Tetratricopeptide repeat protein-associated proteins contribute to the virulence of Porphyromonas gingivalis

Infection and Immunity

Volumn 78, Issue 6, 2010, Pages 2846-2856

  Kondo, Yoshio ^a   Ohara, Naoya ^b   Sato, Keiko ^a   Yoshimura, Mamiko ^c   Yukitake, Hideharu ^a   Naito, Mariko ^a   Fujiwara, Taku ^a   Nakayama, Koji ^a,d  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; TAPA PROTEIN; TAPB PROTEIN; TETRATRICOPEPTIDE REPEAT PROTEIN; TPRA PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMMUNOPRECIPITATION; IN VITRO STUDY; MOUSE; NONHUMAN; OUTER MEMBRANE; PERIODONTAL DISEASE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE; UPREGULATION; WILD TYPE;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BACTEROIDACEAE INFECTIONS; CULTURE MEDIA; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; IMMUNOPRECIPITATION; MICE; MICE, INBRED BALB C; PERIPLASM; PORPHYROMONAS GINGIVALIS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; SOFT TISSUE INFECTIONS; SURFACE PLASMON RESONANCE; TWO-HYBRID SYSTEM TECHNIQUES; VIRULENCE; VIRULENCE FACTORS;

EID: 77952701622     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01448-09     Document Type: Article

References (55)

