Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model

Infection and Immunity

Volumn 74, Issue 4, 2006, Pages 2145-2153

  Schaffer, Adam C ^a,e   Solinga, Robert M ^a   Cocchiaro, Jordan ^a,f   Portoles, Marta ^a,g   Kiser, Kevin B ^a,h   Risley, Allison ^a   Randall, Suzanne M ^a   Valtulina, Viviana ^b   Speziale, Pietro ^b   Walsh, Evelyn ^c   Foster, Timothy ^c   Lee, Jean C ^a,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF PAVIA   (Italy)

^c TRINITY COLLEGE DUBLIN   (Ireland)

^d CHANNING LABORATORY   (United States)

^e WEILL CORNELL MEDICAL CENTER   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

^g MILLIPORE CORPORATION   (United States)

^h Cape Fear Community College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; CLUMPING FACTOR B; COLLAGEN BINDING PROTEIN; FIBRONECTIN BINDING PROTEIN; FIBRONECTIN BINDING PROTEIN A; FIBRONECTIN BINDING PROTEIN B; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CLFB; RECOMBINANT VACCINE; TEICHOIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTEREMIA; BACTERIAL COLONIZATION; CONTROLLED STUDY; DISEASE MODEL; INFECTION RISK; MOUSE; NONHUMAN; NOSE MUCOSA; PRIORITY JOURNAL; PROTEIN ANALYSIS; RISK FACTOR; SOFT TISSUE INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ADHESINS, BACTERIAL; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, BACTERIAL; DISEASE MODELS, ANIMAL; FEMALE; GROWTH INHIBITORS; KERATINS; MALE; MICE; MICE, INBRED ICR; NASAL MUCOSA; RATS; RATS, WISTAR; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCAL VACCINES; STAPHYLOCOCCUS AUREUS; VACCINES, INACTIVATED;

EID: 33645532283     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.4.2145-2153.2006     Document Type: Article

References (55)

