P53-paralog DNp73 oncogene is repressed by IFNα/STAT2 through the recruitment of the Ezh2 polycomb group transcriptional repressor

Oncogene

Volumn 30, Issue 23, 2011, Pages 2670-2678

  Testoni, B ^a   Schinzari, V ^a,b   Guerrieri, F ^a,b   Gerbal Chaloin, S ^b   Blandino, G ^a   Levrero, M ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b INSERM   (France)

Author keywords

apoptosis; chromatin dynamics; epigenetics; p53 family; transcription

Indexed keywords

ALPHA INTERFERON; HISTONE DEACETYLASE; INTERFERON STIMULATED GENE FACTOR 3; STAT2 PROTEIN; TRANSCRIPTION FACTOR EZH2;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; DRUG ACTIVITY; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL CARCINOMA; ONCOGENE; ONCOGENE DNP73; PRIORITY JOURNAL;

BINDING SITES; BLOTTING, WESTERN; CELL LINE, TUMOR; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; COLONIC NEOPLASMS; DNA-BINDING PROTEINS; FEMALE; HEP G2 CELLS; HEPATOCYTES; HISTONES; HUMANS; INTERFERON-ALPHA; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; METHYLATION; MIDDLE AGED; MUTATION; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 79958279832     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.635     Document Type: Article

References (48)

