Porphyromonas gingivalis infection sequesters pro-apoptotic Bad through Akt in primary gingival epithelial cells

Molecular Oral Microbiology

Volumn 25, Issue 2, 2010, Pages 89-101

  Yao, L ^a   Jermanus, C ^a   Barbetta, B ^a   Choi, C ^a   Verbeke, P ^b   Ojcius, D M ^c   Yilmaz, O ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b INSTITUT JACQUES MONOD   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Cell survival; Mitochondria; Persistence; Porphyromonas

Indexed keywords

CASPASE 9; CYTOCHROME C; MESSENGER RNA; PHOSPHATIDYLINOSITOL KINASE; PROTEIN BAD; PROTEIN KINASE B; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; BACTERIAL INFECTION; BACTERIUM CULTURE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; GINGIVA; IMMUNOPRECIPITATION; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PHOSPHORYLATION; PORPHYROMONAS GINGIVALIS; PROTEIN DEPLETION; PROTEIN SECRETION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

APOPTOSIS; BACTEROIDACEAE INFECTIONS; BCL-ASSOCIATED DEATH PROTEIN; CASPASE 9; CELL SURVIVAL; CELLS, CULTURED; EPITHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; GINGIVA; HOST-PATHOGEN INTERACTIONS; HUMANS; MITOCHONDRIA; PHOSPHORYLATION; PORPHYROMONAS GINGIVALIS; PROTEASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STAUROSPORINE;

EID: 77949376775     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2010.00569.x     Document Type: Article

References (35)

1. Belton, C.M., Izutsu, K.T., Goodwin, P.G., Park, Y. and Lamont, R.J. (1999) Fluorescence image analysis of the association between Porphyromonas gingivalis and gingival epithelial cells. Cell Microbiol 1: 215-223.
2. Byrne, G.I. and Ojcius, D.M. (2004) Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat Rev Microbiol 2: 802-808.
3. Chao, D.T. and Korsmeyer, S.J. (1998) BCL-2 family: regulators of cell death. Annu Rev Immunol 16: 395-419.
4. Chen, Y.L., Law, P.Y. and Loh, H.H. (2005) Inhibition of PI3K/Akt signaling: an emerging paradigm for targeted cancer therapy. Curr Med Chem Anticancer Agents 5: 575-589.
5. Collins, M. (1995) Potential roles of apoptosis in viral pathogenesis. Am J Respir Crit Care Med 152: S20-S24.
6. Colombo, A.V., da Silva, C.M., Haffajee, A. and Colombo, A.P. (2007) Identification of intracellular oral species within human crevicular epithelial cells from subjects with chronic periodontitis by fluorescence in situ hybridization. J Periodontal Res 42: 236-243.
7. Cosulich, S.C., Savory, P.J. and Clarke, P.R. (1999) Bcl-2 regulates amplification of caspase activation by cytochrome c. Curr Biol 9: 147-150.
8. Danelishvili, L., McGarvey, J., Li, Y.J. and Bermudez, L.E. (2003) Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell Microbiol 5: 649-660.
9. Datta, S.R., Dukek, H., Tao, X. et al. (1997) Akt phosphorylation of Bad couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241.
10. Datta, S.R., Brunet, A. and Greenberg, M.E. (1999) Cellular survival: a play in three Akts. Genes Dev 13: 2905-2927.
11. Finlay, B.B. and Falkow, S. (1989) Common themes in microbial pathogenecity. Microbiol Rev 53: 210-230.
12. Hacker, G., Kirschnek, S. and Fischer, S.F. (2006) Apoptosis in infectious disease: how bacteria interfere with the apoptotic apparatus. Med Microbiol Immunol (Berlin) 195: 11-19.
13. Jenkinson, H.F. and Lamont, R.J. (2005) Oral microbial communities in sickness and in health. Trends Microbiol 13: 589-595.
14. Kennedy, S.G., Wagner, A.J., Conzen, S.D. et al. (1997) The PI 3-kinase/Akt signaling pathway delivers an antiapoptotic signal. Genes Dev 11: 701-713.
15. Knodler, L.A. and Finlay, B.B. (2001) Salmonella and apoptosis: to live or let die? Microbes Infect 3: 1321-1326.
16. Kuboniwa, M., Hasegawa, Y., Mao, S. et al. (2008) P. gingivalis accelerates gingival epithelial cell progression through the cell cycle. Microbes Infect 10: 122-128.
17. Lamont, R.J. and Yilmaz, O. (2002) In or out: the invasiveness of oral bacteria. Periodontol 2000 30: 61-69.
18. Lamont, R.J., Chan, A., Belton, C.M., Izutsu, K.T., Vasel, D.J. and Weinberg, A. (1995) Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 63: 3878-3885.
19. Mao, S., Park, Y., Hasegawa, Y. et al. (2007) Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Microbiol 9: 1997-2007.
20. Monack, D.M., Raupach, B., Hromockyj, A.E. and Falkow, S. (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838.
21. Nakhjiri, S.F., Park, Y., Yilmaz, O. et al. (2001) Inhibition of epithelial cell apoptosis by Porphyromonas gingivalis. FEMS Microbiol Lett 200: 145-149.
22. Nicholson, D.W. and Thornberry, N.A. (1997) Caspases: killer proteases. Trends Biochem Sci 22: 299-306.
23. Rudney, J.D., Chen, R. and Sedgewick, G.J. (2005) Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are components of a polymicrobial intracellular flora within human buccal cells. J Dent Res 84: 59-63.
24. Seo, Y.S., Chen, Y.-b., Ivanovska, I. et al. (2004) BAD is a pro-survival factor prior to activation of its pro-apoptotic function. J Biol Chem 279: 42240-42249.
25. 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.
26. Thornberry, N.A. and Lazebnik, Y. (1998) Caspases: enemies within. Science 281: 1312-1316.
27. Verbeke, P., Welter-Stahl, L., Ying, S. et al. (2006) Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog 2: e45.
28. Xia, Q., Wang, T., Taub, F. et al. (2007) Quantitative proteomics of intracellular Porphyromonas gingivalis. Proteomics 7: 4323-4337.
29. Yilmaz, O. (2008) The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay. Microbiology 154: 2897-2903.
30. Yilmaz, O., Jungas, T., Verbeke, P. and Ojcius, D.M. (2004) Activation of the phosphatidylinositol 3-kinase/ Akt pathway contributes to survival of primary epithelial cells infected with the periodontal pathogen Porphyromonas gingivalis. Infect Immun 72: 3743-3751.
31. Yilmaz, O., Verbeke, P., Lamont, R.J. and Ojcius, D.M. (2006) Intercellular spreading of Porphyromonas gingivalis infection in primary gingival epithelial cells. Infect Immun 74: 703-710.
32. Yilmaz, O., Yao, L., Maeda, K. et al. (2008) ATP scavenging by the intracellular pathogen Porphyromonas gingivalis inhibits P2X(7)-mediated host-cell apoptosis. Cell Microbiol 10: 863-875.
33. Yin, J.L., Shackel, N.A., Zekry, A. et al. (2001) Real-time reverse transcriptase-polymerase chain reaction (RT-PCR) for measurement of cytokine and growth factor mRNA expression with fluorogenic probes or SYBR Green I. Immunol Cell Biol 79: 213-221.
34. Zhang, H.M., Rao, J.N., Guo, X. et al. (2004) Akt kinase activation blocks apoptosis in intestinal epithelial cells by inhibiting caspase-3 after polyamine depletion. J Biol Chem 279: 22539-22547.
35. Zychlinsky, A., Prevost, M.C. and Sansonetti, P.J. (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169.