Fimbrial proteins of Porphyromonas gingivalis mediate in vivo virulence and exploit TLR2 and complement receptor 3 to persist in macrophages

Journal of Immunology

Volumn 179, Issue 4, 2007, Pages 2349-2358

  Wang, Min ^a   Shakhatreh, Muhamad Ali K ^a   James, Deanna ^a   Liang, Shuang ^a   Nishiyama, So Ichiro ^b   Yoshimura, Fuminobu ^b   Demuth, Donald R ^a,c   Hajishengallis, George ^a,c  

^a UNIVERSITY OF LOUISVILLE SCHOOL OF MEDICINE   (United States)

^b AICHI GAKUIN UNIVERSITY   (Japan)

^c University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 3; FIMBRIA PROTEIN; INTERLEUKIN 12; PROTEIN P70; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CD11B ANTIGEN; FIMBRILLIN; FIMC PROTEIN, BACTERIA; FIMD PROTEIN, BACTERIA; TLR2 PROTEIN, MOUSE;

ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; IN VIVO CULTURE; MACROPHAGE; NONHUMAN; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; ADAPTATION; ANIMAL; BACTERIAL INFECTION; CELL CULTURE; CHRONIC DISEASE; DISEASE MODEL; EVOLUTION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; MOUSE; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY; PERIODONTITIS; PERITONEUM MACROPHAGE;

ADAPTATION, BIOLOGICAL; ANIMALS; ANTIGENS, CD11B; BACTERIAL PROTEINS; BACTEROIDACEAE INFECTIONS; CELLS, CULTURED; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; EVOLUTION; FIMBRIAE PROTEINS; IMMUNITY, NATURAL; INTERLEUKIN-12; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RECEPTORS, COMPLEMENT; TOLL-LIKE RECEPTOR 2;

EID: 34848908962     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.4.2349     Document Type: Article

References (46)

