Transcription factor NF-Y induces apoptosis in cells expressing wild-type p53 through E2F1 upregulation and p53 activation

Cancer Research

Volumn 70, Issue 23, 2010, Pages 9711-9720

  Gurtner, Aymone ^a   Fuschi, Paola ^a   Martelli, Fabio ^b   Manni, Isabella ^a   Artuso, Simona ^a   Simonte, Giacoma ^a   Ambrosino, Valeria ^a   Antonini, Annalisa ^b   Folgiero, Valentina ^a   Falcioni, Rita ^a   Sacchi, Ada ^a   Piaggio, Giulia ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; MESSENGER RNA; NUCLEAR FACTOR Y; PROTEIN P53; TRANSCRIPTION FACTOR E2F1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL GROWTH; CELL PROLIFERATION; CLONOGENESIS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CCAAT-BINDING FACTOR; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; E2F1 TRANSCRIPTION FACTOR; EMBRYO, MAMMALIAN; FIBROBLASTS; HCT116 CELLS; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 78649928650     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0721     Document Type: Article

References (48)

1. Mantovani R.The molecular biology of the CCAAT-binding factor NFY. Gene 1999;239:15-27.
2. Linhart C, Elkon R, Shiloh Y, Shamir R. Deciphering transcriptional regulatory elements that encode specific cell cycle phasing by comparative genomics analysis. Cell Cycle 2005;4:1788-97. (Pubitemid 41827326)
3. Bolognese F, Wesner M, Lange-zu Dohna C, Gurtner A, Ronchi A, Muller H, et al. The cyclin B2 promoter depends on NF-Y, a trimer whose CCAAT-binding activity is cell cycle regulated. Oncogene 1999;18:1845-53. (Pubitemid 29145852)
4. Di Agostino S, Strano S, Emiliozzi V, Zerbini V, Mottolese M, Sacchi A, et al. Gain of function of mutant p53: the mutant p53/NF-Y protein complex reveals an aberrant transcriptional mechanism of cell cycle regulation. Cancer Cell 2006;10:191-202. (Pubitemid 44311070)
5. Farina A, Manni I, Fontemaggi G, Tiainen M, Cenciarelli C, Bellorini M, et al. Down-regulation of cyclin B1 gene transcription in terminally differentiated skeletal muscle cells is associated with loss of functional CCAAT-binding NF-Y complex. Oncogene 1999; 18:2818-27. (Pubitemid 29250871)
6. Gurtner A, Manni I, Fuschi P, Mantovani R, Guadagni F, Sacchi A, et al. Requirement for down-regulation of the CCAAT-binding activity of the NF-Y transcription factor during skeletal muscle differentiation. Mol Biol Cell 2003;14:2706-15. (Pubitemid 36871515)
7. Gurtner A, Fuschi P, Magi F, Colussi C, Gaetano C, Dobbelstein M, et al. NF-Y dependent epigenetic modifications discriminate between proliferating and postmitotic tissue. PLoS One 2008;3:e2047. (Pubitemid 352015915)
8. Korner K, Jerome V, Schmidt T, Muller R. Cell cycle regulation of the murine cdc25B promoter: essential role for NF-Y and a proximal repressor element. J Biol Chem 2001;276:9662-9. (Pubitemid 37391861)
9. Zwicher J, Lucibello FC, Wolfraim LA, Gross C, Truss M, Engeland K, et al. Cell cycle regulation of the cyclin A, cdc25C and cdc2 genes is based on a common mechanism of transcriptional repression. EMBO J 1995;14:4514-22.
10. Manni I, Caretti G, Artuso S, Gurtner A, Emiliozzi V, Sacchi A, et al. Posttranslational regulation of NF-YA modulates NF-Y transcriptional activity. Mol Biol Cell 2008;19:5203-13.
11. Grskovic M, Chaivorapol C, Gaspar-Maia A, Li H, Ramalho-Santos M. Systematic identification of cis-regulatory sequences active in mouse and human embryonic stem cells. PLoS Genet 2007;3:e145.
12. Hu Q, Maity SN. Stable expression of a dominant negative mutant of CCAAT binding factor/NF-Y in mouse fibroblast cells resulting in retardation of cell growth and inhibition of transcription of various cellular genes. J Biol Chem 2000;275:4435-44. (Pubitemid 30094687)
13. Bhattacharya A, Deng JM, Zhang Z, Behringer R, de Crombrugghe B, Maity SN. The B subunit of the CCAAT box binding transcription factor complex (CBF/NF-Y) is essential for early mouse development and cell proliferation. Cancer Res 2003;63:8167-72. (Pubitemid 37549464)
14. Imbriano C, Gurtner A, Cocchiarella F, Di Agostino S, Basile V, Gostissa M, et al. Direct p53 transcriptional repression: in vivo analysis of CCAAT-containing G2/M promoters. Mol Cell Biol 2005;25:3737-51. (Pubitemid 40559579)
15. Manni I, Mazzaro G, Gurtner A, Mantovani R, Haugwitz U, Krause K, et al. NF-Y mediates the transcriptional inhibition of the cyclin B1, cyclin B2, and cdc25C promoters upon induced G2 arrest. J Biol Chem 2001;276:5570-6.
16. Yamanaka K, Mizuarai S, Eguchi T, Itadani H, Hirai H, Kotani H. Expression levels of NF-Y target genes changed by CDKN1B correlate with clinical prognosis in multiple cancers. Genomics 2009; 94:219-27.
17. Goodarzi H, Elemento O, Tavazoie S. Revealing global regulatory perturbations across human cancers. Mol Cell 2009;36:900-11.
