A balance between NF-Y and p53 governs the pro- and anti-apoptotic transcriptional response

Nucleic Acids Research

Volumn 36, Issue 5, 2008, Pages 1415-1428

  Benatti, Paolo ^a   Basile, Valentina ^a,b   Merico, Daniele ^b   Fantoni, Luca Isaia ^a   Tagliafico, Enrico ^a   Imbriano, Carol ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CASPASE 3; CASPASE 7; CASPASE 8; CCAAT BINDING FACTOR; DNA; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HISTONE; MESSENGER RNA; NUCLEAR FACTOR Y; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P53; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL STRAIN HCT116; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME DEGRADATION; FLOW CYTOMETRY; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FAMILY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASES; CCAAT-BINDING FACTOR; CELL CYCLE; CELL LINE, TUMOR; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; HUMANS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 41149094081     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm1046     Document Type: Article

References (60)

1. Bucher,P. (1990) Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol., 212, 563-578.
2. Suzuki,Y., Tsunoda,T., Sese,J., Taira,H., Mizushima-Sugano,J., Hata,H., Ota,T., Isogai,T., Tanaka,T. et al. (2001) Identification and characterization of the potential promoter regions of 1031 kinds of human genes. Genome Res., 11, 677-684.
3. Maity,S.N. and de Crombrugghe,B. (1998) Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem. Sci., 23, 174-178.
4. Mantovani,R. (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene, 239, 15-27.
5. McNabb,D.S., Xing,Y. and Guarente,L. (1995) Cloning of yeast HAP5: A novel subunit of a heterotrimeric complex required for CCAAT binding. Genes Dev., 9, 47-58.
6. Sinha,S., Maity,S.N., Lu,J. and de Crombrugghe,B. (1995) Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. Proc. Natl Acad. Sci. USA, 92, 1624-1628.
7. Romier,C., Cocchiarella,F., Mantovani,R. and Moras,D. (2003) The NF-YB/ NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. J. Biol. Chem., 278, 1336-1345.
8. Li,Q., Herrler,M., Landsberger,N., Kaludov,N., Ogryzko,V.V., Nakatani,Y. and Wolffe,A.P. (1998) Xenopus NF-Y pre-sets chromatin to potentiate p300 and acetylation-responsive transcription from the Xenopus hsp70 promoter in vivo. EMBO J., 17, 6300-6315.
9. Caretti,G., Motta,M.C. and Mantovani,R. (1999) NF-Y associates with H3-H4 tetramers and octamers by multiple mechanisms. Mol. Cell Biol. 19, 8591-8603.
10. Huet,X., Rech,J., Plet,A., Vie,A. and Blanchard,J.M. (1996) Cyclin A expression is under negative transcriptional control during the cell cycle. Mol. Cell Biol., 16, 3789-3798.
11. van Ginkel,P.R., Hsiao,K.M., Schjerven,H. and Farnham,P.J. (1997) E2F-mediated growth regulation requires transcription factor cooperation. J. Biol. Chem., 272, 18367-18374.
12. Bolognese,F., Wasner,M., Dohna,C.L., Gurtner,A., Ronchi,A., Muller,H., Manni,I., Mossner,J., Piaggio,G. et al. (1999) The cyclin B2 promoter depends on NF-Y, a trimer whose CCAAT-binding activity is cell-cycle regulated. Oncogene, 18, 1845-1853.
13. Farina,A., Manni,I., Fontemaggi,G., Tiainen,M., Cenciarelli,C., Bellorini,M., Mantoyani,R. and Piaggio,G. (1999) Down-regulation of cyclin B1 gene transcription in terminally 26 differentiated skeletal muscle cells is associated with loss of functional CCAAT-binding NF-Y complex. Oncogene, 18, 2818-2817.
14. Yun,J., Chae,H.D.,, Choy,H.E., Chung,J., Yoo,H.S., Han,M.H. and Shin,D.Y. (1999) p53 negatively regulates cdc2 transcription via the CCAAT-binding NF-Y transcription factor. J. Biol. Chem., 274 29677-29682.
15. Jung,M.S., Yun,J., Chae,H.D., Kim,J.M., Kim,S.C., Choi,T.S. and Shin,D.Y. (2001) p53 and its homologues, p63 and p71, induce a replicative senescence through inactivation of NF-Y transcription factor. Oncogene, 20, 5818-5825.
16. Manni,I., Mazzaro,G., Gurtner,A., Mantovani,R., Haugwitz,U., Krause,K., Engeland,K., Sacchi,A., Soddu,S. et al. (2001) NF-Y mediates the transcriptional inhibition of the cyclin B1, cyclin B2, and cdc25C promoters upon induced G2 arrest. J.Biol. Chem., 276, 5570-5576.