1. Belloni L, Moretti F, Merlo P, Damalas A, Costanzo A, Blandino G et al. (2006). DNp73 protects myogenic cells from apoptosis. Oncogene 25: 3606-3612. (Pubitemid 43901682)
2. Breitenstein S, Dimitroulis D, Petrowsky H, Puhan MA, Mullhaupt B, Clavien PA. (2009). Systematic review and meta-analysis of interferon after curative treatment of hepatocellular carcinoma in patients with viral hepatitis. Br J Surg 96: 975-981.
3. Caretti G, Di Padova M, Micales B, Lyons GE, Sartorelli V. (2004). The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev 18: 2627-2638. (Pubitemid 39453102)
4. Chattopadhyay D, Manas DM, Reeves HL. (2007). The development of targeted therapies for hepatocellular cancer. Curr Pharm Des 13: 3292-3300. (Pubitemid 350201684)
5. Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC, Silverman RH et al. (2003). Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8: 237-249. (Pubitemid 36749609)
6. Crax A, Camma C (2005). Prevention of hepatocellular carcinoma. Clin Liver Dis, 9, 329-346.
7. El-Serag HB, Rudolph KL. (2007). Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132: 2557-2576. (Pubitemid 46890874)
8. Fattovich G, Stroffolini T, Zagni I, Donato F. (2004). Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 127: S35-S50. (Pubitemid 39423368)
9. Fu XY, Kessler DS, Veals SA, Levy DE, Darnell Jr JE. (1990). ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc Natl Acad Sci USA 87: 8555-8559.
10. Fujioka N, Ariyasu T, Arai N, Ariyasu H, Yamamoto S, Tanimoto T et al. (2006). Role of p53 in the inhibitory effects of interferon-asubtypes on proliferation of hepatocellular carcinoma cells. Biomed Res 27: 219-226. (Pubitemid 44768650)
11. Herzer K, Hofmann TG, Teufel A, Schimanski C, Moeler M, Kanzler S et al. (2009). IFNa-induced apoptosis in hepatocellular carcinoma involves promyelocytic leukemia protein and TRAIL independently of p53. Cancer Res 69: 855-862.
12. Ji J, Shi J, Budhu A, Yu Z, Forgues M, Roessler S. et al. (2009). MicroRNA expression, survival, and response to interferon in liver cancer. N Engl J Med 361: 1437-1447.
13. Keskinen P, Nyqvist M, Sareneva T, Pirhonen J, Melen K, Julkunen I. (1999). Impaired antiviral response in human hepatoma cells. Virology 263: 364-375. (Pubitemid 29521528)
14. Kessler DS, Levy DE, Darnell Jr JE. (1988). Two interferon-induced nuclear factors bind a single promoter element in interferon-stimulated genes. Proc Natl Acad Sci USA 85: 8521-8525. (Pubitemid 19024993)
15. Leung S, Qureshi SA, Kerr IM, Darnell Jr JE, Stark GR. (1995). Role of Stat2 in the alpha interferon signaling pathway. Mol Cell Biol 15: 1312-1317.
16. Levrero M. (2006). Viral hepatitis and liver cancer: the case of hepatitis C. Oncogene 25: 3834-3847. (Pubitemid 43980479)
17. Levrero M, De Laurenzi V, Costanzo A et al. (2000). The p53/p63/p73 family of transcription factors: overlapping and distinct functions. J Cell Sci 113: 1661-1670. (Pubitemid 30333115)
18. Levy DE, Darnell JE Jr. (2002). Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3: 651-662. (Pubitemid 34987786)
19. Lim R, Knight B, Patel K, McHutchison JG, Yeoh GC, Olynyk JK. (2006). Antiproliferative effects of interferon alpha on hepatic progenitor cells in vitro and in vivo. Hepatology 43: 1074-1083. (Pubitemid 43724631)
20. Lok AS, Seeff LB, Morgan TR, di Bisceglie AM, Sterling RK, Curto TM et al. (2009). Incidence of hepatocellular carcinoma and associated risk factors in hepatitis C-related advanced liver disease. Gastroenterology 136: 138-148.
21. Lunghi P, Costanzo A, Mazzera L, Rizzoli V, Levrero M, Bonati A. (2009). The p53 family protein p73 provides new insights into cancer chemosensitivity and targeting. Clin Cancer Res 5: 6495-6502.
22. Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury III WJ et al. (2009). Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461: 762-767.
23. Melen K, Keskinen P, Lehtonen A, Julkunen I. (2000). Interferon-induced gene expression and signaling in human hepatoma cell lines. J Hepatol 33: 764-772.
24. Melino G, De Laurenzi V, Vousden KH. (2002). p73: Friend or foe in tumorigenesis. Nat Rev Cancer 2: 605-615. (Pubitemid 37328927)
25. Miyake Y, Takaki A, Iwasaki Y, Yamamoto K. (2010). Meta-analysis: interferon-alpha prevents the recurrence after curative treatment of hepatitis C virus-related hepatocellular carcinoma. J Viral Hepat 17: 287-292.
26. Montgomery ND, Yee D, Chen A, Kalantry S, Chamberlain SJ, Otte AP et al. (2005). The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol 24: 942-947. (Pubitemid 40772064)
