Porphyromonas gingivalis-mediated shedding of extracellular matrix metalloproteinase inducer (EMMPRIN) by oral epithelial cells: A potential role in inflammatory periodontal disease

Microbes and Infection

Volumn 13, Issue 14-15, 2011, Pages 1261-1269

  Feldman, Mark ^a   La, Vu Dang ^a   Lombardo Bedran, Telma Blanca ^b   Palomari Spolidorio, Denise Madalena ^b   Grenier, Daniel ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Cytokine; EMMPRIN; Epithelial cell; Fibroblast; Periodontitis; Porphyromonas gingivalis

Indexed keywords

CD147 ANTIGEN; CYSTEINE PROTEINASE; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; STROMELYSIN;

ANTIGEN EXPRESSION; ARTICLE; BACTERIAL SHEDDING; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME RELEASE; EPITHELIUM CELL; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; NONHUMAN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

ADHESINS, BACTERIAL; ANTIGENS, CD147; BACTEROIDACEAE INFECTIONS; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FIBROBLASTS; GENE DELETION; GINGIVA; HUMANS; INTERLEUKIN-6; MATRIX METALLOPROTEINASE 3; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS;

PORPHYROMONAS GINGIVALIS;

EID: 81155133857     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2011.07.009     Document Type: Article

References (46)

