Microbial Regulation of p53 Tumor Suppressor

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This review focuses on a novel aspect of host–bacteria interactions:
the direct interplay between bacterial pathogens and tumor suppression mechanisms that protect the host from cancer development. Recent studies revealed that various pathogenic bacteria actively inhibit the major tumor suppression pathway mediated by p53 protein that plays a key role in the regulation of multiple cellular stress responses and prevention of cancerogenesis. Bacterial degradation of p53 was first discovered in the context of Helicobacter pylori infection, which is currently the strongest known risk factor for adenocarcinoma of the stomach. This phenomenon, however, is not limited to H. pylori, and many other bacterial pathogens inhibit p53 using various mechanisms. Inhibition of p53 by bacteria is linked to bacterial modulation of the host cellular responses to DNA damage, metabolic stress, and, potentially, other stressors. This is a dynamic area of research that will continue to evolve and make important contributions to a better understanding of host–microbe interactions and tumorigenesis. These studies may offer new molecular targets and opportunities for drug development.

Vyšlo v časopise: Microbial Regulation of p53 Tumor Suppressor. PLoS Pathog 11(9): e32767. doi:10.1371/journal.ppat.1005099
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005099

Souhrn

Zdroje

1. Lane DP Cancer. p53, guardian of the genome. Nature. 1992;358: 15–16. 1614522

2. Liang Y, Liu J, Feng Z The regulation of cellular metabolism by tumor suppressor p53. Cell Biosci. 2013;3: 9. doi: 10.1186/2045-3701-3-9 23388203

3. Bargonetti J, Reynisdottir I, Friedman PN, Prives C Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev. 1992;6: 1886–1898. 1398068

4. Jiang D, Srinivasan A, Lozano G, Robbins PD SV40 T antigen abrogates p53-mediated transcriptional activity. Oncogene. 1993;8: 2805–2812. 8378089

5. Peden KW, Srinivasan A, Vartikar JV, Pipas JM Effects of mutations within the SV40 large T antigen ATPase/p53 binding domain on viral replication and transformation. Virus Genes. 1998;16: 153–165. 9608660

6. Zhu JY, Abate M, Rice PW, Cole CN The ability of simian virus 40 large T antigen to immortalize primary mouse embryo fibroblasts cosegregates with its ability to bind to p53. J Virol. 1991;65: 6872–6880. 1658380

7. Lane DP, Crawford LV T antigen is bound to a host protein in SV40-transformed cells. Nature. 1979;278: 261–263. 218111

8. Linzer DI, Levine AJ Characterization of a 54K dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell. 1979;17: 43–52. 222475

9. Sarnow P, Ho YS, Williams J, Levine AJ Adenovirus E1b-58kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54 kd cellular protein in transformed cells. Cell. 1982;28: 387–394. 6277513

10. Werness BA, Levine AJ, Howley PM Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science. 1990;248: 76–79. 2157286

11. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell. 1990;63: 1129–1136. 2175676

12. Crook T, Tidy JA, Vousden KH Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation. Cell. 1991;67: 547–556. 1657399

13. Elbel M, Carl S, Spaderna S, Iftner T A comparative analysis of the interactions of the E6 proteins from cutaneous and genital papillomaviruses with p53 and E6AP in correlation to their transforming potential. Virology. 1997;239: 132–149. 9426453

14. Cheng CY, Gilson T, Dallaire F, Ketner G, Branton PE, Blanchette P The E4orf6/E1B55K E3 ubiquitin ligase complexes of human adenoviruses exhibit heterogeneity in composition and substrate specificity. J Virol. 2011;85: 765–775. doi: 10.1128/JVI.01890-10 21068234

15. Forrester NA, Sedgwick GG, Thomas A, Blackford AN, Speiseder T, Dobner T, et al. Serotype-specific inactivation of the cellular DNA damage response during adenovirus infection. J Virol. 2011;85: 2201–2211. doi: 10.1128/JVI.01748-10 21159879

16. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell. 1993;75: 495–505. 8221889

17. Querido E, Blanchette P, Yan Q, Kamura T, Morrison M, Boivin D, et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 2001;15: 3104–3117. 11731475

18. Steegenga WT, Riteco N, Jochemsen AG, Fallaux FJ, Bos JL The large E1B protein together with the E4orf6 protein target p53 for active degradation in adenovirus infected cells. Oncogene. 1998;16: 349–357. 9467960

19. Sato Y, Kamura T, Shirata N, Murata T, Kudoh A, Iwahori S, et al. Degradation of phosphorylated p53 by viral protein-ECS E3 ligase complex. PLoS Pathog. 2009;5: e1000530. doi: 10.1371/journal.ppat.1000530 19649319

20. Wei J, Nagy TA, Vilgelm A, Zaika E, Ogden SR, Romero-Gallo J, et al. Regulation of p53 tumor suppressor by Helicobacter pylori in gastric epithelial cells. Gastroenterology. 2010;139: 1333–1343. doi: 10.1053/j.gastro.2010.06.018 20547161

