Chlamydia infection depends on a functional MDM2-p53 axis

Nature Communications

Volumn 5, Issue , 2014, Pages

  González, Erik ^a   Rother, Marion ^a,b   Kerr, Markus C ^a,c   Al Zeer, Munir A ^a   Abu Lubad, Mohammad ^a   Kessler, Mirjana ^a   Brinkmann, Volker ^a   Loewer, Alexander ^d   Meyer, Thomas F ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b Steinbeis Innovation Center for Systems Biomedicine   (Germany)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORAMPHENICOL; CYCLOHEXIMIDE; CYTOKERATIN 8; PROTEIN MDM2; PROTEIN P53; TUMOR NECROSIS FACTOR ALPHA; VIMENTIN; MDM2 PROTEIN, HUMAN;

APOPTOSIS; CANCER; CARCINOGEN; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; INHIBITION; PATHOGEN;

ARTICLE; CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; FEMALE; HELA CELL LINE; HOST CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; MCF 7 CELL LINE; MESENCHYME CELL; OVARY CANCER; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TIME-LAPSE VIDEO MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; APOPTOSIS; CELL TRANSFORMATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); CHLAMYDIA; MURINAE;

APOPTOSIS; BLOTTING, WESTERN; CELL TRANSFORMATION, NEOPLASTIC; CHLAMYDIA; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; HELA CELLS; HUMANS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84928771542     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6201     Document Type: Article

References (62)

