Natural variability of in vitro adherence to fibrinogen and fibronectin does not correlate with in vivo infectivity of Staphylococcus aureus

Infection and Immunity

Volumn 78, Issue 4, 2010, Pages 1711-1716

  Ythier, Mathilde ^a   Entenza, Jose M ^a   Bille, Jacques ^b   Vandenesch, François ^c,d,e   Bes, Michèle ^c,d,e   Moreillon, Philippe ^a   Sakwinska, Olga ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UNIVERSITÉ DE LYON   (France)

^d INSERM   (France)

^e HOSPICES CIVILS DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRINOGEN; FIBRONECTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL ENDOCARDITIS; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BLOOD CULTURE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; RAT; SCREENING; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ADULT; ANIMALS; BACTERIAL ADHESION; CARRIER STATE; DISEASE MODELS, ANIMAL; ENDOCARDITIS, BACTERIAL; FIBRINOGEN; FIBRONECTINS; GENE EXPRESSION; GENETIC VARIATION; HUMANS; PHENOTYPE; RATS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; YOUNG ADULT;

EID: 77950237415     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01274-09     Document Type: Article

References (49)

1. Boden, M. K., and J. I. Flock. 1989. Fibrinogen binding protein clumping factor from Staphylococcus aureus. Infect. Immun. 57:2358-2363.
2. Cheung, A. L., A. S. Bayer, G. Y. Zhang, H. Gresham, and Y. Q. Xiong. 2004. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 40:1-9.
3. Cheung, A. L., S. J. Yang, A. S. Bayer, and Y. Q. Xiong. 2009. Disparity in the in vitro versus in vivo regulation of fibronectin binding proteins by 2 global regulators, saeRS and sigB, in Staphylococcus aureus. J. Infect. Dis. 200:1371-1374.
4. Entenza, J. M., H. Drugeon, M. P. Glauser, and P. Moreillon. 1995. Treatment of experimental endocarditis due to erythromycin-susceptible or -resistant methicillin-resistant Staphylococcus aureus with RP 59500. Antimicrob. Agents Chemother. 39:1419-1424.
5. Entenza, J. M., T. J. Foster, D. N. Eidhin, P. Vaudaux, P. Francioli, and P. Moreillon. 2000. Contribution of clumping factor B to pathogenesis of experimental endocarditis due to Staphylococcus aureus. Infect. Immun. 68: 5443-5446.
6. B in the expression of Staphylococcus aureus cell wall adhesins ClfA and FnbA and contribution to infectivity in a rat model of experimental endocarditis. Infect. Immun. 73:990-998.
7. Entenza, J. M., J. Vouillamoz, M. P. Glauser, and P. Moreillon. 1997. Levofloxacin versus ciprofloxacin, flucloxacillin, or vancomycin for treatment of experimental endocarditis due to methicillin-susceptible or -resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 41:1662-1667.
8. Feil, E. J., J. E. Cooper, H. Grundmann, D. A. Robinson, M. C. Enright, T. Berendt, S. J. Peacock, J. M. Smith, M. Murphy, B. G. Spratt, C. E. Moore, and N. P. J. Day. 2003. How clonal is Staphylococcus aureus? J. Bacteriol. 185:3307-3316.
9. Flock, J. I., S. A. Hienz, A. Heimdahl, and T. Schennings. 1996. Reconsideration of the role of fibronectin binding in endocarditis caused by Staphylococcus aureus. Infect. Immun. 64:1876-1878.
10. Fowler, V. G., C. L. Nelson, L. M. McIntyre, B. N. Kreiswirth, A. Monk, G. L. Archer, J. Federspiel, S. Naidich, B. Remortel, T. Rude, P. Brown, L. B. Reller, G. R. Corey, and S. R. Gill. 2007. Potential associations between hematogenous complications and bacterial genotype in Staphylococcus aureus infection. J. Infect. Dis. 196:738-747.
11. Goerke, C., S. Campana, M. G. Bayer, G. Doring, K. Botzenhart, and C. Wolz. 2000. Direct quantitative transcript analysis of the agr regulon o Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect. Immun. 68:1304-1311.
12. Gordon, R. J., and F. D. Lowy. 2008. Pathogenesis of methicillin- resistant Staphylococcus aureus infection. Clin. Infect. Dis. 46:S350-S359.
