More than one tandem repeat domain of the extracellular adherence protein of Staphylococcus aureus is required for aggregation, adherence, and host cell invasion but not for leukocyte activation

Infection and Immunity

Volumn 76, Issue 12, 2008, Pages 5615-5623

  Hussain, Muzaffar ^a   Haggar, Axana ^b   Peters, Georg ^a   Chhatwal, Gursharan S ^c   Herrmann, Mathias ^d   Flock, Jan Ingmar ^b   Sinha, Bhanu ^e  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d SAARLAND UNIVERSITY   (Germany)

^e UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; COLLAGEN TYPE 1; EXTRACELLULAR ADHERENCE PROTEIN; FIBRINOGEN; FIBRONECTIN; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; VITRONECTIN;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL AGGREGATION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STAPHYLOCOCCUS AUREUS; SURFACE PLASMON RESONANCE; TANDEM REPEAT;

AGGLUTINATION; BACTERIAL ADHESION; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL PROLIFERATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOTHELIAL CELLS; FIBROBLASTS; HUMANS; PROTEIN BINDING; PROTEIN ISOFORMS; RECOMBINANT PROTEINS; RNA-BINDING PROTEINS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; SURFACE PLASMON RESONANCE; TANDEM REPEAT SEQUENCES;

EID: 57349133705     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00480-08     Document Type: Article

References (42)

