The signal peptide of Staphylococcus aureus Panton Valentine leukocidin LukS component mediates increased adhesion to heparan sulfates

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Tristan, Anne ^a,b,c   Benito, Yvonne ^b,c   Montserret, Roland ^d   Boisset, Sandrine ^a,b,c   Dusserre, Eric ^a,b   Penin, Francois ^d   Ruggiero, Florence ^d   Etienne, Jerome ^a,b,c   Lortat Jacob, Hugues ^e   Lina, Gerard ^a,b,c   Bowden, M Gabriela ^f   Vandenesch, François ^a,b,c  

^a UNIVERSITÉ LYON 1   (France)

^b INSERM   (France)

^c HOSPICES CIVILS DE LYON   (France)

^d UNIVERSITÉ DE LYON   (France)

^e INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^f TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARAN SULFATE; HEPARIN; PANTON VALENTINE LEUKOCIDIN; PROTEIN SUBUNIT; SIGNAL PEPTIDASE; SIGNAL PEPTIDE; SYNTHETIC PEPTIDE; BACTERIAL PROTEIN; LEUKOCIDIN; LEUKOCIDIN S COMPONENT PROTEIN, STAPHYLOCOCCUS; LEUKOCIDIN S-COMPONENT PROTEIN, STAPHYLOCOCCUS; SCLEROPROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIUM ADHERENCE; CARBOXY TERMINAL SEQUENCE; CHEMICAL ANALYSIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; IN VIVO STUDY; NONHUMAN; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SITE DIRECTED MUTAGENESIS; STAPHYLOCOCCUS AUREUS; STRUCTURE ANALYSIS; CHEMISTRY; GENETICS; METABOLISM; OPERON; PHYSIOLOGY; VALIDATION STUDY;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

BACTERIAL ADHESION; BACTERIAL PROTEINS; EXTRACELLULAR MATRIX PROTEINS; HEPARITIN SULFATE; LEUKOCIDINS; OPERON; PROTEIN SORTING SIGNALS; STAPHYLOCOCCUS AUREUS;

EID: 64549096389     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005042     Document Type: Article

References (46)

