Putative coiled-coil structural elements of the BBA68 protein of lyme disease spirochetes are required for formation of its factor H binding site

Journal of Bacteriology

Volumn 187, Issue 4, 2005, Pages 1317-1323

  McDowell, John V ^a   Harlin, Matthew E ^a   Rogers, Elizabeth A ^a   Marconi, Richard T ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3B; COMPLEMENT FACTOR H; FACTOR H LIKE PROTEIN 1; PROTEIN; PROTEIN BBA68; RECOMBINANT PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BORRELIA INFECTION; COILED BODY; GENE MUTATION; LYME DISEASE; MULTIGENE FAMILY; NONHUMAN; OPSONIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; SPIROCHETE; STRAIN DIFFERENCE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BORRELIA BURGDORFERI; COMPLEMENT FACTOR H; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION;

EID: 14544300067     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.4.1317-1323.2005     Document Type: Article

References (38)

1. Alitalo, A., T. Meri, T. Chen, H. Lankinen, Z.-Z. Cheng, T. Sakari Jokiranta, I. J. T. Seppala, P. Lahdenne, P. S. Hefty, D. R. Akins, and S. Meri. 2004. Lysine-dependent multipoint binding of the Borrelia burgdorferi virulence factor pouter surface protein E to the C terminus of factor H. J. Immunol. 172:6195-6201.
2. Alitalo, A., T. Meri, L. Rämö, T. S. Jokiranta, T. Heikkilä, I. J. T. Seppälä, J. Oksi, M. Viljanen, and S. Meri. 2001. Complement evasion by Borrelia burgdorferi: serum-resistant strains promote C3b inactivation. Infect. Immun. 69:3685-3691.
3. Alitalo, A., T. Meri, H. Lankinen, I. Seppala, P. Lahdenne, P. S. Hefty, D. Akins, and S. Meri. 2002. Complement inhibitor factor H binding to Lyme disease spirochetes is mediated by inducible expression of multiple plasmid-encoded outer surface protein E paralogs. J. Immunol. 169:3847-3853.
4. Areschoug, T., M. Stalhammar-Carlemalm, I. Karlsosson, and G. Lindahl. 2002. Streptococcal beta protein has separate binding sites for human factor H and IgA-Fc. J. Biol. Chem. 277:12642-12648.
5. Arthur, T. M., L. C. Anthony, and R. B. Burgess. 2000. Mutational analysis of the B′260-309, a sigma 70 binding site located on Escherichia coli core RNA polymerase. J. Biol. Chem. 275:23113-23119.
6. Asakawa, R., H. Komatsuzawa, T. Kawai, S. Yamada, R. B. Goncalves, S. Izumi, T. Fujiwara, Y. Nakano, H. Shiba, M. A. Taubman, H. Kurihara, and M. Sugai. 2003. Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol. Microbiol. 50:1125-1139.
7. Baranton, G., D. Postic, I. Saint Girons, P. Boerlin, J.-C. Piffaretti, M. Assous, and P. A. D. Grimont. 1992. Delineation of Borrelia burgdorferi sensu stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis. Int. J. Syst. Bacteriol. 42:378-383.
8. Dave, S., S. Carmicle, S. Hammerschmidt, M. K. Panghurn, and L. S. McDaniel. 2004. Dual roles of PspC, a surface protein of Streptococcus pneumoniae, in binding human secretory IgA and factor H. J. ImmunoI. 173:471-477.
9. Duthy, T. G., R. J. Ormsby, E. Giannakis, A. D. Ogunniyi, U. H. Stroeher, J. C. Paton, and D. L. Gordon. 2002. The human complement regulator factor H binds pneumococcal surface protein PspC via short consensus repeats 13 to 15. Infect. Immun. 70:5604-5611.
10. Fraser, C., 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. Fleischman, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. Weidman, T. Utterback, L. Watthey, L. McDonald, P. Artiach, C. Bowman, S. Garland, C. Fujii, M. D. Cotton, K. Horst, K. Roberts, B. Hatch, H. O. Smith, and J. C. Venter. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
11. Giannikis, E., T. S. Jokiranta, D. A. Male, S. Ranganathan, R. J. Ormsby, V. A. Fischetti, C. Mold, and D. L. Gordon. 2003. A common site within factor H SCR 7 responsible for binding heparin, C-reactive protein and streptococcal M protein. Eur. J. Immunol. 33:962-969.
12. Hefty, P. S., C. S. Brooks, A. M. Jett, G. L. White, S. K. Wikel, R. C. Kennedy, and D. R. Akins. 2002. OspE-related, OspF-related and ELp lipoproteins are immunogenic in baboons experimentally infected with Borrelia burgdorferi and in human Lyme disease patients. J. Clin. Microbiol. 40:4256-4265.
13. Hellwage, J., T. Meri, T. Heikkila, A. Alitalo, J. Panelius, P. Lahdenne, I. J. T. Seppala, and S. Meri. 2001. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276:8427-8435.
14. Hovis, K., J. V. McDowell, L. Griffin, and R. T. Marconi. 2004. Identification and characterization of a linear plasmid encoded factor H-binding protein (FhbA) of the relapsing fever spirochete, Borrelia hermsii. J. Bacteriol. 186:2612-2618.
15. Joshi, S. B., R. E. Dutch, and R. A. Lamb. 1998. A core trimer of the Paramyxovirus fusion protein: parallels to influenza virus hemagglutinin and HIV-1 gp41. Virology 248:20-34.
16. Kraiczy, P., J. Hellwage, C. Skerka, H. Becker, M. Kirschfink, M. S. Simon, V. Brade, P. F. Zipfel, and R. Wallich. 2003. Complement resistance of Borrelia burgdorferi correlates with the expression of BbCRASP-1, a novel linear plasmid-encoded surface protein that interacts with human factor H and FHL-1 and is unrelated to Erp proteins. J. Biol. Chem. 279:2421-2429.