13. Greene, C., D. McDevitt, P. Francois, P. E. Vaudaux, D. P. Lew, and T. J. Foster. 1995. Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol. Microbiol. 17:1143-1152.
14. Heraief, E., M. P. Glauser, and L. R. Freedman. 1982. Natural history of aortic-valve endocarditis in rats. Infect. Immun. 37:127-131.
15. Hoen, B., F. Alla, C. Selton-Suty, I. Beguinot, A. Bouvet, S. Briancon, J. P. Casalta, N. Danchin, F. Delahaye, J. Etienne, V. Le Moing, C. Leport, J. L. Mainardi, R. Ruimy, and F. Vandenesch. 2002. Changing profile of infective endocarditis: results of a 1-year survey in France. JAMA 288:75-81.
16. Kluytmans, J., A. van Belkum, and H. Verbrugh. 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10:505-520.
17. Kuhn, G., P. Francioli, and D. S. Blanc. 2006. Evidence for clonal evolution among highly polymorphic genes in methicillin-resistant Staphylococcus aureus. J. Bacteriol. 188:169-178.
18. Laupland, K. B., D. L. Church, M. Mucenski, L. R. Sutherland, and H. D. Davies. 2003. Population-based study of the epidemiology of and the risk factors for invasive Staphylococcus aureus infections. J. Infect. Dis. 187:1452-1459.
19. Lindsay, J. A., C. E. Moore, N. P. Day, S. J. Peacock, A. A. Witney, R. A. Stabler, S. E. Husain, P. D. Butcher, and J. Hinds. 2006. Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J. Bacteriol. 188: 669-676.
20. Loughman, J. A., S. A. Fritz, G. A. Storch, and D. A. Hunstad. 2009. Virulence gene expression in human community acquired Staphylococcus aureus infection. J. Infect. Dis. 199:294-301.
21. Massey, R. C., M. N. Kantzanou, T. Fowler, N. P. J. Day, K. Schofield, E. R. Wann, A. R. Berendt, M. Hook, and S. J. Peacock. 2001. Fibronectin-binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell. Microbiol. 3:839-851.
22. Mazmanian, S. K., G. Liu, T. T. Hung, and O. Schneewind. 1999. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760-763.
23. McDevitt, D., P. Francois, P. Vaudaux, and T. J. Foster. 1994. Molecular characterization of the clumping cactor (fibrinogen receptor) of Staphylococcus aureus. Mol. Microbiol. 11:237-248.
24. McDevitt, D., P. Vaudaux, and T. J. Foster. 1992. Genetic evidence that bound coagulase of Staphylococcus aureus is not clumping factor. Infect. Immun. 60:1514-1523.
25. Melles, D. C., R. F. J. Gorkink, H. A. M. Boelens, S. V. Snijders, J. K. Peeters, M. J. Moorhouse, P. J. van der Spek, W. B. van Leeuwen, G. Simons, H. A. Verbrugh, and A. van Belkum. 2004. Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. J. Clin. Invest. 114:1732-1740.
26. Moreillon, P., J. M. Entenza, P. Francioli, D. McDevitt, T. J. Foster, P. Francois, and P. Vaudaux. 1995. Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect. Immun. 63:4738-4743.
27. Ni Eidhin, D., S. Perkins, P. Francois, P. Vaudaux, M. Hook, and T. J. Foster. 1998. Clumping factor B (ClfB), a new surface-located fibrinogen-binding adhesin of Staphylococcus aureus. Mol. Microbiol. 30:245-257.
28. Novick, R. P., H. F. Ross, S. J. Projan, J. Kornblum, B. Kreiswirth, and S. Moghazeh. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12:3967-3975.
29. Panchaud, A., E. Widmer, M. Kussmann, P. Moreillon, and M. Affolter. 2007. Mass spectrometry as a rapid and powerful alternative to antibodies for detecting LPXTG wall-associated proteins of Staphylococcus aureus. Int. J. Mass Spectrom. 268:234-243.
30. Patti, J. M., B. L. Allen, M. J. McGavin, and M. Hook. 1994. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48:585-617.
31. Peacock, S. J., C. E. Moore, A. Justice, M. Kantzanou, L. Story, K. Mackie, G. O'Neil, and N. P. J. Day. 2002. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect. Immun. 70:4987-4996.