1. Vielfort, K. et al. Neisseria gonorrhoeae infection causes DNA damage and affects the expression of p21, p27 and p53 in non-tumor epithelial cells. J. Cell Sci. 126, 339-347 (2013).
2. Wei, J. et al. Pathogenic bacterium Helicobacter pylori alters the expression profile of p53 protein isoforms and p53 response to cellular stresses. Proc. Natl Acad. Sci. USA 109, E2543-E2550 (2012).
3. Vogelstein, B., Lane, D. & Levine, A. J. Surfing the p53 network. Nature 408, 307-310 (2000).
4. Belland, R., Ojcius, D. M. & Byrne, G. I. Chlamydia. Nat. Rev. Microbiol. 2, 530-531 (2004).
5. Smith, J. S. et al. Chlamydia trachomatis and invasive cervical cancer: a pooled analysis of the IARC multicentric case-control study. Int. J. Cancer 111, 431-439 (2004).
6. Smith, J. S. et al. Evidence for Chlamydia trachomatis as a human papillomavirus cofactor in the etiology of invasive cervical cancer in Brazil and the Philippines. J. Infect. Dis. 185, 324-331 (2002).
7. Wallin, K. L. et al. A population-based prospective study of Chlamydia trachomatis infection and cervical carcinoma. Int. J. Cancer 101, 371-374 (2002).
8. Sharma, M. & Rudel, T. Apoptosis resistance in Chlamydia-infected cells: a fate worse than death? FEMS Immunol. Med. Microbiol. 55, 154-161 (2009).
9. Fan, T. et al. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187, 487-496 (1998).
10. Zhong, Y., Weininger, M., Pirbhai, M., Dong, F. & Zhong, G. Inhibition of staurosporine-induced activation of the proapoptotic multidomain Bcl-2 proteins Bax and Bak by three invasive chlamydial species. J. Infect. 53, 408-414 (2006).
11. Padberg, I., Janssen, S. & Meyer, T. F. Chlamydia trachomatis inhibits telomeric DNA damage signaling via transient hTERT upregulation. Int. J. Med. Microbiol. 303, 463-474 (2013).
12. Chen, A. L., Johnson, K. A., Lee, J. K., Sutterlin, C. & Tan, M. CPAF: a Chlamydial protease in search of an authentic substrate. PLoS Pathog. 8, e1002842 (2012).
13. Lahav, G. et al. Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat. Genet. 36, 147-150 (2004).
14. Tay, S. et al. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 466, 267-271 (2010).
15. Loewer, A., Batchelor, E., Gaglia, G. & Lahav, G. Basal dynamics of p53 reveal transcriptionally attenuated pulses in cycling cells. Cell 142, 89-100 (2010).
16. Wade, M., Li, Y. C. & Wahl, G. M. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat. Rev. Cancer 13, 83-96 (2013).
17. Grossman, S. R. et al. p300/MDM2 complexes participate in MDM2-mediated p53 degradation. Mol. Cell 2, 405-415 (1998).
18. Lill, N. L., Grossman, S. R., Ginsberg, D., DeCaprio, J. & Livingston, D. M. Binding and modulation of p53 by p300/CBP coactivators. Nature 387, 823-827 (1997).
19. Zhou, B. P. et al. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat. Cell Biol. 3, 973-982 (2001).
20. Lee, D. H. & Goldberg, A. L. Proteasome inhibitors: valuable new tools for cell biologists. Trends. Cell Biol. 8, 397-403 (1998).
21. Hou, S. et al. Chlamydia trachomatis outer membrane complex protein B (OmcB) is processed by the protease CPAF. J. Bacteriol. 195, 951-957 (2013).
22. Vassilev, L. T. et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303, 844-848 (2004).
23. Issaeva, N. et al. Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors. Nature Med. 10, 1321-1328 (2004).
24. Kuo, C. C., Wang, S. P. & Grayston, J. T. Antimicrobial activity of several antibiotics and a sulfonamide against Chlamydia trachomatis organisms in cell culture. Antimicrob. Agents Chemother. 12, 80-83 (1977).
25. Häcker, G. The chlamydial protease CPAF: important or not, important for what? Microbes Infect. 16, 367-370 (2014).
26. Chin, E., Kirker, K., Zuck, M., James, G. & Hybiske, K. Actin recruitment to the Chlamydia inclusion is spatiotemporally regulated by a mechanism that requires host and bacterial factors. PLoS One 7, e46949 (2012).
27. Moore, E. R., Mead, D. J., Dooley, C. A., Sager, J. & Hackstadt, T. The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157, 830-838 (2011).
28. Scidmore, M. A., Fischer, E. R. & Hackstadt, T. Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect. Immun. 71, 973-984 (2003).
29. Jorgensen, I. et al. The Chlamydia protease CPAF regulates host and bacterial proteins to maintain pathogen vacuole integrity and promote virulence. Cell Host Microbe 10, 21-32 (2011).
30. Jazedje, T. et al. Human fallopian tube: a new source of multipotent adult mesenchymal stem cells discarded in surgical procedures. J. Transl. Med. 7, 46 (2009).
31. Friedman, M. G., Dvoskin, B. & Kahane, S. Infections with the chlamydia-like microorganism Simkania negevensis, a possible emerging pathogen. Microbes Infect. 5, 1013-1021 (2003).
