A transcriptionally active pRb-E2F1-P/CAF signaling pathway is central to TGFβ-mediated apoptosis

Cell Death and Disease

Volumn 3, Issue 10, 2012, Pages

  Korah, J ^a   Falah, N ^a   Lacerte, A ^a   Lebrun, J J ^a,b  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b ROYAL VICTORIA HOSPITAL   (Canada)

Author keywords

Apoptosis; E2F1; P CAF; pRb; TGF ; Transcriptional regulation

Indexed keywords

HISTONE ACETYLTRANSFERASE PCAF; MULTIPROTEIN COMPLEX; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSFORMING GROWTH FACTOR BETA;

APOPTOSIS; ARTICLE; CANCER CELL; CONTROLLED STUDY; EXPERIMENTAL MODEL; GENE ACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL LINE; E2F1 TRANSCRIPTION FACTOR; HEP G2 CELLS; HUMANS; MICE; MICE, KNOCKOUT; P300-CBP TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; RETINOBLASTOMA PROTEIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84870508046     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2012.146     Document Type: Article

References (42)

1. Massague J. The transforming growth factor-beta family. Annu Rev Cell Biol 1990; 6: 597-641.
2. Pardali K, Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta 2007; 1775: 21-62.
3. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 2000; 19: 1745-1754.
4. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003; 3: 807-821.
5. Ohgushi M, Kuroki S, Fukamachi H, O'Reilly LA, Kuida K, Strasser A et al. Transforming growth factor beta-dependent sequential activation of Smad Bim, and caspase-9 mediates physiological apoptosis in gastric epithelial cells. Mol Cell Biol 2005; 25: 10017-10028.
6. Kim SG, Kim SN, Jong HS, Kim NK, Hong SH, Kim SJ et al. Caspase-mediated Cdk2 activation is a critical step to execute transforming growth factor-beta1-induced apoptosis in human gastric cancer cells. Oncogene 2001; 20: 1254-1265.
7. Jang CW, Chen CH, Chen CC, Chen JY, Su YH, Chen RH. TGF-beta induces apoptosis through Smad-mediated expression of DAP-kinase. Nat Cell Biol 2002; 4: 51-58.
8. Valderrama-Carvajal H, Cocolakis E, Lacerte A, Lee EH, Krystal G, Ali S et al. Activin/TGFbeta induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nat Cell Biol 2002; 4: 963-969.
9. Motyl T, Grzelkowska K, Zimowska W, Skierski J, Wareski P, Ploszaj T et al. Expression of bcl-2 and bax in TGF-beta 1-induced apoptosis of L1210 leukemic cells. Eur J Cell Biol 1998; 75: 367-374.
10. Ramjaun AR, Tomlinson S, Eddaoudi A, Downward J. Upregulation of two BH3-only proteins, Bmf and Bim, during TGF beta-induced apoptosis. Oncogene 2007; 26: 970-981.
11. Lacerte A, Korah J, Roy M, Yang XJ, Lemay S, Lebrun JJ. Transforming growth factor-beta inhibits telomerase through SMAD3 and E2F transcription factors. Cell Signal 2008; 20: 50-59.
12. Dyson N. The regulation of E2F by pRB-family proteins. Genes Dev 1998; 12: 2245-2262.
13. Suzuki T, Yasui W, Yokozaki H, Naka K, Ishikawa T, Tahara E. Expression of the E2F family in human gastrointestinal carcinomas. Int J Cancer 1999; 81: 535-538.
14. Eymin B, Gazzeri S, Brambilla C, Brambilla E. Distinct pattern of E2F1 expression in human lung tumours: E2F1 is upregulated in small cell lung carcinoma. Oncogene 2001; 20: 1678-1687.
15. Wang D, Russell JL, Johnson DG. E2F4 and E2F1 have similar proliferative properties but different apoptotic and oncogenic properties in vivo. Mol Cell Biol 2000; 20: 3417-3424.
16. Yamasaki L, Jacks T, Bronson R, Goillot E, Harlow E, Dyson NJ. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 1996; 85: 537-548.
17. Crosby ME, Almasan A. Opposing roles of E2Fs in cell proliferation and death. Cancer Biol Ther 2004; 3: 1208-1211.
18. Phillips AC, Bates S, Ryan KM, Helin K, Vousden KH. Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev 1997; 11: 1853-1863.
19. Fan G, Ma X, Kren BT, Steer CJ. Unbound E2F modulates TGF-beta1-induced apoptosis in HuH-7 cells. J Cell Sci 2002; 115(Pt 15): 3181-3191.
