Neisseria gonorrhoeae infection protects human endocervical epithelial cells from apoptosis via expression of host antiapoptotic proteins

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3602-3610

  Follows, S A ^a   Murlidharan, J ^a   Massari, P ^a   Wetzler, L M ^a   Genco, C A ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCL2 RELATED PROTEIN A1; CELL PROTEIN; FLICE INHIBITORY PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN CIAP 2; STAUROSPORINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERIAL STRAIN; CELL DEATH; CELL STIMULATION; CONTROLLED STUDY; EPITHELIUM; GENE EXPRESSION; GONORRHEA; HUMAN; HUMAN CELL; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UTERINE ENDOCERVIX;

APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASE 3; CELLS, CULTURED; CERVIX UTERI; FEMALE; GONORRHEA; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; NEISSERIA GONORRHOEAE; NF-KAPPA B; PORINS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASE 2; STAUROSPORINE;

EID: 69049103161     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01366-08     Document Type: Article

References (69)

1. Airenne, S., H. M. Surcel, J. Tuukkanen, M. Leinonen, and P. Saikku. 2002. Chlamydia pneumoniae inhibits apoptosis in human epithelial and monocyte cell lines. Scand. J. Immunol. 55:390-398.
2. Antonsson, B., and J. C. Martinou. 2000. The Bcl-2 protein family. Exp. Cell Res. 256:50-57.
3. Ashkenazi, A., and V. M. Dixit. 1999. Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol. 11:255-260.
4. Bauler, L. D., C. S. Duckett, and M. X. O'Riordan. 2008. XIAP regulates cytosol-specific innate immunity to Listeria infection. PLoS Pathog. 4:e1000142.
5. Billker, O., A. Popp, S. D. Gray-Owen, and T. F. Meyer. 2000. The structural basis of CEACAM-receptor targeting by neisserial Opa proteins. Trends Microbiol. 8:258-260.
6. Binnicker, M. J., R. D. Williams, and M. A. Apicella. 2004. Gonococcal porin IB activates NF-kappaB in human urethral epithelium and increases the expression of host antiapoptotic factors. Infect. Immun. 72:6408-6417.
7. Binnicker, M. J., R. D. Williams, and M. A. Apicella. 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.
8. Bours, V., M. Bentires-Alj, A. C. Hellin, P. Viatour, P. Robe, S. Delhalle, V. Benoit, and M. P. Merville. 2000. Nuclear factor-kappa B, cancer, and apoptosis. Biochem. Pharmacol. 60:1085-1089.
9. Bratton, S. B., M. MacFarlane, K. Cain, and G. M. Cohen. 2000. Protein complexes activate distinct caspase cascades in death receptor and stress-induced apoptosis. Exp. Cell Res. 256:27-33.
10. Cain, K., S. B. Bratton, and G. M. Cohen. 2002. The Apaf-1 apoptosome: a large caspase-activating complex. Biochimie 84:203-214.
11. Chowdhury, I., B. Tharakan, and G. K. Bhat. 2006. Current concepts in apoptosis: the physiological suicide program revisited. Cell. Mol. Biol. Lett. 11:506-525.
12. Cohen, G. M. 1997. Caspases: the executioners of apoptosis. Biochem. J. 326:1-16.
13. Conte, D., M. Holcik, C. A. Lefebvre, E. Lacasse, D. J. Picketts, K. E. Wright, and R. G. Korneluk. 2006. Inhibitor of apoptosis protein cIAP2 is essential for lipopolysaccharide-induced macrophage survival. Mol. Cell. Biol. 26:699-708.
14. da Silva Correia, J., Y. Miranda, N. Leonard, J. Hsu, and R. J. Ulevitch. 2007. Regulation of Nod1-mediated signaling pathways. Cell. Death Differ. 14:830-839.
15. Dehio, C., S. D. Gray-Owen, and T. F. Meyer. 1998. The role of neisserial Opa proteins in interactions with host cells. Trends Microbiol. 6:489-495.
16. Edwards, J. L., and M. A. Apicella. 2004. The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin. Microbiol. Rev. 17:965-981.
17. Ekert, P. G., J. Silke, and D. L. Vaux. 1999. Caspase inhibitors. Cell. Death Differ. 6:1081-1086.
18. Fan, T., H. Lu, H. Hu, L. Shi, G. A. McClarty, D. M. Nance, A. H. Greenberg, and G. Zhong. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187:487-496.
19. Fichorova, R. N., A. O. Cronin, E. Lien, D. J. Anderson, and R. R. Ingalls. 2002. Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of Toll-like receptor 4-mediated signaling. J. Immunol. 168:2424-2432.
20. Fichorova, R. N., P. J. Desai, F. C. Gibson III, and C. A. Genco. 2001. Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect. Immun. 69:5840-5848.
21. Fichorova, R. N., J. G. Rheinwald, and D. J. Anderson. 1997. Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol. Reprod. 57:847-855.
