Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis

Cellular Microbiology

Volumn 9, Issue 8, 2007, Pages 1997-2007

  Mao, Song ^a   Park, Yoonsuk ^a   Hasegawa, Yoshiaki ^a   Tribble, Gena D ^a   James, Chlöe E ^a,b   Handfield, Martin ^a   Stavropoulos, M Franci ^a   Yilmaz, Özlem ^a   Lamont, Richard J ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; JANUS KINASE;

APOPTOSIS; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL CULTURE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; EPITHELIUM CELL; FIMBRIA; GENE EXPRESSION; GENETIC CONSERVATION; GINGIVA; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

APOPTOSIS; BACTEROIDACEAE INFECTIONS; CASPASE 3; CELLS, CULTURED; ENZYME ACTIVATION; EPITHELIAL CELLS; GINGIVA; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; JANUS KINASE 1; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NEOPLASM PROTEINS; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

PORPHYROMONAS GINGIVALIS;

EID: 34447646305     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00931.x     Document Type: Article

References (68)

1. Aaronson, D.S., and Horvath, C.M. (2002) A road map for those who don't know JAK-STAT. Science 296: 1653-1655.
2. Albandar, J.M. (2005) Epidemiology and risk factors of periodontal diseases. Dent Clin North Am 49: 517-532.
3. Amiri, K.I., and Richmond, A. (2005) Role of nuclear factor-kappa B in melanoma. Cancer Metastasis Rev 24: 301-313.
4. Belton, C.M., Izutsu, K.T., Goodwin, P.C., 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.
5. Beyaert, R., Van Loo, G., Heyninck, K., and Vandenabeele, P. (2002) Signaling to gene activation and cell death by tumor necrosis factor receptors and Fas. Int Rev Cytol 214: 225-272.
6. Binnicker, M.J., Williams, R.D., and Apicella, M.A. (2003) Infection of human urethral epithelium with Neisseria gonorrhoeae elicits an upregulation of host anti-apoptotic factors and protects cells from staurosporine-induced apoptosis. Cell Microbiol 5: 549-560.
7. Brozovic, S., Sahoo, R., Barve, S., Shiba, H., Uriarte, S., Blumberg, R.S., and Kinane, D.F. (2006) Porphyromonas gingivalis enhances FasL expression via up-regulation of NFkappaB-mediated gene transcription and induces apoptotic cell death in human gingival epithelial cells. Microbiology 152: 797-806.
8. 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.
9. Calo, V., Migliavacca, M., Bazan, V., Macaluso, M., Buscemi, M., Gebbia, N., and Russo, A. (2003) STAT proteins: From normal control of cellular events to tumorigenesis. J Cell Physiol 197: 157-168.
10. Dauer, D.J., Ferraro, B., Song, L., Yu, B. Mora, L., Buettner, R., et al. (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24: 3397-3408.
11. Earnshaw, W.C., Martins, L.M., and Kaufmann, S.H. (1999) Mammalian caspases: Structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383-424.
12. Fadeel, B., and Orrenius, S. (2005) Apoptosis: A basic biological phenomenon with wide-ranging implications in human disease. J Intern Med 258: 479-517.
13. Feng, Z., and Weinberg, A. (2006) Role of bacteria in health and disease of periodontal tissues. Periodontol 2000 40: 50-76.
14. Gao, L.Y., and Kwaik, Y.A. (2000) The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol 8: 306-313.
15. Gemmell, E., Prajaneh, S., Grieco, D.A., Taylor, J.J., and Seymour, G.J. (1999) Apoptosis in Porphyromonas gingivalis-specific T-cell lines. Oral Microbiol Immunol 14: 331-338.
16. Graves, D.T., 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.
17. Hacker, G., Kirschnek, S., and Fischer, S.F. (2006) Apoptosis in infectious disease: How bacteria interfere with the apoptotic apparatus. Med Microbiol Immunol 195: 11-19.
18. Haffajee, A.D., Cugini, M.A., Tanner, A., Pollack, R.P., Smith, C., Kent, R.L., Jr and Socransky, S.S. (1998) Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 25: 346-353.
19. Hail, N., Jr, Carter, B.Z., Konopleva, M., and Andreeff, M. (2006) Apoptosis effector mechanisms: A requiem performed in different keys. Apoptosis 11: 889-904.