20. Gatti R, Belletti S, Orlandini G, Bussolati O, Dall'Asta V, Gazzola GC. Comparison of annexin V and calcein-AM as early vital markers of apoptosis in adherent cells by confocal laser microscopy. J Histochem Cytochem 1998; 46: 895-900.
21. Furukawa Y, Nishimura N, Satoh M, Endo H, Iwase S, Yamada H et al. Apaf-1 is a mediator of E2F-1-induced apoptosis. J Biol Chem 2002; 277: 39760-39768.
22. Elliott MJ, Dong YB, Yang H, McMasters KM. E2F-1 up-regulates c-Myc and p14(ARF) and induces apoptosis in colon cancer cells. Clin Cancer Res 2001; 7: 3590-3597.
23. Irwin M, Marin MC, Phillips AC, Seelan RS, Smith DI, Liu W et al. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000; 407: 645-648.
24. Yang HL, Dong YB, Elliott MJ, Liu TJ, McMasters KM. Caspase activation and changes in Bcl-2 family member protein expression associated with E2F-1-mediated apoptosis in human esophageal cancer cells. Clin Cancer Res 2000; 6: 1579-1589.
25. Rogoff HA, Pickering MT, Frame FM, Debatis ME, Sanchez Y, Jones S et al. Apoptosis associated with deregulated E2F activity is dependent on E2F1 and Atm/Nbs1/Chk2. Mol Cell Biol 2004; 24: 2968-2977.
26. Kherrouche Z, Blais A, Ferreira E, De Launoit Y, Monte D. ASK-1 (apoptosis signalregulating kinase 1) is a direct E2F target gene. Biochem J 2006; 396: 547-556.
27. XieW, Jiang P, Miao L, Zhao Y, Zhimin Z, Qing L et al. Novel link between E2F1 and Smac/DIABLO: proapoptotic Smac/DIABLO is transcriptionally upregulated by E2F1. Nucleic Acids Res 2006; 34: 2046-2055.
28. Li JM, Hu PP, Shen X, Yu Y, Wang XF. E2F4-RB and E2F4-p107 complexes suppress gene expression by transforming growth factor beta through E2F binding sites. Proc Natl Acad Sci USA. 1997; 94: 4948-4953.
29. Spender LC, Inman GJ. TGF-beta induces growth arrest in Burkitt lymphoma cells via transcriptional repression of E2F-1. J Biol Chem 2009; 284: 1435-1442.
30. Lukas J, Petersen BO, Holm K, Bartek J, Helin K. Deregulated expression of E2F family members induces S-phase entry and overcomes p16INK4 A-mediated growth suppression. Mol Cell Biol 1996; 16: 1047-1057.
31. Itoh S, Ericsson J, Nishikawa J, Heldin CH, ten Dijke P. The transcriptional co-activator P/CAF potentiates TGF-beta/Smad signaling. Nucleic Acids Res 2000; 28: 4291-4298.
32. Nahle Z, Polakoff J, Davuluri RV, McCurrach ME, Jacobson MD, Narita M et al. Direct coupling of the cell cycle and cell death machinery by E2F. Nat Cell Biol 2002; 4: 859-864.
33. Ianari A, Natale T, Calo E, Ferretti E, Alesse E, Screpanti I et al. Proapoptotic function of the retinoblastoma tumor suppressor protein. Cancer Cell 2009; 15: 184-194.
34. Lin WC, Lin FT, Nevins Jr. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev 2001; 15: 1833-1844.
35. Martinez-Balbas MA, Bauer UM, Nielsen SJ, Brehm A, Kouzarides T. Regulation of E2F1 activity by acetylation. EMBO J 2000; 19: 662-671.
36. Wang B, Liu K, Lin FT, Lin WC. A role for 14-3-3 tau in E2F1 stabilization and DNA damage-induced apoptosis. J Biol Chem 2004; 279: 54140-54152.
37. Hofmann F, Martelli F, Livingston DM, Wang Z. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev 1996; 10: 2949-2959.
38. Laiho M, DeCaprio JA, Ludlow JW, Livingston DM, Massague J. Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell 1990; 62: 175-185.
39. Dick FA, Dyson N. pRB contains an E2F1-specific binding domain that allows E2F1-induced apoptosis to be regulated separately from other E2F activities. Mol Cell 2003; 12: 639-649.
40. Iavarone A, Massague J. E2F and histone deacetylase mediate transforming growth factor beta repression of cdc25A during keratinocyte cell cycle arrest. Mol Cell Biol 1999; 19: 916-922.
41. Chen CR, Kang Y, Siegel PM, Massague J. E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 2002; 110: 19-32.
42. Frederick JP, Liberati NT, Waddell DS, Shi Y, Wang XF. Transforming growth factor betamediated transcriptional repression of c-myc is dependent on direct binding of Smad3 to a novel repressive Smad binding element. Mol Cell Biol 2004; 24: 2546-2559.