1. Pihlstrom, B. L., B. S. Michalowicz, and N. W. Johnson. 2005. Periodontal diseases. Lancet 366: 1809-1820.
2. Holt, S. C., and J. L. Ebersole. 2005. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex," a prototype polybacterial pathogenic consortium in periodontitis. Periodontology 2000 38: 72-122.
3. Zambon, J. J., S. Grossi, R. Dunford, V. I. Harazsthy, H. Preus, and R. J. Genco. 1994. Epidemiology of subgingival bacterial pathogens in periodontal diseases. In Molecular Pathogenesis of Periodontal Disease. R. J. Genco, S. Hamada, J. R. Lehrer, J. R. McGhee, and S. Mergenhangen, eds. American Society for Microbiology, Washington, D.C. pp. 3-12.
4. Kozarov, E. V., B. R. Dorn, C. E. Shelburne, W. A. Dunn, Jr., and A. Progulske-Fox. 2005. Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler. Thromb. Vasc. Biol. 25: e17-e18.
5. Gibson, F. C., III, C. Hong, H. H. Chou, H. Yumoto, J. Chen, E. Lien, J. Wong, and C. A. Genco. 2004. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 109: 2801-2806.
6. Pussinen, P. J., G. Alfthan, P. Jousilahti, S. Paju, and J. Tuomilehto. 2006. Systemic exposure to Porphyromonas gingivalis predicts incident stroke. Atherosclerosis. 193: 222-228.
7. Lamont, R. J., and H. F. Jenkinson. 1998. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62: 1244-1263.
8. Malek, R., J. G. Fisher, A. Caleca, M. Stinson, C. J. van Oss, J. Y. Lee, M. I. Cho, R. J. Genco, R. T. Evans, and D. W. Dyer. 1994. Inactivation of Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats. J. Bacteriol. 176: 1052-1059.
9. Noiri, Y., L. Li, F. Yoshimura, and S. Ebisu. 2004. Localization of Porphyromonas gingivalis-carrying fimbriae in situ in human periodontal pockets. J. Dent. Res. 83: 941-945.
10. Wu, Y. M., J. Yan, L. L. Chen, and Z. Y. Gu. 2007. Association between infection of different strains of Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in subgingival plaque and clinical parameters in chronic periodontitis. J. Zhejiang Univ. Sci. B. 8: 121-131.
11. Hajishengallis, G., P. Ratti, and E. Harokopakis. 2005. Peptide mapping of bacterial fimbrial epitopes interacting with pattern recognition receptors. J. Biol. Chem. 280: 38902-38913.
12. Hajishengallis, G., R. I. Tapping, E. Harokopakis, S.-I. Nishiyama, P. Ratti, R. E. Schifferle, E. A. Lyle, M. Triantafilou, K. Triantafilou, and F. Yoshimura. 2006. Differential interactions of fimbriae and lipopolysaccharide from Porphyromonas gingivalis with the Toll-like receptor 2-centered pattern recognition apparatus. Cell. Microbiol. 8: 1557-1570.
13. 2 integrin adhesive activity and promote binding to and internalization by macrophages. Infect. Immun. 74: 5658-5666.
14. Harokopakis, E., M. H. Albzreh, M. H. Martin, and G. Hajishengallis. 2006. TLR2 transmodulates monocyte adhesion and transmigration via Rac1- and PI3K-mediated inside-out signaling in response to Porphyromonas gingivalis fimbriae. J. Immunol. 176: 7645-7656.
15. Harokopakis, E., and G. Hajishengallis. 2005. Integrin activation by bacterial fimbriae through a pathway involving CD14, Toll-like receptor 2, and phosphatidylinositol-3-kinase. Eur. J. Immunol. 35: 1201-1210.
16. Hajishengallis, G. 2007. Peptide mapping of a functionally versatile fimbrial adhesin from Porphyromonas gingivalis. Int. J. Pept. Res. Ther. In press.
17. Yoshimura, F., Y. Takahashi, E. Hibi, T. Takasawa, H. Kato, and D. P. Dickinson. 1993. Proteins with molecular masses of 50 and 80 kilodaltons encoded by genes downstream from the fimbrilin gene ( fimA) are components associated with fimbriae in the oral anaerobe Porphyromonas gingivalis. Infect. Immun. 61: 5181-5189.
18. Nishiyama, S.-I., Y. Murakami, H. Nagata, S. Shizukuishi, I. Kawagishi, and F. Yoshimura. 2007. Involvement of minor components associated with the FimA fimbriae of Porphyromonas gingivalis in adhesive functions. Microbiology 153: 1916-1925.
19. Watanabe, K., T. Onoe, M. Ozeki, Y. Shimizu, T. Sakayori, H. Nakamura, and F. Yoshimura. 1996. Sequence and product analyses of the four genes downstream from the fimbrilin gene ( fimA) of the oral anaerobe Porphyromonas gingivalis. Microbiol. Immunol. 40: 725-734.
20. Nishikawa, K., F. Yoshimura, and M. J. Duncan. 2004. A regulation cascade controls expression of Porphyromonas gingivalis fimbriae via the FimR response regulator. Mol. Microbiol. 54: 546-560.
