Life or death: p53-induced apoptosis requires DNA binding cooperativity

Cell Cycle

Volumn 9, Issue 20, 2010, Pages 4068-4076

  Schlereth, Katharina ^a   Charles, Joël P ^a   Bretz, Anne C ^a   Stiewe, Thorsten ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Cell cycle arrest apoptosis; DNA binding; p53; Transcription factor; Tumor supressor

Indexed keywords

DNA; PROTEIN BAX; PROTEIN MDM2; PROTEIN NOXA; PROTEIN P53;

ACETYLATION; ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; CANCER CELL; CELL AGING; CELL CYCLE ARREST; CELL FATE; CELL LOSS; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; DNA BINDING; DNA METHYLATION; GEL MOBILITY SHIFT ASSAY; HUMAN; LIVER CANCER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; SUMOYLATION; TRANSACTIVATION; UBIQUITINATION; X RAY CRYSTALLOGRAPHY;

EID: 77958515009     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.20.13595     Document Type: Review

References (72)

1. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:38-44.
2. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9:402-12. (Pubitemid 351574202)
3. Levine AJ, Oren M. The first 30 years of p53: growing ever more complex. Nat Rev Cancer 2009; 9:749-58.
4. Budanov AV, Karin M. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 2008; 134:451-60.
5. Korotchkina LG, Demidenko ZN, Gudkov AV, Blagosklonny MV. Cellular quiescence caused by the Mdm2 inhibitor nutlin-3A. Cell Cycle 2009; 8:3777-81.
6. Steelman LS, McCubrey JA. Intriguing novel abilities of Nutlin-3A: induction of cellular quiescence as opposed to cellular senescence - implications for chemotherapy. Cell Cycle 2009; 8:3634-5.
7. Demidenko ZN, Korotchkina LG, Gudkov AV, Blagosklonny MV. Paradoxical suppression of cellular senescence by p53. Proc Natl Acad Sci USA 2010; 107:9660-4.
8. Korotchkina LG, Leontieva OV, Bukreeva EI, Demidenko ZN, Gudkov AV, Blagosklonny MV. The choice between p53-induced senescence and quiescence is determined in part by the mTOR pathway. Aging (Albany NY) 2010; 2:344-52.
9. Schlereth K, Beinoraviciute-Kellner R, Zeitlinger MK, Bretz AC, Sauer M, Charles JP, et al. DNA binding cooperativity of p53 modulates the decision between cell cycle arrest and apoptosis. Mol Cell 2010; 38:356-68.
10. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445:656-60. (Pubitemid 46232886)
11. Meyer M, Rubsamen D, Slany R, Illmer T, Stabla K, Roth P, et al. Oncogenic RAS enables DNA damage- and p53-dependent differentiation of acute myeloid leukemia cells in response to chemotherapy. PLoS One 2009; 4:7768.
12. Aylon Y, Oren M. Living with p53, dying of p53. Cell 2007; 130:597-600.
13. Murray-Zmijewski F, Slee EA, Lu X. A complex barcode underlies the heterogeneous response of p53 to stress. Nat Rev Mol Cell Biol 2008; 9:702-12.
14. Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009; 458:1127-30.
15. Morselli E, Galluzzi L, Kepp O, Kroemer G. Nutlin kills cancer cells via mitochondrial p53. Cell Cycle 2009; 8:1647-8.
16. Vaseva AV, Marchenko ND, Moll UM. The transcription- independent mitochondrial p53 program is a major contributor to nutlin-induced apoptosis in tumor cells. Cell Cycle 2009; 8:1711-9.
17. Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D, et al. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 2004; 116:499-509. (Pubitemid 38264428)