22. Fischer, S. F., C. Schwarz, J. Vier, and G. Hacker. 2001. Characterization of antiapoptotic activities of Chlamydia pneumoniae in human cells. Infect. Immun. 69:7121-7129.
23. Fulcher, N. B. 2004. The role of Neisseria gonorrhoeae opacity proteins in host cell interactions and pathogenesis. Ph.D. dissertation. The University of North Carolina, Chapel Hill.
24. Gao, L. Y., and Y. A. Kwaik. 2000. The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol. 8:306-313.
25. Gesellchen, V., D. Kuttenkeuler, M. Steckel, N. Pelte, and M. Boutros. 2005. An RNA interference screen identifies inhibitor of apoptosis protein 2 as a regulator of innate immune signalling in Drosophila. EMBO Rep. 6:979-984.
26. Groesdonk, H. V., S. Schlottmann, F. Richter, M. Georgieff, and U. Senftleben. 2006. Escherichia coli prevents phagocytosis-induced death of macrophages via classical NF-kappaB signaling, a link to T-cell activation. Infect. Immun. 74:5989-6000.
27. Gross, A., J. M. McDonnell, and S. J. Korsmeyer. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899-1911.
28. Hacker, G., and S. F. Fischer. 2002. Bacterial anti-apoptotic activities. FEMS Microbiol. Lett. 211:1-6.
29. Hedges, S. R., D. A. Sibley, M. S. Mayo, E. W. Hook III, and M. W. Russell. 1998. Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J. Infect. Dis. 178:742-751.
30. Hornef, M. W., M. J. Wick, M. Rhen, and S. Normark. 2002. Bacterial strategies for overcoming host innate and adaptive immune responses. Nat. Immunol. 3:1033-1040.
31. Howie, H. L., M. Glogauer, and M. So. 2005. The N. gonorrhoeae type IV pilus stimulates mechanosensitive pathways and cytoprotection through a pilT-dependent mechanism. PLoS Biol. 3:e100.
32. Howie, H. L., S. L. Shiflett, and M. So. 2008. Extracellular signal-regulated kinase activation by Neisseria gonorrhoeae downregulates epithelial cell proapoptotic proteins Bad and Bim. Infect. Immun. 76:2715-2721.
33. Huh, J. R., I. Foe, I. Muro, C. H. Chen, J. H. Seol, S. J. Yoo, M. Guo, J. M. Park, and B. A. Hay. 2007. The Drosophila inhibitor of apoptosis (IAP) DIAP2 is dispensable for cell survival, required for the innate immune response to gram-negative bacterial infection, and can be negatively regulated by the reaper/hid/grim family of IAP-binding apoptosis inducers. J. Biol. Chem. 282:2056-2068.
34. Huppertz, B., H. G. Frank, and P. Kaufmann. 1999. The apoptosis cascade - morphological and immunohistochemical methods for its visualization. Anat. Embryol. (Berlin) 200:1-18.
35. Jarvis, G. A., J. Li, and K. V. Swanson. 1999. Invasion of human mucosal epithelial cells by Neisseria gonorrhoeae upregulates expression of intercellular adhesion molecule 1 (ICAM-1). Infect. Immun. 67:1149-1156.
36. Kleino, A., S. Valanne, J. Ulvila, J. Kallio, H. Myllymaki, H. Enwald, S. Stoven, M. Poidevin, R. Ueda, D. Hultmark, B. Lemaitre, and M. Ramet. 2005. Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J. 24:3423-3434.
37. Kroemer, G., B. Dallaporta, and M. Resche-Rigon. 1998. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60:619-642.
38. Le Bras, M., M. V. Clement, S. Pervaiz, and C. Brenner. 2005. Reactive oxygen species and the mitochondrial signaling pathway of cell death. Histol. Histopathol. 20:205-219.
39. Leulier, F., N. Lhocine, B. Lemaitre, and P. Meier. 2006. The Drosophila inhibitor of apoptosis protein DIAP2 functions in innate immunity and is essential to resist gram-negative bacterial infection. Mol. Cell. Biol. 26:7821-7831.
40. Losick, V. P., and R. R. Isberg. 2006. NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J. Exp. Med. 203:2177-2189.
41. Maisey, K., G. Nardocci, M. Imarai, H. Cardenas, M. Rios, H. B. Croxatto, J. E. Heckels, M. Christodoulides, and L. A. Velasquez. 2003. Expression of proinflammatory cytokines and receptors by human fallopian tubes in organ culture following challenge with Neisseria gonorrhoeae. Infect. Immun. 71: 527-532.
42. Massari, P., Y. Ho, and L. M. Wetzler. 2000. Neisseria meningitidis porin PorB interacts with mitochondria and protects cells from apoptosis. Proc. Natl. Acad. Sci. USA 97:9070-9075.
43. Massari, P., C. A. King, A. Y. Ho, and L. M. Wetzler. 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.