1. Baker, C. J. 1972. Fatal septicemia due to Staphylococcus aureus 502A. Report of a case and review of the infectious complications of bacterial interference programs. Am. J. Dis. Child. 123:45-48.
2. Barbour, M. L., R. T. Mayon-White, C. Coles, D. W. M. Crook, and E. R. Moxon. 1995. The impact of conjugate vaccine on carriage of Haemophilus influenzae type b. J. Infect. Dis. 171:93-98.
3. Beenken, K. E., J. S. Blevins, and M. S. Smeltzer. 2003. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 71:4206-4211.
4. Cassat, J. E., P. M. Dunman, F. McAleese, E. Murphy, S. J. Projan, and M. S. Smeltzer. 2005. Comparative genomics of Staphylococcus aureus musculoskeletal isolates. J. Bacteriol. 187:576-592.
5. Cole, A. M., S. Tahk, A. Oren, D. Yoshioka, Y. H. Kim, A. Park, and T. Ganz. 2001. Determinants of Staphylococcus aureus nasal carriage. Clin. Diagn. Lab Immunol. 8:1064-1069.
6. Cramton, S. E., C. Gerke, N. F. Schnell, W. W. Nichols, and F. Gotz. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
7. Cunnion, K. M., J. C. Lee, and M. M. Frank. 2001. Capsule production and growth phase influence binding of complement to Staphylococcus aureus. Infect. Immun. 69:6796-6803.
8. Dryden, M. S., S. Dailly, and M. Crouch. 2004. A randomized, controlled trial of tea tree topical preparations versus a standard topical regimen for the clearance of MRSA colonization. J. Hosp. Infect 56:283-286.
9. Dryla, A., S. Prustomersky, D. Gelbmann, M. Hanner, E. Bettinger, B. Kocsis, T. Kustos, T. Henics, A. Meinke, and E. Nagy. 2005. Comparison of antibody repertoires against Staphylococcus aureus in healthy individuals and in acutely infected patients. Clin. Diagn. Lab. Immunol. 12:387-398.
10. Ghaffar, F., T. Barton, J. Lozano, L. S. Muniz, P. Hicks, V. Gan, N. Ahmad, and G. H. McCracken, Jr. 2004. Effect of the 7-valent pneumococcal conjugate vaccine on nasopharyngeal colonization by Streptococcus pneumoniae in the first 2 years of life. Clin. Infect. Dis. 39:930-938.
11. Gomes, A. R., S. Vinga, M. Zavolan, and H. de Lencastre. 2005. Analysis of the genetic variability of virulence-related loci in epidemic clones of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 49:366-379.
12. Gonzalez-Zorn, B., J. P. Senna, L. Fiette, S. Shorte, A. Testard, M. Chignard, P. Courvalin, and C. Grillot-Courvalin. 2005. Bacterial and host factors implicated In nasal carriage of methicillin-resistant Staphylococcus aureus in mice. Infect. Immun. 73:1847-1851.
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. 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.
15. Jarraud, S., G. J. Lyon, A. M. Figueiredo, L. Gerard, F. Vandenesch, J. Etienne, T. W. Muir, and R. P. Novick. 2000. Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J. Bacteriol. 182:6517-6522.
16. Kauppi, M., L. Saarinen, and H. Kayhty. 1993. Anti-capsular polysaccharide antibodies reduce nasopharyngeal colonization by Haemophilus influenzae type b in infant rats. J. Infect. Dis. 167:365-371.
17. Kiser, K. B., N. Bhasin, L. Deng, and J. C. Lee. 1999. Staphylococcus aureus cap5P encodes a UDP-N-acetylglucosamine 2-epimerase with functional redundancy. J. Bacteriol. 181:4818-4824.
18. Kiser, R. B., J. M. Cantey-Kiser, and J. C. Lee. 1999. Development and characterization of a Staphylococcus aureus nasal colonization model in mice. Infect. Immun. 67:5001-5006.
19. 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.
20. Kluytmans, J. A., J. W. Mouton, M. F. VandenBergh, M. J. Manders, A. P. Maat, J. H. Wagenvoort, M. F. Michel, and H. A. Verbrugh. 1996. Reduction of surgical-site infections in cardiothoracic surgery by elimination of nasal carriage of Staphylococcus aureus. Infect. Control Hosp. Epidemiol. 17:780-785.
21. Kohler, G., and C. Milstein. 1975. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256:495-497.
22. Kokai-Kun, J. F., S. M. Walsh, T. Chanturiya, and J. J. Mond. 2003. Lysostaphin cream eradicates Staphylococcus aureus nasal colonization in a cotton rat model. Antimicrob. Agents Chemother. 47:1589-1597.
23. Kornblum, J., B. N. Kreiswirth, S. J. Projan, H. Ross, and R. P. Novick. 1990. agr: a polycistronic locus regulating exoprotein synthesis in Staphylococcus aureus, p. 373-402. In R. P. Novick (ed.), Molecular biology of the staphylococci. VCH Publishers, Inc., New York, NY.
24. Kruszewska, D., H. G. Sahl, G. Bierbaum, U. Pag, S. O. Hynes, and A. Ljungh. 2004. Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model. J. Antimicrob. Chemother. 54:648-653.
25. Lee, J. C., N. E. Perez, C. A. Hopkins, and G. B. Pier. 1988. Purified capsular polysaccharide-induced immunity to Staphylococcus aureus infection. J. Infect. Dis. 157:723-730.
26. Mazmanian, S. K., G. Liu, E. R. Jensen, E. Lenoy, and O. Schneewind. 2000. Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc. Natl. Acad. Sci. USA 97:5510-5515.
27. Mazmanian, S. K., G. Liu, H. Ton-That, and O. Schneewind. 1999. Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285:760-763.
28. McAleese, F. M., E. J. Walsh, M. Sieprawska, J. Potempa, and T. J. Foster. 2001. Loss of clumping factor B fibrinogen binding activity by Staphylococcus aureus involves cessation of transcription, shedding and cleavage by metalloprotease. J. Biol. Chem. 276:29969-29978.
29. McGavin, M. J., C. Zahradka, K. Rice, and J. E. Scott. 1997. Modification of the Staphylococcus aureus fibronectin binding phenotype by V8 protease. Infect. Immun. 65:2621-2628.
30. Mempel, M., T. Schmidt, S. Weidinger, C. Schnopp, T. Foster, J. Ring, and D. Abeck. 1998. Role of Staphylococcus aureus surface-associated proteins in the attachment to cultured HaCaT keratinocytes in a new adhesion assay. J. Investig. Dermatol. 111:452-456.