17. Elkon,R., Linhart,C., Sharan,R., Shamir,R. and Shiloh,Y. (2003) Genome-wide in silico identification of transcriptional regulatros controlling the cell cycle in human cells. Genome Res., 13, 773-780.
18. Caretti,G., Salsi,V., Vecchi,C., Imbriano,C. and Mantovani,R. (2003) Dynamic recruitment of NF-Y and histone acetyltransferases on cell-cycle promoters. J. Biol. Chem., 278, 30435-30440.
19. Li,X.Y., Hooft van Huijsduijnen,R., Mantovani,R., Benoist,C and Mathis,D. (1992) Intron-exon organization of the NF-Y genes. Tissue-specific splicing modifies an activation domain. J. Biol. Chem., 267, 8984-8990.
20. Frontini,M., Imbriano,C., Manni,I. and Mantovani,R. (2004) Cell cycle regulation of NF-YC nuclear localization. Cell Cycle, 3, 217-222.
21. Gurtner,A., Manni,I., Fuschi,P., Mantovani,R., Guadagni,F., Sacchi,A. and Piaggio,G. (2003) Requirement for down-regulation of the CCAAT binding activity of the NF-Y transcription factor during skeletal muscle differentiation. Mol. Biol. Cell, 14, 12706-12715.
22. Yun,J., Chae,H.D., Choi,T.S., Kim,E.H., Bang,Y.J., Chung,J., Choi,K.S., Mantovani,R. and Shin,D.Y. (2003) Cdk2-dependent phosphorylation of the NF-Y transcription factor and its involvement in the p53-p21 signaling pathway. J. Biol. Chem., 278, 36966-36972.
23. Adachi,N., Nomoto,M., Kohno,K. and Koyama,H. (2000) Cell-cycle regulation of the DNA topoisomerase IIalpha promoter is mediated by proximal CCAAT boxes: Possible involvement of acetylation. Gene, 245, 49-57.
24. Imbriano,C., Gurtner,A., Cocchiarelia,F., Di Agostino,S., Basile,V., Gostissa,M., Dobbelstein,M., Del Sal,G., Piaggio,G. et al. (2005) Direct p53 transcriptional repression: In vivo analysis of CCAAT-containing G2/M promoters. Mol. Cell Biol., 25, 3737-3751.
25. Di Agostino,S., Strano,S., Emiliozzi,V., Zerbini,V., Mottolese,M., Sacchi,A., Blandino,G. and Piaggio,G. (2006) Gain of function of mutant p53: The mutant p53/NF-Y protein complex reveals an aberrant transcriptional mechanism of cell cycle regulation. Cancer Cell, 10, 191-202.
26. Peart,M.J. and Prives,C. (2006) Mutant p53 gain of function: The NF-Y connection. Cancer Cell, 10, 173-174.
27. Tabach,Y., Milyavsky,M., Shats,I., Brosh,R., Zuk,O., Yitzhaky,A., Mantovani,R., Domany,E., Rotter,V. et al. (2005) The promoters of human cell cycle genes integrate signals from two tumor suppressive pathways during cellular transformation. Mol. Syst. Biol., 1 1-15.
28. Bhattacharya,A., Deng,J. M., Zhang,Z., Behringer,R., de Crombrugghe,B. and Maity,S.N. (2003) 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., 63, 8167-8172.
29. Hu,Q. and Maity,S. N. (2000) Stable expression of a dominant negative mutant pf CBF/NF-Y in mouse fibroblast cells resulting in retardation of cell growth and iphibition of transtription of various cellular genes. J. Biol. Chem., 275, 4435-4444.
30. Basile,V., Mantovani,R. and Imbriano,C. (2006) DNA damage promotes histone deacetylase 4 nuclear localization and repression of G2/M promoters, via p53 C-terminal lysines. J. Biol. Chem., 281, 2347-2357.
31. Tagliafico,E., Tenedini,E., Manfredini,R., Grande,A., Ferrari,F., Roncaglia,E., Bicciato,S., Zini,R., Salati,S. et al. (2006) Identification of a molecular signature predictive of sensitivity to differentiation induction in acute myeloid leukemia. Leukemia, 20, 1751-1758.
32. Tusher,V.G., Tibshirani,R. and Chu,G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl Acad. Sci. USA, 98, 5116-5121.
33. Ceribelli,M., Alcalay,M., Vigano,M.A. and Mantovani,R. (2006) Repression of new p53 targets revealed by ChIP on chip experiments. Cell Cycle 5, 1102-1110.
34. Shieh,S.-Y., Ikeda,M., Taya,Y. and Prives,C. (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell, 91 325-334.
35. Tibbetts,R.S., Brumbaugh,K.M., Williams,J.M., Sarkaria,J.N., Cliby,W.A., Shich,S., Taya,Y., Prives,C. and Abraham,R.T. (1999) A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev., 13 152-157.
36. Mantovani,R., Li,X.Y., Pessara,U., Hooft van Huisjduijnen,R., Benoist,C. and Mathis,D. (1994) Dominant negative analogs of NF-YA. J. Biol. Chem., 269, 20340-20346.
37. Scheffner,M., Huibregtse,J.M., Vierstra,R.D. and Howley,P.M. (1993) The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell, 75, 495-505.
