Fibronectin binding protein BBK32 of the Lyme disease spirochete promotes bacterial attachment to glycosaminoglycans

Infection and Immunity

Volumn 74, Issue 1, 2006, Pages 435-441

  Fischer, Joshua R ^a   LeBlanc, Kimberly T ^a   Leong, John M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CELL SURFACE PROTEIN; DERMATAN SULFATE; FIBRONECTIN BINDING PROTEIN; FIBRONECTIN BINDING PROTEIN BBK32; GLYCOSAMINOGLYCAN; HEPARIN; LIPOPROTEIN; PROTEIN BGP; PROTEIN DBPA; PROTEIN DBPB; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BORRELIA BURGDORFERI; CELL TYPE; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; LYME DISEASE; MAMMAL CELL; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; RAT; SHUTTLE VECTOR; SPIROCHETE; SYSTEMIC DISEASE;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; CELL LINE; CELL LINE, TUMOR; CELL WALL; FIBRONECTINS; GLYCOSAMINOGLYCANS; HEPARIN; HUMANS; LIPOPROTEINS; LYME DISEASE; RATS;

EID: 29644446929     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.1.435-441.2006     Document Type: Article

References (54)

1. Akins, D. R., K. W. Bourell, M. J. Caimano, M. V. Norgard, and J. D. Radolf. 1998. A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J. Clin. Investig. 101:2240-2250.
2. Barbour, A. G. 1988. Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent. J. Clin. Microbiol. 26:475-478.
3. Brooks, C. S., P. S. Hefty, S. E. Jolliff, and D. R. Akins. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:3371-3383.
4. Brown, E. L., R. M. Wooten, B. J. Johnson, R. V. Iozzo, A. Smith, M. C. Dolan, B. P. Guo, J. J. Weis, and M. Hook. 2001. Resistance to Lyme disease in decorin-deficient mice. J. Clin. Investig. 107:845-852.
5. Cadavid, D., V. Bundoc, and A. G. Barbour. 1993. Experimental infection of the mouse brain by a relapsing fever Borrelia species: a molecular analysis. J. Infect. Dis. 168:143-151.
6. Cluss, R. G., D. A. Silverman, and T. R. Stafford. 2004. Extracellular secretion of the Borrelia burgdorferi Oms28 porin and Bgp, a glycosaminoglycan binding protein. Infect. Immun. 72:6279-6286.
7. 3-chain integrin ligand identified using a phage display library. Mol. Microbiol. 34:926-940.
8. 11bβ 3 mediates binding of the Lyme disease agent Borrelia burgdorferi to human platelets. Proc. Natl. Acad. Sci. USA 90:7059-7063.
9. Comstock, L. E., and D. D. Thomas. 1989. Penetration of endothelial cell monolayers by Borrelia burgdorferi. Infect. Immun. 57:1626-1628.
10. Dean, D. C., T. M. Birkenmeier, G. D. Rosen, and S. J. Weintraub. 1991. Glycoprotein synthesis and secretion. Expression of fibronectin and its cell surface receptors. Am. Rev. Respir. Dis. 144:S25-S28.
11. Dorward, D. W., E. R. Fischer, and D. M. Brooks. 1997. Invasion and cytopathic killing of human lymphocytes by spirochetes causing Lyme disease. Clin. Infect. Dis. 25(Suppl. 1):S2-S8.
12. Dramsi, S., F. Bourdichon, D. Cabanes, M. Lecuit, H. Fsihi, and P. Cossart. 2004. FbpA, a novel multifunctional Listeria monocytogenes virulence factor. Mol. Microbiol. 53:639-649.
13. Eggers, C. H., M. J. Caimano, M. L. Clawson, W. G. Miller, D. S. Samuels, and J. D. Radolf. 2002. Identification of loci critical for replication and compatibility of a Borrelia burgdorferi cp32 plasmid and use of a cp32-based shuttle vector for the expression of fluorescent reporters in the Lyme disease spirochaete. Mol. Microbiol. 43:281-295.
14. Fikrig, E., S. W. Barthold, W. Sun, W. Feng, S. R. Telford III, and R. A. Flavell. 1997. Borrelia burgdorferi P35 and P37 proteins, expressed in vivo, elicit protective immunity. Immunity 6:531-539.
