Transcriptional repression by p53 promotes a Bcl-2-insensitive and mitochondria-independent pathway of apoptosis

Nucleic Acids Research

Volumn 32, Issue 15, 2004, Pages 4480-4490

  Godefroy, Nelly ^b   Bouleau, Sylvina ^b   Gruel, Gaëtan ^a   Renaud, Flore ^b   Rincheval, Vincent ^b   Mignotte, Bernard ^b   Tronik Le Roux, Diana ^a   Vayssière, Jean Luc ^b  

^a DIF   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; COMPLEMENTARY DNA; PROTEIN BCL 2; PROTEIN P53; BENZYLOXYCARBONYLVALYL ALANYL ASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLVALYL-ALANYL-ASPARTYL FLUOROMETHYL KETONE; CYSTEINE PROTEINASE INHIBITOR; PEPTIDE CHLOROMETHYL KETONE; REPRESSOR PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA MICROARRAY; EMBRYO; ENZYME INHIBITION; FIBROBLAST; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; MITOCHONDRION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA HYBRIDIZATION; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; WESTERN BLOTTING; ANIMAL; CELL LINE; DRUG ANTAGONISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; CASPASES; CELL LINE; CYSTEINE PROTEINASE INHIBITORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 4344599150     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh773     Document Type: Article

References (54)