32. Pilhofer, M. et al. Architecture and host interface of environmental chlamydiae revealed by electron cryotomography. Environ. Microbiol. 16, 417-429 (2014).
33. Kreutmayer, S. et al. Chlamydia pneumoniae infection acts as an endothelial stressor with the potential to initiate the earliest heat shock protein 60-dependent inflammatory stage of atherosclerosis. Cell. Stress Chaperones 18, 259-268 (2013).
34. Olive, A. J. et al. Chlamydia trachomatis-induced alterations in the host cell proteome are required for intracellular growth. Cell Host Microbe 15, 113-124 (2014).
35. Reiling, J. H. et al. A CREB3-ARF4 signalling pathway mediates the response to Golgi stress and susceptibility to pathogens. Nat. Cell Biol. 15, 1473-1485 (2013).
36. Chumduri, C., Gurumurthy, R. K., Zadora, P. K., Mi, Y. & Meyer, T. F. Chlamydia infection promotes host DNA damage and proliferation but impairs the DNA damage response. Cell Host Microbe 13, 746-758 (2013).
37. Mayo, L. D. & Donner, D. B. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc. Natl Acad. Sci. USA 98, 11598-11603 (2001).
38. Meek, D. W. & Knippschild, U. Posttranslational modification of MDM2. Mol. Cancer Res. 1, 1017-1026 (2003).
39. Verbeke, P. et al. Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog. 2, e45 (2006).
40. Mehlitz, A. et al. Tarp regulates early Chlamydia-induced host cell survival through interactions with the human adaptor protein SHC1. J. Cell Biol. 190, 143-157 (2010).
41. Rajalingam, K. et al. Mcl-1 is a key regulator of apoptosis resistance in Chlamydia trachomatis-infected cells. PLoS One 3, e3102 (2008).
42. Kun, D., Xiang-Lin, C., Ming, Z. & Qi, L. Chlamydia inhibit host cell apoptosis by inducing Bag-1 via the MAPK/ERK survival pathway. Apoptosis 18, 1083-1092 (2013).
43. Sharma, M. et al. HIF-1alpha is involved in mediating apoptosis resistance to Chlamydia trachomatis-infected cells. Cell Microbiol. 13, 1573-1585 (2011).
44. Nguyen, B. D. et al. Lipooligosaccharide is required for the generation of infectious elementary bodies in Chlamydia trachomatis. Proc. Natl Acad. Sci. USA 108, 10284-10289 (2011).
45. Maddocks, O. D. & Vousden, K. H. Metabolic regulation by p53. J. Mol. Med. (Berl.) 89, 237-245 (2011).
46. Idahl, A. et al. Chlamydia trachomatis and Mycoplasma genitalium plasma antibodies in relation to epithelial ovarian tumors. Infect. Dis. Obstet. Gynecol. 2011, 824627 (2011).
47. Chaturvedi, A. K. et al. Chlamydia pneumoniae infection and risk for lung cancer. Cancer Epidemiol. Biomarkers Prev. 19, 1498-1505 (2010).
48. Stanley, M. Pathology and epidemiology of HPV infection in females. Gynecol. Oncol. 117, S5-S10 (2010).
49. Koskela, P. et al. Chlamydia trachomatis infection as a risk factor for invasive cervical cancer. Int. J. Cancer 85, 35-39 (2000).
50. Safaeian, M. et al. Chlamydia trachomatis and risk of prevalent and incident cervical premalignancy in a population-based cohort. J. Natl Cancer Inst. 102, 1794-1804 (2010).
51. Crook, T., Tidy, J. A. & Vousden, K. H. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and transactivation. Cell 67, 547-556 (1991).
52. Boyer, S. N., Wazer, D. E. & Band, V. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56, 4620-4624 (1996).
53. Dyson, N., Howley, P. M., Munger, K. & Harlow, E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243, 934-937 (1989).
54. Scheffner, M., Huibregtse, J. M., Vierstra, R. D. & Howley, P. M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75, 495-505 (1993).
55. Werness, B. A., Levine, A. J. & Howley, P. M. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248, 76-79 (1990).
56. Kurman, R. J. & Shih, Ie, M. Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer - shifting the paradigm. Hum. Pathol. 42, 918-931 (2011).
57. Perets, R. et al. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models. Cancer Cell 24, 751-765 (2013).
58. Piek, J. M. et al. Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer. J. Pathol. 195, 451-456 (2001).
59. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615 (2011).
60. Saleemuddin, A. et al. Risk factors for a serous cancer precursor ("p53 signature") in women with inherited BRCA mutations. Gynecol. Oncol. 111, 226-232 (2008).
61. Christian, J. G. et al. Targeting of a chlamydial protease impedes intracellular bacterial growth. PLoS Pathog. 7, e1002283 (2011).
62. Al-Zeer, M. A., Al-Younes, H. M., Lauster, D., Abu Lubad, M. & Meyer, T. F. Autophagy restricts Chlamydia trachomatis growth in human macrophages via IFNG-inducible guanylate binding proteins. Autophagy 9, 50-62 (2013).