1. Boden, M. K., and J. I. Flock. 1992. Evidence for three different fibrinogen-binding proteins with unique properties from Staphylococcus aureus strain Newman. Microb. Pathog. 12:289-298.
2. Buckling, A., J. Neilson, J. Lindsay, R. Ffrench-Constant, M. Enright, N. Day, and R. C. Massey. 2005. Clonal distribution and phase-variable expression of a major histocompatibility complex analogue protein in Staphylococcus aureus. J. Bacteriol. 187:2917-2919.
3. Chavakis, T., M. Hussain, S. M. Kanse, G. Peters, R. G. Bretzel, J. I. Flock, M. Herrmann, and K. T. Preissner. 2002. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat. Med. 8:687-693.
4. Flock, J. I., G. Gröman, K. Jönsson, B. Guss, C. Signäs, B. Nilsson, G. Raucci, M. Höök, T. Wadström, and M. Lindberg. 1987. Cloning and expression of the gene for a fibronectin-binding protein from Staphylococcus aureus. EMBO J. 6:2351-2357.
5. Foster, T. J., and M. Hook. 1998. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 6:484-488.
6. Geisbrecht, B. V., B. Y. Hamaoka, B. Perman, A. Zemla, and D. J. Leahy. 2005. The crystal structures of EAP domains from Staphylococcus aureus reveal an unexpected homology to bacterial superantigens. J. Biol. Chem. 280:17243-17250.
7. Grundmeier, M., M. Hussain, P. Becker, C. Heilmann, G. Peters, and B. Sinha. 2004. Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect. Immun. 72:7155-7163.
8. Haggar, A., C. Ehrnfelt, J. Holgersson, and J. I. Flock. 2004. The extracellular adherence protein from Staphylococcus aureus inhibits neutrophil binding to endothelial cells. Infect. Immun. 72:6164-6167.
9. Haggar, A., M. Hussain, H. Lonnies, M. Herrmann, A. Norrby-Teglund, and J. I. Flock. 2003. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect. Immun. 71:2310-2317.
10. Haggar, A., O. Shannon, A. Norrby-Teglund, and J. I. Flock. 2005. Dual effects of extracellular adherence protein from Staphylococcus aureus on peripheral blood mononuclear cells. J. Infect. Dis. 192:210-217.
11. Hammel, M., D. Nemecek, J. A. Keightley, G. J. Thomas, Jr., and B. V. Geisbrecht. 2007. The Staphylococcus aureus extracellular adherence protein (Eap) adopts an elongated but structured conformation in solution. Protein Sci. 16:2605-2617.
12. Hansen, U., M. Hussain, D. Villone, M. Herrmann, H. Robenek, G. Peters, B. Sinha, and P. Bruckner. 2006. The anchorless adhesin Eap (extracellular adherence protein) from Staphylococcus aureus selectively recognizes extracellular matrix aggregates but binds promiscuously to monomeric matrix macromolecules. Matrix Biol. 25:252-260.
13. Hienz, S. A., T. Schennings, A. Heimdahl, and J. I. Flock. 1996. Collagen binding of Staphylococcus aureus is a virulence factor in experimental endocarditis. J. Infect. Dis. 174:83-88.
14. Hofer, M. F., K. Newell, R. C. Duke, P. M. Schlievert, J. H. Freed, and D. Y. Leung. 1996. Differential effects of staphylococcal toxic shock syndrome toxin-1 on B cell apoptosis. Proc. Natl. Acad. Sci. USA 93:5425-5430.
15. Hussain, M., C. von Eiff, B. Sinha, I. Joost, M. Herrmann, G. Peters, and K. Becker. 2008. The eap gene as a novel target for specific identification of Staphylococcus aureus. J. Clin. Microbiol. 46:470-476.
16. Hussain, M., K. Becker, C. von Eiff, G. Peters, and M. Herrmann. 2001. Analogs of Eap protein are conserved and prevalent in clinical Staphylococcus aureus isolates. Clin. Diagn. Lab. Immunol. 8:1271-1276.
17. Hussain, M., A. Haggar, C. Heilmann, G. Peters, J. I. Flock, and M. Herrmann. 2002. Insertional inactivation of eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect. Immun. 70:2933-2940.
18. Jahreis, A., P. Beckheinrich, and U. F. Haustein. 2000. Effects of two novel cationic staphylococcal proteins (NP-tase and p70) and enterotoxin B on IgE synthesis and interleukin-4 and interferon-gamma production in patients with atopic dermatitis. Br. J. Dermatol. 142:680-687.
19. Jahreis, A., Y. Yousif, J. A. Rump, R. Drager, A. Vogt, H. H. Peter, and M. Schleisier. 1995. Two novel cationic staphylococcal proteins induce IL-2 secretion, proliferation and immunoglobulin synthesis in peripheral blood mononuclear cells (PBMC) of both healthy controls and patients with common variable immunodeficiency (CVID). Clin. Exp. Immunol. 100:406-411.
20. Jönsson, K., D. McDevitt, M. H. McGavin, J. M. Patti, and M. Höök. 1995. Staphylococcus aureus expresses a major histocompatibility complex class II analog. J. Biol. Chem. 270:21457- 21460.
