Infection of human urethral epithelium with Neisseria gonorhoeae elicits an upregulation of host anti-apoptotic factors and protects cells from staurosporine-induced apoptosis

Cellular Microbiology

Volumn 5, Issue 8, 2003, Pages 549-560

  Binnicker, Matthew J ^a   Williams, Richard D ^a   Apicella, Michael A ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE INHIBITOR; CYCLOOXYGENASE 2; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN MCL 1; REGULATOR PROTEIN; RIBONUCLEASE; STAUROSPORINE;

APOPTOSIS; ARTICLE; BACTERIAL SURVIVAL; BLADDER EPITHELIUM; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GONORRHEA; HOST CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

APOPTOSIS; CELL LINE; ENZYME INHIBITORS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENES, BCL-2; GONORRHEA; HUMANS; NEISSERIA GONORRHOEAE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN KINASE INHIBITORS; STAUROSPORINE; UP-REGULATION; URETHRA;

BACTERIA (MICROORGANISMS); NEISSERIA; NEISSERIA GONORRHOEAE;

EID: 0042697098     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2003.00300.x     Document Type: Article

References (54)

1. Antoni, B.A., Sabbatini, P., Rabson, A.B., and White, E. (1995) Inhibition of apoptosis in human immunodeficiency virus-infected cells enhances virus production and facilitates persistent infection. J Virol 69: 2384-2392.
2. Apicella, M.A., Ketterer, M., Lee, F.K., Zhou, D., Rice, P.A., and Blake, M.S. (1996) The pathogenesis of gonococcal urethritis in men: confocal and immunoelectron microscopic analysis of urethral exudates from men infected with Neisseria gonorrhoeae. J Infect Dis 173: 636-646.
3. Bossy-Wetzel, E., Newmeyer, D.D., and Green, D.R. (1998) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 17: 37-49.
4. Chen, Y., Smith, M.R., Thirumalai, K., and Zychlinsky, A. (1996) A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J 15: 3853-3860.
5. Cohen, M.S., Cannon, J.G., Jerse, A.E., Charniga, L.M., Isbey, S.F., and Whicker, L.G. (1994) Human experimentation with Neisseria gonorrhoeae: rationale, methods, and implications for the biology of infection and vaccine development. J Infect Dis 169: 532-537.
6. D'Souza, B., Rowe, M., and Walls, D. (2000) The bfl-1 gene is transcriptionally upregulated by the Epstein-Barr virus LMP1, and its expression promotes the survival of a Burkitt's lymphoma cell line. J Virol 74: 6652-6658.
7. Densen, P., MacKeen, L.A., and Clark, R.A. (1982) Dissemination of gonococcal infection is associated with delayed stimulation of complement-dependent neutrophil chemotaxis in vitro. Infect Immun 38: 563-572.
8. Deveraux, Q.L., Roy, N., Stennicke, H.R., Van Arsdale, T., Zhou, Q., Srinivasula, S.M., et al. (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 17: 2215-2223.
9. Dudas, K.C., and Apicella, M.A. (1988) Selection and immunochemical analysis of lipooligosaccharide mutants of Neisseria gonorrhoeae. Infect Immun 56: 499-504.
10. Edwards, J.L., Shao, J.Q., Ault, K.A., and Apicella, M.A. (2000) Neisseria gonorrhoeae elicits membrane ruffling and cytoskeletal rearrangements upon infection of primary human endocervical and ectocervical cells. Infect Immun 68: 5354-5363.
11. Fan, T., Lu, H., Hu, H., Shi, L., McClarty, G.A., Nance, D.M., et al. (1998) Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med 187: 487-496.
12. Fischer, S.F., Schwarz, C., Vier, J., and Hacker, G. (2001) Characterization of anti-apoptotic activities of Chlamydia pneumoniae in human cells. Infect Immun 69: 7121-7129.
