Residues essential for panton-valentine leukocidin S component binding to its cell receptor suggest both plasticity and adaptability in its interaction surface

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Laventie, Benoit Joseph ^a   Guérin, Frédéric ^b,c   Mourey, Lionel ^b,c   Tawk, Mira Y ^a   Jover, Emmanuel ^a   Maveyraud, Laurent ^b,c   Prévost, Gilles ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; COMPLEMENT COMPONENT C5A RECEPTOR; PANTON VALENTINE LEUKOCIDIN; PANTON VALENTINE LEUKOCIDIN S COMPONENT; UNCLASSIFIED DRUG; BACTERIAL TOXIN; EXOTOXIN; LEUKOCIDIN; PANTON-VALENTINE LEUKOCIDIN; PROTEIN BINDING; RECOMBINANT PROTEIN; TYROSINE;

ARTICLE; BINDING AFFINITY; CELL INTERACTION; CHANNEL GATING; CONTROLLED STUDY; CRYSTALLIZATION; EVOLUTIONARY ADAPTATION; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; LEUKOCYTE MEMBRANE; NEUTROPHIL; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; BINDING SITE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; STAPHYLOCOCCUS AUREUS;

ALANINE; AMINO ACID SEQUENCE; BACTERIAL TOXINS; BINDING SITES; CELL LINE; ESCHERICHIA COLI; EXOTOXINS; GENE EXPRESSION; HUMANS; KINETICS; LEUKOCIDINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NEUTROPHILS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; STAPHYLOCOCCUS AUREUS; TYROSINE;

EID: 84898639720     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092094     Document Type: Article

References (59)

