Structure of factor H-binding protein B (FhbB) of the periopathogen, Treponema denticola: Insights into progression of periodontal disease

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 12715-12722

  Miller, Daniel P ^a   Bell, Jessica K ^a   McDowell, John V ^a   Conrad, Daniel H ^a   Burgner, John W ^a   Héroux, Annie ^b   Marconi, Richard T ^a  

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

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT CONTROL PROTEINS; H-BINDING; MICROMOLAR RANGE; MOLECULAR BASIS; PERIODONTAL DISEASE; SITE DIRECTED MUTAGENESIS; SUCROSE OCTASULFATE;

SUGAR (SUCROSE);

PROTEINS;

BINDING PROTEIN; COMPLEMENT FACTOR H; FACTOR H BINDING PROTEIN B; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; DISEASE COURSE; PERIODONTAL DISEASE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE; THERMOSTABILITY; TREPONEMA DENTICOLA;

BACTERIAL PROTEINS; BINDING SITES; COMPLEMENT FACTOR H; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DISEASE PROGRESSION; GLYCOSAMINOGLYCANS; HUMANS; MUTAGENESIS, SITE-DIRECTED; PERIODONTAL DISEASES; PROTEIN STRUCTURE, TERTIARY; SURFACE PLASMON RESONANCE; TREPONEMA DENTICOLA;

TREPONEMA DENTICOLA;

EID: 84859759081     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.339721     Document Type: Article

References (51)

