Phenol-soluble modulins

International Journal of Medical Microbiology

Volumn 304, Issue 2, 2014, Pages 164-169

  Otto, Michael ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Biofilm; Cytolysis; Leukotoxin; Neutrophils; Phenol soluble modulins; Staphylococcus aureus; Staphylococcus epidermidis; Toxins

Indexed keywords

BIOFILM; CYTOLYSIS; LEUKOTOXIN; NEUTROPHILS; PHENOL-SOLUBLE MODULINS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TOXINS;

ANIMALS; BACTERIAL TOXINS; BIOFILMS; HUMANS; STAPHYLOCOCCUS; SURFACE-ACTIVE AGENTS; VIRULENCE FACTORS;

EID: 84893746228     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2013.11.019     Document Type: Short Survey

References (67)

1. Alksne L.E., Projan S.J. Bacterial virulence as a target for antimicrobial chemotherapy. Curr. Opin. Biotechnol. 2000, 11:625-636.
2. Angelini T.E., Roper M., Kolter R., Weitz D.A., Brenner M.P. Bacillus subtilis spreads by surfing on waves of surfactant. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18109-18113.
3. Bhakdi S., Tranum-Jensen J. Alpha-toxin of Staphylococcus aureus. Microbiol. Rev. 1991, 55:733-751.
4. Boles B.R., Thoendel M., Singh P.K. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol. Microbiol. 2005, 57:1210-1223.
5. Bowden M.G., Chen W., Singvall J., Xu Y., Peacock S.J., Valtulina V., Speziale P., Hook M. Identification and preliminary characterization of cell-wall-anchored proteins of Staphylococcus epidermidis. Microbiology 2005, 151:1453-1464.
6. Carnes E.C., Lopez D.M., Donegan N.P., Cheung A., Gresham H., Timmins G.S., Brinker C.J. Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat. Chem. Biol. 2010, 6:41-45.
7. Chatterjee S.S., Chen L., Joo H.S., Cheung G.Y., Kreiswirth B.N., Otto M. Distribution and regulation of the mobile genetic element-encoded phenol-soluble modulin PSM-mec in methicillin-resistant Staphylococcus aureus. PLoS ONE 2011, 6:e28781.
8. Chatterjee S.S., Joo H.S., Duong A.C., Dieringer T.D., Tan V.Y., Song Y., Fischer E.R., Cheung G.Y., Li M., Otto M. Essential Staphylococcus aureus toxin export system. Nat. Med. 2013, 19:364-367.
9. 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. 2012, 14:380-386.
10. Cheung G.Y., Rigby K., Wang R., Queck S.Y., Braughton K.R., Whitney A.R., Teintze M., DeLeo F.R., Otto M. Staphylococcus epidermidis strategies to avoid killing by human neutrophils. PLoS Pathog. 2010, 6:e1001133.
11. Cogen A.L., Yamasaki K., Sanchez K.M., Dorschner R.A., Lai Y., MacLeod D.T., Torpey J.W., Otto M., Nizet V., Kim J.E., Gallo R.L. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J. Invest. Dermatol. 2010, 130:192-200.
12. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284:1318-1322.
13. Donvito B., Etienne J., Denoroy L., Greenland T., Benito Y., Vandenesch F. Synergistic hemolytic activity of Staphylococcus lugdunensis is mediated by three peptides encoded by a non-agr genetic locus. Infect. Immun. 1997, 65:95-100.
14. DuMont A.L., Yoong P., Surewaard B.G., Benson M.A., Nijland R., van Strijp J.A., Torres V.J. Staphylococcus aureus elaborates leukocidin AB to mediate escape from within human neutrophils. Infect. Immun. 2013, 81:1830-1841.
15. Duong A.C., Cheung G.Y., Otto M. Interaction of phenol-soluble modulins with phosphatidylcholine vesicles. Pathogens 2012, 1:3-11.
16. Foster T.J. Immune evasion by staphylococci. Nat. Rev. Microbiol. 2005, 3:948-958.
17. Fowler V.G., Sakoulas G., McIntyre L.M., Meka V.G., Arbeit R.D., Cabell C.H., Stryjewski M.E., Eliopoulos G.M., Reller L.B., Corey G.R., Jones T., Lucindo N., Yeaman M.R., Bayer A.S. Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidal protein. J. Infect. Dis. 2004, 190:1140-1149.
18. Frenette M., Beaudet R., Bisaillon J.G., Sylvestre M., Portelance V. Chemical and biological characterization of a gonococcal growth inhibitor produced by Staphylococcus haemolyticus isolated from urogenital flora. Infect. Immun. 1984, 46:340-345.
19. Geiger T., Francois P., Liebeke M., Fraunholz M., Goerke C., Krismer B., Schrenzel J., Lalk M., Wolz C. The stringent response of Staphylococcus aureus and its impact on survival after phagocytosis through the induction of intracellular PSMs expression. PLoS Pathog. 2012, 8:e1003016.
20. Goerke C., Campana S., Bayer M.G., Doring G., Botzenhart K., Wolz C. Direct quantitative transcript analysis of the agr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect. Immun. 2000, 68:1304-1311.