17. Kraiczy, P., J. Hellwage, C. Skerka, M. Kirschfink, V. Brade, P. F. Zipfel, and R. Wallich. 2003. Immune evasion of Borrelia burgdorferi: mapping of a complement inhibitor factor H-binding site of BbCRASP-3, a novel member of the Erp protein family. Eur. J. Immunol. 33:697-707.
18. Kraiczy, P., C. Skerka, and P. F. Zipfel. 2001. Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi. Infect. Immun. 69:7800-7809.
19. Kwok, S. C., and R. S. Hodges. 2004. Stabilizing and destabilizing clusters in the hydrophobic core of long two-stranded alpha helical coiled-coils. J. Biol. Chem. 279:21576-21588.
20. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164.
21. Malashkevich, V. N., M. Singh, and P. S. Kim. 2001. The trimer-of-hairpins motif in membrane fusion: Visna virus. Proc. Natl. Acad. Sci. USA 98:8502-8506.
22. McDowell, J. V., S. Y. Sung, L. T. Hu, and R. T. Marconi. 2002. Evidence that the variable regions of the central domain of VlsE are antigenic during infection with the Lyme disease spirochetes. Infect. Immun. 70:4196-4203.
23. McDowell, J. V., S.-Y. Sung, G. Price, and R. T. Marconi. 2001. Demonstration of the genetic stability and temporal expression of select members of the Lyme disease spirochete OspF protein family during infection in mice. Infect. Immun. 69:4831-4838.
24. McDowell, J. V., E. Tran, D. Hamilton, J. Wolfgang, K. Miller, and R. T. Marconi. 2003. Analysis of the ability of spirochete species associated with relapsing fever, avian borreliosis, and epizootic bovine abortion to bind factor H and cleave C3b. J. Clin. Microbiol. 41:3905-3910.
25. McDowell, J. V., J. Wolfgang, L. Senty, C. M. Sundy, M. J. Noto, and R. T. Marconi. 2004. Demonstration of the involvement of outer surface protein E coiled-coil structural domains and higher order structural elements in the binding of infection-induced antibody and the complement-regulatory protein, factor H. J. Immunol. 173:7471-7480.
26. McDowell, J. V., J. Wolfgang, E. Tran, M. S. Metts, D. Hamilton, and R. T. Marconi. 2003. Comprehensive analysis of the factor H binding capabilities of Borrelia species associated with Lyme disease: delineation of two distinct classes of factor H binding proteins. Infect. Immun. 71:3597-3602.
27. Meri, T., A. Hartmann, D. Lenk, R. Eck, R. Wurzner, J. Hellwage, S. Meri, and P. F. Zipfel. 2002. The yeast Candida albicans binds complement regulators factor H and FHL-1. Infect. Immun. 70:5185-5192.
28. Meri, T., T. S. Jokiranta, J. Hellwage, A. Bialonski, P. F. Zipfel, and S. Meri. 2002. Onchocerca volvulus microfilariae avoid complement attack by direct binding of factor H. J. Infect. Dis. 185:1786-1793.
29. Metts, S., J. V. McDowell, M. Theisen, P. R. Hansen, and R. T. Marconi. 2003. Analysis of the OspE determinants involved in the binding of factor H and OspE targeting antibodies elicited during infection in mice. Infect. Immun. 71:3587-3596.
30. Nguyen, T.-P. K., T. T. Lam, S. W. Barthold, S. R. Telford III, R. A. Flavell, and E. Fikrig. 1994. Partial destruction of Borrelia burgdorferi within ticks that engorged on OspE- or OspF-immunized mice. Infect. Immun. 62:2079-2084.
31. Ram, S., D. P. McQuillen, S. Gulati, C. Elkins, M. K. Pangburn, and P. A. Rice. 1998. Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialyated Neiserria gonorrhoeae. J. Exp. Med. 188:671-680.
32. Roberts, D., M. Caimano, J. McDowell, M. Theisen, A. Holm, S. Alban, E. Orff, D. Nelson, S. Wikel, J. Radolf, and R. Marconi. 2002. Environmental regulation and differential expression of members of the Bdr protein family of Borrelia burgdorferi. Infect. Immun. 70:7033-7041.
33. Sung, S. Y., J. McDowell, J. A. Carlyon, and R. T. Marconi. 2000. Mutation and recombination in the upstream homology box-flanked ospE-related genes of the Lyme disease spirochetes result in the development of new antigenic variants during infection. Infect. Immun. 68:1319-1327.
34. Sung, S. Y., J. V. McDowell, and R. T. Marconi. 2001. Evidence for the contribution of point mutations to vlsE variation and for apparent constraints on the net accumulation of sequence changes in vlsE during infection with the Lyme disease spirochetes. J. Bacteriol. 168:5855-5861.
35. Whaley, K., and S. Ruddy. 1976. Modulation of the alternative complement pathways by beta 1 H globulin. J. Exp. Med. 144:1147-1163.
36. Zhang, J.-R., J. M. Hardham, A. G. Barbour, and A. G. Norris. 1997. Antigenic variation in Lyme disease borreliae by promiscuous recombination of vmp like sequence cassettes. Cell 89:275-285.
37. Zhang, J. R., and S. J. Norris. 1998. Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect. Immun. 66:3698-3704.
38. Zipfel, P. F., C. Skerka, J. Hellwage, S. T. Jokiranta, S. Meri, V. Brade, P. Kraiczy, M. Noris, and G. Remuzzi. 2002. Structure-function studies of the complement system. Biochem. Soc. Trans. 30:971-978.