Fibroblast apoptosis induced by Porphyromonas gingivalis is stimulated by a gingipain and caspase-independent pathway that involves apoptosis-inducing factor

Cellular Microbiology

Volumn 9, Issue 11, 2007, Pages 2667-2675

  Desta, Tesfahun ^a   Graves, Dana T ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CASPASE 3; CASPASE INHIBITOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; GINGIPAIN R; MESSENGER RNA; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CELL DEATH; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; ENZYME ACTIVITY; FIBROBLAST; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MOUTH FLORA; PATHOGENESIS; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; TOOTH INFECTION;

ADHESINS, BACTERIAL; AMINO ACID CHLOROMETHYL KETONES; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASE 2; CASPASE 3; CASPASES; CYSTEINE ENDOPEPTIDASES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; IN SITU NICK-END LABELING; ISOQUINOLINES; PORPHYROMONAS GINGIVALIS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SULFONAMIDES; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS;

EID: 34848876415     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00987.x     Document Type: Article

References (39)

1. Alikhani, M., Alikhani, Z., and Graves, D. (2005) FOXO1 functions as a master switch that regulates gene expression necessary for TNF-induced fibroblast apoptosis. J Biol Chem 280: 12096-12102.
2. Andrian, E., Grenier, D., and Rouabhia, M. (2004) In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect Immun 72: 4689-4698.
3. Basak, C., Pathak, S.K., Bhattacharyya, A., Pathak, S., Basu, J., and Kundu, M. (2005) The secreted peptidyl prolyl cis,trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4- and apoptosis signal-regulating kinase 1-dependent manner. J Immunol 174: 5672-5680.
4. Braun, J.S., Novak, R., Murray, P.J., Eischen, C.M., Susin, S.A., Kroemer, G., et al. (2001) Apoptosis-inducing factor mediates microglial and neuronal apoptosis caused by pneumococcus. J Infect Dis 184: 1300-1309.
5. Brozovic, S., Sahoo, R., Barve, S., Shiba, H., Uriarte, S., Blumberg, R.S., and Kinane, D.F. (2006) Porphyromonas gingivalis enhances FasL expression via upregulation of NFkappaB-mediated gene transcription and induces apoptotic cell death in human gingival epithelial cells. Microbiology 152: 797-806.
6. Cande, C., Cecconi, F., Dessen, P., and Kroemer, G. (2002) Apoptosis-inducing factor (AIF): Key to the conserved caspase-independent pathways of cell death? J Cell Sci 115: 4727-4734.
7. Chen, Z., Casiano, C.A., and Fletcher, H.M. (2001) Protease-active extracellular protein preparations from Porphyromonas gingivalis W83 induce N-cadherin proteolysis, loss of cell adhesion, and apoptosis in human epithelial cells. J Periodontol 72: 641-650.
8. Chijiwa, T., Mishima, A., Hagiwara, M., Sano, M., Hayashi, K., Inoue, T., et al. (1990) Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J Biol Chem 265: 5267-5272.
9. Graves, D.T., Jiang, Y., and Genco, C. (2000) Bacterial virulence factors host response and impact on systemic health. Curr Op Inf Dis 13: 227-232.
10. Graves, D., Oskoui, M., Volejnikova, S., Naguib, G., Cai, S., Desta, T., et al. (2001) Tumor necrosis factor modulates fibroblast apoptosis, PMN recruitment, and osteoclast formation in response to P. gingivalis infection. J Dent Res 80: 1875-1879.
11. Graves, D., Liu, R., Alikhani, M., Al-Mashat, H., and Trackman, P. (2006) Diabetes-enhanced inflammation and apoptosis - impact on periodontal pathology. J Dent Res 85f: 15-21.
12. Green, D. (2000) Apoptotic pathways: Paper wraps stone blunts scissors. Cell 102: 1-4.
13. Harris, J.I., Russell, R.R., Curtis, M.A., Aduse-Opoku, J., and Taylor, J.J. (2002) Molecular mediators of Porphyromonas gingivalis-induced T-cell apoptosis. Oral Microbiol Immunol 17: 224-230.
14. Houle, M.A., Grenier, D., Plamondon, P., and Nakayama, K. (2003) The collagenase activity of Porphyromonas gingivalis is due to Arg-gingipain. FEMS Microbiol Lett 221: 181-185.
15. Imamura, T., Travis, J., and Potempa, J. (2003) The biphasic virulence activities of gingipains: Activation and inactivation of host proteins. Curr Protein Pept Sci 4: 443-450.
16. Johansson, A., and Kalfas, S. (1998) Characterization of the proteinase-dependent cytotoxicity of Porphyromonas gigivalis. European J Oral Sci 106: 863-871.
17. Koulouri, O., Lapping, D., Radvar, M., and Kinane, D. (1999) Cell division, synthetic capacity and apoptosis in periodontal lesions analyzed by in situ hybridization an immunohistochemistry. J Clin Periodotology 26: 552-559.