21. Grice E.A., Kong H.H., Conlan S., Deming C.B., Davis J., Young A.C., Bouffard G.G., Blakesley R.W., Murray P.R., Green E.D., Turner M.L., Segre J.A. Topographical and temporal diversity of the human skin microbiome. Science 2009, 324:1190-1192.
22. Inoshima I., Inoshima N., Wilke G.A., Powers M.E., Frank K.M., Wang Y., Bubeck Wardenburg J. A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat. Med. 2011, 17:1310-1314.
23. 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. 2011, 286:8933-8940.
24. Joo H.S., Otto M. Molecular basis of in vivo biofilm formation by bacterial pathogens. Chem. Biol. 2012, 19:1503-1513.
25. Kaito C., Saito Y., Ikuo M., Omae Y., Mao H., Nagano G., Fujiyuki T., Numata S., Han X., Obata K., Hasegawa S., Yamaguchi H., Inokuchi K., Ito T., Hiramatsu K., Sekimizu K. Mobile genetic element SCCmec-encoded psm-mec RNA suppresses translation of agra and attenuates MRSA virulence. PLoS Pathog. 2013, 9:e1003269.
26. Kim H.K., Thammavongsa V., Schneewind O., Missiakas D. Recurrent infections and immune evasion strategies of Staphylococcus aureus. Curr. Opin. Microbiol. 2012, 15:92-99.
27. Kloos W.E., Musselwhite M.S. Distribution and persistence of Staphylococcus and Micrococcus species and other aerobic bacteria on human skin. Appl. Microbiol. 1975, 30:381-385.
28. Kobayashi S.D., Malachowa N., Whitney A.R., Braughton K.R., Gardner D.J., Long D., Bubeck Wardenburg J., Schneewind O., Otto M., DeLeo F.R. Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection. J. Infect. Dis. 2011, 204:937-941.
29. Kocianova S., Vuong C., Yao Y., Voyich J.M., Fischer E.R., DeLeo F.R., Otto M. Key role of poly-gamma-dl-glutamic acid in immune evasion and virulence of Staphylococcus epidermidis. J. Clin. Invest. 2005, 115:688-694.
30. Kretschmer D., Gleske A.K., Rautenberg M., Wang R., Koberle M., Bohn E., Schoneberg T., Rabiet M.J., Boulay F., Klebanoff S.J., van Kessel K.A., van Strijp J.A., Otto M., Peschel A. Human formyl peptide receptor 2 senses highly pathogenic Staphylococcus aureus. Cell Host Microbe 2010, 7:463-473.
31. Loffler B., Hussain M., Grundmeier M., Bruck M., Holzinger D., Varga G., Roth J., Kahl B.C., Proctor R.A., Peters G. Staphylococcus aureus Panton-Valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog. 2010, 6:e1000715.
32. Lowy F.D. Staphylococcus aureus infections. N. Engl. J. Med. 1998, 339:520-532.
33. McKevitt A.I., Bjornson G.L., Mauracher C.A., Scheifele D.W. Amino acid sequence of a deltalike toxin from Staphylococcus epidermidis. Infect. Immun. 1990, 58:1473-1475.
34. Mehlin C., Headley C.M., Klebanoff S.J. An inflammatory polypeptide complex from Staphylococcus epidermidis: isolation and characterization. J. Exp. Med. 1999, 189:907-918.
35. Novick R.P., Schlievert P., Ruzin A. Pathogenicity and resistance islands of staphylococci. Microbes Infect. 2001, 3:585-594.
36. O'Toole G., Kaplan H.B., Kolter R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54:49-79.
37. Otto M. Virulence factors of the coagulase-negative staphylococci. Front. Biosci. 2004, 9:841-863.
38. Otto M. Staphylococcus epidermidis - the 'accidental' pathogen. Nat. Rev. Microbiol. 2009, 7:555-567.
39. Otto M. Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu. Rev. Microbiol. 2010, 64:143-162.
40. Otto M. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu. Rev. Med. 2013, 64:175-188.
41. Periasamy S., Chatterjee S.S., Cheung G.Y., Otto M. Phenol-soluble modulins in staphylococci: what are they originally for?. Commun. Integr. Biol. 2012, 5:275-277.
42. Periasamy S., Joo H.S., Duong A.C., Bach T.H., Tan V.Y., Chatterjee S.S., Cheung G.Y., Otto M. How Staphylococcus aureus biofilms develop their characteristic structure. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1281-1286.
43. Queck S.Y., Jameson-Lee M., Villaruz A.E., Bach T.H., Khan B.A., Sturdevant D.E., Ricklefs S.M., Li M., Otto M. RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell 2008, 32:150-158.
44. Queck S.Y., Khan B.A., Wang R., Bach T.H., Kretschmer D., Chen L., Kreiswirth B.N., Peschel A., DeLeo F.R., Otto M. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. PLoS Pathog. 2009, 5:e1000533.
