Phenol-soluble modulins and staphylococcal infection

Nature Reviews Microbiology

Volumn 11, Issue 10, 2013, Pages 667-673

  Peschel, Andreas ^a   Otto, Michael ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; ANTISTAPHYLOCOCCAL DRUG; AUROGRAB; BACTERIAL TOXIN; MONOCLONAL ANTIBODY; PEPTIDE; PHENOL SOLUBLE MODULIN; STAPHYLOCOCCUS VACCINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBACTERIAL ACTIVITY; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOFILM; CYTOLYSIS; DRUG TARGETING; GENE STRUCTURE; HOST RESISTANCE; IMMUNE RESPONSE; INNATE IMMUNITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NEUTROPHIL; PATHOGENESIS; PEPTIDE ANALYSIS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS INFECTION; TOXIN ANALYSIS; VACCINATION;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL TOXINS; BIOFILMS; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HUMANS; MOLECULAR SEQUENCE DATA; NEUTROPHILS; PHAGOCYTOSIS; QUORUM SENSING; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

STAPHYLOCOCCUS AUREUS;

EID: 84884279163     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3110     Document Type: Review

References (65)

1. Wertheim, H. F. et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 5, 751-762 (2005). (Pubitemid 41688980)
2. Lowy, F. D. Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532 (1998).
3. Klevens, R. M. et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298, 1763-1771 (2007). (Pubitemid 47598444)
4. Otto, M. Staphylococcus epidermidis - the 'accidental' pathogen. Nature Rev. Microbiol. 7, 555-567 (2009).
5. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322 (1999). (Pubitemid 29289651)
6. Foster, T. J. Immune evasion by staphylococci. Nature Rev. Microbiol. 3, 948-958 (2005). (Pubitemid 43078158)
7. Wang, R. et al. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nature Med. 13, 1510-1514 (2007). (Pubitemid 350224240)
8. Kobayashi, S. D. et al. Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection. J. Infect. Dis. 204, 937-941 (2011).
9. Mehlin, C., Headley, C. M. & Klebanoff, S. J. An inflammatory polypeptide complex from Staphylococcus epidermidis: isolation and characterization. J. Exp. Med. 189, 907-918 (1999).
10. McKevitt, A. I., Bjornson, G. L., Mauracher, C. A. & Scheifele, D. W. Amino acid sequence of a deltalike toxin from Staphylococcus epidermidis. Infect. Immun. 58, 1473-1475 (1990). (Pubitemid 20151818)
11. Kretschmer, D. et al. Human formyl peptide receptor 2 senses highly pathogenic Staphylococcus aureus. Cell Host Microbe 7, 463-473 (2010).
12. Hajjar, A. M. et al. Cutting edge: functional interactions between Toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J. Immunol. 166, 15-19 (2001). (Pubitemid 32038411)
13. Liles, W. C., Thomsen, A. R., O'Mahony, D. S. & Klebanoff, S. J. Stimulation of human neutrophils and monocytes by staphylococcal phenol-soluble modulin. J. Leukoc. Biol. 70, 96-102 (2001). (Pubitemid 32613668)
14. Otto, M., O'Mahoney, D. S., Guina, T. & Klebanoff, S. J. Activity of Staphylococcus epidermidis phenol-soluble modulin peptides expressed in Staphylococcus carnosus. J. Infect. Dis. 190, 748-755 (2004). (Pubitemid 39050005)
15. Periasamy, S., Chatterjee, S. S., Cheung, G. Y. & Otto, M. Phenol-soluble modulins in staphylococci: What are they originally for? Commun. Integr. Biol. 5, 275-277 (2012).
16. Cheung, G. Y. et al. Staphylococcus epidermidis strategies to avoid killing by human neutrophils. PLoS Pathog. 6, e1001133 (2010).
17. Rautenberg, M., Joo, H. S., Otto, M. & Peschel, A. Neutrophil responses to staphylococcal pathogens and commensals via the formyl peptide receptor 2 relates to phenol-soluble modulin release and virulence. Faseb J. 25, 1254-1263 (2011).
18. Kornblum, J., Kreiswirth, B., Projan, S. J., Ross, H. & Novick, R. P. in Molecular Biology of the Staphylococci (ed. Novick, R. P.) 373-402 (VCH Publishers, 1990).