15. Fikrig, E., W. Feng, S. W. Barthold, S. R. Telford III, and R. A. Flavell. 2000. Arthropod- and host-specific Borrelia burgdorferi bbk32 expression and the inhibition of spirochete transmission. J. Immunol. 164:5344-5351.
16. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
17. Fischer, J. R., N. Parveen, L. Magoun, and J. M. Leong. 2003. Decorin-binding proteins A and B confer distinct mammalian cell type-specific attachment by Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. USA. 100:7307-7312.
18. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. C. Venter, et al. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
19. Galbe, J. L., E. Guy, J. M. Zapatero, E. I. Peerschke, and J. L. Benach. 1993. Vascular clearance of Borrelia burgdorferi in rats. Microb. Pathog. 14:187-201.
20. Garcia-Monco, J. C., B. Fernandez-Villar, and J. L. Benach. 1989. Adherence of the Lyme disease spirochete to glial cells and cells of glial origin. J. Infect. Dis. 160:497-506.
21. Grab, D. J., C. Givens, and R. Kennedy. 1998. Fibronectin-binding activity in Borrelia burgdorferi. Biochim. Biophys. Acta 1407:135-145.
22. Guo, B. P., E. L. Brown, D. W. Dorward, L. C. Rosenberg, and M. Hook. 1998. Decorin-binding adhesins from Borrelia burgdorferi. Mol. Microbiol. 30:711-723.
23. Guo, B. P., S. J. Norris, L. C. Rosenberg, and M. Hook. 1995. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect. Immun. 63:3467-3472.
24. Isaacs, R. 1994. Borrelia burgdorferi bind to epithelial cell proteoglycan. J. Clin. Investig. 93:809-819.
25. Johnson, R. C., N. Marek, and C. Kodner. 1984. Infection of Syrian hamsters with Lyme disease spirochetes. J. Clin. Microbiol. 20:1099-1101.
26. Kim, J. H., J. Singvall, U. Schwarz-Linek, B. J. Johnson, J. R. Potts, and M. Hook. 2004. BBK32, a fibronectin binding MSCRAMM from Borrelia burgdorferi, contains a disordered region that undergoes a conformational change on ligand binding. J. Biol. Chem. 279:41706-41714.
27. Labandeira-Rey, M., and J. T. Skare. 2001. Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect. Immun. 69:446-455.
28. Leong, J. M., R. Fournier, and R. R. Isberg. 1990. Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein. EMBO J. 9:1979-1989.
29. Leong, J. M., P. E. Morrissey, E. Ortega-Barria, M. E. Pereira, and J. Coburn. 1995. Hemagglutination and proteoglycan binding by the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63:874-883.
30. Leong, J. M., D. Robbins, L. Rosenfeld, B. Lahiri, and N. Parveen. 1998. Structural requirements for glycosaminoglycan recognition by the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 66:6045-6048.
31. Leong, J. M., H. Wang, L. Magoun, J. A. Field, P. E. Morrissey, D. Robbins, J. B. Tatro, J. Coburn, and N. Parveen. 1998. Different classes of proteoglycans contribute to the attachment of Borrelia burgdorferi to cultured endothelial and brain cells. Infect. Immun. 66:994-999.
32. Liang, F. T., E. L. Brown, T. Wang, R. V. Iozzo, and E. Fikrig. 2004. Protective niche for Borrelia burgdorferi to evade humoral immunity. Am. J. Pathol. 165:977-985.
33. Magoun, L., W. R. Zuckert, D. Robbins, N. Parveen, K. R. Alugupalli, T. G. Schwan, A. G. Barbour, and J. M. Leong. 2000. Variable small protein (Vsp)-dependent and Vsp-independent pathways for glycosaminoglycan recognition by relapsing fever spirochaetes. Mol. Microbiol. 36:886-897.
34. Norris, S. J., J. K. Howell, S. A. Garza, M. S. Ferdows, and A. G. Barbour. 1995. High- and low-infectivity phenotypes of clonal populations of in vitro-cultured Borrelia burgdorferi. Infect. Immun. 63:2206-2212.
