Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Ventura, Christy L ^a,c   Malachowa, Natalia ^a   Hammer, Carl H ^b   Nardone, Glenn A ^b   Robinson, Mary Ann ^b   Kobayashi, Scott D ^a   DeLeo, Frank R ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

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

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEUKOTOXIN; BACTERIAL PROTEIN; EXOTOXIN;

ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL SURFACE; CHANNEL GATING; CONTROLLED STUDY; CULTURE MEDIUM; CYTOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PROTEIN ANALYSIS; PROTEIN SECRETION; PROTEOMICS; STAPHYLOCOCCUS AUREUS; TANDEM MASS SPECTROMETRY; WILD TYPE; CELL CULTURE; CELL MEMBRANE; DRUG EFFECT; GENETICS; IMMUNOBLOTTING; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; NEUTROPHIL; POLYACRYLAMIDE GEL ELECTROPHORESIS;

BACTERIA (MICROORGANISMS); METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; ORYCTOLAGUS CUNICULUS; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; CELL MEMBRANE; CELLS, CULTURED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXOTOXINS; HUMANS; IMMUNOBLOTTING; MASS SPECTROMETRY; NEUTROPHILS; PROTEOMICS; STAPHYLOCOCCUS AUREUS;

EID: 77955399259     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011634     Document Type: Article

References (55)

1. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF (2010) Communityassociated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557- 1568.
2. King MD, Humphrey BJ, Wang YF, Kourbatova EV, Ray SM, et al. (2006) 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: 309-317.
3. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, et al. (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355: 666-674.
4. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, et al. (2003) Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 41: 5113-5120.
5. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, et al. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
6. Li M, Diep BA, Villaruz AE, Braughton KR, Jiang X, et al. (2009) Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 106: 5883-5888.
7. 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.
8. DeLeo FR, Diep BA, Otto M (2009) Host defense and pathogenesis in Staphylococcus aureus infections. Infect Dis Clin North Am 23: 17-34.
9. Rodriguez-Ortega MJ, Norais N, Bensi G, Liberatori S, Capo S, et al. (2006) Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol 24: 191-197. nbt1179 [pii];10.1038/nbt1179 [doi].
10. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48: 1429-1449.
11. Gardy JL, Laird MR, Chen F, Rey S, Walsh CJ, et al. (2005) PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21: 617-623. bti057 [pii];10.1093/bioinformatics/bti057 [doi].
12. Sakata N, Terakubo S, Mukai T (2005) Subcellular location of the soluble lytic transglycosylase homologue in Staphylococcus aureus. Curr Microbiol 50: 47-51. 10.1007/s00284-004-4381-9 [doi].
13. Gatlin CL, Pieper R, Huang ST, Mongodin E, Gebregeorgis E, et al. (2006) Proteomic profiling of cell envelope-associated proteins from Staphylococcus aureus. Proteomics 6: 1530-1549.
14. Jones RC, Deck J, Edmondson RD, Hart ME (2008) Relative quantitative comparisons of the extracellular protein profiles of Staphylococcus aureus UAMS-1 and its sarA, agr, and sarA agr regulatory mutants using onedimensional polyacrylamide gel electrophoresis and nanocapillary liquid chromatography coupled with tandem mass spectrometry. J Bacteriol 190: 5265-5278. JB.00383-08 [pii];10.1128/JB.00383-08 [doi].
15. Nandakumar R, Nandakumar MP, Marten MR, Ross JM (2005) Proteome analysis of membrane and cell wall associated proteins from Staphylococcus aureus. J Proteome Res 4: 250-257. 10.1021/pr049866k [doi].
16. Taverna F, Negri A, Piccinini R, Zecconi A, Nonnis S, et al. (2007) Characterization of cell wall associated proteins of a Staphylococcus aureus isolated from bovine mastitis case by a proteomic approach. Vet Microbiol 119: 240-247. S0378-1135(06)00376-2 [pii];10.1016/j.vetmic.2006.09.007 [doi].
17. Clarke SR, Foster SJ (2006) Surface adhesins of Staphylococcus aureus. Adv Microb Physiol 51: 187-224. S0065-2911(06)51004-5 [pii];10.1016/S0065- 2911(06)51004-5 [doi].
18. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
19. Luong T, Sau S, Gomez M, Lee JC, Lee CY (2002) Regulation of Staphylococcus aureus capsular polysaccharide expression by agr and sarA. Infect Immun 70: 444-450.
20. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731-739.
21. Nygaard TK, DeLeo FR, Voyich JM (2008) Community-associated methicillinresistant Staphylococcus aureus skin infections: advances toward identifying the key virulence factors. Curr Opin Infect Dis 21: 147-152. 10.1097/QCO.0- b013e3282f64819 [doi];00001432-200804000-00007 [pii].
22. Luong TT, Dunman PM, Murphy E, Projan SJ, Lee CY (2006) Transcription profiling of the mgrA Regulon in Staphylococcus aureus. J Bacteriol 188: 1899-1910.
23. Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, et al. (2006) Is Panton-Valentine leukocidin the major virulence determinant in communityassociated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194: 1761-1770.
24. Palazzolo-Ballance AM, Reniere ML, Braughton KR, Sturdevant DE, Otto M, et al. (2008) Neutrophil microbicides induce a pathogen survival response in community-associated methicillin-resistant Staphylococcus aureus. J Immunol 180: 500-509.
25. Bae T, Schneewind O (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
26. Graves SF, Kobayashi SD, Braughton KR, Diep BA, Chambers HF, et al. (2010) Relative contribution of Panton-Valentine leukocidin to PMN plasma membrane permeability and lysis caused by USA300 and USA400 culture supernatants. Microbes Infect, S1286-4579(10)00053-5 [pii];10.1016/j.micinf. 2010.02.005 [doi].
27. Diep BA, Palazzolo-Ballance AM, Tattevin P, Basuino L, Braughton KR, et al. (2008) Contribution of Panton-Valentine leukocidin in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. PLoS ONE 3: e3198.
28. Solis N, Larsen MR, Cordwell SJ (2010) Improved accuracy of cell surface shaving proteomics in Staphylococcus aureus using a false-positive control. Proteomics 10: 2037-2049. 10.1002/pmic.200900564 [doi].
29. Rahman A, Izaki K, Kamio Y (1993) Gamma-hemolysin genes in the same family with lukF and lukS genes in methicillin resistant Staphylococcus aureus. Biosci Biotechnol Biochem 57: 1234-1236.
30. Prevost G, Cribier B, Couppie P, Petiau P, Supersac G, et al. (1995) Panton- Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect Immun 63: 4121-4129.
31. Gravet A, Colin DA, Keller D, Girardot R, Monteil H, et al. (1998) Characterization of a novel structural member, LukE-LukD, of the bicomponent staphylococcal leucotoxins family. FEBS Lett 436: 202-208.
32. Choorit W, Kaneko J, Muramoto K, Kamio Y (1995) Existence of a new protein component with the same function as the LukF component of leukocidin or gamma-hemolysin and its gene in Staphylococcus aureus P83. FEBS Lett 357: 260-264. 0014-5793(94)01372-8 [pii].
33. Woodin AM (1960) Purification of the two components of leucocidin from Staphylococcus aureus. Biochem J 75: 158-165.
34. Panton PN, Valentine FCO (1932) Staphylococcal toxin. Lancet 219: 506-508.
35. Rahman A, Nariya H, Izaki K, Kato I, Kamio Y (1992) Molecular cloning and nucleotide sequence of leukocidin F-component gene (lukF) from methicillin resistant Staphylococcus aureus. Biochem Biophys Res Commun 184: 640-646. 0006-291X(92)90637-Z [pii].
36. Rahman A, Izaki K, Kato I, Kamio Y (1991) Nucleotide sequence of leukocidin S-component gene (lukS) from methicillin resistant Staphylococcus aureus. Biochem Biophys Res Commun 181: 138-144. S0006-291X(05)81392-0 [pii].
37. Kaneko J, Kimura T, Kawakami Y, Tomita T, Kamio Y (1997) Pantonvalentine leukocidin genes in a phage-like particle isolated from mitomycin Ctreated Staphylococcus aureus V8 (ATCC 49775). Biosci Biotechnol Biochem 61: 1960-1962.
38. Finck-Barbancon V, Prevost G, Piemont Y (1991) Improved purification of leukocidin from Staphylococcus aureus and toxin distribution among hospital strains. Res Microbiol 142: 75-85.
39. Kaneko J, Kimura T, Narita S, Tomita T, Kamio Y (1998) Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 215: 57-67.
40. Szmigielski S, Prevost G, Monteil H, Colin DA, Jeljaszewicz J (1999) Leukocidal toxins of staphylococci. Zentralbl Bakteriol 289: 185-201.
41. Szmigielski S, Sobiczewska E, Prevost G, Monteil H, Colin DA, et al. (1998) Effect of purified staphylococcal leukocidal toxins on isolated blood polymorphonuclear leukocytes and peritoneal macrophages in vitro. Zentralbl Bakteriol 288: 383-394.
42. Jayasinghe L, Bayley H (2005) The leukocidin pore: evidence for an octamer with four LukF subunits and four LukS subunits alternating around a central axis. Protein Sci 14: 2550-2561.
43. Prevost G, Mourey L, Colin DA, Menestrina G (2001) Staphylococcal poreforming toxins. Curr Top Microbiol Immunol 257: 53-83.
44. von Eiff C, Friedrich AW, Peters G, Becker K (2004) Prevalence of genes encoding for members of the staphylococcal leukotoxin family among clinical isolates of Staphylococcus aureus. Diagn Microbiol Infect Dis 49: 157-162.
45. Holmes A, Ganner M, McGuane S, Pitt TL, Cookson BD, et al. (2005) Staphylococcus aureus isolates carrying Panton-Valentine leucocidin genes in England and Wales: frequency, characterization, and association with clinical disease. J Clin Microbiol 43: 2384-2390.
46. Robert J, Etienne J, Bertrand X (2005) Methicillin-resistant Staphylococcus aureus producing Panton-Valentine leukocidin in a retrospective case series from 12 French hospital laboratories, 2000-2003. Clin Microbiol Infect 11: 585-587.
47. Kennedy AD, Otto M, Braughton KR, Whitney AR, Chen L, et al. (2008) Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc Natl Acad Sci U S A 105: 1327-1332.
48. Gasteiger E, Hoogland C, Gattiker A, Duvand S, Wilkins MR (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM, ed. The Proteomics Protocols Handbook. pp 571-607.
49. Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17: 849-850.
50. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971. nprot.2007.131 [pii];10.1038/nprot.2007.131 [doi].
51. Billion A, Ghai R, Chakraborty T, Hain T (2006) Augur-a computational pipeline for whole genome microbial surface protein prediction and classification. Bioinformatics 22: 2819-2820. btl466 [pii];10.1093/bioinformatics/btl466 [doi].
52. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. btm404 [pii];10.1093/bioinformatics/btm404 [doi].
53. 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.
54. Laemmli UK (1970) Cleavage of structural protein during assembly of the head of bacteriophage T4. Nature 222: 680-685.
55. Kobayashi SD, Voyich JM, Buhl CL, Stahl RM, DeLeo FR (2002) 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 USA 99: 6901-6906.