1. Armitage, G. C. 1996. Periodontal diseases: diagnosis. Ann. Periodontol. 1:37-215.
2. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
3. Blatch, G. L., and M. Lassle. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932-939.
4. Bröms, J. E., P. J. Edqvist, A. Forsberg, and M. S. Francis. 2006. Tetratricopeptide repeats are essential for PcrH chaperone function in Pseudomonas aeruginosa type III secretion. FEMS Microbiol. Lett. 256:57-66.
5. Bröms, J. E., A. L. Forslund, A. Forsberg, and M. S. Francis. 2003. PcrH of Pseudomonas aeruginosa is essential for secretion and assembly of the type III translocon. J. Infect. Dis. 188:1909-1921.
6. Chen, Y. Y., K. J. Cross, R. A. Paolini, J. E. Fielding, N. Slakeski, and E. C. Reynolds. 2002. CPG70 is a novel basic metallocarboxypeptidase with C-terminal polycystic kidney disease domains from Porphyromonas gingivalis. J. Biol. Chem. 277:23433-23440.
7. Christersson, L. A., C. L. Fransson, R. G. Dunford, and J. J. Zambon. 1992. Subgingival distribution of periodontal pathogenic microorganisms in adult periodontitis. J. Periodontol. 63:418-425.
8. Core, L., and M. Perego. 2003. TPR-mediated interaction of RapC with ComA inhibits response regulator-DNA binding for competence development in Bacillus subtilis. Mol. Microbiol. 49:1509-1522. (Pubitemid 37153512)
9. Curtis, M. A., A. Thickett, J. M. Slaney, M. Rangarajan, J. Aduse-Opoku, P. Shepherd, N. Paramonov, and E. F. Hounsell. 1999. Variable carbohydrate modifications to the catalytic chains of the RgpA and RgpB proteases of Porphyromonas gingivalis W50. Infect. Immun. 67:3816-3823.
10. D'Andrea, L. D., and L. Regan. 2003. TPR proteins: the versatile helix. Trends Biochem. Sci. 28:655-662.
11. Das, A. K., P. W. Cohen, and D. Barford. 1998. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17:1192-1199.
12. Delgado-Partin, V. M., and R. E. Dalbey. 1998. The proton motive force, acting on acidic residues, promotes translocation of amino-terminal domains of membrane proteins when the hydrophobicity of the translocation signal is low. J. Biol. Chem. 273:9927-9934.
13. Diaz, P. I., N. Slakeski, E. C. Reynolds, R. Morona, A. H. Rogers, and P. E. Kolenbrander. 2006. Role of oxyR in the oral anaerobe Porphyromonas gingivalis. J. Bacteriol. 188:2454-2462.
14. Dodt, G., and S. J. Gould. 1996. Multiple PEX genes are required for proper subcellular distribution and stability of Pex5p, the PTS1 receptor: evidence that PTS1 protein import is mediated by a cycling receptor. J. Cell Biol. 135:1763-1774. (Pubitemid 27036439)
15. Genco, C. A., C. W. Cutler, D. Kapczynski, K. Maloney, and R. R. Arnold. 1991. A novel mouse model to study the virulence of and host response to Porphyromonas (Bacteroides) gingivalis. Infect. Immun. 59:1255-1263.
16. Grenier, D., and D. Mayrand. 1987. Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. J. Clin. Microbiol. 25: 738-740.
17. Haffajee, A. D., and S. S. Socransky. 1994. Microbial etiological agents of destructive periodontal diseases. Periodontol. 2000 5:78-111.
18. Hirano, T., N. Kinoshita, K. Morikawa, and M. Yanagida. 1990. Snap helix with knob and hole: essential repeats in S. pombe nuclear protein nuc2+. Cell 60:319-328. (Pubitemid 20055925)
19. Hosogi, Y., and M. J. Duncan. 2005. Gene expression in Porphyromonas gingivalis after contact with human epithelial cells. Infect. Immun. 73:2327-2335.
20. Hughes, T. R., M. J. Marton, A. R. Jones, C. J. Roberts, R. Stoughton, C. D. Armour, H. A. Bennett, E. Coffey, H. Dai, Y. D. He, M. J. Kidd, A. M. King, M. R. Meyer, D. Slade, P. Y. Lum, S. B. Stepaniants, D. D. Shoemaker, D. Gachotte, K. Chakraburtty, J. Simon, M. Bard, and S. H. Friend. 2000. Functional discovery via a compendium of expression profiles. Cell 102:109-126.
21. Irfan, U. M., D. V. Dawson, and N. F. Bissada. 2001. Epidemiology of periodontal disease: a review and clinical perspectives. J. Int. Acad. Periodontol. 3:14-21.
22. King, R. W., J. M. Peters, S. Tugendreich, M. Rolfe, P. Hieter, and M. W. Kirschner. 1995. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81:279-288.
23. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Lo, A. W., C. A. Seers, J. D. Boyce, S. G. Dashper, N. Slakeski, J. P. Lissel, and E. C. Reynolds. 2009. Comparative transcriptomic analysis of Porphyromonas gingivalis biofilm and planktonic cells. BMC Microbiol. 9:18.
25. Masuda, T., Y. Murakami, T. Noguchi, and F. Yoshimura. 2006. Effects of various growth conditions in a chemostat on expression of virulence factors in Porphyromonas gingivalis. Appl. Environ. Microbiol. 72:3458-3467.
26. Murakami, Y., M. Imai, H. Nakamura, and F. Yoshimura. 2002. Separation of the outer membrane and identification of major outer membrane proteins from Porphyromonas gingivalis. Eur. J. Oral Sci. 110:157-162.
27. Nakayama, K. 2003. Molecular genetics of Porphyromonas gingivalis: gingipains and other virulence factors. Curr. Protein Pept. Sci. 4:389-395.
28. Neiders, M. E., P. B. Chen, H. Suido, H. S. Reynolds, J. J. Zambon, M. Shlossman, and R. J. Genco. 1989. Heterogeneity of virulence among strains of Bacteroides gingivalis. J. Periodontal Res. 24:192-198.
29. Newton, H. J., F. M. Sansom, J. Dao, A. D. McAlister, J. Sloan, N. P. Cianciotto, and E. L. Hartland. 2007. Sel1 repeat protein LpnE is a Legionella pneumophila virulence determinant that influences vacuolar trafficking. Infect. Immun. 75:5575-5585.
30. Nguyen, K. A., J. Travis, and J. Potempa. 2007. Does the importance of the C-terminal residues in the maturation of RgpB from Porphyromonas gingivalis reveal a novel mechanism for protein export in a subgroup of gramnegative bacteria? J. Bacteriol. 189:833-843.