27. Moradpour D, Blum HE. (2005). Pathogenesis of hepatocellular carcinoma. Eur J Gastroenterol Hepatol 17: 477-483. (Pubitemid 40592703)
28. Mu+ller M, Schilling T, Sayan AE, Kairat A, Lorenz K, Schulze-Bergkamen H et al. (2005). Tap73/DeltaNp73 influences apoptotic response, chemosensitivity and prognosis in hepatocellular carcinoma. Cell Death Differ 12: 1564-1577. (Pubitemid 41679162)
29. Nakaji M, Yano Y, Ninomiya T, Seo Y, Hamano K, Yoon S et al. (2004). IFN-alpha prevents the growth of pre-neoplastic lesions and inhibits the development of hepatocellular carcinoma in the rat. Carcinogenesis 25: 389-397. (Pubitemid 38344406)
30. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. (1991). A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 139: 271-279.
31. Noguchi R, Yoshjij H, Ikenaka Y, Kitade M, Kaji K, Yoshi J et al. (2008). Different tumoricidal effects of interferon subclasses and p53 status on hepatocellular carcinoma development and neovascular-isation. Int J Oncol 32: 193-199. (Pubitemid 351176078)
32. Obi S, Yoshida H, Toune R, Unuma T, Kanda M, Sato S et al. (2006). Combination therapy of intraarterial 5-fluorouracil and systemic interferon-alpha for advanced hepatocellular carcinoma with portal venous invasion. Cancer 106: 1990-1997. (Pubitemid 43673215)
33. Pestka S, Krause CD, Walter MR. (2004). Interferons, interferon-like cytokines and their receptors. Immunol Rev 202: 8-32. (Pubitemid 39576902)
34. Pichard-Garcia L, Gerbal-Chaloin S, Ferrini JB, Fabre JM, Maurel P. (2002). Use of long-term cultures of human hepatocytes to study cytochrome P450 gene expression. Methods Enzymol 357: 311-321. (Pubitemid 35231367)
35. Radaeva S, Jaruga B, Hong F, Kim WH, Fan S, Cai H et al. (2002). Interferon-alpha activates multiple STAT signals and down-regulates c-Met in primary human hepatocytes. Gastroenterology 122: 1020-1034. (Pubitemid 34267285)
36. Shiratori Y, Ito Y, Yokosuka O, Imazeki F, Nakata R, Tanaka N et al. (2005). Antiviral therapy for cirrhotic hepatitis C: association with reduced hepatocellular carcinoma development and improved survival. Ann Intern Med 142: 105-114.
37. Steele JC, Torr EE, Noakes KL, Kalk E, Moss PA, Reynolds GM et al. (2006). The polycomb group proteins, BMI-1 and EZH2, are tumour-associated antigens. Br J Cancer 95: 1202-1211. (Pubitemid 44658484)
38. Stiewe T. (2007). The p53 family in differentiation and tumorigenesis. Nat Rev Cancer 7: 165-168.
39. Stiewe T, Tuve S, Peter M, Tannapfel A, Elmaagacli AH, Putzer BM. (2004). Quantitative TP73 transcript analysis in hepatocellular carcinomas. Clin Cancer Res 10: 626-633. (Pubitemid 38174002)
40. Sudo T, Utsunomiya T, Mimori K, Nagahara H, Ogawa K, Inoue H et al. (2005). Clinicopathological significance of EZH2 mRNA expression in patients with hepatocellular carcinoma. Br J Cancer 92: 1754-1758. (Pubitemid 40756488)
41. Testoni B, Borrelli S, Tenedini E, Alotto D, Castagnoli C, Piccolo S et al. (2006). Identification of new p63 targets in human keratinocytes. Cell Cycle 5: 2805-2811. (Pubitemid 44901743)
42. Testoni B, Voellenkle C, Guerrieri F, Gerbal-Chaloin S, Blandino G, Levrero M. Chromatin dynamics of gene activation and repression in response to IFNa reveal new roles for STAT2 and P-STAT2 (submitted).
43. Uddin S, Platanias LC. (2004). Mechanisms of Type-I interferon signal transduction. J Biochem Mol Biol 37: 635-641. (Pubitemid 40221522)
44. Uka K, Aikata H, Mori N, Takaki S, Kawakami Y, Azakami T et al. (2008). Combination therapy of oral fluoropyrimidine anticancer drug S-1 and interferon alpha for HCC patients with extrahepatic metastases. Oncology 75: 8-16.
45. Van der Vlag J, Otte AP. (1999). Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation. Nat Genet 23: 474-478.
46. Vossio S, Palescandolo E, Pediconi N, Moretti F, Balsano C, Levrero M et al. (2002). DNp73 is activated after DNA damage in a p53-dependent manner to regulate p53-induced cell cycle arrest. Oncogene 21: 3796-3803. (Pubitemid 34620543)
47. Xu D, Erickson S, Szeps M, Gruber A, Sangfelt O, Einhorn S et al. (2000). Interferon alpha down-regulates telomerase reverse transcriptase and telomerase activity in human malignant and nonmalignant hematopoietic cells. Blood 96: 4313-4318.
48. Yonemitsu Y, Imazeki F, Chiba T, Fukai K, Nagai Y, Miyagi S et al. (2009). Distinct expression of polycomb group proteins EZH2 and BMI1 in hepatocellular carcinoma. Hum Pathol 40: 1304-1311.