1. Cheung GYC, Otto M (2012) The potential use of toxin antibodies as a strategy for controlling acute Staphylococcus aureus infections. Expert Opin Ther Targets 16: 601-612. doi: 10.1517/14728222.2012.682573
2. Watkins RR, David MZ, Salata RA (2012) Current concepts on the virulence mechanisms of meticillin-resistant Staphylococcus aureus. J Med Microbiol 61: 1179-1193. doi: 10.1099/jmm.0.043513-0
3. Gouaux JE, Braha O, Hobaugh MR, Song LZ, Cheley S, et al. (1994) Subunit stoichiometry of staphylococcal a-hemolysin in crystals and on membranes - a heptameric transmembrane pore. Proc Natl Acad Sci USA 91: 12828-12831
4. 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 (Pubitemid 41395582)
5. Joubert O, Voegelin J, Guillet V, Tranier S, Werner S, et al. (2007) Distinction between pore assembly by staphylococcal a-toxin versus leukotoxins. J Biomed Biotechnol 2007: 25935
6. Miles G, Movileanu L, Bayley H (2002) Subunit composition of a bicomponent toxin: staphylococcal leukocidin forms an octameric transmembrane pore. Prot Science 11: 894-902 (Pubitemid 34241297)
7. Yamashita K, Kawai Y, Tanaka Y, Hirano N, Kaneko J, et al. (2011) Crystal structure of the octameric pore of staphylococcal c-hemolysin reveals the bbarrel pore formation mechanism by two components. Proc Natl Acad Sci USA 108: 17314-17319. doi: 10.1073/pnas.111040210
8. Woodin AM (1960) Purification of the two components of leucocidin from Staphylococcus aureus. Biochem J 75: 158-165
9. Kaneko J, Muramoto K, Kamio Y (1997) Gene of LukF-PV-like component of Panton-Valentine leukocidin in Staphylococcus aureus P83 is linked with lukM. Biosci Biotechnol Biochem 61: 541-544 (Pubitemid 27213595)
10. Cooney J, Kienle Z, Foster TJ, O'Toole PW (1993) The c-hemolysin locus of Staphylococcus aureus comprises three linked genes, two of which are identical to the genes for the F and S components of leukocidin. Infect Immun 61: 768-771 (Pubitemid 23030872)
11. Prévost G, Cribier B, Couppié P, Petiau P, Supersac G, et al. (1995) Panton- Valentine leucocidin and c-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect Immun 63: 4121-4129
12. 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 (Pubitemid 28468556)
13. Morinaga N, Kaihou Y, Noda M (2003) Purification, cloning and characterization of variant LukE-LukD with strong leukocidal activity of staphylococcal bi-component leukotoxin family. Microbiol Immunol 47: 81-90 (Pubitemid 36119655)
14. Ventura CL, Malachowa N, Hammer CH, Nardone GA, Robinson MA, et al. (2010) Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. Plos One 5: e11634. doi: 10.1371/journal.- pone.0011634
15. Dumont AL, Nygaard TK, Watkins RL, Smith A, Kozhaya L, et al. (2011) Characterization of a new cytotoxin that contributes to Staphylococcus aureus pathogenesis. Mol Microbiol 79: 814-825. doi: 10.1111/j.1365- 2958.2010.07490.x.
16. Prévost G, Bouakham T, Piémont Y, Monteil H (1995) Characterisation of a synergohymenotropic toxin produced by Staphylococcus intermedius. FEBS Lett 376: 135-140
17. Badiou C, Dumitrescu O, Croze M, Gillet Y, Dohin B, et al. (2008) Panton- Valentine leukocidin is expressed at toxic levels in human skin abscesses. Clin Microbiol Infect 14: 1180-1183. doi: 10.1111/j.1469-0691.2008.02105.x.
18. Cribier B, Prévost G, Couppié P, Finck-Barbançon V, Grosshans E, et al. (1992) Staphylococcus aureus leukocidin: a new virulence factor in cutaneous infections? An epidemiological and experimental study. Dermatology 185: 175-180
19. Diep BA, Chan L, Tattevin P, Kajikawa O, Martin TR, et al. (2010) Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc Natl Acad Sci USA 107: 5587-5592. doi: 10.1073/pnas.0912403107
20. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, et al. (2002) Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359: 753-759 (Pubitemid 34215075)
21. Labandeira-Rey M, Couzon F, Boisset S, Brown EL, Bes M, et al. (2007) Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315: 1130-1133 (Pubitemid 46328024)
22. Prévost G, Couppié P, Prévost P, Gayet S, Petiau P, et al. (1995) Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J Med Microbiol 42: 237-245
23. 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 (Pubitemid 38891721)
24. Girgis DO, Sloop GD, Reed JM, OCallaghan RJ (2005) Effects of toxin production in a murine model of Staphylococcus aureus keratitis. Invest Ophthalmol Vis Sci 46: 2064-2070
25. Supersac G, Piémont Y, Kubina M, Prévost G, Foster TJ (1998) Assessment of the role of c-toxin in experimental endophthalmitis using a hlg-deficient mutant of Staphylococcus aureus. Microb Pathog 24: 241-251 (Pubitemid 28180051)
26. Gravet A, Couppié P, Meunier O, Clyti E, Moreau B, et al. (2001) Staphylococcus aureus isolated in cases of impetigo produces both epidermolysin A or B and LukE-LukD in 78% of 131 retrospective and prospective cases. J Clin Microbiol 39: 4349-4356 (Pubitemid 33117122)
27. Joubert O, Viero G, Keller D, Martinez E, Colin DA, et al. (2006) Engineered covalent leucotoxin heterodimers form functional pores: insights into S-F interactions. Biochem J 396: 381-389 (Pubitemid 43837254)
28. Prévost G, Mourey L, Colin DA, Monteil H, Dalla Serra M, et al. (2006) Alphahelix and b-barrel pore-forming toxins (leucocidins, a-, c-, and d-cytolysins) of Staphylococcus aureus. In: Alouf JE, Popoff MR, editors. The Comprehensive Sourcebook of Bacterial Protein Toxins Third ed: Academic Press. pp. 590-607
29. Viero G, Gropuzzo A, Joubert O, Keller D, Prévost G, et al. (2008) A molecular pin to study the dynamics of b-barrel formation in pore-forming toxins on erythrocytes: a sliding model. Cell Mol Life Sci 65: 312-323 (Pubitemid 351161485)
30. Baba Moussa L, Werner S, Colin DA, Mourey L, Pédelacq JD, et al. (1999) Discoupling the Ca(2+)-activation from the pore-forming function of the bicomponent Panton-Valentine leucocidin in human PMNs. FEBS Lett 461: 280-286 (Pubitemid 29533348)