13. Geng, Y., Shane, R.B., Berencsi, K., Gonczol, E., Zaki, M.H., Margolis, D.J., et al. (2000) Chlamydia pneumoniae inhibits apoptosis in human peripheral blood mononuclear cells through induction of IL-10. J Immunol 164: 5522-5529.
14. Grassmé, H., Jendrossek, V., and Gulbins, E. (2001) Molecular mechanisms of bacteria induced apoptosis. Apoptosis 6: 441-445.
15. Harvey, H.A., Ketterer, M.R., Preston, A., Lubaroff, D., Williams, R., and Apicella, M.A. (1997) Ultrastructural analysis of primary human urethral epithelial cell cultures infected with Neisseria gonorrhoeae. Infect Immun 65: 2420-2427.
16. Harvey, H.A., Jennings, M.P., Campbell, C.A., Williams, R., and Apicella, M.A. (2001) Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol Microbiol 42: 659-672.
17. Harvey, H.A., Post, D.M., and Apicella, M.A. (2002) Immortalization of human urethral epithelial cells: a model for the study of the pathogenesis of and the inflammatory cytokine response to Neisseria gonorrhoeae infection. Infect Immun 70: 5808-5815.
18. Hengartner, M.O. (2000) The biochemistry of apoptosis. Nature 407: 770-776.
19. Hersh, D., Monack, D.M., Smith, M.R., Ghori, N., Falkow, S., and Zychlinsky, A. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96: 2396-2401.
20. 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.
21. Hsu, S.Y., Kaipia, A., McGee, E., Lomeli, M., and Hsueh, A.J. (1997) Bok is a pro-apoptotic Bcl-2 protein with restricted expression in reproductive tissues and heterodimerizes with selective anti-apoptotic Bcl-2 family members. Proc Natl Acad Sci USA 94: 12401-12406.
22. John, C.M., Griffiss, J.M., Apicella, M.A., Mandrell, R.E., and Gibson, B.W. (1991) The structural basis for pyocin resistance in Neisseria gonorrhoeae lipooligosaccharides. J Biol Chem 266: 19303-19311.
23. Jürgensmeier, J.M., Xie, Z., Deveraux, Q., Ellerby, L., Bredesen, D., and Reed, J.C. (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci USA 95: 4997-5002.
24. Kelekar, A., Chang, B.S., Harlan, J.E., Fesik, S.W., and Thompson, C.B. (1997) Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-XL. Mol Cell Biol 17: 7040-7046.
25. Kim, J.M., Kim, J.S., Jung, H.C., Song, I.S., and Kim, C.Y. (2000) Upregulated cyclooxygenase-2 inhibits apoptosis of human gastric epithelial cells infected with Helicobacter pylori. Dig Dis Sci 45: 2436-2443.
26. Kluck, R.M., Bossy-Wetzel, E., Green, D.R., and Newmeyer, D.D. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136.
27. Li, H., Zhu, H., Xu, C.J., and Yuan, J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501.
28. Lin, M.T., Lee, R.C., Yang, P.C., Ho, F.M., and Kuo, M.L. (2001) Cyclooxygenase-2 inducing Mcl-1-dependent survival mechanism in human lung adenocarcinoma CL1.0 cells. Involvement of phosphatidylinositol 3- kinase/Akt pathway. J Biol Chem 276: 48997-49002.
29. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94: 481-490.
30. Massari, P., Ho, Y., and Wetzler, L.M. (2000) Neisseria meningitidis porin PorB interacts with mitochondria and protects cells from apoptosis. Proc Natl Acad Sci USA 97: 9070-9075.
31. Massari, P., King, C., Ho, Y., and Wetzler, L.M. (2003) Neisserial PorB is translocated to the mitochondria of HeLa cells infected with Neisseria meningitidis and protects cells from apoptosis. Cell Microbiol 5: 99-109.
32. Müller, A., Gunther, D., Dux, F., Naumann, M., Meyer, T.F., and Rudel, T. (1999) Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. EMBO J 18: 339-352.
33. Müller, A., Gunther, D., Brinkmann, V., Hurwitz, R., Meyer, T.F., and Rudel, T. (2000) Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. EMBO J 19: 5332-5343.