32. Piroth, L., Y. A. Que, E. Widmer, A. Panchaud, S. Piu, J. M. Entenza, and P. Moreillon. 2008. The fibrinogen- and fibronectin-binding domains of Staphylococcus aureus fibronectin-binding protein A synergistically promote endothelial invasion and experimental endocarditis. Infect. Immun. 76:3824-3831.
33. Pragman, A. A., and P. M. Schlievert. 2004. Virulence regulation in Staphylococcus aureus: the need for in vivo analysis of virulence factor regulation. FEMS Immunol. Med. Microbiol. 42:147-154.
34. Que, Y. A., J. A. Haefliger, P. Francioli, and P. Moreillon. 2000. Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis subsp. cremoris using a new shuttle vector. Infect. Immun. 68:3516-3522.
35. Que, Y. A., J. A. Haefliger, L. Piroth, P. Francois, E. Widmer, J. M. Entenza, B. Sinha, M. Herrmann, P. Francioli, P. Vaudaux, and P. Moreillon. 2005. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J. Exp. Med. 201: 1627-1635.
36. Recsei, P., B. Kreiswirth, M. Oreilly, P. Schlievert, A. Gruss, and R. P. Novick. 1986. Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Mol. Gen. Genet. 202:58-61.
37. Roche, F. M., R. Downer, F. Keane, P. Speziale, P. W. Park, and T. J. Foster. 2004. The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J. Biol. Chem. 279: 38433-38440.
38. Roche, F. M., R. Massey, S. J. Peacock, N. P. J. Day, L. Visai, P. Speziale, A. Lam, M. Pallen, and T. J. Foster. 2003. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 149:643-654.
39. Sakwinska, O., G. Kuhn, C. Balmelli, P. Francioli, M. Giddey, V. Perreten, A. Riesen, F. Zysset, D. S. Blanc, and P. Moreillon. 2009. Genetic diversity and ecological success of Staphylococcus aureus strains colonizing humans. Appl. Environ. Microbiol. 75:175-183.
40. Shenkman, B., E. Rubinstein, A. L. Cheung, G. E. Brill, R. Dardik, I. Tamarin, N. Savion, and D. Varon. 2001. Adherence properties of Staphylococcus aureus under static and flow conditions: roles of agr and sar loci, platelets, and plasma ligands. Infect. Immun. 69:4473-4478.
41. von Eiff, C., K. Becker, K. Machka, H. Stammer, and G. Peters. 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. N. Engl. J. Med. 344:11-16.
42. Wann, E. R., S. Gurusiddappa, and M. Hook. 2000. The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J. Biol. Chem. 275:13863-13871.
43. Weinstein, H. J. 1959. The relation between nasal-staphylococcal-carrier state and the incidence of postoperative complications. N. Engl. J. Med. 260:1303-1308.
44. Wertheim, H. F. L., D. C. Melles, M. C. Vos, W. van Leeuwen, A. van Belkum, H. A. Verbrugh, and J. L. Nouwen. 2005. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 5:751-762.
45. Wertheim, H. F. L., M. C. Vos, A. Ott, A. van Belkum, A. Voss, J. Kluytmans, P. H. J. van Keulen, C. Vandenbroucke-Grauls, M. H. M. Meester, and H. A. Verbrugh. 2004. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364:703-705.
46. Widmer, E., Y. A. Que, J. M. Entenza, and P. Moreillon. 2006. New concepts in the pathophysiology of infective endocarditis. Curr. Infect. Dis. Rep. 8:271-279.
47. Xiong, Y. Q., A. S. Bayer, M. R. Yeaman, W. van Wamel, A. C. Manna, and A. L. Cheung. 2004. Impacts of sarA and agr in Staphylococcus aureus strain Newman on fibronectin-binding protein A gene expression and fibronectin adherence capacity in vitro and in experimental infective endocarditis. Infect. Immun. 72:1832-1836.
48. Xiong, Y. Q., V. G. Fowler, M. R. Yeaman, F. Perdreau-Remington, B. N. Kreiswirth, and A. S. Bayer. 2009. Phenotypic and genotypic characteristics of persistent methicillin-resistant Staphylococcus aureus bacteremia in vitro and in an experimental endocarditis model. J. Infect. Dis. 199:201-208.
49. Yarwood, J. M., and P. M. Schlievert. 2003. Quorum sensing in Staphylococcus infections. J. Clin. Invest. 112:1620-1625.