Neisseria gonorrhoeae infection causes DNA damage and affects the expression of p21, p27 and p53 in non-tumor epithelial cells

Journal of Cell Science

Volumn 126, Issue 1, 2013, Pages 339-347

  Vielfort, Katarina ^a   Söderholm, Niklas ^a   Weyler, Linda ^a   Vare, Daniel ^a   Löfmark, Sonja ^b   Aro, Helena ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

Author keywords

DNA damage; N.gonorrhoeae; VK2 E6E7

Indexed keywords

BROXURIDINE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DOUBLE STRANDED DNA; HISTONE H2AX; PROTEIN P53;

ARTICLE; CELL ASSAY; CELL CULTURE; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DNA DAMAGE; DNA DETERMINATION; DNA STRAND BREAKAGE; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; GONORRHEA; HISTONE PHOSPHORYLATION; HOST CELL; HUMAN; HUMAN CELL; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; EPITHELIAL CELLS; FLOW CYTOMETRY; HUMANS; NEISSERIA GONORRHOEAE; PROLIFERATING CELL NUCLEAR ANTIGEN; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE;

EID: 84875579702     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.117721     Document Type: Article

References (45)

1. Binnicker, M. J., Williams, R. D. and Apicella, M. A. (2003). Infection of human urethral epithelium with Neisseria gonorrhoeae elicits an upregulation of host antiapoptotic factors and protects cells from staurosporine-induced apoptosis. Cell. Microbiol. 5, 549-560.
2. Binnicker, M. J., Williams, R. D. and Apicella, M. A. (2004). Gonococcal porin IB activates NF-kappaB in human urethral epithelium and increases the expression of host antiapoptotic factors. Infect. Immun. 72, 6408-6417.
3. Cleaver, J. E. (2011). γH2Ax: biomarker of damage or functional participant in DNA repair "all that glitters is not gold!". Photochem. Photobiol. 87, 1230-1239.
4. Cuevas-Ramos, G., Petit, C. R., Marcq, I., Boury, M., Oswald, E. and Nougayrède, J. P. (2010). Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc. Natl. Acad. Sci. USA 107, 11537-11542.
5. Deva, R., Sczepanski, M., Saha, S., Zafiriou, M. P., Kerstin, N., Jakobsson, P. J., Inoue, Y. and Nigam, S. (2010). C. albicans activates cyclooxygenase but not its product prostaglandin E2 in HPV 16-stabilized cells. Eur. J. Obstet. Gynecol. Reprod. Biol. 152, 205-209.
6. Erixon, K. and Ahnström, G. (1979). Single-strand breaks in DNA during repair of UV-induced damage in normal human and xeroderma pigmentosum cells as determined by alkaline DNA unwinding and hydroxylapatite chromatography: effects of hydroxyurea, 5-fluorodeoxyuridine and 1-beta-D-arabinofuranosylcytosine on the kinetics of repair. Mutat. Res. 59, 257-271.
7. Fichorova, R. N., Desai, P. J., Gibson, F. C., 3rd and Genco, C. A. (2001). Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect. Immun. 69, 5840-5848.
8. Follows, S. A., Murlidharan, J., Massari, P., Wetzler, L. M. and Genco, C. A. (2009). Neisseria gonorrhoeae infection protects human endocervical epithelial cells from apoptosis via expression of host antiapoptotic proteins. Infect. Immun. 77, 3602-3610.
9. Friedberg, E. C. (1995). Out of the shadows and into the light: the emergence of DNA repair. Trends Biochem. Sci. 20, 381.
10. Gartel, A. L. and Tyner, A. L. (2002). The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol. Cancer Ther. 1, 639-649.
11. Howie, H. L., Shiflett, S. L. and So, M. (2008). Extracellular signal-regulated kinase activation by Neisseria gonorrhoeae downregulates epithelial cell proapoptotic proteins Bad and Bim. Infect. Immun. 76, 2715-2721.
12. Hu, L. and Kopecko, D. J. (1999). Campylobacter jejuni 81-176 associates with microtubules and dynein during invasion of human intestinal cells. Infect. Immun. 67, 4171-4182.
13. Jacinto, A., Martinez-Arias, A. and Martin, P. (2001). Mechanisms of epithelial fusion and repair. Nat. Cell Biol. 3, E117-E123.
14. Jones, A., Jonsson, A. B. and Aro, H. (2007). Neisseria gonorrhoeae infection causes a G1 arrest in human epithelial cells. FASEB J. 21, 345-355.
15. Källström, H., Liszewski, M. K., Atkinson, J. P. and Jonsson, A. B. (1997). Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol. Microbiol. 25, 639-647.
16. Källström, H., Islam, M. S., Berggren, P. O. and Jonsson, A. B. (1998). Cell signaling by the type IV pili of pathogenic Neisseria. J. Biol. Chem. 273, 21777-21782.
17. Källström, H., Hansson-Palo, P. and Jonsson, A. B. (2000). Cholera toxin and extracellular Ca2+ induce adherence of non-piliated Neisseria: evidence for an important role of G-proteins and Rho in the bacteria-cell interaction. Cell. Microbiol. 2, 341-351.
18. Kellogg, D. S., Jr, Cohen, I. R., Norins, L. C., Schroeter, A. L. and Reising, G. (1968). Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro. J. Bacteriol. 96, 596-605.