38. Huibregtse,J.M., Scheffner,M. and Howley,P.M. (1993a) Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol. Cell Biol., 13, 775-784.
39. Huibregtse,J.M., Scheffner,M. and Howley,P.M. (1993b) Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol. Cell Biol., 13, 4918-4927.
40. Werness,B.A., Levine,A.J. and Howley,P.M. (1990) Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science, 248, 76-79.
41. Zhu,Z., Shendure,J. and Church,G.M. (2006) Discovering functional transcription factors combinations in the human cell cycle. Genome Res., 15, 848-855.
42. Zwicker,J., Gross,C., Lucibello,F.C., Truss,M., Ehlert,F., Engeland,K. and Muller,R. (1995) Cell cycle regulation of cdc25C transcription is mediated by the periodic repression of the glutamine-rich activators NF-Y and Spl. Nucleic Acid Res., 23, 3822-3830.
43. Zwicker,J., Lucibello,F.C., Wolfraim,L.A., Gross,C., Truss,M., Engeland,K. and Muller,R. (1995) Cell cycle regulation of the cyclin A, cdc25C and cdc2 genes is based on a common mechanism of transcriptional repression. EMBO J., 14, 4514-4522.
44. Hu,Q., Lu,J.F., Luo,R., sen,S., and Maity,S.N. (2006) Inhibition of CBF/ NF-Y midiated transcription activation arrests cells at G/M phase and suppresses expression of genes activated at G2/M phase of the cell cycle. Nucleic Acid Res., 34, 6272-6285.
45. Marziali,G., Perrotti,E., Ilari,R., Coccia,E.M., Mantovani,R., Testa,U. and Battistini,A. (1999) The activity of the CCAAT-box binding factor NF-Y is modulated through the regulated expression of its A subunit during monocyte to macrophage differentiation: Regulation of tissue-specific genes through a ubiquitous transcription factor. Blood, 93, 519-526.
46. Chang,Z.F., Huang,D.Y. and Hu,S.F. (1999) NF-Y-mediated trans-activation of the human thymidine kinase promoter is closely linked to activation of cyclin-dependent kinase. Mol. Cell Biochem., 75, 300-309.
47. Good,L.F. and Chen,K.Y. (1996) Cell cycle- and age-dependent transcriptional regulation of human thymidine kinase gene: The role of NF-Y in the CBP/tk binding complex. Biol. Signals, 5, 163-169.
48. Brooks,C.L. and Gu,W. (2003) Ubiquitination, phosphorylation and acetylation: The molecular basis for p53 regulation. Curr. Opin. Cell Biol., 15, 164-171.
49. Donati,G., Imbriano,C. and Mantovani,R. (2006) Dynamic recruitment of transcription factors and epigenetic changes on the ER stress response gene promoters. Nucleic Acids Res., 34, 3116-3127.
50. Bourdon,J.C., De Laurenzi, V., Melino,G. and Lane,D. (2003) p53: 25 years of research and more questions to answer. Cell Death Diff., 10, 397-399.
51. Miyashita,T. and Reed,J.C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell, 80, 293-299.
52. Nakano,K. and Vousden,K.H. (2001) PUMA, a novel proapoptotic gene, is induced by p53, Mol. Cell, 7, 683-694.
53. Oda,E., Ohki,R., Murasawa,H., Nemoto,J., Shibue,T., Yamashita,T., Tokino,T., Tanikuchi,T. and Tanaka,N. (2000a) Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science, 288, 1053-1058.
54. Oda,K., Arakawa,H., Tanaka,T., Matsuda,K., Tanikawa,C., Mori,T., Nishimori,H., Tamai,K., Tokino,T. el al. (2000) p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell, 102, 849-862.
55. Owen-Schaub,L.B,, Zhang,W., Cusack,J.C., Angelo,L.S., Santee,S.M., Fujiwara,T., Roth,J.A., Deisseroth,A.B., Zhang,W.W. et al. (1995) Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol. Cell Biol., 15, 3032-3040.
56. Miyashita,T., Krajewski,S., Krajewyska,M., Wang,H.G., Lin,H.K., Liebermann,D.A., Hoffman,B. and Reed,J.C. (1994) Tumor suppresor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene, 9, 1799-1805.
57. Letai,A., Bassik,M.C., Walensky,L.D., Sorcinelli,M.D., Weiler,S. and Korsmeyer,S.J. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell, 2, 183-192.
58. Budihardjo, I., Oliver,H., Lutter,M., Luo,X. and Wang,X. (1999) Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol., 15, 269-290.
59. Wang,X. (2001) The expanding role of mitochondria in apoptosis. Genes Dev, 15, 2922-2933.
60. Melino,G., Bernassola,F., Ranalli,M., Yee,K., Zong,W.X., Corzzari,M., Knight,R.A., Green,D.R., Thompson,C. et al. (2004) p73 induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. J. Biol. Chem., 279, 8076-8083.