19. Vuong, C. et al. Regulated expression of pathogen-associated molecular pattern molecules in Staphylococcus epidermidis: quorum-sensing determines pro-inflammatory capacity and production of phenol-soluble modulins. Cell. Microbiol. 6, 753-759 (2004). (Pubitemid 39077381)
20. Yao, Y., Sturdevant, D. E. & Otto, M. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J. Infect. Dis. 191, 289-298 (2005). (Pubitemid 40096388)
21. Tsompanidou, E. et al. Distinct roles of phenol-soluble modulins in spreading of Staphylococcus aureus on wet surfaces. Appl. Environ. Microbiol. 79, 886-895 (2013).
22. Periasamy, S. et al. How Staphylococcus aureus biofilms develop their characteristic structure. Proc. Natl Acad. Sci. USA 109, 1281-1286 (2012).
23. Wang, R. et al. Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J. Clin. Invest. 121, 238-248 (2011).
24. Donvito, B. et al. Synergistic hemolytic activity of Staphylococcus lugdunensis is mediated by three peptides encoded by a non-agr genetic locus. Infect. Immun. 65, 95-100 (1997). (Pubitemid 27008908)
25. Watson, D. C., Yaguchi, M., Bisaillon, J. G., Beaudet, R. & Morosoli, R. The amino acid sequence of a gonococcal growth inhibitor from Staphylococcus haemolyticus. Biochem. J. 252, 87-93 (1988).
26. Cheung, G. Y., Wang, R., Khan, B. A., Sturdevant, D. E. & Otto, M. Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect. Immun. 79, 1927-1935 (2011).
27. Kretschmer, D., Nikola, N., Durr, M., Otto, M. & Peschel, A. The virulence regulator Agr controls the staphylococcal capacity to activate human neutrophils via the formyl peptide receptor 2. J. Innate Immun. 4, 201-212 (2012).
28. Queck, S. Y. et al. RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell 32, 150-158 (2008).
29. Queck, S. Y. et al. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. PLoS Pathog. 5, e1000533 (2009).
30. Chatterjee, S. S. et al. Distribution and regulation of the mobile genetic element-encoded phenol-soluble modulin PSM-mec in methicillin-resistant Staphylococcus aureus. PLoS ONE 6, e28781 (2011).
31. Kaito, C. et al. Transcription and translation products of the cytolysin gene psm-mec on the mobile genetic element SCCmec regulate Staphylococcus aureus virulence. PLoS Pathog. 7, e1001267 (2011).
32. Kaito, C. et al. Mobile genetic element SCCmec-encoded psm-mec RNA suppresses translation of agrA and attenuates MRSA virulence. PLoS Pathog. 9, e1003269 (2013).
33. Somerville, G. A. et al. Synthesis and deformylation of Staphylococcus aureus δ-toxin are linked to tricarboxylic acid cycle activity. J. Bacteriol. 185, 6686-6694 (2003). (Pubitemid 37385889)
34. Chatterjee, S. S. et al. Essential Staphylococcus aureus toxin export system. Nature Med. 19, 346-347 (2013).
35. Otto, M. Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu. Rev. Microbiol. 64, 143-162 (2010).
36. Loffler, B. et al. Staphylococcus aureus Panton- Valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog. 6, e1000715 (2010).
37. Cheung, G. Y., Duong, A. C. & Otto, M. Direct and synergistic hemolysis caused by Staphylococcus phenol-soluble modulins: implications for diagnosis and pathogenesis. Microbes Infect. 14, 380-386 (2012).
38. Li, M. et al. Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc. Natl Acad. Sci. USA 106, 5883-5888 (2009).
39. Rasigade, J. P. et al. PSMs of hypervirulent Staphylococcus aureus act as intracellular toxins that kill infected osteoblasts. PLoS ONE 8, e63176 (2013).
40. Surewaard, B. G. et al. Inactivation of staphylococcal phenol soluble modulins by serum lipoprotein particles. PLoS Pathog. 8, e1002606 (2012).
41. Surewaard, B. et al. Staphylococcal alpha-phenol soluble modulins contribute to neutrophil lysis after phagocytosis. Cell. Microbiol. 15, 1427-1437 (2013).
42. Geiger, T. et al. The stringent response of Staphylococcus aureus and its impact on survival after phagocytosis through the induction of intracellular PSMs expression. PLoS Pathog. 8, e1003016 (2012).