18. Hearnes JM, Mays DJ, Schavolt KL, Tang L, Jiang X, Pietenpol JA. Chromatin immunoprecipitation-based screen to identify functional genomic binding sites for sequence-specific transactivators. Mol Cell Biol 2005; 25:10148-58. (Pubitemid 41572759)
19. Smeenk L, van Heeringen SJ, Koeppel M, van Driel MA, Bartels SJ, Akkers RC, et al. Characterization of genome-wide p53-binding sites upon stress response. Nucleic Acids Res 2008; 36:3639-54. (Pubitemid 351917528)
20. Wei CL, Wu Q, Vega VB, Chiu KP, Ng P, Zhang T, et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006; 124:207-19. (Pubitemid 43069320)
21. Funk WD, Pak DT, Karas RH, Wright WE, Shay JW. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol Cell Biol 1992; 12:2866-71.
22. el-Deiry WS, Kern SE, Pietenpol JA, Kinzler KW, Vogelstein B. Definition of a consensus binding site for p53. Nat Genet 1992; 1:45-9.
23. Das S, Boswell SA, Aaronson SA, Lee SW. p53 promoter selection: choosing between life and death. Cell Cycle 2008; 7:154-7. (Pubitemid 351366513)
24. Blattner C. Regulation of p53: the next generation. Cell Cycle 2008; 7:3149-53.
25. Georges SA, Chau BN, Braun CJ, Zhang X, Dobbelstein M. Cell cycle arrest or apoptosis by p53: are microRNAs-192/215 and -34 making the decision? Cell Cycle 2009; 8:680-1.
26. Trigiante G, Lu X. ASPP [corrected] and cancer. Nat Rev Cancer 2006; 6:217-26.
27. Samuels-Lev Y, O'Connor DJ, Bergamaschi D, Trigiante G, Hsieh JK, Zhong S, et al. ASPP proteins specifically stimulate the apoptotic function of p53. Mol Cell 2001; 8:781-94. (Pubitemid 33030212)
28. Bergamaschi D, Samuels Y, O'Neil NJ, Trigiante G, Crook T, Hsieh JK, et al. iASPP oncoprotein is a key inhibitor of p53 conserved from worm to human. Nat Genet 2003; 33:162-7. (Pubitemid 36177067)
29. Bergamaschi D, Samuels Y, Sullivan A, Zvelebil M, Breyssens H, Bisso A, et al. iASPP preferentially binds p53 proline-rich region and modulates apoptotic function of codon 72-polymorphic p53. Nat Genet 2006; 38:1133-41. (Pubitemid 44470358)
30. Perez-Sanchez C, Budhram-Mahadeo VS, Latchman DS. Distinct promoter elements mediate the co-operative effect of Brn-3a and p53 on the p21 promoter and their antagonism on the Bax promoter. Nucleic Acids Res 2002; 30:4872-80. (Pubitemid 35414647)
31. Budhram-Mahadeo VS, Bowen S, Lee S, Perez- Sanchez C, Ensor E, Morris PJ, et al. Brn-3b enhances the proapoptotic effects of p53 but not its induction of cell cycle arrest by cooperating in trans-activation of bax expression. Nucleic Acids Res 2006; 34:6640-52. (Pubitemid 46017957)
32. Hudson CD, Morris PJ, Latchman DS, Budhram- Mahadeo VS. Brn-3a transcription factor blocks p53-mediated activation of proapoptotic target genes Noxa and Bax in vitro and in vivo to determine cell fate. J Biol Chem 2005; 280:11851-8.
33. 2 phase checkpoint induced by DNA damage. Mol Cell Biol 2006; 26:502-12.
34. Sharma S, Dimasi D, Higginson K, Della NG. RZF, a zinc-finger protein in the photoreceptors of human retina. Gene 2004; 342:219-29. (Pubitemid 39452341)
35. Das S, Raj L, Zhao B, Kimura Y, Bernstein A, Aaronson SA, et al. Hzf Determines cell survival upon genotoxic stress by modulating p53 transactivation. Cell 2007; 130:624-37. (Pubitemid 47277418)
36. Miao L, Song Z, Jin L, Zhu YM, Wen LP, Wu M. ARF antagonizes the ability of Miz-1 to inhibit p53-mediated transactivation. Oncogene 2010; 29:711-22.