20. Handfield, M., Mans, J.J., Zheng, G., Lopez, M.C., Mao, S., Progulske-Fox, A., et al. (2005) Distinct transcriptional profiles characterize oral epithelium-microbiota interactions. Cell Microbiol 7: 811-823.
21. 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.
22. Hiroi, M., Shimojima, T., Kashimata, M., Miyata, T., Takano, H., Takahama, M., and Sakagami, H. (1998) Inhibition by Porphyromonas gingivalis LPS of apoptosis induction in human peripheral blood polymorphonuclear leukocytes. Anticancer Res 18: 3475-3479.
23. Holt, S.C., and Ebersole, J.L. (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: The 'red complex', a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38: 72-122.
24. Hosogi, Y., and Duncan, M.J. (2005) Gene expression in Porphyromonas gingivalis after contact with human epithelial cells. Infect Immun 73: 2327-2335.
25. Hsieh, F.C., Cheng, G., and Lin, J. (2005) Evaluation of potential Stat3-regulated genes in human breast cancer. Biochem Biophys Res Commun 335: 292-299.
26. Inaba, H., Kawai, S., Kato, T., Nakagawa, I., and Amano, A. (2006) Association between epithelial cell death and invasion by microspheres conjugated to Porphyromonas gingivalis vesicles with different types of fimbriae. Infect Immun 74: 734-739.
27. Isogai, E., Isogal, H., Kimura, K., Fujii, N., Takagi, S., Hirose, K., and Hayashi, M. (1996) In vivo induction of apoptosis and immune responses in mice by administration of lipopolysaccharide from Porphyromonas gingivalis. Infect Immun 64: 1461-1466.
28. Janes, K.A., Albeck, J.G., Gaudet, S., Sorger, P.K., Lauffenburger, D.A., and Yaffe, M.B. (2005) A systems model of signaling identifies a molecular basis set for cytokine-induced apoptosis. Science 310: 1646-1653.
29. Johnson, M.E., and Howerth, E.W. (2004) Survivin: A bifunctional inhibitor of apoptosis protein. Vet Pathol 41: 599-607.
30. Johnson, N.C., Dan, H.C., Cheng, J.Q., and Kruk, P.A. (2004) BRCA1 185delAG mutation inhibits Akt-dependent, IAP-mediated caspase 3 inactivation in human ovarian surface epithelial cells. Exp Cell Res 298: 9-16.
31. Katz, J., Ward, D.C., and Michalek, S.M. (1996) Effect of host responses on the pathogenicity of strains of Porphyromonas gingivalis. Oral Microbiol Immunol 11: 309-318.
32. Khwaja, A. (2006) The role of Janus kinases in haemopoiesis and haematological malignancy. Br J Haematol 134: 366-384.
33. Knodler, L.A., Finlay, B.B., and Steele-Mortimer, O. (2005) The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 280: 9058-9064.
34. Lamont, R.J., and Jenkinson, H.F. (1998) Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 62: 1244-1263.
35. Lamont, R.J., Chan, A., Belton, C.M., Izutsu, K.T., Vasel, D., and Weinberg, A. (1995) Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 63: 3878-3885.
36. Liu, A.M., Lo, R.K., Wong, C.S., Morris, C., Wise, H., and Wong, Y.H. (2006) Activation of STAT3 by G alpha(s) distinctively requires protein kinase A, JNK, and phosphatidylinositol 3-kinase. J Biol Chem 281: 35812-35825.
37. Madianos, P.N., Papapanou, P.N., Nannmark, U., Dahlen, G., and Sandros, J. (1996) Porphyromonas gingivalis FDC381 multiplies and persists within human oral epithelial cells in vitro. Infect Immun 64: 660-664.
38. Marsh, P.D. (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149: 279-294.
39. Murray, D.A., and Wilton, J.M. (2003) Lipopolysaccharide from the periodontal pathogen Porphyromonas gingivalis prevents apoptosis of HL60-derived neutrophils in vitro. Infect Immun 71: 7232-7235.
40. 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.
41. Narimatsu, M., Maeda, H., Itoh, S., Atsumi, T., Ohtani, T., Nishida, K., et al. (2001) Tissue-specific autoregulation of the stat3 gene and its role in interleukin-6-induced survival signals in T cells. Mol Cell Biol 21: 6615-6625.
42. Noiri, Y., Ozaki, K., Nakae, H., Matsuo, T., and Ebisu, S. (1997) An immunohistochemical study on the localization of Porphyromonas gingivalis, Campylobacter rectus and Actinomyces viscosus in human periodontal pockets. J Periodontal Res 32: 598-607.
43. Noiri, Y., Li, L., Yoshimura, F., and Ebisu, S. (2004) Localization of Porphyromonas gingivalis-carrying fimbriae in situ in human periodontal pockets. J Dent Res 83: 941-945.