21. Yoshimura, F., K. Takahashi, Y. Nodasaka, and T. Suzuki. 1984. Purification and characterization of a novel type of fimbriae from the oral anaerobe Bacteroides gingivalis. J. Bacteriol. 160: 949-957.
22. Hajishengallis, G., R. I. Tapping, M. H. Martin, H. Nawar, E. A. Lyle, M. W. Russell, and T. D. Connell. 2005. Toll-like receptor 2 mediates cellular activation by the B subunits of type II heat-labile enterotoxins. Infect. Immun. 73: 1343-1349.
23. Lamont, R. J., A. Chan, C. M. Belton, K. T. Izutsu, D. Vasel, and A. Weinberg. 1995. Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 63: 3878-3885.
24. Baker, P. J., M. Dixon, and D. C. Roopenian. 2000. Genetic control of susceptibility to Porphyromonas gingivalis-induced alveolar bone loss in mice. Infect. Immun. 68: 5864-5868.
25. Genco, C. A., T. Van Dyke, and S. Amar. 1998. Animal models for Porphyromonas gingivalis-mediated periodontal disease. Trends Microbiol. 6: 444-449.
26. Linton, M. F., and S. Fazio. 2003. Macrophages, inflammation, and atherosclerosis. Int. J. Obes. Relat. Metab. Disord. 27(Suppl. 3): S35-S40.
27. Teng, Y. T. 2006. Protective and destructive immunity in the periodontium. 1. Innate and humoral immunity and the periodontium. J. Dent. Res. 85: 198-208.
28. Socransky, S. S., A. D. Haffajee, M. A. Cugini, C. Smith, and R. L. Kent, Jr. 1998. Microbial complexes in subgingival plaque. J. Clin. Periodontol. 25: 134-144.
29. Mosser, D. M., and C. L. Karp. 1999. Receptor mediated subversion of macrophage cytokine production by intracellular pathogens. Curr. Opin. Immunol. 11: 406-411.
30. Lowell, C. A. 2006. Rewiring phagocytic signal transduction. Immunity 24: 243-245.
31. Vieira, O. V., R. J. Botelho, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366: 689-704.
32. Payne, N. R., and M. A. Horwitz. 1987. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J. Exp. Med. 166: 1377-1389.
33. Ehlers, M. R. W., and M. Daffe. 1998. Interactions between Mycobacterium tuberculosis and host cells: are mycobacterial sugars the key? Trends Microbiol. 6: 328-335.
34. Hellwig, S. M., H. F. van Oirschot, W. L. Hazenbos, A. B. van Spriel, F. R. Mooi, and J. G. van De Winkel. 2001. Targeting to Fcγ receptors, but not CR3 (CD11b/ CD18), increases clearance of Bordetella pertussis. J. Infect. Dis. 183: 871-879.
35. Romani, L., F. Bistoni, and P. Puccetti. 2002. Fungi, dendritic cells and receptors: a host perspective of fungal virulence. Trends Microbiol. 10: 508-514.
36. Wright, S. D., and S. C. Silverstein. 1983. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J. Exp. Med. 158: 2016-2023.
37. Berton, G., C. Laudanna, C. Sorio, and F. Rossi. 1992. Generation of signals activating neutrophil functions by leukocyte integrins: LFA-1 and gp150/95, but not CR3, are able to stimulate the respiratory burst of human neutrophils. J. Cell Biol. 116: 1007-1017.
38. Yamamoto, K., and R. B. Johnston, Jr. 1984. Dissociation of phagocytosis from stimulation of the oxidative metabolic burst in macrophages. J. Exp. Med. 159: 405-416.
39. Caron, E., and A. Hall. 1998. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282: 1717-1721.
40. Burns, E., G. Bachrach, L. Shapira, and G. Nussbaum. 2006. Cutting edge: TLR2 is required for the innate response to Porphyromonas gingivalis: activation leads to bacterial persistence and TLR2 deficiency attenuates induced alveolar bone resorption. J. Immunol. 177: 8296-8300.
41. Kaufmann, S. H. 1999. Cell-mediated immunity: dealing a direct blow to pathogens. Curr. Biol. 9: R97-R99.
42. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
43. Belanger, M., P. H. Rodrigues, W. A. Dunn, Jr., and A. Progulske-Fox. 2006. Autophagy: a highway for Porphyromonas gingivalis in endothelial cells. Autophagy 2: 165-170.
44. Montminy, S. W., N. Khan, S. McGrath, M. J. Walkowicz, F. Sharp, J. E. Conlon, K. Fukase, S. Kusumoto, C. Sweet, K. Miyake, et al. 2006. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7: 1066-1073.
45. Soto, G. E., and S. J. Hultgren. 1999. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol. 181: 1059-1071.
46. Finlay, B. B., and G. McFadden. 2006. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124: 767-782.