Acetylation of the p53 DNA-Binding Domain Regulates Apoptosis Induction

Molecular Cell

Volumn 24, Issue 6, 2006, Pages 841-851

  Sykes, Stephen M ^a,b,c   Mellert, Hestia S ^a,b,c   Holbert, Marc A ^d   Li, Keqin ^d   Marmorstein, Ronen ^d   Lane, William S ^e   McMahon, Steven B ^a,b,d  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d WISTAR INSTITUTE   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

CELLCYCLE

Indexed keywords

ACETIC ACID DERIVATIVE; ARGININE; DNA; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE MYST; LYSINE; MUTANT PROTEIN; PROTEIN MOF; PROTEIN P53; PROTEIN TIP60;

ACETYLATION; APOPTOSIS; ARTICLE; BAX GENE; CANCER GENETICS; CELL CYCLE ARREST; CONTROLLED STUDY; DNA BINDING MOTIF; DNA DAMAGE; GENE; GENE ACTIVATION; GENE CONTROL; GENE MUTATION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MDM2 GENE; P21 GENE; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PUMA GENE; REGULATORY MECHANISM; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ACETYLATION; AMINO ACID SEQUENCE; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BINDING SITES; CELL CYCLE; HISTONE ACETYLTRANSFERASES; HUMANS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33845656738     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.11.026     Document Type: Article

References (49)