1. Tristan A, Bes M, Meugnier H, Lina G, Bozdogan B, et al. (2007) Global distribution of Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus, 2006. Emerging Infect Dis 13: 594-600.
2. Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, et al. (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29: 1128-1132.
3. 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.
4. Gillet Y, Vanhems P, Lina G, Bes M, Vandenesch F, et al. (2007) Factors predicting mortality in necrotizing community-acquired pneumonia caused by Staphylococcus aureus containing Panton-Valentine leukocidin. Clin Infect Dis 45: 315-321.
5. de Bentzmann S, Tristan A, Etienne J, Brousse N, Vandenesch F, et al. (2004) Staphylococcus aureus isolates associated with necrotizing pneumonia bind to basement membrane type I and IV collagens and laminin. J Infect Dis 190: 1506-1515.
6. O'Brien LM, Walsh EJ, Massey RC, Peacock SJ, Foster TJ (2002) Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell Microbiol 4: 759-770.
7. 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.
8. Bishop JR, Schuksz M, Esko JD (2007) Heparan sulphate proteoglycans finetune mammalian physiology. Nature 446: 1030-1037.
9. Delacoux F, Fichard A, Cogne S, Garrone R, Ruggiero F (2000) Unraveling the amino acid sequence crucial for heparin binding to collagen V. J Biol Chem 275: 29377-29382.
10. San Antonio JD, Lander AD, Karnovsky MJ, Slayter HS (1994) Mapping the heparin-binding sites on type I collagen monomers and fibrils. J Cell Biol 125: 1179-1188.
11. Montserret R, Aubert-Foucher E, McLeish MJ, Hill JM, Ficheux D, et al. (1999) Structural analysis of the heparin-binding site of the NC1 domain of collagen XIV by CD and NMR. Biochemistry 38: 6479-6488.
12. Montserret R, McLeish MJ, Bockmann A, Geourjon C, Penin F (2000) Involvement of electrostatic interactions in the mechanism of peptide folding induced by sodium dodecyl sulfate binding. Biochemistry 39: 8362-8373.
13. Tartaglia GG, Vendruscolo M (2008) The Zyggregator method for predicting protein aggregation propensities. Chem Soc Rev 37: 1395-1401.
14. Lyon GJ, Novick RP (2004) Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25: 1389-1403.
15. Watson DC, Yaguchi M, Bisaillon JG, Beaudet R, Morosoli R (1988) The amino acid sequence of a gonococcal growth inhibitor from Staphylococcus haemolyticus. Biochem J 252: 87-93.
16. Firth N, Fink PD, Johnson L, Skurray RA (1994) A lipoprotein signal peptide encoded by the staphylococcal conjugative plasmid pSK41 exhibits an activity resembling that of Enterococcus faecalis pheromone cAD1. J Bacteriol 176: 5871-5873.
17. Martoglio B (2003) Intramembrane proteolysis and post-targeting functions of signal peptides. Biochem Soc Trans 31: 1243-1247.
18. Lemberg MK, Bland FA, Weihofen A, Braud VM, Martoglio B (2001) Intramembrane proteolysis of signal peptides: an essential step in the generation of HLA-E epitopes. J Immunol 167: 6441-6446.
19. Alken M, Rutz C, Kochl R, Donalies U, Oueslati M, et al. (2005) The signal peptide of the rat corticotropin-releasing factor receptor 1 promotes receptor expression but is not essential for establishing a functional receptor. Biochem J 390: 455-464.
20. Martoglio B, Graf R, Dobberstein B (1997) Signal peptide fragments of preprolactin and HIV-1 p-gp160 interact with calmodulin. EMBO J 16: 6636-6645.
21. van Wely KH, Swaving J, Freudl R, Driessen AJ (2001) Translocation of proteins across the cell envelope of Gram-positive bacteria. FEMS Microbiol Rev 25: 437-454.
22. von Heijne G (1998) Life and death of a signal peptide. Nature 396: 111, 113.
23. Reddy GL, Nagara R (1989) Circular dichroism studies on synthetic signal peptides indicate beta-conformation as a common structural feature in highly hydrophobic environment. J Biol Chem 264: 16591-16597.
24. Harraghy N, Hussain M, Haggar A, Chavakis T, Sinha B, et al. (2003) The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology 149: 2701-2707.
25. Vives RR, Crublet E, Andrieu JP, Gagnon J, Rousselle P, et al. (2004) A novel strategy for defining critical amino acid residues involved in protein/glycosaminoglycan interactions. J Biol Chem 279: 54327-54333.
26. Imberty A, Lortatjacob H, Perez S (2007) Structural view of glycosaminoglycan - protein interactions. Carbohydrate Research 342: 430-439.
27. Kjellen L, Lindahl U (1991) Proteoglycans: structures and interactions. Annu Rev Biochem 60: 443-475.
28. Laguri C, Arenzana-Seisdedos F, Lortat-Jacob H (2008) Relationships between glycosaminoglycan and receptor binding sites in chemokines-the CXCL12 example. Carbohydr Res 343: 2018-2023.
29. Clarke SR, Foster SJ (2006) Surface adhesins of Staphylococcus aureus. Adv Microb Physiol 51: 187-224.
30. Hayashida A, Bartlett AH, Foster TJ, Park PW (2009) Staphylococcus aureus betatoxin induces lung injury through syndecan-1. Am J Pathol 174: 509-518.
31. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, et al. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
32. Genestier AL, Michallet MC, Prévost G, Bellot G, Chalabreysse L, et al. (2005) Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J Clin Invest 115: 3117-3127.
33. Que YA, Haefliger JA, Francioli P, Moreillon P (2000) Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis subsp. cremoris using a new shuttle vector. Infect Immun 68: 3516-3522.
34. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manuel. New-York: Cold Spring Harbor Laboratories Press.
35. Arnaud M, Chastanet A, Debarbouille M (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
36. Jones CL, Khan SA (1986) Nucleotide sequence of the enterotoxin B gene from Staphylococcus aureus. J Bacteriol 166: 29-33.
37. Chanut-Delalande H, Fichard A, Bernocco S, Garrone R, Hulmes DJ, et al. (2001) Control of heterotypic fibril formation by collagen V is determined by chain stoichiometry. J Biol Chem 276: 24352-24359.
38. Fichard A, Tillet E, Delacoux F, Garrone R, Ruggiero F (1997) Human recombinant alpha1(V) collagen chain. Homotrimeric assembly and subsequent processing. J Biol Chem 272: 30083-30087.
39. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, et al. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21: 1353-1366.
40. 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.
41. Sarrazin S, Bonnaffe D, Lubineau A, Lortat-Jacob H (2005) Heparan sulfate mimicry: a synthetic glycoconjugate that recognizes the heparin binding domain of interferon-gamma inhibits the cytokine activity. J Biol Chem 280: 37558-37564.
42. Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32: W668-673.
43. Manavalan P, Johnson WC Jr (1987) Variable selection method improves the prediction of protein secondary structure from circular dichroism spectra. Anal Biochem 167: 76-85.
44. Novick RP (1963) Analysis by Transduction of Mutations Affecting Penicillinase Formation in Staphylococcus Aureus. J Gen Microbiol 33: 121-136.
45. Peng HL, Novick RP, Kreiswirth B, Kornblum J, Schlievert P (1988) Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 170: 4365-4372.
46. Horinouchi S, Weisblum B (1982) Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J Bacteriol 150: 815-825.