44. Massari, P., C. A. King, H. MacLeod, and L. M. Wetzler. 2005. Improved purification of native meningococcal porin PorB and studies on its structure/function. Protein Expr. Purif. 44:136-146.
45. McCarthy, J. V., J. Ni, and V. M. Dixit. 1998. RIP2 is a novel NF-kappaB-activating and cell death-inducing kinase. J. Biol. Chem. 273:16968-16975.
46. McGee, Z. A., C. M. Clemens, R. L. Jensen, J. J. Klein, L. R. Barley, and G. L. Gorby. 1992. Local induction of tumor necrosis factor as a molecular mechanism of mucosal damage by gonococci. Microb. Pathog. 12:333-341.
47. Mistry, D., and R. A. Stockley. 2006. IgA1 protease. Int. J. Biochem. Cell Biol. 38:1244-1248.
48. Miyairi, I., and G. I. Byrne. 2006. Chlamydia and programmed cell death. Curr. Opin. Microbiol. 9:102-108.
49. Morales, P., P. Reyes, M. Vargas, M. Rios, M. Imarai, H. Cardenas, H. Croxatto, P. Orihuela, R. Vargas, J. Fuhrer, J. E. Heckels, M. Christodoulides, and L. Velasquez. 2006. Infection of human fallopian tube epithelial cells with Neisseria gonorrhoeae protects cells from tumor necrosis factor alpha-induced apoptosis. Infect. Immun. 74:3643-3650.
50. Muenzner, P., M. Naumann, T. F. Meyer, and S. D. Gray-Owen. 2001. Pathogenic Neisseria trigger expression of their carcinoembryonic antigen-related cellular adhesion molecule 1 (CEACAM1; previously CD66a) receptor on primary endothelial cells by activating the immediate early response transcription factor, nuclear factor-kappaB. J. Biol. Chem. 276:24331-24340.
51. Muenzner, P., M. Rohde, S. Kneitz, and C. R. Hauck. 2005. CEACAM engagement by human pathogens enhances cell adhesion and counteracts bacteria-induced detachment of epithelial cells. J. Cell Biol. 170:825-836.
52. Muller, A., D. Gunther, V. Brinkmann, R. Hurwitz, T. F. Meyer, and T. Rudel. 2000. Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. EMBO J. 19:5332-5343.
53. Muller, A., D. Gunther, F. Dux, M. Naumann, T. F. Meyer, and T. Rudel. 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.
54. Naumann, M., S. Wessler, C. Bartsch, B. Wieland, and T. F. Meyer. 1997. Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor kappaB and activator protein 1 and the induction of inflammatory cytokines. J. Exp. Med. 186:247-258.
55. Pahl, H. L. 1999. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18:6853-6866.
56. Paland, N., K. Rajalingam, N. Machuy, A. Szczepek, W. Wehrl, and T. Rudel. 2006. NF-kappaB and inhibitor of apoptosis proteins are required for apoptosis resistance of epithelial cells persistently infected with Chlamydophila pneumoniae. Cell. Microbiol. 8:1643-1655.
57. Platt, N., R. P. da Silva, and S. Gordon. 1998. Recognizing death: the phagocytosis of apoptotic cells. Trends Cell Biol. 8:365-372.
58. Quayle, A. J. 2002. The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells. J. Reprod. Immunol. 57:61-79.
59. Rajalingam, K., H. Al-Younes, A. Muller, T. F. Meyer, A. J. Szczepek, and T. Rudel. 2001. Epithelial cells infected with Chlamydophila pneumoniae (Chlamydia pneumoniae) are resistant to apoptosis. Infect. Immun. 69:7880-7888.
60. Ramsey, K. H., H. Schneider, A. S. Cross, J. W. Boslego, D. L. Hoover, T. L. Staley, R. A. Kuschner, and C. D. Deal. 1995. Inflammatory cytokines produced in response to experimental human gonorrhea. J. Infect. Dis. 172:186-191.
61. Rath, P. C., and B. B. Aggarwal. 1999. TNF-induced signaling in apoptosis. J. Clin. Immunol. 19:350-364.
62. Rooijakkers, S. H., and J. A. van Strijp. 2007. Bacterial complement evasion. Mol. Immunol. 44:23-32.
63. Schmitz, I., S. Kirchhoff, and P. H. Krammer. 2000. Regulation of death receptor-mediated apoptosis pathways. Int. J. Biochem. Cell Biol. 32:1123-1136.
64. Simons, M. P., W. M. Nauseef, T. S. Griffith, and M. A. Apicella. 2006. Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes. Cell. Microbiol. 8:1780-1790.
65. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
66. Tramont, E. C. 1981. Adhesion of Neisseria gonorrhoeae and disease. Ciba Found. Symp. 80:188-201.
67. Tsujimoto, Y. 2003. Cell death regulation by the Bcl-2 protein family in the mitochondria. J. Cell Physiol. 195:158-167.
68. van der Woude, M. W., and A. J. Bäumler. 2004. Phase and antigenic variation in bacteria. Clin. Microbiol. Rev. 17:581-611.
69. Zychlinsky, A., and P. J. Sansonetti. 1997. Apoptosis as a proinflammatory event: what can we learn from bacteria-induced cell death? Trends Microbiol. 5:201-204.