19. Koomey, M. (2001). Implications of molecular contacts and signaling initiated by Neisseria gonorrhoeae. Curr. Opin. Microbiol. 4, 53-57.
20. Kundu, J. K. and Surh, Y. J. (2008). Inflammation: gearing the journey to cancer. Mutat. Res. 659, 15-30.
21. Lara-Tejero, M. and Galán, J. E. (2000). A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science 290, 354-357.
22. Lindahl, T. and Barnes, D. E. (2000). Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol. 65, 127-134.
23. Löfmark, S., de Klerk, N. and Aro, H. (2011). Neisseria gonorrhoeae infection induces altered amphiregulin processing and release. PLoS ONE 6, e16369.
24. Merz, A. J., Rifenbery, D. B., Arvidson, C. G. and So, M. (1996). Traversal of a polarized epithelium by pathogenic Neisseriae: facilitation by type IV pili and maintenance of epithelial barrier function. Mol. Med. 2, 745-754.
25. Merz, A. J., Enns, C. A. and So, M. (1999). Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells. Mol. Microbiol. 32, 1316-1332.
26. Michaud, D. S. (2007). Chronic inflammation and bladder cancer. Urol. Oncol. 25, 260-268.
27. Muenzner, P., Bachmann, V., Zimmermann, W., Hentschel, J. and Hauck, C. R. (2010). Human-restricted bacterial pathogens block shedding of epithelial cells by stimulating integrin activation. Science 329, 1197-1201.
28. Naumann, M., Wessler, S., Bartsch, C., Wieland, B. and Meyer, T. F. (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.
29. Nias, A. H. W. (1998). An Introduction to Radiobiology. p. 69. London, UK: John Wiley & Sons Ltd.
30. Nikjoo, H., O'Neill, P., Terrissol, M. and Goodhead, D. T. (1994). Modelling of radiation-induced DNA damage: the early physical and chemical event. Int. J. Radiat. Biol. 66, 453-457.
31. Nougayrède, J. P., Taieb, F., De Rycke, J. and Oswald, E. (2005). Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol. 13, 103-110.
32. Oswald, E., Nougayrède, J. P., Taieb, F. and Sugai, M. (2005). Bacterial toxins that modulate host cell-cycle progression. Curr. Opin. Microbiol. 8, 83-91.
33. Popp, A., Billker, O. and Rudel, T. (2001). Signal transduction pathways induced by virulence factors of Neisseria gonorrhoeae. Int. J. Med. Microbiol. 291, 307-314.
34. Rodríguez-Vilarrupla, A., Díaz, C., Canela, N., Rahn, H. P., Bachs, O. and Agell, N. (2002). Identification of the nuclear localization signal of p21(cip1) and consequences of its mutation on cell proliferation. FEBS Lett. 531, 319-323.
35. Russo, T., Zambrano, N., Esposito, F., Ammendola, R., Cimino, F., Fiscella, M., Jackman, J., O'Connor, P. M., Anderson, C. W. and Appella, E. (1995). A p53-independent pathway for activation of WAF1/CIP1 expression following oxidative stress. J. Biol. Chem. 270, 29386-29391.
36. Scanlon, M., Shaw, A. P., Zhou, C. J., Visvesvara, G. S. and Leitch, G. J. (2000). Infection by microsporidia disrupts the host cell cycle. J. Eukaryot. Microbiol. 47, 525-531.
37. Sherr, C. J. and Roberts, J. M. (1995). Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9, 1149-1163.
38. Sutcliffe, S., Giovannucci, E., De Marzo, A. M., Leitzmann, M. F., Willett, W. C. and Platz, E. A. (2006a). Gonorrhea, syphilis, clinical prostatitis, and the risk of prostate cancer. Cancer Epidemiol. Biomarkers Prev. 15, 2160-2166.
39. Sutcliffe, S., Zenilman, J. M., Ghanem, K. G., Jadack, R. A., Sokoll, L. J., Elliott, D. J., Nelson, W. G., De Marzo, A. M., Cole, S. R., Isaacs, W. B. et al. (2006b). Sexually transmitted infections and prostatic inflammation/cell damage as measured by serum prostate specific antigen concentration. J. Urol. 175, 1937-1942.
40. Swanson, J. (1973). Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J. Exp. Med. 137, 571-589.
41. Swanson, J., Robbins, K., Barrera, O. and Koomey, J. M. (1987). Gene conversion variations generate structurally distinct pilin polypeptides in Neisseria gonorrhoeae. J. Exp. Med. 165, 1016-1025.
42. Toller, I. M., Neelsen, K. J., Steger, M., Hartung, M. L., Hottiger, M. O., Stucki, M., Kalali, B., Gerhard, M., Sartori, A. A., Lopes, M. et al. (2011). Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc. Natl. Acad. Sci. USA 108, 14944-14949.
43. Vermeulen, K., Van Bockstaele, D. R. and Berneman, Z. N. (2003). The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif. 36, 131-149.
44. Ward, I. M., Minn, K., Jorda, K. G. and Chen, J. (2003). Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278, 19579-19582.
45. Wei, J., Nagy, T. A., Vilgelm, A., Zaika, E., Ogden, S. R., Romero-Gallo, J., Piazuelo, M. B., Correa, P., Washington, M. K., El-Rifai, W. et al. (2010). Regulation of p53 tumor suppressor by Helicobacter pylori in gastric epithelial cells. Gastroenterology 139, 1333-1343.