureus. J Infect Dis 195 2 (2007) 202-211
96. Moncada S., and Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 329 27 (1993) 2002-2012
97. Bhakdi S., and Tranum-Jensen J. Alpha-toxin of Staphylococcus aureus. Microbiol Rev 55 4 (1991) 733-751
98. Valeva A., Walev I., Pinkernell M., et al. Transmembrane beta-barrel of staphylococcal alpha-toxin forms in sensitive but not in resistant cells. Proc Natl Acad Sci U S A 94 21 (1997) 11607-11611
99. Diep B.A., Chambers H.F., Graber C.J., et al. Emergence of multidrug-resistant, community-associated, methicillin-resistant Staphylococcus aureus clone USA300 in men who have sex with men. Ann Intern Med 148 4 (2008) 249-257
100. Montgomery C.P., Boyle-Vavra S., Adem P.V., et al. Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J Infect Dis 198 4 (2008) 561-570