21. Herrera V, Parsonnet J Helicobacter pylori and gastric adenocarcinoma. Clin Microbiol Infect. 2009;15: 971–976. doi: 10.1111/j.1469-0691.2009.03031.x 19874380

22. Hatakeyama M Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe. 2014;15: 306–316. doi: 10.1016/j.chom.2014.02.008 24629337

23. Zhu Y, Zhong X, Zheng S, Du Q, Xu W Transformed immortalized gastric epithelial cells by virulence factor CagA of Helicobacter pylori through Erk mitogen-activated protein kinase pathway. Oncogene. 2005;24: 3886–3895. 15856031

24. Ohnishi N, Yuasa H, Tanaka S, Sawa H, Miura M, Matsui A, et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci U S A. 2008;105: 1003–1008. doi: 10.1073/pnas.0711183105 18192401

25. Neal JT, Peterson TS, Kent ML, Guillemin K H. pylori virulence factor CagA increases intestinal cell proliferation by Wnt pathway activation in a transgenic zebrafish model. Dis Model Mech. 2013;6: 802–810. doi: 10.1242/dmm.011163 23471915

26. Wandler AM, Guillemin K Transgenic expression of the Helicobacter pylori virulence factor CagA promotes apoptosis or tumorigenesis through JNK activation in Drosophila. PLoS Pathog. 2012;8: e1002939. doi: 10.1371/journal.ppat.1002939 23093933

27. Baik SC, Youn HS, Chung MH, Lee WK, Cho MJ, Ko GH, et al. Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa. Cancer Res. 1996;56: 1279–1282. 8640814

28. Toller IM, Neelsen KJ, Steger M, Hartung ML, Hottiger MO, Stucki M, et al. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci U S A. 2011;108: 14944–14949. doi: 10.1073/pnas.1100959108 21896770

29. Buti L, Spooner E, Van der Veen AG, Rappuoli R, Covacci A, Ploegh HL Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc Natl Acad Sci U S A. 2011;108: 9238–9243. doi: 10.1073/pnas.1106200108 21562218

30. Umehara S, Higashi H, Ohnishi N, Asaka M, Hatakeyama M Effects of Helicobacter pylori CagA protein on the growth and survival of B lymphocytes, the origin of MALT lymphoma. Oncogene. 2003;22: 8337–8342. 14614457

31. Wei J, O'Brien D, Vilgelm A, Piazuelo MB, Correa P, Washington MK, et al. Interaction of Helicobacter pylori with gastric epithelial cells is mediated by the p53 protein family. Gastroenterology. 2008;134: 1412–1423. doi: 10.1053/j.gastro.2008.01.072 18343378

32. Wei J, Noto JM, Zaika E, Romero-Gallo J, Piazuelo MB, Schneider B, et al. Bacterial CagA protein induces degradation of p53 protein in a p14ARF-dependent manner. Gut. 2015:64: 1040–8. doi: 10.1136/gutjnl-2014-307295 25080447

33. Cho SJ, Kang NS, Park SY, Kim BO, Rhee DK, Pyo S Induction of apoptosis and expression of apoptosis related genes in human epithelial carcinoma cells by Helicobacter pylori VacA toxin. Toxicon. 2003;42: 601–611. 14602115

34. Peek RM Jr., Blaser MJ, Mays DJ, Forsyth MH, Cover TL, Song SY, et al. Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res. 1999;59: 6124–6131. 10626802

35. Tsugawa H, Suzuki H, Saya H, Hatakeyama M, Hirayama T, Hirata K, et al. Reactive oxygen species-induced autophagic degradation of Helicobacter pylori CagA is specifically suppressed in cancer stem-like cells. Cell Host Microbe. 2012;12: 764–777. doi: 10.1016/j.chom.2012.10.014 23245321

36. Nagappan A, Park HS, Park KI, Hong GE, Yumnam S, Lee HJ, et al. Helicobacter pylori infection combined with DENA revealed altered expression of p53 and 14-3-3 isoforms in Gulo-/- mice. Chem Biol Interact. 2013;206: 143–152. doi: 10.1016/j.cbi.2013.09.002 24035909

37. Shu X, Yang Z, Li ZH, Chen L, Zhou XD, Xie Y, et al. Helicobacter pylori Infection Activates the Akt-Mdm2-p53 Signaling Pathway in Gastric Epithelial Cells. Dig Dis Sci. 2014: 876–886. doi: 10.1007/s10620-014-3470-2 25480405

38. Bhardwaj V, Noto JM, Wei J, Andl C, El-Rifai W, Peek RM, et al. Helicobacter pylori bacteria alter the p53 stress response via ERK-HDM2 pathway. Oncotarget. 2015;6: 1531–1543. 25605238

39. Chen D, Kon N, Li M, Zhang W, Qin J, Gu W ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell. 2005;121: 1071–1083. 15989956

40. Kamijo T, Weber JD, Zambetti G, Zindy F, Roussel MF, Sherr CJ Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc Natl Acad Sci U S A. 1998;95: 8292–8297. 9653180

