Production of an Attenuated Phenol-Soluble Modulin Variant Unique to the MRSA Clonal Complex 30 Increases Severity of Bloodstream Infection

PLoS Pathogens

Volumn 10, Issue 8, 2014, Pages

  Cheung, Gordon Y C ^a   Kretschmer, Dorothee ^b   Duong, Anthony C ^a   Yeh, Anthony J ^a   Ho, Trung V ^a   Chen, Yan ^a   Joo, Hwang Soo ^a   Kreiswirth, Barry N ^c   Peschel, Andreas ^b   Otto, Michael ^a  

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

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOXIN; BACTERIAL TOXIN; STAPHYLOCOCCAL DELTA TOXIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEREMIA; BLOODSTREAM INFECTION; CALCIUM TRANSPORT; CYTOLYSIS; DISEASE SEVERITY; GENE EXPRESSION; GENETIC VARIABILITY; HEMOLYSIS; HISTOPATHOLOGY; HUMAN; IMMUNE EVASION; IMMUNE RESPONSE; LEUKOCYTE ACTIVATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PLASMID; POINT MUTATION; SKIN INFECTION; STAPHYLOCOCCUS INFECTION; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOLOGY; INNATE IMMUNITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NEUTROPHIL;

ANIMALS; BACTEREMIA; BACTERIAL TOXINS; BLOTTING, WESTERN; CHEMOTAXIS, LEUKOCYTE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; NEUTROPHIL INFILTRATION; NEUTROPHILS; STAPHYLOCOCCAL INFECTIONS;

EID: 84922807659     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004298     Document Type: Article

References (39)