1. Ebersole J.L., Taubman M.A. The protective nature of host responses in periodontal diseases. Periodontol. 2000 1994, 5:112-141.
2. Darveau R.P. The oral microbial consortium's interaction with the periodontal innate defense system. DNA Cell Biol. 2009, 28:389-395.
3. Kornman K.S., Page R.C., Tonetti M.S. The host response to the microbial challenge in periodontitis: assembling the players. Periodontol. 2000 1997, 14:33-53.
4. Slots J., Bragd L., Wikstrom M., Dahlen G. The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults. J. Clin. Periodontol. 1986, 13:570-577.
5. Curtis M.A., Aduse-Opoku J., Rangarajan M. Cysteine proteases of Porphyromonas gingivalis. Crit. Rev. Oral Biol. Med. 2001, 12:192-216.
6. Dixon D.R., Darveau R.P. Lipopolysaccharide heterogeneity: innate host responses to bacterial modification of lipid a structure. J. Dent. Res. 2005, 84:584-595.
7. Hajishengallis G., Sojar H., Genco R.J., DeNardin E. Intracellular signaling and cytokine induction upon interactions of Porphyromonas gingivalis fimbriae with pattern-recognition receptors. Immunol. Invest. 2004, 33:157-172.
8. Andrian E., Rouabhia M. In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect. Immun. 2004, 72:4689-4698.
9. Andrian E., Grenier D., Rouabhia M. Porphyromonas gingivalis gingipains mediate the shedding of syndecan-1 from the surface of gingival epithelial cells. Oral Microbiol. Immunol. 2006, 21:123-128.
10. Mahtout H., Chandad F., Rojo J.M., Grenier D. Porphyromonas gingivalis mediates the shedding and proteolysis of complement regulatory protein CD46 expressed by oral epithelial cells. Oral Microbiol. Immunol. 2009, 24:396-400.
11. Kinane D.F., Lappin D.F. Clinical, pathological and immunological aspects of periodontal disease. Acta Odontol. Scand. 2001, 59:154-160.
12. Madianos P.N., Bobetsis Y.A., Kinane D.F. Generation of inflammatory stimuli: how bacteria set up inflammatory responses in the gingiva. J. Clin. Periodontol. 2005, 32(Suppl. 6):57-71.
13. Ejeil A.L., Igondjo-Tchen S., Ghomrasseni S., Pellat B., Godeau G., Gogly B. Expression of matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs) in healthy and diseased human gingiva. J. Periodontol. 2003, 74:188-195.
14. Sorsa T., Tjaderhane L., Konttinen Y.T., Lauhio A., Salo T., Lee H.M., Golub L.M., Brown D.L., Mantyla P. Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Ann. Med. 2006, 38:306-321.
15. Page-McCaw A., Ewald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8:221-233.
16. Biswas C., Zhang Y., DeCastro R., Guo H., Nakamura T., Kataoka H., Nabeshima K. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res. 1995, 55:434-439.
17. Kanekura T., Chen X., Kanzaki T. Basigin (CD147) is expressed on melanoma cells and induces tumor cell invasion by stimulating production of matrix metalloproteinases by fibroblasts. Int. J. Cancer 2002, 99:520-528.
18. Zucker S., Hymowitz M., Rollo E.E., Mann R., Conner C.E., Cao J., Foda H.D., Tompkins D.C., Toole B.P. Tumorigenic potential of extracellular matrix metalloproteinase inducer. Am. J. Pathol. 2001, 158:1921-1928.
19. Gabison E.E., Hoang-Xuan T., Mauviel A., Menashi S. EMMPRIN/CD147, an MMP modulator in cancer, development and tissue repair. Biochimie 2005, 87:361-368.
20. Huet E., Gabison E.E., Mourah S., Menashi S. Role of emmprin/CD147 in tissue remodeling. Connect. Tissue Res. 2008, 49:175-179.
21. Emingil G., Tervahartiala T., Mantyla P., Maatta M., Sorsa T., Atilla G. Gingival crevicular fluid matrix metalloproteinase (MMP)-7, extracellular MMP inducer, and tissue inhibitor of MMP-1 levels in periodontal disease. J. Periodontol. 2006, 77:2040-2050.
22. Dong W., Xiang J., Li C., Cao Z., Huang Z. Increased expression of extracellular matrix metalloproteinase inducer is associated with matrix metalloproteinase-1 and -2 in gingival tissues from patients with periodontitis. J. Periodontal Res. 2009, 44:125-132.
23. Xiang J., Cao Z., Dong W., Li C. Expression of extracellular matrix metalloproteinase inducer (EMMPRIN) in healthy and inflamed human gingival. Quintessence Int. 2009, 40:683-690.
24. Emingil G., Atilla G., Sorsa T., Tervahartiala T. The effect of adjunctive subantimicrobial dose doxycycline therapy on GCF EMMPRIN levels in chronic periodontitis. J. Periodontol. 2008, 79:469-476.
25. Liu L., Li C., Cai X., Xiang J., Cao Z., Dong W. The temporal expression and localization of extracellular matrix metalloproteinase inducer (EMMPRIN) during the development of periodontitis in an animal model. J. Periodontal Res. 2010, 45:541-549.