1. Krauss, J. L., Potempa, J., Lambris, J. D., and Hajishengallis, G. (2010) Complementary tolls in the periodontium. How periodontal bacteria modify complement and Toll-like receptor responses to prevail in the host. Periodontol. 2000 52, 141-162
2. Darveau, R. P. (2010) Periodontitis. A polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 8, 481-490
3. Van Dyke, T. E., and Serhan, C. N. (2003) Resolution of inflammation. A new paradigm for the pathogenesis of periodontal diseases. J. Dent. Res. 82, 82-90 (Pubitemid 41764116)
4. Paster, B. J., Olsen, I., Aas, J. A., and Dewhirst, F. E. (2006) The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol. 2000 42, 80-87 (Pubitemid 44286048)
5. Paster, B. J., Boches, S. K., Galvin, J. L., Ericson, R. E., Lau, C. N., Levanos, V. A., Sahasrabudhe, A., and Dewhirst, F. E. (2001) Bacterial diversity in human subgingival plaque. J. Bacteriol. 183, 3770-3783 (Pubitemid 32510445)
6. Ellen, R. P., and Galimanas, V. B. (2005) Spirochetes at the forefront of periodontal infections. Periodontology 2000 38, 13-32 (Pubitemid 43034321)
7. Dewhirst, F. E., Tamer, M. A., Ericson, R. E., Lau, C. N., Levanos, V. A., Boches, S. K., Galvin, J. L., and Paster, B. J. (2000) The diversity of periodontal spirochetes by 16 S rRNA analysis. Oral Microbiol. Immunol. 15, 196-202 (Pubitemid 30208582)
8. Socransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C., and Kent, R. L., Jr. (1998) Microbial complexes in subgingival plaque. J. Clin Periodontol. 25, 134-144 (Pubitemid 128705944)
9. Boackle, R. J. (1991) The interaction of salivary secretions with the human complement system. A model for the study of host defense systems on inflamed mucosal surfaces. Crit. Rev. Oral Biol. Med. 2, 355-367
10. Boackle, R. J., Pruitt, K. M., Silverman, M. S., and Glymph, J. L., Jr. (1978) The effects of human saliva on the hemolytic activity of complement. J. Dent. Res. 57, 103-110 (Pubitemid 8385881)
11. Schenkein, H. A. (1991) The role of complement in periodontal diseases. Crit. Rev. Oral. Biol. Med. 2, 65-81
12. Schenkein, H. A., and Genco, R. J. (1977) Gingival fluid and serum in periodontal diseases. I. Quantitative study of immunoglobulins, complement components, and other plasma proteins. J. Periodontol. 48, 772-777 (Pubitemid 8254482)
13. Ruddy, S., and Austen, K. F. (1971) C3b inactivator of man. II. Fragments produced by C3b inactivator cleavage of cell-bound or fluid phase C3b. J. Immunol. 107, 742-750
14. Zipfel, P. F., and Skerka, C. (2009) Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9, 729-740
15. Zipfel, P. F., Skerka, C., Hellwage, J., Jokiranta, S. T., Meri, S., Brade, V., Kraiczy, P., Noris, M., and Remuzzi, G. (2002) Factor H family proteins. On complement, microbes, and human diseases. Biochem. Soc. Trans. 30, 971-978 (Pubitemid 36002390)
16. Jarva, H., Jokiranta, T. S., Hellwage, J., Zipfel, P. F., and Meri, S. (1999) Regulation of complement activation by C-reactive protein. Targeting the complement inhibitory activity of factor H by an interaction with short consensus repeat domains 7 and 8-11. J. Immunol. 163, 3957-3962 (Pubitemid 29450924)
17. Ferreira, V. P., Pangburn, M. K., and Cortés, C. (2010) Complement control protein factor H. The good, the bad, and the inadequate. Mol. Immunol. 47, 2187-2197
18. Schmidt, C. Q., Herbert, A. P., Hocking, H. G., Uhrín, D., and Barlow, P. N. (2008) Translational mini-review series on complement factor H. Structural and functional correlations for factor H. Clin. Exp. Immunol. 151,14-24 (Pubitemid 350231000)
19. Holers, V. M. (2008) The spectrum of complement alternative pathway-mediated diseases. Immunol. Rev. 223, 300-316
20. McDowell, J. V., Lankford, J., Stamm, L., Sadlon, T., Gordon, D. L., and Marconi, R. T. (2005) Demonstration of factor H-like protein 1 binding to Treponema denticola, a pathogen associated with periodontal disease in humans. Infect. Immun. 73, 7126-7132 (Pubitemid 41587609)
21. McDowell, J. V., Frederick, J., Stamm, L., and Marconi, R. T. (2007) Identification of the gene encoding the FhbB protein of Treponema denticola, a highly unique factor H-like protein 1-binding protein. Infect. Immun. 75, 1050-1054 (Pubitemid 46203472)
22. McDowell, J. V., Frederick, J., Miller, D. P., Goetting-Minesky, M. P., Goodman, H., Fenno, J. C., and Marconi, R. T. (2011) Identification of the primary mechanism of complement evasion by the periodontal pathogen, Treponema denticola. Mol. Oral Microbiol. 26, 140-149
23. McDowell, J. V., Huang, B., Fenno, J. C., and Marconi, R. T. (2009) Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect. Immun. 77, 1417-1425
24. Uitto, V. J., Grenier, D., Chan, E. C., and McBride, B. C. (1988) Isolation of a chymotrypsin-like enzyme from Treponema denticola. Infect. Immun. 56, 2717-2722