31. Miller, M. A., A. Dascal, J. Portnoy, and J. Mendelson. 1996. Development of mupirocin-resistance among methicillin-resistant Staphylococcus aureus after widespread use of nasal mupirocin ointment. Infect. Control Hosp. Epidemiol. 17:811-813.
32. Nemeth, J., and J. C. Lee. 1995. Antibodies to capsular polysaccharides are not protective against experimental Staphylococcus aureus endocarditis. Infect. Immun. 63:375-380.
33. Ni Eidhin, D., S. Perkins, P. Francois, P. Vaudaux, M. Hook, and T. J. Foster. 1998. Clumping factor B (CIfB), a new surface-located fibrinogen-binding adhesin of Staphylococcus aureus. Mol. Microbiol. 30:245-257.
34. Novick, R. P. 1963. Analysis by transduction of mutations affecting penicillinase formation in Staphylococcus aureus. J. Gen. Microbiol. 33:121-136.
35. O'Brien, L., S. W. Kerrigan, G. Kaw, M. Hogan, J. Penades, D. Litt, D. J. Fitzgerald, T. J. Foster, and D. Cox. 2002. Multiple mechanisms for the activation of human platelet aggregation by Staphylococcus aureus: roles for the clumping factors CIfA and CIfB, the serine-aspartate repeat protein SdrE and protein A. Mol. Microbiol. 44:1033-1044.
36. O'Brien, L. M., E. J. Walsh, R. C. Massey, S. J. Peacock, and T. J. Foster. 2002. Staphylococcus aureus clumping factor B (CIfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell. Microbiol. 4:759-770.
37. Patti, J. M., T. Bremell, D. Krajewska-Pietrasik, A. Abdelnour, A. Tarkowski, C. Ryden, and M. Hook. 1994. The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect. Immun. 62:152-161.
38. Pelton, S. I., A. M. Loughlin, and C. D. Marchant. 2004. Seven valent pneumococcal conjugate vaccine immunization in two Boston communities: changes in serotypes and antimicrobial susceptibility among Streptococcus pneumoniae isolates. Pediatr. Infect. Dis. J. 23:1015-1022.
39. Perkins, S., E. J. Walsh, C. C. Deivanayagam, S. V. Narayana, T. J. Foster, and M. Hook. 2001. Structural organization of the fibrinogen-binding region of the clumping factor B MSCRAMM of Staphylococcus aureus. J. Biol. Chem. 276:44721-44728.
40. Perl, T. M., J. J. Cullen, R. P. Wenzel, M. B. Zimmerman, M. A. Pfaller, D. Sheppard, J. Twombley, P. P. French, and L. A. Herwaldt. 2002. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N. Engl. J. Med. 346:1871-1877.
41. Pohlmann-Dietze, P., M. Ulrich, K. B. Kiser, G. Doring, J. C. Lee, J. M. Fournier, K. Botzenhart, and C. Wolz. 2000. Adherence of Staphylococcus aureus to endothelial cells: influence of the capsular polysaccharide, the global regulator agr, and the bacterial growth phase. Infect. Immun. 68:4865-4871.
42. Poole-Warren, L. A., M. D. Hallett, P. W. Hone, S. H. Burden, and P. C. Farrell. 1991. Vaccination for prevention of CAPD associated staphylococcal infection-results of a prospective multicentre clinical trial. Clin. Nephrol. 35:198-206.
43. Robbins, J., R. Schneerson, and S. Szu. 1995. Perspective: hypothesis: serum IgG antibody is sufficient to confer protection against infectious disease by inactivating the inoculum. J. Infect. Dis. 171:1387-1388.
44. Speziale, P., D. Joh, L. Visai, S. Bozzini, K. House-Pompeo, M. Lindberg, and M. Hook. 1996. A monoclonal antibody enhances ligand binding of fibronectin MSCRAMM (adhesin) from Streptococcus dysgalactiae. J. Biol. Chem. 271:1371-1378.
45. Tacconelli, E., Y. Carmeli, A. Aizer, G. Ferreira, M. G. Foreman, and E. M. D'Agata. 2003. Mupirocin prophylaxis to prevent Staphylococcus aureus infection in patients undergoing dialysis: a meta-analysis. Clin. Infect. Dis. 37:1629-1638.
46. Upton, A., S. Lang, and H. Heffernan. 2003. Mupirocin and Staphylococcus aureus: a recent paradigm of emerging antibiotic resistance. J. Antimicrob. Chemother. 51:613-617.
47. Visai, L., S. Rindi, P. Speziale, P. Petrini, S. Fare, and M. C. Tanzi. 2002. In vitro interactions of biomedical polyurethanes with macrophages and bacterial cells. J. Biomater. Appl. 16:191-214.
48. 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.
49. Walsh, E. J., L. M. O'Brien, X. Liang, M. Hook, and T. J. Foster. 2004. Clumping factor B, a fibrinogen-binding MSCRAMM (microbial surface components recognizing adhesive matrix molecules) adhesin of Staphylococcus aureus, also binds to the tail region of type I cytokeratin 10. J. Biol. Chem. 279:50691-50699.
50. Weidenmaier, C., J. F. Kokai-Kun, S. A. Kristian, T. Chanturiya, H. Kalbacher, M. Gross, G. Nicholson, B. Neumeister, J. J. Mond, and A. Peschel. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10:243-245.
51. Wenzel, R. P., and T. M. Perl. 1995. The significance of nasal carriage of Staphylococcus aureus and the incidence of postoperative wound infection. J. Hosp. Infect 31:13-24.
52. Wertheim, H. F., J. Verveer, H. A. Boelens, A. van Belkum, H. A. Verbrugh, and M. C. Vos. 2005. Effect of mupirocin treatment on nasal, pharyngeal, and perineal carriage of Staphylococcus aureus in healthy adults. Antimicrob. Agents Chemother. 49:1465-1467.
53. Wertheim, H. F., M. C. Vos, A. Ott, A. van Belkum, A. Voss, J. A. Kluytmans, P. H. van Keulen, C. M. Vandenbroucke-Grauls, M. H. Meester, and H. A. Verbrugh. 2004. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364:703-705.
54. Wertheim, H. F., M. C. Vos, A. Ott, A. Voss, J. A. Kluytmans, C. M. Vandenbroucke-Grauls, M. H. Meester, P. H. van Keulen, and H. A. Verbrugh. 2004. Mupirocin prophylaxis against nosocomial Staphylococcus aureus infections in nonsurgical patients: a randomized study. Ann. Intern. Med. 140:419-425.
55. Wu, H.-Y., A. Virolainen, B. Mathews, J. King, M. W. Russell, and D. E. Briles. 1997. Establishment of a Streptococcus pneumoniae nasopharyngeal colonization model in adult mice. Microb. Pathog. 23:127-137.