18. Kurita-Ochiai, T., Ochiai, K., and Fukushima, K. (1998) Volatile fatty acid, metabolic by-product of periodontopathic bacteria, induces apoptosis in WEHI 231 and RAJI B lymphoma cells and splenic B cells. Infect Immun 66: 2587-2594.
19. Lamont, R., and Jenkinson, H. (1998) Life below the gum line: Pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 62: 1244-1263.
20. Lipton, S.A., and Bossy-Wetzel, E. (2002) Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111: 147-150.
21. Liu, R., Desta, T., He, H., and Graves, D. (2004) Diabetes alters the response to bacteria by enhancing fibroblast apoptosis. Endocrinology 145: 2997-3003.
22. Liu, R., Bal, H.S., Desta, T., Behl, Y., and Graves, D.T. (2006) Tumor necrosis factor-alpha mediates diabetes-enhanced apoptosis of matrix-producing cells and impairs diabetic healing. Am J Pathol 168: 757-764.
23. Morioka, M., Hinode, D., Nagata, A., Hayashi, H., Ichimiya, S., Ueda, M., et al. (1993) Cytotoxicity of Porphyromonas gingivalis toward cultured human gingival fibroblasts. Oral Microbiol Immunol 8: 203-207.
24. Muniz, M., Alonso, M., Hidalgo, J., and Velasco, A. (1996) A regulatory role for cAMP-dependent protein kinase in protein traffic along the exocytic route. J Biol Chem 271: 30935-30941.
25. Muniz, M., Martin, M.E., Hidalgo, J., and Velasco, A. (1997) Protein kinase A activity is required for the budding of constitutive transport vesicles from the trans-Golgi network. Proc Natl Acad Sci USA 94: 14461-14466.
26. Nakhjiri, S.F., Park, Y., Yilmaz, O., Chung, W.O., Watanabe, K., El-Sabaeny, A., et al. (2001) Inhibition of epithelial cell apoptosis by Porphyromonas gingivalis. FEMS Microbiol Lett 200: 145-149.
27. O'Brien-Simpson, N.M., Pathirana, R.D., Paolini, R.A., Chen, Y.Y., Veith, P.D., Tam, V., et al. (2005) An immune response directed to proteinase and adhesin functional epitopes protects against Porphyromonas gingivalis-induced periodontal bone loss. J Immunol 175: 3980-3989.
28. Park, S.Y., Cho, S.J., Kwon, H.C., Lee, K.R., Rhee, D.K., and Pyo, S. (2005) Caspase-independent cell death by allicin in human epithelial carcinoma cells: Involvement of PKA. Cancer Lett 224: 123-132.
29. Rangarajan, M., Smith, S.J., U, S., and Curtis, M.A. (1997) Biochemical characterization of the arginine-specific proteases of Porphyromonas gingivalis W50 suggests a common precursor. Biochem J 323: 701-709.
30. Sheets, S.M., Potempa, J., Travis, J., Casiano, C.A., and Fletcher, H.M. (2005) Gingipains from Porphyromonas gingivalis W83 induce cell adhesion molecule cleavage and apoptosis in endothelial cells. Infect Immun 73: 1543-1552.
31. Sordet, O., Khan, Q.A., and Pommier, Y. (2004) Apoptotic topoisomerase I-DNA complexes induced by oxygen radicals and mitochondrial dysfunction. Cell Cycle 3: 1095-1097.
32. Susin, S.A., Daugas, E., Ravagnan, L., Samejima, K., Zamzami, N., Loeffler, M., et al. (2000) Two distinct pathways leading to nuclear apoptosis. J Exp Med 192: 571-580.
33. Takii, R., Kadowaki, T., Baba, A., Tsukuba, T., and Yamamoto, K. (2005) A functional virulence complex composed of gingipains, adhesins, and lipopolysaccharide shows high affinity to host cells and matrix proteins and escapes recognition by host immune systems. Infect Immun 73: 883-893.
34. Thomas, L.R., Henson, A., Reed, J.C., Salsbury, F.R., and Thorburn, A. (2004) Direct binding of Fas-associated death domain (FADD) to the tumor necrosis factor-related apoptosis-inducing ligand receptor DR5 is regulated by the death effector domain of FADD. J Biol Chem 279: 32780-32785.
35. Thorburn, A. (2004) Death receptor-induced cell killing. Cell Signal 16: 139-144.
36. Tonetti, M., Cortellini, D., and Lang, N. (1998) In situ detection of apoptosis at sites of chronic bacterially induced inflammation in human gingival. Infection Immunity 66: 5190-5195.
37. Urnowey, S., Ansai, T., Bitko, V., Nakayama, K., Takehara, T., and Barik, S. (2006) Temporal activation of anti- and pro-apoptotic factors in human gingival fibroblasts infected with the periodontal pathogen, Porphyromonas gingivalis: Potential role of bacterial proteases in host signalling. BMC Microbiol 6: 26.
38. Wang, P., Shirasu, S., Shinohara, M., Daito, M., Oido, M., Kowashi, Y., and Ohura, K. (1999) Induction of apoptosis in human gingival fibroblasts by a Porphyromonas gingivalis protease preparation. Arch Oral Biol 44: 337-342.
39. Zappa, U., Reinking-Zappa, M., Graf, H., and Chase, D. (1992) Cell populations associated with active probing attachment loss. J Periodontology 63: 748-752.