34. Nakagawa, I., Nakata, M., Kawabata, S., and Hamada, S. (2001) Cytochrome c-mediated caspase-9 activation triggers apoptosis in Streptococcus pyogenes-infected epithelial cells. Cell Microbiol 3: 395-405.
35. 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.
36. van Ooij, C., van Kalman, L.I., Nishijima, M., Hanada, K., Mostov, K., and Engel, J.N. (2000) Host cell-derived sphingolipids are required for the intracellular growth of Chlamydia trachomatis. Cell Microbiol 2: 627-637.
37. Reynolds, J.E., Yang, T., Qian, L., Jenkinson, J.D., Zhou, P., Eastman, A., and Craig, R.W. (1994) Mcl-1, a member of the Bcl-2 family, delays apoptosis induced by c-Myc overexpression in Chinese hamster ovary cells. Cancer Res 54: 6348-6352.
38. Reynolds, J.E., Li, J., Craig, R.W., and Eastman, A. (1996) BCL-2 and MCL-1 expression in Chinese hamster ovary cells inhibits intracellular acidification and apoptosis induced by staurosporine. Exp Cell Res 225: 430-436.
39. Roy, N., Deveraux, Q.L., Takahashi, R., Salvesen, G.S., and Reed, J.C. (1997) The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J 16: 6914-6925.
40. Ruckdeschel, K., Mannel, O., Richter, K., Jacobi, C.A., Trulzsch, K., Rouot, B., and Heesemann, J. (2001) Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages. J Immunol 166: 1823-1831.
41. Savill, J., and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature 407: 784-788.
42. Schneider, H., Cross, A.S., Kuschner, R.A., Taylor, D.N., Sadoff, J.C., Boslego, J.W., and Deal, C.D. (1995) Experimental human gonococcal urethritis: 250 Neisseria gonorrhoeae MS11mkC are infective. J Infect Dis 172: 180-185.
43. Shen, Y., and Shenk, T.E. (1995) Viruses and apoptosis. Curr Opin Genet Dev 5: 105-111.
44. Shim, Y.H., Byun, E.K., Lee, M.J., Huh, J., and Kim, C.W. (2000) Anti-apoptotic role of Bfl-1 in staurosporine-treated B-lymphoblastic cells. Int J Hematol 72: 484-490.
45. Shirin, H., Sordillo, E.M., Kolevska, T.K., Hibshoosh, H., Kawabata, Y., Oh, S.H., et al. (2000) Chronic Helicobacter pylori infection induces an apoptosis-resistant phenotype associated with decreased expression of p27 (kip1). Infect Immun 68: 5321-5328.
46. Smith, W.L., DeWitt, D.L., and Garavito, R.M. (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 69: 145-182.
47. Tsai, P.J., Lin, Y.S., Kuo, C.F., Lei, H.Y., and Wu, J.J. (1999) Group A Streptococcus induces apoptosis in human epithelial cells. Infect Immun 67: 4334-4339.
48. Tsujii, M., Kawano, S., Tsuji, S., Sawaoka, H., Hori, M., and DuBois, R.N. (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93: 705-716.
49. Tsujimoto, Y., and Shimizu, S. (2000) Bcl-2 family: life-or-death switch. FEBS Lett 466: 6-10.
50. Vander Heiden, M.G., Chandel, N.S., Williamson, E.K., Schumacker, P.T., and Thompson, C.B. (1997) Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 91: 627-637.
51. Werner, A.B., de Vries, E., Tait, S.W., Bontjer, I., and Borst, J. (2002) Bcl-2 family member Bfl-1/A1 sequesters truncated bid to inhibit is collaboration with pro-apoptotic Bak or Bax. J Biol Chem 277: 22781-22788.
52. Yang, J., Liu, X., Bhalla, K., Kim, C.N., Ibrado, A.M., Cai, J., et al. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132.
53. Zhang, H., Cowan-Jacob, S.W., Simonen, M., Greenhalf, W., Heim, J., and Meyhack, B. (2000) Structural basis of BFL-1 for its interaction with BAX and its anti-apoptotic action in mammalian and yeast cells. J Biol Chem 275: 11092-11099.
54. Zychlinsky, A., Prevost, M.C., and Sansonetti, P.J. (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169.