43. Carnes, E. C. et al. Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nature Chem. Biol. 6, 41-45 (2010).
44. DeLeo, F. R. & Otto, M. An antidote for Staphylococcus aureus pneumonia? J. Exp. Med. 205, 271-274 (2008). (Pubitemid 351281592)
45. O'Toole, G. A. To build a biofilm. J. Bacteriol. 185, 2687-2689 (2003). (Pubitemid 36514578)
46. Vuong, C., Gerke, C., Somerville, G. A., Fischer, E. R. & Otto, M. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J. Infect. Dis. 188, 706-718 (2003). (Pubitemid 37115184)
47. Vuong, C., Kocianova, S., Yao, Y., Carmody, A. B. & Otto, M. Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo. J. Infect. Dis. 190, 1498-1505 (2004). (Pubitemid 39332191)
48. Vuong, C., Saenz, H. L., Gotz, F. & Otto, M. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182, 1688-1693 (2000).
49. Yarwood, J. M., Bartels, D. J., Volper, E. M. & Greenberg, E. P. Quorum sensing in Staphylococcus aureus biofilms. J. Bacteriol. 186, 1838-1850 (2004). (Pubitemid 38314529)
50. Schwartz, K., Syed, A. K., Stephenson, R. E., Rickard, A. H. & Boles, B. R. Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog. 8, e1002744 (2012).
51. Cogen, A. L. et al. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J. Invest. Dermatol. 130, 192-200 (2010).
52. Joo, H. S., Cheung, G. Y. & Otto, M. Antimicrobial activity of community-associated methicillin-resistant Staphylococcus aureus is caused by phenol-soluble modulin derivatives. J. Biol. Chem. 286, 8933-8940 (2011).
53. Ye, R. D. et al. International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol. Rev. 61, 119-161 (2009).
54. Bloes, D. A., Otto, M., Peschel, A. & Kretschmer, D. Enterococcus faecium stimulates human neutrophils via the formyl-peptide receptor 2. PLoS ONE 7, e39910 (2012).
55. Liu, M. et al. Formylpeptide receptors are critical for rapid neutrophil mobilization in host defense against Listeria monocytogenes. Sci. Rep. 2, 786 (2012).
56. Schreiner, J. et al. Staphylococcus aureus phenol-soluble modulin peptides modulate dendritic cell functions and increase in vitro priming of regulatory T cells. J. Immunol. 190, 3417-3426 (2013).
57. Prat, C., Bestebroer, J., de Haas, C. J., van Strijp, J. A. & van Kessel, K. P. A new staphylococcal anti-inflammatory protein that antagonizes the formyl peptide receptor-like 1. J. Immunol. 177, 8017-8026 (2006). (Pubitemid 44846319)
58. Prat, C. et al. A homolog of formyl peptide receptor-like 1 (FPRL1) inhibitor from Staphylococcus aureus (FPRL1 inhibitory protein) that inhibits FPRL1 and FPR. J. Immunol. 183, 6569-6578 (2009).
59. Romano, M. Lipoxin and aspirin-triggered lipoxins. ScientificWorldJournal 10, 1048-1064 (2010).
60. Forsman, H., Christenson, K., Bylund, J. & Dahlgren, C. Receptor-dependent and -independent immunomodulatory effects of phenol-soluble modulin peptides from Staphylococcus aureus on human neutrophils are abrogated through peptide inactivation by reactive oxygen species. Infect. Immun. 80, 1987-1995 (2012).
61. Kennedy, A. D. et al. Targeting of α-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J. Infect. Dis. 202, 1050-1058 (2010).
62. Anderson, A. S. et al. Staphylococcus aureus manganese transport protein C is a highly conserved cell surface protein that elicits protective immunity against S. aureus and Staphylococcus epidermidis. J. Infect. Dis. 205, 1688-1696 (2012).
63. Burnie, J. P. et al. Identification of an immunodominant ABC transporter in methicillin-resistant Staphylococcus aureus infections. Infect. Immun. 68, 3200-3209 (2000). (Pubitemid 30340410)
64. Otto, M. Novel targeted immunotherapy approaches for staphylococcal infection. Expert Opin. Biol. Ther. 10, 1049-1059 (2010).
65. Doshi, R., Gutmann, D. A., Khoo, Y. S., Fagg, L. A. & van Veen, H. W. The choreography of multidrug export. Biochem. Soc. Trans. 39, 807-811 (2011).