26. Nakayama K., Kadowaki T., Okamoto K., Yamamoto K. Construction and characterization of arginine-specific cysteine proteinase (Arg-gingipain)-deficient mutants of Porphyromonas gingivalis. Evidence for significant contribution of Arg-gingipain to virulence. J. Biol. Chem. 1995, 270:23619-23626.
27. Shi Y., Ratnayake D.B., Okamoto K., Abe N., Yamamoto K., Nakayama K. Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis. Construction of mutants with a combination of rgpA, rgpB, kgp, and hagA. J. Biol. Chem. 1999, 274:17955-17960.
28. Gilchrist E.P., Moyer M.P., Shillitoe E.J., Clare N., Murrah V.A. Establishment of a human polyclonal oral epithelial cell line. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2000, 90:340-347.
29. Sato T., Ota T., Watanabe M., Imada K., Nomizu M., Ito A. Identification of an active site of EMMPRIN for the augmentation of matrix metalloproteinase-1 and -3 expression in a co-culture of human uterine cervical carcinoma cells and fibroblasts. Gynecol. Oncol. 2009, 114:337-342.
30. Vaahtoniemi L.H., Raisanen S., Stenfors L.E. Attachment of bacteria to oral epithelial cells in vivo: a possible correlation to gingival health status. J. Periodontal Res. 1993, 28:308-311.
31. Arribas J., Borroto A. Protein ectodomain shedding. Chem. Rev. 2002, 102:4627-4638.
32. Hanata K., Yamaguchi N., Yoshikawa K., Mezaki Y., Miura M., Suzuki S., Senoo H., Ishikawa K. Soluble EMMPRIN (extra-cellular matrix metalloproteinase inducer) stimulates the migration of HEp-2 human laryngeal carcinoma cells, accompanied by increased MMP-2 production in fibroblasts. Arch. Histol. Cytol. 2007, 70:267-277.
33. Sidhu S.S., Mengistab A.T., Tauscher A.N., LaVail J., Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 2004, 23:956-963.
34. Imamura T., Travis J., Potempa J. The biphasic virulence activities of gingipains: activation and inactivation of host proteins. Curr. Protein Pept. Sci. 2003, 4:443-450.
35. Amano A., Nakamura T., Kimura S., Morisaki I., Nakagawa I., Kawabata S., Hamada S. Molecular interactions of Porphyromonas gingivalis fimbriae with host proteins: kinetic analyses based on surface plasmon resonance. Infect. Immun. 1999, 67:2399-2405.
36. Rapala-Kozik M., Bras G., Chruscicka B., Karkowska-Kuleta J., Sroka A., Herwald H., Nguyen K.A., Eick S., Potempa J., Kozik A. Adsorption of components of the plasma kinin-forming system on the surface of Porphyromonas gingivalis involves gingipains as the major docking platforms. Infect. Immun. 2011, 79:797-805.
37. Andrian E., Mostefaoui Y., Rouabhia M., Grenier D. Regulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases by Porphyromonas gingivalis in an engineered human oral mucosa model. J. Cell. Physiol. 2007, 211:56-62.
38. Hassell T.M. Tissues and cells of the periodontium. Periodontol. 2000 1993, 3:9-38.
39. Takashiba S., Naruishi K., Murayama Y. Perspective of cytokine regulation for periodontal treatment: fibroblast biology. J. Periodontol. 2003, 74:103-110.
40. Dean N.R., Knowles J.A., Helman E.E., Aldridge J.C., Carroll W.R., Magnuson J.S., Clemons L., Ziober B., Rosenthal E.L. Anti-EMMPRIN monoclonal antibody as a novel agent for therapy of head and neck cancer. Clin. Cancer Res. 2009, 15:4058-4065.
41. Irwin C.R., Myrillas T.T. The role of IL-6 in the pathogenesis of periodontal disease. Oral Dis. 1998, 4:43-47.
42. Takahashi K., Takashiba S., Nagai A., Takigawa M., Myoukai F., Kurihara H., Murayama Y. Assessment of interleukin-6 in the pathogenesis of periodontal disease. J. Periodontol. 1994, 65:147-153.
43. Ishimi Y., Miyaura C., Jin C.H., Akatsu T., Abe E., Nakamura Y., Yamaguchi A., Yoshiki S., Matsuda T., Hirano T. IL-6 is produced by osteoblasts and induces bone resorption. J. Immunol. 1990, 145:3297-3303.
44. Kim Do Y., Jun J.H., Lee H.L., Woo K.M., Ryoo H.M., Kim G.S., Baek J.H., Han S.B. N-acetylcysteine prevents LPS-induced pro-inflammatory cytokines and MMP2 production in gingival fibroblasts. Arch. Pharm. Res. 2007, 30:1283-1292.
45. Alpagot T., Bell C., Lundergan W., Chambers D.W., Rudin R. Longitudinal evaluation of GCF MMP-3 and TIMP-1 levels as prognostic factors for progression of periodontitis. J. Clin. Periodontol. 2001, 28:353-359.
46. Birkedal-Hansen H., Moore W.G., Bodden M.K., Windsor L.J., Birkedal-Hansen B., DeCarlo A. Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med. 1993, 4:197-250.