31. Gauduchon V, Werner S, Prévost G, Monteil H, Colin DA (2001) Flow cytometric determination of Panton-Valentine leucocidin S component binding. Infect Immun 69: 2390-2395 (Pubitemid 32239708)
32. Tseng CW, Kyme P, Low J, Rocha MA, Alsabeh R, et al. (2009) Staphylococcus aureus Panton-Valentine leukocidin contributes to inflammation and muscle tissue injury. Plos One 4: e6387. doi: 10.1371/journal.pone.0006387
33. Pédelacq JD, Maveyraud L, Prévost G, Baba-Moussa L, Gonzalez A, et al. (1999) The structure of a Staphylococcus aureus leucocidin component (LukF-PV) reveals the fold of the water-soluble species of a family of transmembrane poreforming toxins. Structure 7: 277-287 (Pubitemid 29159687)
34. Olson R, Nariya H, Yokota K, Kamio Y, Gouaux E (1999) Crystal structure of staphylococcal LukF delineates conformational changes accompanying formation of a transmembrane channel. Nat Struct Biol 6: 134-140 (Pubitemid 29069775)
35. Guillet V, Roblin P, Werner S, Coraiola M, Menestrina G, et al. (2004) Crystal structure of leucotoxin S component: new insight into the Staphylococcal bbarrel pore-forming toxins. J Biol Chem 279: 41028-41037 (Pubitemid 39287704)
36. Roblin P, Guillet V, Joubert O, Keller D, Erard M, et al. (2008) A covalent S-F heterodimer of leucotoxin reveals molecular plasticity of b-barrel pore-forming toxins. Proteins 71: 485-496. doi: 10.1002/prot.21900 (Pubitemid 351358626)
37. Valeva A, Palmer M, Bhakdi S (1997) Staphylococcal a-toxin: formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry 36: 13298-13304 (Pubitemid 27473377)
38. Vecsey-Semjen B, Lesieur C, Mollby R, van der Goot FG (1997) Conformational changes due to membrane binding and channel formation by staphylococcal a-toxin. J Biol Chem 272: 5709-5717 (Pubitemid 27102399)
39. Aman MJ, Karauzum H, Bowden MG, Nguyen TL (2010) Structural model of the pre-pore ring-like structure of Panton-Valentine leukocidin: providing dimensionality to biophysical and mutational data. J Biomol Struct Dyn 28: 1-12
40. Colin DA, Mazurier I, Sire S, Finck-Barbançon V (1994) Interaction of the two components of leukocidin from Staphylococcus aureus with human polymorphonuclear leukocyte membranes: sequential binding and subsequent activation. Infect Immun 62: 3184-3188 (Pubitemid 24232099)
41. Spaan AN, Henry T, van Rooijen WJ, Perret M, Badiou C, et al. (2013) The staphylococcal toxin Panton-Valentine leukocidin targets human C5a receptors. Cell Host Microbe 13: 584-594. doi: 10.1016/j.chom.2013.04.006
42. Alonzo F III, Kozhaya L, Rawlings SA, Reyes-Robles T, DuMont AL, et al. (2013) CCR5 is a receptor for Staphylococcus aureus leukotoxin ED. Nature 493: 51-55. doi: 10.1038/nature11724
43. Reyes-Robles T, Alonzo F III, Kozhaya L, Lacy DB, Unutmaz D, et al. (2013) Staphylococcus aureus leukotoxin ED targets the chemokine receptors CXCR1 and CXCR2 to kill leukocytes and promote infection. Cell Host Microbe 14: 453-459. doi: 10.1016/j.chom.2013.09.005
44. Dumont AL, Yoong P, Day CJ, Alonzo F III, McDonald WH, et al. (2013) Staphylococcus aureus LukAB cytotoxin kills human neutrophils by targeting the CD11b subunit of the integrin Mac-1. Proc Natl Acad Sci USA. doi: 10.1073/ pnas.1305121110
45. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, et al. (1996) Structure of staphylococcal a-hemolysin, a heptameric transmembrane pore. Science 274: 1859-1866 (Pubitemid 26424757)
46. Finck-Barbançon V, Duportail G, Meunier O, Colin DA (1993) Pore formation by a two-component leukocidin from Staphylococcus aureus within the membrane of human polymorphonuclear leukocytes. Biochim Biophys Acta 1182: 275-282 (Pubitemid 23310053)
47. Meyer F, Girardot R, Piémont Y, Prévost G, Colin DA (2009) Analysis of the specificity of Panton-Valentine leucocidin and c-hemolysin F component binding. Infect Immun 77: 266-273. doi: 10.1128/IAI.00402-0
48. Ferreras M, Hoper F, Dalla Serra M, Colin DA, Prévost G, et al. (1998) The interaction of Staphylococcus aureus bi-component c-hemolysins and leucocidins with cells and lipid membranes. Biochim Biophys Acta 1414: 108-126 (Pubitemid 28511044)
49. Nariya H, Nishiyama A, Kamio Y (1997) Identification of the minimum segment in which the threonine246 residue is a potential phosphorylated site by protein kinase A for the LukS-specific function of staphylococcal leukocidin. FEBS Lett 415: 96-100 (Pubitemid 27402057)
50. Dumont AL, Yoong P, Liu X, Day CJ, Chumbler NM, et al. (2013) Identification of a crucial residue required for Staphylococcus aureus LukAB cytotoxicity and receptor recognition. Infect Immun in press doi: 10.1128/ IAI.01444-13
51. Kew RR, Peng T, DiMartino SJ, Madhavan D, Weinman SJ, et al. (1997) Undifferentiated U937 cells transfected with chemoattractant receptors: a model system to investigate chemotactic mechanisms and receptor structure/function relationships. J Leukoc Biol 61: 329-337 (Pubitemid 27149912)
52. Meunier O, Falkenrodt A, Monteil H, Colin DA (1995) Application of flow cytometry in toxinology: pathophysiology of human polymorphonuclear leukocytes damaged by a pore-forming toxin from Staphylococcus aureus. Cytometry 21: 241-247
53. Cheng Y, Prusoff WH (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 22: 3099-3108
54. Vonrhein C, Flensburg C, Keller P, Sharff A, Smart O, et al. (2011) Data processing and analysis with the autoPROC toolbox. Acta Crystallogr sect D Biol Crystallogr 67: 293-302. doi: 10.1107/S0907444911007773
55. Kabsch W (2010) Xds. Acta Crystallogr sect D Biol Crystallogr 66: 125-132. doi: 10.1107/S0907444909047337.
56. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr sect D Biol Crystallogr 62: 72-82
57. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr sect D Biol Crystallogr 67: 235-242. doi: 10.1107/S0907444910045749
58. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674 (Pubitemid 47080256)
59. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr sect D Biol Crystallogr 60: 2126-2132. (Pubitemid 41742764)