44. Oda, D., and Watson, E. (1990) Human oral epithelial cell culture I. Improved conditions for reproducible culture in serum-free medium. In Vitro Cell Dev Biol 26: 589-595.
45. O'Shea, J.J., Kanno, Y., Chen, X., and Levy, D.E. (2005) Cell signaling. Stat acetylation - a key facet of cytokine signaling? Science 307: 217-218.
46. Ozaki, K., and Hanazawa, S. (2001) Porphyromonas gingivalis fimbriae inhibit caspase-3-mediated apoptosis of monocytic THP-1 cells under growth factor deprivation via extracellular signal-regulated kinase-dependent expression of p21 Cip/WAF1. Infect Immun 69: 4944-4950.
47. Rudney, J.D., Chen, R., and Sedgewick, G.J. (2001) Intracellular Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in buccal epithelial cells collected from human subjects. Infect Immun 69: 2700-2707.
48. Sah, N.K., Khan, Z., Khan, G.J., and Bisen, P.S. (2006) Structural, functional and therapeutic biology of survivin. Cancer Lett 244: 164-171.
49. Sen, P., Mukherjee, S., Ray, D., and Raha, S. (2003) Involvement of the Akt/PKB signaling pathway with disease processes. Mol Cell Biochem 253: 241-246.
50. Sheets, S.M., Potempa, J., Travis, J., Fletcher, H.M., and Casiano, C.A. (2006) Gingipains from Porphyromonas gingivalis W83 synergistically disrupt endothelial cell adhesion and can induce caspase-independent apoptosis. Infect Immun 74: 5667-5678.
51. Shen, Y., and White, E. (2001) p53-dependent apoptosis pathways. Adv Cancer Res 82: 55-84.
52. Simons, M.P., Nauseef, W.M., Griffith, T.S., and Apicella, M.A. (2006) Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes. Cell Microbiol 8: 1780-1790.
53. Spierings, D., McStay, G., Saleh, M., Bender, C., Chipuk, J., Maurer, U., and Green, D.R. (2005) Connected to death: The (unexpurgated) mitochondrial pathway of apoptosis. Science 310: 66-67.
54. 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.
55. Vitkov, L., Krautgartner, W.D., and Hannig, M. (2005) Bacterial internalization in periodontitis. Oral Microbiol Immunol 20: 317-321.
56. Wang, C.Y., Mayo, M.W., Korneluk, R.G., Goeddel, D.V., and Baldwin, A.S., Jr (1998) NF-kappaB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281: 1680-1683.
57. Watanabe, K., Yamaji, Y., and Umemoto, T. (1992) Correlation between cell-adherent activity and surface structure in Porphyromonas gingivalis. Oral Microbiol Immunol 7: 357-363.
58. Watanabe, K., Yilmaz, O., Nakhjiri, S.F., Belton, C.M., and Lamont, R.J. (2001) Association of mitogen-activated protein kinase pathways with gingival epithelial cell responses to Porphyromonas gingivalis infection. Infect Immun 69: 6731-6737.
59. Wheatley, S.P., and McNeish, I.A. (2005) Survivin: A protein with dual roles in mitosis and apoptosis. Int Rev Cytol 247: 35-88.
60. van Winkelhoff, A.J., Appelmelk, B.J., Kippuw, N., and de Graaff, J. (1993) K-antigens in Porphyromonas gingivalis are associated with virulence. Oral Microbiol Immunol 8: 259-265.
61. Ximenez-Fyvie, L.A., Haffajee, A.D., and Socransky, S.S. (2000) Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol 27: 648-657.
62. Yilmaz, O., Watanabe, K., and Lamont, R.J. (2002) Involvement of integrins in fimbriae-mediated binding and invasion by Porphyromonas gingivalis. Cell Microbiol 4: 305-314.
63. Yilmaz, O., Young, P.A., Lamont, R.J., and Kenny, G.E. (2003) Gingival epithelial cell signalling and cytoskeletal responses to Porphyromonas gingivalis invasion. Microbiology 149: 2417-2426.
64. 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.
65. 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.
66. Yin, J.L., Shackel, N.A., Zekry, A., McGuinness, P.H., Richards, C., Putten, K.V., 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.
67. Zhang, Y., Wang, T., Chen, W., Yilmaz, O., Park, Y., Jung, I.Y., et al. (2005) Differential protein expression by Porphyromonas gingivalis in response to secreted epithelial cell components. Proteomics 5: 198-211.
68. Zhong, Z., Wen, Z., and Darnell, J.E., Jr (1994) Stat3: A STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264: 95-98.