1. Ard P.G., Chatterjee C., Kunjibettu S., Adside L.R., Gralinski L.E., and McMahon S.B. Transcriptional regulation of the mdm2 oncogene by p53 requires TRRAP acetyltransferase complexes. Mol. Cell. Biol. 22 (2002) 5650-5661
2. Berns K., Hijmans E.M., Mullenders J., Brummelkamp T.R., Velds A., Heimerikx M., Kerkhoven R.M., Madiredjo M., Nijkamp W., Weigelt B., et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 428 (2004) 431-437
3. Budanov A.V., Sablina A.A., Feinstein E., Koonin E.V., and Chumakov P.M. Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304 (2004) 596-600
4. Bulavin D.V., Saito S., Hollander M.C., Sakaguchi K., Anderson C.W., Appella E., and Fornace Jr. A.J. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18 (1999) 6845-6854
5. Chipuk J.E., Maurer U., Green D.R., and Schuler M. Pharmacologic activation of p53 elicits Bax-dependent apoptosis in the absence of transcription. Cancer Cell 4 (2003) 371-381
6. Chittum H.S., Lane W.S., Carlson B.A., Roller P.P., Lung F.D., Lee B.J., and Hatfield D.L. Rabbit beta-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps. Biochemistry 37 (1998) 10866-10870
7. Cho Y., Gorina S., Jeffrey P.D., and Pavletich N.P. Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science 265 (1994) 346-355
8. Deissler H., Kafka A., Schuster E., Sauer G., Kreienberg R., and Zeillinger R. Spectrum of p53 mutations in biopsies from breast cancer patients selected for preoperative chemotherapy analysed by the functional yeast assay to predict therapeutic response. Oncol. Rep. 11 (2004) 1281-1286
9. Dou Y., Milne T.A., Tackett A.J., Smith E.R., Fukuda A., Wysocka J., Allis C.D., Chait B.T., Hess J.L., and Roeder R.G. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121 (2005) 873-885
10. Doyon Y., Selleck W., Lane W.S., Tan S., and Cote J. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol. Cell. Biol. 24 (2004) 1884-1896
11. el-Deiry W.S., Tokino T., Velculescu V.E., Levy D.B., Parsons R., Trent J.M., Lin D., Mercer W.E., Kinzler K.W., and Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 75 (1993) 817-825
12. Eng J.K., McCormack A.L., and Yates J.R.I. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5 (1994) 976-989
13. Friedler A., Veprintsev D.B., Rutherford T., von Glos K.I., and Fersht A.R. Binding of Rad51 and other peptide sequences to a promiscuous, highly electrostatic binding site in p53. J. Biol. Chem. 280 (2005) 8051-8059
14. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell 102 (2000) 1-4
15. Gu W., and Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90 (1997) 595-606
16. Gupta A., Sharma G.G., Young C.S., Agarwal M., Smith E.R., Paull T.T., Lucchesi J.C., Khanna K.K., Ludwig T., and Pandita T.K. Involvement of human MOF in ATM function. Mol. Cell. Biol. 25 (2005) 5292-5305
17. Hashimoto T., Tokuchi Y., Hayashi M., Kobayashi Y., Nishida K., Hayashi S., Ishikawa Y., Tsuchiya S., Nakagawa K., Hayashi J., and Tsuchiya E. p53 null mutations undetected by immunohistochemical staining predict a poor outcome with early-stage non-small cell lung carcinomas. Cancer Res. 59 (1999) 5572-5577
18. Hayes V.M., Dirven C.M., Dam A., Verlind E., Molenaar W.M., Mooij J.J., Hofstra R.M., and Buys C.H. High frequency of TP53 mutations in juvenile pilocytic astrocytomas indicates role of TP53 in the development of these tumors. Brain Pathol. 9 (1999) 463-467
19. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., and Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102 (2000) 463-473
20. Jack M.T., Woo R.A., Hirao A., Cheung A., Mak T.W., and Lee P.W. Chk2 is dispensable for p53-mediated G1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. USA 99 (2002) 9825-9829
21. Jeffers J.R., Parganas E., Lee Y., Yang C., Wang J., Brennan J., MacLean K.H., Han J., Chittenden T., Ihle J.N., et al. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 4 (2003) 321-328
22. Kim J.H., Kim B., Cai L., Choi H.J., Ohgi K.A., Tran C., Chen C., Chung C.H., Huber O., Rose D.W., et al. Transcriptional regulation of a metastasis suppressor gene by Tip60 and beta-catenin complexes. Nature 434 (2005) 921-926
23. Kitayner M., Rozenberg H., Kessler N., Rabinovich D., Shaulov L., Haran T.E., and Shakked Z. Structural basis of DNA recognition by p53 tetramers. Mol. Cell 22 (2006) 741-753
24. Knights C.D., Catania J., Di Giovanni S., Muratoglu S., Perez R., Swartzbeck A., Quong A.A., Zhang X., Beerman T., Pestell R.G., and Avantaggiati M.L. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J. Cell Biol. 173 (2006) 533-544
25. Kusch T., Florens L., Macdonald W.H., Swanson S.K., Glaser R.L., Yates III J.R., Abmayr S.M., Washburn M.P., and Workman J.L. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306 (2004) 2084-2087
26. Legube G., Linares L.K., Lemercier C., Scheffner M., Khochbin S., and Trouche D. Tip60 is targeted to proteasome-mediated degradation by Mdm2 and accumulates after UV irradiation. EMBO J. 21 (2002) 1704-1712
27. Legube G., Linares L.K., Tyteca S., Caron C., Scheffner M., Chevillard-Briet M., and Trouche D. Role of the histone acetyl transferase Tip60 in the p53 pathway. J. Biol. Chem. 279 (2004) 44825-44833
28. Leitao M.M., Soslow R.A., Baergen R.N., Olvera N., Arroyo C., and Boyd J. Mutation and expression of the TP53 gene in early stage epithelial ovarian carcinoma. Gynecol. Oncol. 93 (2004) 301-306
29. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell 88 (1997) 323-331
30. Lo W.S., Trievel R.C., Rojas J.R., Duggan L., Hsu J.Y., Allis C.D., Marmorstein R., and Berger S.L. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5 (2000) 917-926
31. Meyers F.J., Chi S.G., Fishman J.R., deVere White R.W., and Gumerlock P.H. p53 mutations in benign prostatic hyperplasia. J. Natl. Cancer Inst. 85 (1993) 1856-1858
32. Oda K., Arakawa H., Tanaka T., Matsuda K., Tanikawa C., Mori T., Nishimori H., Tamai K., Tokino T., Nakamura Y., and Taya Y. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102 (2000) 849-862
33. Patel J.H., and McMahon S.B. Targeting of MIZ-1 is essential for MYC mediated apoptosis. J. Biol. Chem. 281 (2006) 3283-3289
34. Sakaguchi K., Herrera J.E., Saito S., Miki T., Bustin M., Vassilev A., Anderson C.W., and Appella E. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 12 (1998) 2831-2841
35. Samuels-Lev Y., O'Connor D.J., Bergamaschi D., Trigiante G., Hsieh J.K., Zhong S., Campargue I., Naumovski L., Crook T., and Lu X. ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell 8 (2001) 781-794
36. Squatrito M., Gorrini C., and Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol. 16 (2006) 433-442
37. Sun Z.W., and Allis C.D. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418 (2002) 104-108
38. Sun Y., Jiang X., Chen S., Fernandes N., and Price B.D. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl. Acad. Sci. USA 102 (2005) 13182-13187
39. Taipale M., Rea S., Richter K., Vilar A., Lichter P., Imhof A., and Akhtar A. hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol. Cell. Biol. 25 (2005) 6798-6810
40. Thompson T., Tovar C., Yang H., Carvajal D., Vu B.T., Xu Q., Wahl G.M., Heimbrook D.C., and Vassilev L.T. Phosphorylation of p53 on key serines is dispensable for transcriptional activation and apoptosis. J. Biol. Chem. 279 (2004) 53015-53022
41. Tyteca S., Vandromme M., Legube G., Chevillard-Briet M., and Trouche D. Tip60 and p400 are both required for UV-induced apoptosis but play antagonistic roles in cell cycle progression. EMBO J. 25 (2006) 1680-1689
42. Villunger A., Michalak E.M., Coultas L., Mullauer F., Bock G., Ausserlechner M.J., Adams J.M., and Strasser A. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 302 (2003) 1036-1038
43. Vogelstein B., Lane D., and Levine A.J. Surfing the p53 network. Nature 408 (2000) 307-310
44. Vousden K.H., and Lu X. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2 (2002) 594-604
45. Yu J., Wang Z., Kinzler K.W., Vogelstein B., and Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc. Natl. Acad. Sci. USA 100 (2003) 1931-1936
46. Zhang L., Yu J., Park B.H., Kinzler K.W., and Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science 290 (2000) 989-992
47. Zhang X.Y., DeSalle L.M., Patel J.H., Capobianco A.J., Yu D., Thomas-Tikhonenko A., and McMahon S.B. Metastasis-associated protein 1 (MTA1) is an essential downstream effector of the c-MYC oncoprotein. Proc. Natl. Acad. Sci. USA 102 (2005) 13968-13973
48. Zhao K., Chai X., Johnston K., Clements A., and Marmorstein R. Crystal structure of the mouse p53 core DNA-binding domain at 2.7 Å resolution. J. Biol. Chem. 276 (2001) 12120-12127 10.1074/jbc.M011644200 Published online January 4, 2001
49. Zupnick A., and Prives C. Mutational analysis of the p53 core domain L1 loop. J. Biol. Chem. 281 (2006) 20464-20473 10.1074/jbc.M603387200 Published online May 10, 2006