37. Herold S, Wanzel M, Beuger V, Frohme C, Beul D, Hillukkala T, et al. Negative regulation of the mammalian UV response by Myc through association with Miz-1. Mol Cell 2002; 10:509-21. (Pubitemid 35284171)
38. D'Orazi G, Cecchinelli B, Bruno T, Manni I, Higashimoto Y, Saito S, et al. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 2002; 4:11-9.
39. Rinaldo C, Prodosmo A, Mancini F, Iacovelli S, Sacchi A, Moretti F, et al. MDM2-regulated degradation of HIPK2 prevents p53Ser46 phosphorylation and DNA damage-induced apoptosis. Mol Cell 2007; 25:739-50. (Pubitemid 46341925)
40. Taira N, Nihira K, Yamaguchi T, Miki Y, Yoshida K. DYRK2 is targeted to the nucleus and controls p53 via Ser46 phosphorylation in the apoptotic response to DNA damage. Mol Cell 2007; 25:725-38. (Pubitemid 46341924)
41. Hofmann TG, Moller A, Sirma H, Zentgraf H, Taya Y, Droge W, et al. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat Cell Biol 2002; 4:1-10. (Pubitemid 34071974)
42. Perfettini JL, Castedo M, Nardacci R, Ciccosanti F, Boya P, Roumier T, et al. Essential role of p53 phosphorylation by p38 MAPK in apoptosis induction by the HIV-1 envelope. J Exp Med 2005; 201:279-89. (Pubitemid 40189437)
43. Yoshida K, Liu H, Miki Y. Protein kinase C delta regulates Ser46 phosphorylation of p53 tumor suppressor in the apoptotic response to DNA damage. J Biol Chem 2006; 281:5734-40. (Pubitemid 43847672)
44. Okoshi R, Ozaki T, Yamamoto H, Ando K, Koida N, Ono S, et al. Activation of AMP-activated protein kinase induces p53-dependent apoptotic cell death in response to energetic stress. J Biol Chem 2008; 283:3979-87.
45. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, et al. p53AIP1, a potential mediator of p53-dependent apoptosis and its regulation by Ser- 46-phosphorylated p53. Cell 2000; 102:849-62.
46. Mantovani F, Tocco F, Girardini J, Smith P, Gasco M, Lu X, et al. The prolyl isomerase Pin1 orchestrates p53 acetylation and dissociation from the apoptosis inhibitor iASPP. Nat Struct Mol Biol 2007; 14:912-20. (Pubitemid 47525182)
47. Sykes SM, Mellert HS, Holbert MA, Li K, Marmorstein R, Lane WS, et al. Acetylation of the p53 DNA-binding domain regulates apoptosis induction. Mol Cell 2006; 24:841-51. (Pubitemid 44960096)
48. Tang Y, Luo J, Zhang W, Gu W. Tip60-dependent acetylation of p53 modulates the decision between cell cycle arrest and apoptosis. Mol Cell 2006; 24:827-39. (Pubitemid 44960094)
49. Knights CD, Catania J, Di Giovanni S, Muratoglu S, Perez R, Swartzbeck A, et al. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J Cell Biol 2006; 173:533-44. (Pubitemid 43765200)
50. Chao C, Wu Z, Mazur SJ, Borges H, Rossi M, Lin T, et al. Acetylation of mouse p53 at lysine 317 negatively regulates p53 apoptotic activities after DNA damage. Mol Cell Biol 2006; 26:6859-69. (Pubitemid 44387635)
51. Le Cam L, Linares LK, Paul C, Julien E, Lacroix M, Hatchi E, et al. E4F1 is an atypical ubiquitin ligase that modulates p53 effector functions independently of degradation. Cell 2006; 127:775-88. (Pubitemid 44716249)
52. Jansson M, Durant ST, Cho EC, Sheahan S, Edelmann M, Kessler B, et al. Arginine methylation regulates the p53 response. Nat Cell Biol 2008; 10:1431-9.
53. Durant ST, Cho EC, La Thangue NB. p53 methylation - the Argument is clear. Cell Cycle 2009; 8:801-2.