21. Kreikemeyer, B., D. McDevitt, and A. Podbielski. 2002. The role of the Map protein in Staphylococcus aureus matrix protein and eukaryotic cell adherence. Int. J. Med. Microbiol. 292:283-295.
22. Kuroda, M., T. Ohta, I. Uchiyama, T. Baba, H. Yuzawa, I. Kobayashi, L. Cui, A. Oguchi, K. Aoki, Y. Nagai, J. Lian, T. Ito, M. Kanamori, H. Matsumaru, A. Maruyama, H. Murakami, A. Hosoyama, Y. Mizutani-Ui, N. K. Takahashi, T. Sawano, R. Inoue, C. Kaito, K. Sekimizu, H. Hirakawa, S. Kuhara, S. Goto, J. Yabuzaki, M. Kanehisa, A. Yamashita, K. Oshima, K. Furuya, C. Yoshino, T. Shiba, M. Hattori, N. Ogasawara, H. Hayashi, and K. Hiramatsu. 2001. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225-1240.
23. Kuypers, J. M., and R. A. Proctor. 1989. Reduced adherence to traumatized rat heart valves by a low-fibronectin-binding mutant of Staphylococcus aureus. Infect. Immun. 57:2306-2312.
24. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
25. Massey, R. C., T. J. Scriba, E. L. Brown, R. E. Phillips, and A. K. Sewell. 2007. Use of peptide-major histocompatibility complex tetramer technology to study interactions between Staphylococcus aureus proteins and human cells. Infect. Immun. 75:5711-5715.
26. McDevitt, D., P. Francois, P. E. Vaudaux, and T. J. Foster. 1994. Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol. Microbiol. 11:237-248.
27. Moreillon, P., J. M. Entenza, P. Francioli, D. McDevitt, T. J. Foster, P. Francois, and P. E. Vaudaux. 1995. Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect. Immun. 63:4738-4743.
28. Palma, M., A. Haggar, and J. I. Flock. 1999. Adherence of Staphylococcus aureus is enhanced by an endogenous secreted protein with broad binding activity. J. Bacteriol. 181:2840-2845.
29. Patti, J. M., T. Bremell, D. Krajewska-Pietrasik, A. Abdelnour, A. Tarkowski, C. Rydén, and M. Höök. 1994. The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect. Immun. 62:152-161.
30. Patti, J. M., and M. Höök. 1994. Microbial adhesins recognizing extracellular matrix macromolecules. Curr. Opin. Cell Biol. 6:752-758.
31. Patti, J. M., H. Jonsson, B. Guss, L. M. Switalski, K. Wiberg, M. Lindberg, and M. Hook. 1992. Molecular characterization and expression of a gene encoding a Staphylococcus aureus collagen adhesin. J. Biol. Chem. 267:4766-4772. (Erratum, 269:11672, 1994.)
32. Peacock, S. J., T. J. Foster, B. J. Cameron, and A. R. Berendt. 1999. Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology 145:3477-3486.
33. Proctor, R. A., G. Christman, and D. F. Mosher. 1984. Fibronectin-induced agglutination of Staphylococcus aureus correlates with invasiveness. J. Lab. Clin. Med. 104:455-469.
34. 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.
35. Schneider, D., L. Liaw, C. Daniel, A. N. Athanasopoulos, M. Herrmann, K. T. Preissner, P. P. Nawroth, and T. Chavakis. 2007. Inhibition of breast cancer cell adhesion and bone metastasis by the extracellular adherence protein of Staphylococcus aureus. Biochem. Biophys. Res. Commun. 357: 282-288.
36. Sinha, B., P. Francois, Y. A. Que, M. Hussain, C. Heilmann, P. Moreillon, D. Lew, K. H. Krause, G. Peters, and M. Herrmann. 2000. Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect. Immun. 68:6871-6878.
37. 1. Cell. Microbiol. 1:101-117.
38. Sinha, B., M. Herrmann, and K. H. Krause. 2000. Is Staphylococcus aureus an intracellular pathogen? Response. Trends Microbiol. 8:343-344.
39. Sinha B, and M. Herrmann. 2005. Mechanism and consequences of invasion of endothelial cells by Staphylococcus aureus. Thromb. Haemost. 94:266-277.
40. Sobke, A. C., D. Selimovic, V. Orlova, M. Hassan, T. Chavakis, A. N. Athanasopoulos, U. Schubert, M. Hussain, G. Thiel, K. T. Preissner, and M. Herrmann. 2006. The extracellular adherence protein from Staphylococcus aureus abrogates angiogenic responses of endothelial cells by blocking Ras activation. FASEB J. 20:2621-2623.
41. Xie, C., P. Alcaide, B. V. Geisbrecht, D. Schneider, M. Herrmann, K. T. Preissner, F. W. Luscinskas, and T. Chavakis. 2006. Suppression of experimental autoimmune encephalomyelitis by extracellular adherence protein of Staphylococcus aureus. J. Exp. Med. 203:985-994.
42. Yatohgo, T., M. Izumi, H. Kashiwagi, and M. Hayashi. 1988. Novel purification of vitronectin from human plasma by heparin affinity chromatography. Cell Struct. Funct. 13:281-292.