25. Cordes, F. S., Roversi, P., Kraiczy, P., Simon, M. M., Brade, V., Jahraus, O., Wallis, R., Skerka, C., Zipfel, P. F., Wallich, R., and Lea, S. M. (2005) A novel fold for the factor H-binding protein BbCRASP-1 of Borrelia burgdorferi. Nat. Struct. Mol. Biol. 12, 276-277 (Pubitemid 43079371)
26. Schneider, M. C., Prosser, B. E., Caesar, J. J., Kugelberg, E., Li, S., Zhang, Q., Quoraishi, S., Lovett, J. E., Deane, J. E., Sim, R. B., Roversi, P., Johnson, S., Tang, C. M., and Lea, S. M. (2009) Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates. Nature 458, 890-893
27. Miller, D. P., McDowell, J. V., Bell, J. K., and Marconi, R. T. (2011) Crystallization of the factor H-binding protein, FhbB, from the periopathogen Treponema denticola. Acta Crystallogr Sect. F Struct. Biol. Cryst. Commun. 67, 678-681
28. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
29. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
30. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
31. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
32. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
33. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr.DBiol. Crystallogr. 50, 760-763
34. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity. All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
35. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity. All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
36. Holm, L., and Rosenström, P. (2010) Dali server. Conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
37. McDowell, J. V., Wolfgang, J., Tran, E., Metts, M. S., Hamilton, D., and Marconi, R. T. (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 (Pubitemid 36637589)
38. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
39. Schuck, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320, 104-124
40. Morgan, H. P., Schmidt, C. Q., Guariento, M., Blaum, B. S., Gillespie, D., Herbert, A. P., Kavanagh, D., Mertens, H. D., Svergun, D. I., Johansson, C. M., Uhrín, D., Barlow, P. N., and Hannan, J. P. (2011) Structural basis for engagement by complement factorHof C3b on a self-surface. Nat. Struct. Mol. Biol. 18, 463-470
41. Wu, J., Wu, Y. Q., Ricklin, D., Janssen, B. J., Lambris, J. D., and Gros, P. (2009) Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat. Immunol. 10, 728-733
42. Rossmann, E., Kraiczy, P., Herzberger, P., Skerka, C., Kirschfink, M., Simon, M. M., Zipfel, P. F., and Wallich, R. (2007) Dual binding specificity of a Borrelia hermsii-associated complement regulator-acquiring surface protein for factor H and plasminogen discloses a putative virulence factor of relapsing fever spirochetes. J. Immunol. 178, 7292-7301 (Pubitemid 46847456)
43. Giannakis, E., Jokiranta, T. S., Male, D. A., Ranganathan, S., Ormsby, R. J., Fischetti, V. A., Mold, C., and Gordon, D. L. (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 (Pubitemid 36546684)
44. Hovis, K. M., Jones, J. P., Sadlon, T., Raval, G., Gordon, D. L., and Marconi, R. T. (2006) Molecular analyses of the interaction of Borrelia hermsii FhbA with the complement regulatory proteins factor H and factor H-like protein 1. Infect. Immun. 74, 2007-2014
45. Seshu, J., Esteve-Gassent, M. D., Labandeira-Rey, M., Kim, J. H., Trzeciakowski, J. P., Höök, M., and Skare, J. T. (2006) Inactivation of the fibronectin-binding adhesin gene bbk32 significantly attenuates the infectivity potential of Borrelia burgdorferi. Mol. Microbiol. 59, 1591-1601
46. Prosser, B. E., Johnson, S., Roversi, P., Herbert, A. P., Blaum, B. S., Tyrrell, J., Jowitt, T. A., Clark, S. J., Tarelli, E., Uhrín, D., Barlow, P. N., Sim, R. B., Day, A. J., and Lea, S. M. (2007) Structural basis for complement factor H linked age-related macular degeneration. J. Exp. Med. 204, 2277-2283 (Pubitemid 47529315)
47. Zipfel, P. F., Würzner, R., and Skerka, C. (2007) Complement evasion of pathogens. Common strategies are shared by diverse organisms. Mol. Immunol. 44, 3850-3857 (Pubitemid 47332624)
48. McDowell, J. V., Harlin, M. E., Rogers, E. A., and Marconi, R. T. (2005) Putative coiled-coil structural elements of the BBA68 protein of Lyme disease spirochetes are required for formation of its factor H-binding site. J. Bacteriol. 187, 1317-1323 (Pubitemid 40299456)
49. McDowell, J. V., Wolfgang, J., Senty, L., Sundy, C. M., Noto, M. J., and Marconi, R. T. (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 complementregulatory protein, factor H. J. Immunol. 173, 7471-7480 (Pubitemid 39628187)
50. Gomes-Filho, I. S., Freitas Coelho, J. M., da Cruz, S. S., Passos, J. S., Teixeira de Freitas, C. O., Aragão Farias, N. S., Amorim da Silva, R., Silva Pereira, M. N., Lima, T. L., and Barreto, M. L. (2011) Chronic periodontitis and C-reactive protein levels. J. Periodontol. 82, 969-978
51. Kang, Y. H., Urban, B. C., Sim, R. B., and Kishore, U. (2011) Immunobiology 217, 455-464