1. Vogelstein,B., Lane,D. and Levine,A.J. (2000) Surfing the p53 network. Nature, 408, 307-310.
2. Momand,J., Wu,H.H. and Dasgupta,G. (2000) MDM2 - master regulator of the p53 tumor suppressor protein. Gene, 242, 15-29.
3. 2/M cell cycle checkpoint. Proc. Natl Acad. Sci. USA, 96, 3706-3711.
4. 2 arrest in the Xenopus oocyte: a role for 14-3-3-mediated inhibition of Cdc25 nuclear import. EMBO J., 18, 2174-2183.
5. Wu,G.S., Burns,T.F., McDonald,E.R.,III, Jiang,W., Meng,R., Krantz,I.D., Kao,G., Gan,D.D., Zhou,J.Y., Muschel,R., Hamilton,S.R., Spinner,N.B., Markowitz,S., Wu,G. and el-Deiry,W.S. (1997) KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nature Genet., 17, 141-143.
6. Oda,E., Ohki,R., Murasawa,H., Nemoto,J., Shibue,T., Yamashita,T., Tokino,T., Taniguchi,T. and Tanaka,N. (2000) Noxa, a BH3-only member of the bcl-2 family and candidate mediator of p53-induced apoptosis. Science, 288, 1053-1058.
7. Oda,K., Arakawa,H., Tanaka,T., Matsuda,K., Tanikawa,C., Mori,T., Nishimori,H., Tamai,K., Tokino,T., Nakamura,Y. and Taya,Y. (2000) p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell, 102, 849-862.
8. Haupt,Y., Rowan,S., Shaulian,E., Kazaz,A., Vousden,K. and Oren,M. (1997) p53 mediated apoptosis in HeLa cells: transcription dependent and independent mechanisms. Leukemia, 11 (Suppl. 3), 337-339.
9. Caelles,C., Helmberg,A. and Karin,M. (1994) p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature, 370, 220-223.
10. Wagner,A.J., Kokontis,J.M. and Hay,N. (1994) Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21waf1/cip1. Genes Dev., 8, 2817-2830.
11. Seto,E., Usheva,A., Zambetti,G.P., Momand,J., Horikoshi,N., Weinmann,R., Levine,A.J. and Shenk,T. (1992) Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc. Natl Acad. Sci. USA, 89, 12028-12032.
12. Sabbatini,P., Chiou,S.K., Rao,L. and White,E. (1995) Modulation of p53-mediated transcriptional repression and apoptosis by the adenovirus E1B 19K protein. Mol. Cell. Biol., 15, 1060-1070.
13. Ahn,J., Murphy,M., Kratowicz,S., Wang,A., Levine,A.J. and George,D.L. (1999) Down-regulation of the stathmin/Op18 and FKBP25 genes following p53 induction. Oncogene, 18, 5954-5958.
14. Zhai,W. and Comai,L. (2000) Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol. Cell. Biol., 20, 5930-5938.
15. Koumenis,C., Alarcon,R., Hammond,E., Sutphin,P., Hoffman,W., Murphy,M., Derr,J., Taya,Y., Lowe,S.W., Kastan,M. and Giaccia,A. (200 1) Regulation of p53 by hypoxia: dissociation of transcriptional repression and apoptosis from p53-dependent transactivation. Mol. Cell. Biol., 21, 1297-1310.
16. May,P. and May,E. (1999) Twenty years of p53 research: structural and functional aspects of the p53 protein. Oncogene, 18, 7621-7636.
17. Johnson,R.A., Ince,T.A. and Scotto,K.W. (2001) Transcriptional repression by p53 through direct binding to a novel DNA element.J. Biol. Chem., 276, 27716-27720.
18. Ding,H.F., Lin,Y.L., McGill,G., Juo,P., Zhu,H., Blenis,J., Yuan,J. and Fisher,D.E. (2000) Essential role for caspase-8 in transcription-independent apoptosis triggered by p53. J. Biol. Chem., 275, 38905-38911.
19. Marchenko,N.D., Zaika,A. and Moll,U.M. (2000) Death signal-induced localization of p53 protein to mitochondria.J. Biol. Chem., 275, 16202-16212.
20. Zheng,D.Q., Vayssière,J.L., Lecoeur,H., Petit,P.X., Spatz,A., Mignotte,B. and Feunteun,J. (1994) Apoptosis is antagonized by large T antigens in the pathway to immortalization by polyomaviruses. Oncogene, 9, 3345-3351.
21. Vayssière,J.L., Petit,P.X., Risler,Y. and Mignotte,B. (1994) Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with Simian Virus 40. Proc. Natl Acad. Sci. USA, 91, 11752-11756.
22. Rincheval,V., Renaud,F., Lemaire,C., Mignotte,B. and Vayssière,J.L. (1999) Inhibition of Bcl-2-dependent cell survival by a caspase inhibitor: a possible new pathway for Bcl-2 to regulate cell death. FEBS Lett., 460, 203-206.
23. Godefroy,N., Lemaire,C., Renaud,F., Rincheval,V., Perez,S., Parvu-Ferecatu,I., Mignotte,B. and Vayssière,J.L. (2004) p53 can promote mitochondria- and caspase-independent apoptosis. Cell Death Differ., 11, 785-787.
24. Mathiaen,I.S. and Jaattela,M. (2002) Triggering caspase-independent cell death to combat cancer. Trends Mol. Med., 8, 212-220.
25. Gozuacik,D. and Kimchi,A. (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene, 23, 2891-2906.
26. Petit,C.A., Gardes,M.Y. and Feunteun,J. (1983) Immortalization of rodent embryo fibroblast by SV40 is maintained by the A gene. Virology, 127, 74-82.
27. Guénal,I., Sidoti-de Fraisse,C., Gaumer,S. and Mignotte,B. (1997) Bcl-2 and Hsp27 act at different levels to suppress programmed cell death. Oncogene, 15, 347-360.
28. Towbin,H., Staehelin,T. and Gordon,J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354.