41. Zhang Y, Xiong Y, Yarbrough WG ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell. 1998;92: 725–734. 9529249

42. Kang GH, Lee HJ, Hwang KS, Lee S, Kim JH, Kim JS Aberrant CpG island hypermethylation of chronic gastritis, in relation to aging, gender, intestinal metaplasia, and chronic inflammation. Am J Pathol. 2003;163: 1551–1556. 14507661

43. Wei J, Noto J, Zaika E, Romero-Gallo J, Correa P, El-Rifai W, et al. Pathogenic bacterium Helicobacter pylori alters the expression profile of p53 protein isoforms and p53 response to cellular stresses. Proc Natl Acad Sci U S A. 2012;109: E2543–2550. 22927405

44. Beswick EJ, Pinchuk IV, Suarez G, Sierra JC, Reyes VE Helicobacter pylori CagA-dependent macrophage migration inhibitory factor produced by gastric epithelial cells binds to CD74 and stimulates procarcinogenic events. J Immunol. 2006;176: 6794–6801. 16709839

45. Matsumoto Y, Marusawa H, Kinoshita K, Endo Y, Kou T, Morisawa T, et al. Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat Med. 2007;13: 470–476. 17401375

46. Machida K, Cheng KT, Sung VM, Shimodaira S, Lindsay KL, Levine AM, et al. Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes. Proc Natl Acad Sci U S A. 2004;101: 4262–4267. 14999097

47. Ishikawa C, Nakachi S, Senba M, Sugai M, Mori N Activation of AID by human T-cell leukemia virus Tax oncoprotein and the possible role of its constitutive expression in ATL genesis. Carcinogenesis. 2011;32: 110–119. doi: 10.1093/carcin/bgq222 20974684

48. Vieira VC, Leonard B, White EA, Starrett GJ, Temiz NA, Lorenz LD, et al. Human papillomavirus E6 triggers upregulation of the antiviral and cancer genomic DNA deaminase APOBEC3B. MBio. 2014;5: e02234–02214. doi: 10.1128/mBio.02234-14 25538195

49. Rohaly G, Korf K, Dehde S, Dornreiter I Simian virus 40 activates ATR-Delta p53 signaling to override cell cycle and DNA replication control. J Virol. 2010;84: 10727–10747. doi: 10.1128/JVI.00122-10 20686026

50. Terrier O, Marcel V, Cartet G, Lane DP, Lina B, Rosa-Calatrava M, et al. Influenza A viruses control expression of proviral human p53 isoforms p53beta and Delta133p53alpha. J Virol. 2012;86: 8452–8460. doi: 10.1128/JVI.07143-11 22647703

51. Gonzalez E, Rother M, Kerr MC, Al-Zeer MA, Abu-Lubad M, Kessler M, et al. Chlamydia infection depends on a functional MDM2-p53 axis. Nat Commun. 2014;5: 5201. doi: 10.1038/ncomms6201 25392082

52. Siegl C, Prusty BK, Karunakaran K, Wischhusen J, Rudel T Tumor suppressor p53 alters host cell metabolism to Limit Chlamydia trachomatis infection. Cell Rep. 2014;9: 918–929. doi: 10.1016/j.celrep.2014.10.004 25437549

53. Bergounioux J, Elisee R, Prunier AL, Donnadieu F, Sperandio B, Sansonetti P, et al. Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium's epithelial niche. Cell Host Microbe. 2012;11: 240–252. doi: 10.1016/j.chom.2012.01.013 22423964

54. Wu S, Ye Z, Liu X, Zhao Y, Xia Y, Steiner A, et al. Salmonella typhimurium infection increases p53 acetylation in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2010;298: G784–794. doi: 10.1152/ajpgi.00526.2009 20224008

55. Caini S, Gandini S, Dudas M, Bremer V, Severi E, Gherasim A Sexually transmitted infections and prostate cancer risk: a systematic review and meta-analysis. Cancer Epidemiol. 2014;38: 329–338. doi: 10.1016/j.canep.2014.06.002 24986642

56. Vielfort K, Soderholm N, Weyler L, Vare D, Lofmark S, Aro H Neisseria gonorrhoeae infection causes DNA damage and affects the expression of p21, p27 and p53 in non-tumor epithelial cells. J Cell Sci. 2013;126: 339–347. doi: 10.1242/jcs.117721 23108670

57. Logunov DY, Scheblyakov DV, Zubkova OV, Shmarov MM, Rakovskaya IV, Gurova KV, et al. Mycoplasma infection suppresses p53, activates NF-kappaB and cooperates with oncogenic Ras in rodent fibroblast transformation. Oncogene. 2008;27: 4521–4531. doi: 10.1038/onc.2008.103 18408766

58. Menendez D, Shatz M, Resnick MA Interactions between the tumor suppressor p53 and immune responses. Curr Opin Oncol. 2013;25: 85–92. doi: 10.1097/CCO.0b013e32835b6386 23150340