35. Parveen, N., and J. M. Leong. 2000. Identification of a candidate glycosaminoglycan-binding adhesin of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 35:1220-1234.
36. Parveen, N., D. Robbins, and J. M. Leong. 1999. Strain variation in glycosaminoglycan binding influences cell type-specific binding among Lyme disease spirochetes. Infect. Immun. 67:1743-1749.
37. Parveen, N., M. Caimano, J. D. Radolf, and J. M. Leong. 2003. Adaptation of the Lyme disease spirochaete to the mammalian host environment results in enhanced glycosaminoglycan and host cell binding. Mol. Microbiol. 47:1433-1444.
38. Pennington, P. M., D. Cadavid, and A. G. Barbour. 1999. Characterization of VspB of Borrelia turicatae: a major outer membrane protein expressed in blood and tissues of mice. Infect. Immun. 67:4637-4645.
39. Probert, W. S., and B. J. Johnson. 1998. Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol. Microbiol. 30:1003-1015.
40. Probert, W. S., J. H. Kim, M. Hook, and B. J. Johnson. 2001. Mapping the ligand-binding region of Borrelia burgdorferi fibronectin-binding protein BBK32. Infect. Immun. 69:4129-4133.
41. Purser, J. E., and S. J. Norris. 2000. Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA. 97:13865-13870.
42. Raibaud, S., U. Schwarz-Linek, J. H. Kim, H. T. Jenkins, E. R. Baines, S. Gurusidappa, M. Hook, and J. R. Potts. 2005. Borrelia burgdorferi binds fibronectin through a tandem beta zipper-a common mechanism. J. Biol. Chem. 280:18803-18809.
43. Sadziene, A., B. Wilske, M. Ferdows, and A. Barbour. 1993. The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid. Infect. Immun. 61:2192-2195.
44. Seinost, G., D. E. Dykhuizen, R. J. Dattwyler, W. T. Golde, J. J. Dunn, I. N. Wang, G. P. Wormser, M. E. Schriefer, and B. J. Luft. 1999. Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect. Immun. 67:3518-3524.
45. Simpson, W. J., C. F. Garon, and T. G. Schwan. 1990. Analysis of supercoiled circular plasmids in infectious and non-infectious Borrelia burgdorferi. Microb. Pathog. 8:109-118.
46. Steere, A. C., J. Coburn, and L. Glickstein. 2004. The emergence of Lyme disease. J. Clin. Investig. 113:1093-1101.
47. Stewart, P. E., R. Thalken, J. L. Bono, and P. Rosa. 2001. Isolation of a circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi. Mol. Microbiol. 39:714-721.
48. Sugahara, K., T. Mikami, T. Uyama, S. Mizuguchi, K. Nomura, and H. Kitagawa. 2003. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13:612-620.
49. Szczepanski, A., M. B. Furie, J. L. Benach, B. P. Lane, and H. B. Fleit. 1990. Interaction between Borrelia burgdorferi and endothelium in vitro. J. Clin. Investig. 85:1637-1647.
50. Thomas, D. D., and L. E. Comstock. 1989. Interaction of Lyme disease spirochetes with cultured eucaryotic cells. Infect. Immun. 57:1324-1326.
51. Tokarz, R., J. M. Anderton, L. I. Katona, and J. L. Benach. 2004. Combined effects of blood and temperature shift on Borrelia burgdorferi gene expression as determined by whole genome DNA array. Infect. Immun. 72:5419-5432.
52. Wang, G., C. Ojaimi, H. Wu, V. Saksenberg, R. Iyer, D. Liveris, S. A. McClain, G. P. Wormser, and I. Schwartz. 2002. Disease severity in a murine model of lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. J. Infect. Dis. 186:782-791.
53. Wang, G., A. P. van Dam, I. Schwartz, and J. Dankert. 1999. Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin. Microbiol. Rev. 12:633-653.
54. Zuckert, W. R., J. E. Lloyd, P. E. Stewart, P. A. Rosa, and A. G. Barbour. 2004. Cross-species surface display of functional spirochetal lipoproteins by recombinant Borrelia burgdorferi. Infect. Immun. 72:1463-1469.