54. Dehner A, Klein C, Hansen S, Muller L, Buchner J, Schwaiger M, et al. Cooperative binding of p53 to DNA: regulation by protein-protein interactions through a double salt bridge. Angew Chem Int Ed Engl 2005; 44:5247-51. (Pubitemid 41223875)
55. Madhumalar A, Jun LH, Lane DP, Verma CS. Dimerization of the core domain of the p53 family: a computational study. Cell Cycle 2009; 8:137-48.
56. Klein C, Planker E, Diercks T, Kessler H, Kunkele KP, Lang K, et al. NMR spectroscopy reveals the solution dimerization interface of p53 core domains bound to their consensus DNA. J Biol Chem 2001; 276:49020-7.
57. Kitayner M, Rozenberg H, Kessler N, Rabinovich D, Shaulov L, Haran TE, et al. Structural basis of DNA recognition by p53 tetramers. Mol Cell 2006; 22:741-53.
58. Ho WC, Fitzgerald MX, Marmorstein R. Structure of the p53 core domain dimer bound to DNA. J Biol Chem 2006; 281:20494-502. (Pubitemid 44065822)
59. Tidow H, Melero R, Mylonas E, Freund SM, Grossmann JG, Carazo JM, et al. Quaternary structures of tumor suppressor p53 and a specific p53 DNA complex. Proc Natl Acad Sci USA 2007; 104:12324-9. (Pubitemid 47206136)
60. Hager GL, McNally JG, Misteli T. Transcription dynamics. Mol Cell 2009; 35:741-53.
61. Perissi V, Rosenfeld MG. Controlling nuclear receptors: the circular logic of cofactor cycles. Nat Rev Mol Cell Biol 2005; 6:542-54. (Pubitemid 40943045)
62. Misteli T. Beyond the sequence: cellular organization of genome function. Cell 2007; 128:787-800. (Pubitemid 46273571)
63. Beckerman R, Prives C. Transcriptional regulation by p53. Cold Spring Harb Perspect Biol 2010; 2:935.
64. An W, Kim J, Roeder RG. Ordered cooperative functions of PRMT1, p300 and CARM1 in transcriptional activation by p53. Cell 2004; 117:735-48.
65. Karpova TS, Kim MJ, Spriet C, Nalley K, Stasevich TJ, Kherrouche Z, et al. Concurrent fast and slow cycling of a transcriptional activator at an endogenous promoter. Science 2008; 319:466-9. (Pubitemid 351160580)
66. McNally JG, Muller WG, Walker D, Wolford R, Hager GL. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science 2000; 287:1262-5. (Pubitemid 30112147)
67. Metivier R, Penot G, Hubner MR, Reid G, Brand H, Kos M, et al. Estrogen receptor-alpha directs ordered, cyclical and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003; 115:751-63. (Pubitemid 38030303)
68. Chen X, Ko LJ, Jayaraman L, Prives C. p53 levels, functional domains and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev 1996; 10:2438-51. (Pubitemid 26341879)
69. Horvath MM, Wang X, Resnick MA, Bell DA. Divergent evolution of human p53 binding sites: cell cycle versus apoptosis. PLoS Genet 2007; 3:127.
70. Ma B, Pan Y, Zheng J, Levine AJ, Nussinov R. Sequence analysis of p53 response-elements suggests multiple binding modes of the p53 tetramer to DNA targets. Nucleic Acids Res 2007; 35:2986-3001. (Pubitemid 47073637)
71. Frebourg T, Kassel J, Lam KT, Gryka MA, Barbier N, Andersen TI, et al. Germ-line mutations of the p53 tumor suppressor gene in patients with high risk for cancer inactivate the p53 protein. Proc Natl Acad Sci USA 1992; 89:6413-7.
72. Sauer M, Bretz AC, Beinoraviciute-Kellner R, Beitzinger M, Burek C, Rosenwald A, et al. C-terminal diversity within the p53 family accounts for differences in DNA binding and transcriptional activity. Nucleic Acids Res 2008; 36:1900-12. (Pubitemid 351494234)