29. Chirgwin,J.M., Przybyla,A.E., Mac Donald,R.J. and Rutter,W.J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry, 18, 5294-5299.
30. Renaud,F., Desset,S., Oliver,L., Gimenez-Gallego,G., Van Obberghen,E., Courtois,Y. and Laurent,M. (1996) The neurotrophic activity of fibroblast growth factor 1 (FGF1) depends on endogenous FGF1 expression and is independent of the mitogen-activated protein kinase cascade pathway. J. Biol. Chem., 271, 2801-2811.
31. Preisser,L., Houot,L., Teillet,L., Kortulewski,T., Morel,A., Tronik-Le Roux,D. and Corman,B. (2004) Gene expression in aging kidney and pituitary. Biogerontology, 5, 39-47.
32. Delmar,P., Robin,S., Tronik-Le Roux,D. and Daudin,J.J. (2004) Mixture model on the variance for the differential analysis of gene expression data. J. R. Stat. Soc., Ser. C Appl. Stat., in press.
33. Yang,Y.H., Dudoit,S., Luu,P. and Speed,T.P. (2001) Normalization for cDNA microarray data. SPIE Bios., 83, 596-610.
34. Cleveland,W.S. and Devlin,S.J. (1988) Locally-weighted regression: an approach to regression analysis by local fitting. J. Am. Stat. Assoc., 83, 596-610.
35. May,E., Jeltsch,J.M. and Gannon,F. (1981) Characterisation of a gene encoding a 115K super T antigen expressed by a SV40-transformed rat cell line. Nucleic Acids Res., 9, 4111-4128.
36. Murphy,M., Hinman,A. and Levine,A.J. (1996) Wild-type p53 negatively regulates the expression of a microtubule-associated protein. Genes Dev., 10, 2971-2980.
37. Zhao,R., Gish,K., Murphy,M., Yin,Y., Notterman,D., Hoffman,W.H., Tom,E., Mack,D.H. and Levine,A.J. (2000) Analysis of p53-regulated gene expression patterns using oligonucleotide arrays. Genes Dev., 14, 981-993.
38. Kannan,K., Amariglio,N., Rechavi,G., Jakob-Hirsch,J., Kela,I., Kaminski,N., Getz,G., Domany,E. and Givol,D. (2001) DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene, 20, 2225-2234.
39. Yu,J., Zhang,L., Hwang,P.M., Rago,C., Kinzler,K.W. and Vogelstein,B. (1999) Identification and classification of p53-regulated genes. Proc. Natl Acad. Sci. USA, 96, 14517-14522.
40. Sionov,R.V. and Haupt,Y. (1999) The cellular response to p53: the decision between life and death. Oncogene, 18, 6145-6157.
41. Roperch,J.P., Alvaro,V., Prieur,S., Tuynder,M., Nemani,M., Lethrosne,F., Piouffre,L., Gendron,M.C., Israeli,D., Dausset,J., Oren,M., Amson,R. and Telerman,A. (1998) Inhibition of presenilin 1 expression is promoted by p53 and p21WAF-1 and results in apoptosis and tumor suppression. Nature Med., 4, 835-838.
42. Venot,C., Maratrat,M., Dureuil,C., Conseiller,E., Bracco,L. and Debussche,L. (1998) The requirement for the p53 proline-rich functional domain for mediation of apoptosis is correlated with specific PIG3 gene transactivation and with transcriptional repression. EMBO J., 17, 4668-4679.
43. Murphy,M., Ahn,J., Walker,K.K., Hoffman,W.H., Evans,R.M., Levine,A.J. and George,D.L. (1999) Transcriptional repression by wild-type p53 utilizes histone deacetylases, mediated by interaction with mSin3a. Genes Dev., 13, 2490-2501.
44. Haupt,Y., Rowan,S., Shaulian,E., Vousden,K.H. and Oren,M. (1995) Induction of apoptosis in HeLa cells by trans-activation-deficient p53. Genes Dev., 9, 2170-2183.
45. Ryan,K.M. and Vousden,K.H. (1998) Characterization of structural p53 mutants which show selective defects in apoptosis but not cell cycle arrest. Mol. Cell. Biol., 18, 3692-3698.
46. Hoffman,W.H., Biade,S., Zilfou,J.T., Chen,J. and Murphy,M. (2002) Transcriptional repression of the anti-apoptotic survivin gene by wild-type p53. J. Biol. Chem., 277, 3247-3257.
47. 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.
48. Manni,I., Mazzaro,G., Gurtner,A., Mantovani,R., Haugwitz,U., Krause,K., Engeland,K., Sacchi,A., Soddu,S. and Piaggio,G. (2001) NF-Y mediates the transcriptional inhibition ofthe cyclin B1, cyclin B2, and cdc25C promoters upon induced G2 arrest. J. Biol. Chem., 276, 5570-5576.
49. 2/M transition by p53. Oncogene, 20, 1803-1815.
50. Bustin,M. (1999) Regulation of DNA-dependent activities by the functional motifs ofthe high-mobility-group chromosomal proteins. Mol. Cell. Biol., 19, 5237-5246.
51. Okamura,S., Ng,C.C., Koyama,K., Takei,Y., Arakawa,H., Monden,M. and Nakamura,Y. (1999) Identification of seven genes regulated by wild-type p53 in a colon cancer cell line carrying a well-controlled wild-type p53 expression system. Oncol. Res., 11, 281-285.
52. 1/S transition. Biochem. Biophys. Res. Commun., 298, 282-288.
53. Zilfou,J.T., Hoffman,W.H., Sank,M.. George,D.L. and Murphy,M. (2001) The corepressor mSin3a interacts with the proline-rich domain of p53 and protects p53 from proteasome-mediated degradation. Mol. Cell. Biol., 21, 3974-3785.
54. Hsieh,J.K., Chan,F.S., O'Connor,D.J., Mittnacht,S., Zhong,S. and Lu,X. (1999) RB regulates the stability and the apoptotic function of p53 via MDM2. Mol. Cell, 3, 181-193.