18. Vermeulen K, Berneman ZN, Van Bockstaele DR. Cell cycle and apoptosis. Cell Prolif 2003;36:165-75.
19. Elkon R, Linhart C, Sharan R, Shamir R, Shiloh Y. Genome-wide in silico identification of transcriptional regulators controlling the cell cycle in human cells. Genome Res 2003;13:773-80. (Pubitemid 36621737)
20. Salsi V, Caretti G, Wasner M, Reinhard W, Haugwitz U, Engeland K, et al. Interactions between p300 and multiple NF-Y trimers govern cyclin B2 promoter function. J Biol Chem 2003;278:6642-50. (Pubitemid 36800650)
21. Sciortino S, Gurtner A, Manni I, Fontemaggi G, Dey A, Sacchi A, et al. The cyclin B1 gene is actively transcribed during mitosis in HeLa cells. EMBO Rep 2001;2:1018-23. (Pubitemid 33130609)
22. Yun J, Chae HD, Choi TS, Kim EH, Bang YJ, Chung J, et al. Cdk2- dependent phosphorylation of the NF-Y transcription factor and its involvement in the p53-p21 signaling pathway. J Biol Chem 2003;278:36966-72. (Pubitemid 37140032)
23. Jin S, Levine AJ. The p53 functional circuit. J Cell Sci 2001;114: 4139-40.
24. Hermeking H, Wolf DA, Kohlhuber F, Dickmanns A, Billaud M, Fanning E, et al. Role of c-myc in simian virus 40 large tumor antigen-induced DNA synthesis in quiescent 3T3-L1 mouse fibroblasts. Proc Natl Acad Sci U S A 1994;91:10412-6. (Pubitemid 24329007)
25. Leone G, Sears R, Huang E, Rempel R, Nuckolls F, Park CH, et al.Myc requires distinct E2F activities to induce S phase and apoptosis. Mol Cell 2001;8:105-13.
26. Johnson DG, Degregori J. Putting the oncogenic and tumor suppressive activities of E2F into context. Curr Mol Med 2006;6:731-8.
27. Kowalik TF, DeGregori J, Schwarz JK, Nevins JR. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J Virol 1995;69:2491-500.
28. Qin XQ, Livingston DM, Kaelin WG Jr, Adams PD. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53- mediated apoptosis. Proc Natl Acad Sci U S A 1994;91:10918-22.
29. Wu X, Levine AJ. p53 and E2F-1 cooperate to mediate apoptosis. Proc Natl Acad Sci U S A 1994;91:3602-6. (Pubitemid 24139478)
30. Macleod K. pRb and E2f-1 in mouse development and tumorigenesis. Curr Opin Genet Dev 1999;9:31-9.
31. Matsumura I, Tanaka H, Kanakura Y. E2F1 and c-Myc in cell growth and death. Cell Cycle 2003;2:333-8.
32. Iaquinta PJ, Lees JA. Life and death decisions by the E2F transcription factors. Curr Opin Cell Biol 2007;19:649-57.
33. Hershko T, Chaussepied M, Oren M, Ginsberg D. Novel link between E2F and p53: proapoptotic cofactors of p53 are transcriptionally upregulated by E2F. Cell Death Differ 2005;12:377-83. (Pubitemid 40520689)
34. Hiebert SW, Packham G, Strom DK, Haffner R, Oren M, Zambetti G, et al. E2F-1:DP-1 induces p53 and overrides survival factors to trigger apoptosis. Mol Cell Biol 1995;15:6864-74.
35. Rogoff HA, Pickering MT, Debatis ME, Jones S, Kowalik TF. E2F1 induces phosphorylation of p53 that is coincident with p53 accumulation and apoptosis. Mol Cell Biol 2002;22:5308-18. (Pubitemid 34755744)
36. Porrello A, Cerone MA, Coen S, Gurtner A, Fontemaggi G, Cimino L, et al. p53 regulates myogenesis by triggering the differentiation activity of pRb. J Cell Biol 2000;151:1295-304.
37. Ruley HE. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature 1983;304:602-6.
38. Kabe Y, Yamada J, Uga H, Yamaguchi Y, Wada T, Handa H. NF-Y is essential for the recruitment of RNA polymerase II and inducible transcription of several CCAAT box-containing genes. Mol Cell Biol 2005;25:512-22. (Pubitemid 40039839)
39. Caretti G, Salsi V, Vecchi C, Imbriano C, Mantovani R. Dynamic recruitment of NF-Y and histone acetyltransferases on cell-cycle promoters. J Biol Chem 2003;278:30435-40. (Pubitemid 36994546)
40. Van Ginkel PR, Hsiao KM, Schjerven H, Farnham PJ. E2F-mediated growth regulation requires transcription factor cooperation. J Biol Chem 1997;272:18367-74.
41. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007;129:823-37. (Pubitemid 46802390)
42. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007;447:407-12.
43. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell 2007;128:707-19.
44. Polager S, Ginsberg D. p53 and E2F: partners in life and death. Nat Rev Cancer 2009;9:738-48.
45. Brosh R, Rotter V. When mutants gain new powers: news from the mutant p53 field. Nat Rev Cancer 2009;9:701-13.
46. Hong S, Paulson QX, Johnson DG. E2F1 and E2F3 activate ATM through distinct mechanisms to promote E1A-induced apoptosis. Cell Cycle. 2008;7:391-400. (Pubitemid 351366503)
47. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003;421:499-506.
48. Martelli F, Hamilton T, Silver DP, Sharpless NE, Bardeesy N, Rokas M, et al. p19ARF targets certain E2F species for degradation. Proc Natl Acad Sci USA 2001;98:4455-60. (Pubitemid 32294998)