31. Nguyen, K. A., J. Zylicz, P. Szczesny, A. Sroka, N. Hunter, and J. Potempa. 2009. Verification of a topology model of PorT as an integral outer-membrane protein in Porphyromonas gingivalis. Microbiology 155:328-337.
32. O'Brien-Simpson, N. M., P. D. Veith, S. G. Dashper, and E. C. Reynolds. 2003. Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr. Protein Pept. Sci. 4:409-426.
33. O'Brien-Simpson, N. M., R. A. Paolini, B. Hoffmann, N. Slakeski, S. G. Dashper, and E. C. Reynolds. 2001. Role of RgpA, RgpB, and Kgp proteinases in virulence of Porphyromonas gingivalis W50 in a murine lesion model. Infect. Immun. 69:7527-7534.
34. Okabe, M., T. Yakushi, and M. Homma. 2005. Interactions of MotX with MotY and with the PomA/PomB sodium ion channel complex of the Vibrio alginolyticus polar flagellum. J. Biol. Chem. 280:25659-25664.
35. Okano, S., Y. Shibata, T. Shiroza, and Y. Abiko. 2006. Proteomics-based analysis of a counter-oxidative stress system in Porphyromonas gingivalis. Proteomics 6:251-258.
36. Oliver, R. C., L. J. Brown, and H. Loe. 1998. Periodontal diseases in the United States population. J. Periodontol. 69:269-278. (Pubitemid 128518357)
37. Papapanou, P. N. 1999. Epidemiology of periodontal diseases: an update. J. Int. Acad. Periodontol. 1:110-116.
38. Park, Y., O. Yilmaz, I. Y. Jung, and R. J. Lamont. 2004. Identification of Porphyromonas gingivalis genes specifically expressed in human gingival epithelial cells by using differential display reverse transcription-PCR. Infect. Immun. 72:3752-3758.
39. Pathirana, R. D., N. M. O'Brien-Simpson, G. C. Brammar, N. Slakeski, and E. C. Reynolds. 2007. Kgp and RgpB, but not RgpA, are important for Porphyromonas gingivalis virulence in the murine periodontitis model. Infect. Immun. 75:1436-1442.
40. Potempa, J., R. Pike, and J. Travis. 1995. The multiple forms of trypsin-like activity present in various strains of Porphyromonas gingivalis are due to the presence of either Arg-gingipain or Lys-gingipain. Infect. Immun. 63:1176-1182.
41. Rodrigues, P. H., and A. Progulske-Fox. 2005. Gene expression profile analysis of Porphyromonas gingivalis during invasion of human coronary artery endothelial cells. Infect. Immun. 73:6169-6173.
42. Sato, K., M. Naito, H. Yukitake, H. Hirakawa, M. Shoji, M. J. McBride, R. G. Rhodes, and K. Nakayama. 2010. A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 107:276-281.
43. Sato, K., E. Sakai, P. D. Veith, M. Shoji, Y. Kikuchi, H. Yukitake, N. Ohara, M. Naito, K. Okamoto, E. C. Reynolds, and K. Nakayama. 2005. Identification of a new membrane-associated protein that influences transport/maturation of gingipains and adhesins of Porphyromonas gingivalis. J. Biol. Chem. 280:8668-8677.
44. Scott, A. E., E. Simon, S. K. Park, P. Andrews, and D. R. Zusman. 2008. Site-specific receptor methylation of FrzCD in Myxococcus xanthus is controlled by a tetra-trico peptide repeat (TPR) containing regulatory domain of the FrzF methyltransferase. Mol. Microbiol. 69:724-735.
45. Seers, C. A., N. Slakeski, P. D. Veith, T. Nikolof, Y. Y. Chen, S. G. Dashper, and E. C. Reynolds. 2006. The RgpB C-terminal domain has a role in attachment of RgpB to the outer membrane and belongs to a novel C-terminal-domain family found in Porphyromonas gingivalis. J. Bacteriol. 188: 6376-6386.
46. Shelburne, C. E., R. M. Gleason, G. R. Germaine, L. F. Wolff, B. H. Mullally, W. A. Coulter, and D. E. Lopatin. 2002. Quantitative reverse transcription polymerase chain reaction analysis of Porphyromonas gingivalis gene expression in vivo. J. Microbiol. Methods 49:147-156.
47. Sikorski, R. S., M. S. Boguski, M. Goebl, and P. Hieter. 1990. A repeating amino acid motif in CDC23 defines a family of proteins and a new relationship among genes required for mitosis and RNA synthesis. Cell 60:307-317.
48. Smoot, L. M., J. C. Smoot, M. R. Graham, G. A. Somerville, D. E. Sturdevant, C. A. Migliaccio, G. L. Sylva, and J. M. Musser. 2001. Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Proc. Natl. Acad. Sci. U. S. A. 98:10416-10421.
49. Tachibana-Ono, M., A. Yoshida, S. Kataoka, T. Ansai, Y. Shintani, Y. Takahashi, K. Toyoshima, and T. Takehara. 2008. Identification of the genes associated with a virulent strain of Porphyromonas gingivalis using the subtractive hybridization technique. Oral Microbiol. Immunol. 23:84-87.
50. Tzamarias, D., and K. Struhl. 1994. Functional dissection of the yeast Cyc8-Tup1 transcriptional co-repressor complex. Nature 369:758-761.
51. Veith, P. D., G. H. Talbo, N. Slakeski, S. G. Dashper, C. Moore, R. A. Paolini, and E. C. Reynolds. 2002. Major outer membrane proteins and proteolytic processing of RgpA and Kgp of Porphyromonas gingivalis W50. Biochem. J. 363:105-115.
52. Wattiau, P., B. Bernier, P. Deslee, T. Michiels, and G. R. Cornelis. 1994. Individual chaperones required for Yop secretion by Yersinia. Proc. Natl. Acad. Sci. U. S. A. 91:10493-10497.
53. Yoshimura, M., Y. Nakano, Y. Yamashita, T. Oho, T. Saito, and T. Koga. 2000. Formation of methyl mercaptan from L-methionine by Porphyromonas gingivalis. Infect. Immun. 68:6912-6916.
54. Yoshimura, M., N. Ohara, Y. Kondo, M. Shoji, S. Okano, Y. Nakano, Y. Abiko, and K. Nakayama. 2008. Proteome analysis of Porphyromonas gingivalis cells placed in a subcutaneous chamber of mice. Oral Microbiol. Immunol. 23:413-418.
55. Zhang, Y., T. Wang, W. Chen, O. Yilmaz, Y. Park, I. Y. Jung, M. Hackett, and R. J. Lamont. 2005. Differential protein expression by Porphyromonas gingivalis in response to secreted epithelial cell components. Proteomics 5:198-211.