45. Rasigade J.P., Trouillet-Assant S., Ferry T., Diep B.A., Sapin A., Lhoste Y., Ranfaing J., Badiou C., Benito Y., Bes M., Couzon F., Tigaud S., Lina G., Etienne J., Vandenesch F., Laurent F. PSMs of hypervirulent Staphylococcus aureus act as intracellular toxins that kill infected osteoblasts. PLoS ONE 2013, 8:e63176.
46. 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. 2011, 25:1254-1263.
47. Rooijakkers S.H., van Kessel K.P., van Strijp J.A. Staphylococcal innate immune evasion. Trends Microbiol. 2005, 13:596-601.
48. Schreiner J., Kretschmer D., Klenk J., Otto M., Buhring H.J., Stevanovic S., Wang J.M., Beer-Hammer S., Peschel A., Autenrieth S.E. Staphylococcus aureus phenol-soluble modulin peptides modulate dendritic cell functions and increase in vitro priming of regulatory T cells. J. Immunol. 2013, 190:3417-3426.
49. 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. 2012, 8:e1002744.
50. Shopsin B., Drlica-Wagner A., Mathema B., Adhikari R.P., Kreiswirth B.N., Novick R.P. Prevalence of agr dysfunction among colonizing Staphylococcus aureus strains. J. Infect. Dis. 2008, 198:1171-1174.
51. Somerville G.A., Beres S.B., Fitzgerald J.R., DeLeo F.R., Cole R.L., Hoff J.S., Musser J.M. In vitro serial passage of Staphylococcus aureus: changes in physiology, virulence factor production, and agr nucleotide sequence. J. Bacteriol. 2002, 184:1430-1437.
52. Surewaard B., de Haas C., Vervoort F., Rigby K., DeLeo F., Otto M., van Strijp J., Nijland R. Staphylococcal alpha-phenol soluble modulins contribute to neutrophil lysis after phagocytosis. Cell. Microbiol. 2013, 15:1427-1437.
53. Surewaard B.G., Nijland R., Spaan A.N., Kruijtzer J.A., de Haas C.J., van Strijp J.A. Inactivation of staphylococcal phenol soluble modulins by serum lipoprotein particles. PLoS Pathog. 2012, 8:e1002606.
54. Talbot J.C., Thiaudiere E., Vincent M., Gallay J., Siffert O., Dufourcq J. Dynamics and orientation of amphipathic peptides in solution and bound to membranes: a steady-state and time-resolved fluorescence study of staphylococcal delta-toxin and its synthetic analogues. Eur. Biophys. J. 2001, 30:147-161.
55. Traber K.E., Lee E., Benson S., Corrigan R., Cantera M., Shopsin B., Novick R.P. agr Function in clinical Staphylococcus aureus isolates. Microbiology 2008, 154:2265-2274.
56. Tsompanidou E., Denham E.L., Becher D., de Jong A., Buist G., van Oosten M., Manson W.L., Back J.W., van Dijl J.M., Dreisbach A. Distinct roles of phenol-soluble modulins in spreading of Staphylococcus aureus on wet surfaces. Appl. Environ. Microbiol. 2013, 79:886-895.
57. Valeva A., Walev I., Pinkernell M., Walker B., Bayley H., Palmer M., Bhakdi S. Transmembrane beta-barrel of staphylococcal alpha-toxin forms in sensitive but not in resistant cells. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:11607-11611.
58. Vandenesch F., Naimi T., Enright M.C., Lina G., Nimmo G.R., Heffernan H., Liassine N., Bes M., Greenland T., Reverdy M.E., Etienne J. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg. Infect. Dis. 2003, 9:978-984.
59. Ventura C.L., Malachowa N., Hammer C.H., Nardone G.A., Robinson M.A., Kobayashi S.D., DeLeo F.R. Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS ONE 2010, 5:e11634.
60. Voyich J.M., Braughton K.R., Sturdevant D.E., Whitney A.R., Said-Salim B., Porcella S.F., Long R.D., Dorward D.W., Gardner D.J., Kreiswirth B.N., Musser J.M., DeLeo F.R. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 2005, 175:3907-3919.
61. Vuong C., Durr M., Carmody A.B., Peschel A., Klebanoff S.J., Otto M. 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. 2004, 6:753-759.
62. Vuong C., Gerke C., Somerville G.A., Fischer E.R., Otto M. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J. Infect. Dis. 2003, 188:706-718.
63. 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. 2004, 190:1498-1505.
64. 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. 2000, 182:1688-1693.
65. Wang R., Braughton K.R., Kretschmer D., Bach T.H., Queck S.Y., Li M., Kennedy A.D., Dorward D.W., Klebanoff S.J., Peschel A., DeLeo F.R., Otto M. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat. Med. 2007, 13:1510-1514.
66. Wang R., Khan B.A., Cheung G.Y., Bach T.H., Jameson-Lee M., Kong K.F., Queck S.Y., Otto M. Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J. Clin. Invest. 2011, 121:238-248.
67. 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. 2005, 191:289-298.