1. Lowy FD, (1998) Staphylococcus aureus infections. N Engl J Med 339: 520–532.
2. Foster TJ, (2005) Immune evasion by staphylococci. Nat Rev Microbiol 3: 948–958.
3. Otto M, (2012) MRSA virulence and spread. Cell Microbiol 14: 1513–1521.
4. Otto M, (2013) Community-associated MRSA: what makes them special? Int J Med Microbiol 303: 324–330.
5. Cox RA, Conquest C, Mallaghan C, Marples RR, (1995) A major outbreak of methicillin-resistant Staphylococcus aureus caused by a new phage-type (EMRSA-16). J Hosp Infect 29: 87–106.
6. Johnson AP, Aucken HM, Cavendish S, Ganner M, Wale MC, et al. (2001) Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS). J Antimicrob Chemother 48: 143–144.
7. McAdam PR, Templeton KE, Edwards GF, Holden MT, Feil EJ, et al. (2012) Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 109: 9107–9112.
8. Fowler VG, JrNelson CL, McIntyre LM, Kreiswirth BN, Monk A, et al. (2007) Potential associations between hematogenous complications and bacterial genotype in Staphylococcus aureus infection. J Infect Dis 196: 738–747.
9. DeLeo FR, Kennedy AD, Chen L, Bubeck Wardenburg J, Kobayashi SD, et al. (2011) Molecular differentiation of historic phage-type 80/81 and contemporary epidemic Staphylococcus aureus. Proc Natl Acad Sci U S A 108: 18091–18096.
10. Peschel A, Otto M, (2013) Phenol-soluble modulins and staphylococcal infection. Nat Rev Microbiol 11: 667–673.
11. Wang R, Braughton KR, Kretschmer D, Bach TH, Queck SY, et al. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13: 1510–1514.
12. Cheung GY, Duong AC, Otto M, (2012) Direct and synergistic hemolysis caused by Staphylococcus phenol-soluble modulins: implications for diagnosis and pathogenesis. Microbes Infect 14: 380–386.
13. Rasigade JP, Trouillet-Assant S, Ferry T, Diep BA, Sapin A, et al. (2013) PSMs of hypervirulent Staphylococcus aureus act as intracellular toxins that kill infected osteoblasts. PLoS One 8: e63176.
14. Kretschmer D, Gleske AK, Rautenberg M, Wang R, Koberle M, et al. (2010) Human formyl peptide receptor 2 senses highly pathogenic Staphylococcus aureus. Cell Host Microbe 7: 463–473.
15. Cheung GY, Joo HS, Chatterjee SS, Otto M, (2013) Phenol-soluble modulins - critical determinants of staphylococcal virulence. FEMS Microbiol Rev doi: 10.1111/1574-6976.12057. [Epub ahead of print]
16. Graves SF, Kobayashi SD, Braughton KR, Whitney AR, Sturdevant DE, et al. (2012) Sublytic concentrations of Staphylococcus aureus Panton-Valentine leukocidin alter human PMN gene expression and enhance bactericidal capacity. J Leukoc Biol 92: 361–374.
17. Joo HS, Otto M, (2014) The isolation and analysis of phenol-soluble modulins of Staphylococcus epidermidis. Methods Mol Biol 1106: 93–100.
18. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, et al. (2004) 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: 9786–9791.
19. Queck SY, Jameson-Lee M, Villaruz AE, Bach TH, Khan BA, et al. (2008) 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.
20. Traber KE, Lee E, Benson S, Corrigan R, Cantera M, et al. (2008) agr function in clinical Staphylococcus aureus isolates. Microbiology 154: 2265–2274.
21. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, et al. (1993) Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12: 3967–3975.
22. Joo HS, Cheung GY, Otto M, (2011) Antimicrobial activity of community-associated methicillin-resistant Staphylococcus aureus is caused by phenol-soluble modulin derivatives. J Biol Chem 286: 8933–8940.
23. Prat C, Bestebroer J, de Haas CJ, van Strijp JA, van Kessel KP, (2006) A new staphylococcal anti-inflammatory protein that antagonizes the formyl peptide receptor-like 1. J Immunol 177: 8017–8026.
24. de Haas CJ, Veldkamp KE, Peschel A, Weerkamp F, Van Wamel WJ, et al. (2004) Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 199: 687–695.
25. Duong AC, Cheung GY, Otto M, (2012) Interaction of phenol-soluble modulins with phosphatidylcholine vesicles. Pathogens 1: 3–11.
26. Kobayashi SD, Malachowa N, Whitney AR, Braughton KR, Gardner DJ, et al. (2011) Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection. J Infect Dis 204: 937–941.
27. Surewaard BG, de Haas CJ, Vervoort F, Rigby KM, DeLeo FR, et al. (2013) Staphylococcal alpha-phenol soluble modulins contribute to neutrophil lysis after phagocytosis. Cell Microbiol 15: 1427–1437.
28. Spaan AN, Surewaard BG, Nijland R, van Strijp JA, (2013) Neutrophils versus Staphylococcus aureus: a biological tug of war. Annu Rev Microbiol 67: 629–650.
29. Holzinger D, Gieldon L, Mysore V, Nippe N, Taxman DJ, et al. (2012) Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome. J Leukoc Biol 92: 1069–1081.
30. Yoong P, Pier GB, (2012) Immune-activating properties of Panton-Valentine leukocidin improve the outcome in a model of methicillin-resistant Staphylococcus aureus pneumonia. Infect Immun 80: 2894–2904.
31. Hermos CR, Yoong P, Pier GB, (2010) High levels of antibody to Panton-Valentine leukocidin are not associated with resistance to Staphylococcus aureus-associated skin and soft-tissue infection. Clin Infect Dis 51: 1138–1146.
32. Yoong P, Pier GB, (2010) Antibody-mediated enhancement of community-acquired methicillin-resistant Staphylococcus aureus infection. Proc Natl Acad Sci U S A 107: 2241–2246.
33. Fowler VG, JrSakoulas G, McIntyre LM, Meka VG, Arbeit RD, et al. (2004) 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 190: 1140–1149.
34. Paulander W, Nissen Varming A, Baek KT, Haaber J, Frees D, et al. (2013) Antibiotic-mediated selection of quorum-sensing-negative Staphylococcus aureus. mBio 3: e00459-00412.
35. Cheung GY, Kretschmer D, Queck SY, Joo HS, Wang R, et al. (2014) Insight into structure-function relationship in phenol-soluble modulins using an alanine screen of the phenol-soluble modulin (PSM) alpha3 peptide. FASEB J 28: 153–161.
36. Chatterjee SS, Joo HS, Duong AC, Dieringer TD, Tan VY, et al. (2013) Essential Staphylococcus aureus toxin export system. Nat Med 19: 364–367.
37. Bae T, Schneewind O, (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58–63.
38. Peschel A, Ottenwalder B, Gotz F, (1996) Inducible production and cellular location of the epidermin biosynthetic enzyme EpiB using an improved staphylococcal expression system. FEMS Microbiol Lett 137: 279–284.
39. Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, et al. (2006) Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194: 1761–1770.