Nutlin-3a activates p53 to both down-regulate inhibitor of growth 2 and up-regulate mir-34a, mir-34b, and mir-34c expression, and induce senescence

Cancer Research

Volumn 68, Issue 9, 2008, Pages 3193-3203

  Kumamoto, Kensuke ^a,c   Spillare, Elisa A ^a   Fujita, Kaori ^a   Horikawa, Izumi ^a   Yamashita, Taro ^a   Appella, Ettore ^a   Nagashima, Makoto ^b   Takenoshita, Seiichi ^c   Yokota, Jun ^d   Harris, Curtis C ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b TOHO UNIVERSITY SAKURA MEDICAL CENTER   (Japan)

^c FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^d NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NUTLIN 3; PROTEIN P53; CELL RECEPTOR; HOMEODOMAIN PROTEIN; IMIDAZOLE DERIVATIVE; ING2 PROTEIN, HUMAN; MICRORNA; MICRORNA 34A, HUMAN; PIPERAZINE DERIVATIVE; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; GENE ACTIVATION; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; SENESCENCE; UPREGULATION; CELL AGING; CELL CULTURE; CELL STRAIN HCT116; DRUG EFFECT; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

BASE SEQUENCE; CELL AGING; CELLS, CULTURED; DOWN-REGULATION; FIBROBLASTS; GENE EXPRESSION REGULATION; HCT116 CELLS; HOMEODOMAIN PROTEINS; HUMANS; IMIDAZOLES; MICRORNAS; PIPERAZINES; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 44849091255     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-2780     Document Type: Article

References (53)

1. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007;8:275-83.
2. Itahana K, Dimri G, Campisi J. Regulation of cellular senescence by p53. Eur J Biochem 2001;268:2784-91.
3. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997;88:593-602.
4. Hayflick L, Moorhead PS. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1961;25:585-621.
5. Collado M, Gil J, Efeyan A, et al. Tumour biology: senescence in premalignant tumours. Nature 2005;436:642.
6. Braig M, Schmitt CA. Oncogene-induced senescence: putting the brakes on tumor development. Cancer Res 2006;66:2881-4.
7. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997;387:296-9.
8. Oliner JD, Kinzler KW, Meltzer PS, George DL, Vogelstein B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 1992;358:80-3.
9. Pomerantz J, Schreiber-Agus N, Liegeois NJ, et al. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 1998;92:713-23.
10. Zhang Y, Xiong Y, Yarbrough WG. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 1998;92:725-34.
11. Vassilev LT. MDM2 inhibitors for cancer therapy. Trends Mol Med 2007;13:23-31.
12. Vassilev LT. p53 Activation by small molecules: application in oncology. J Med Chem 2005;48:4491-9.
13. Vassilev LT, Vu BT, Graves B, et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004;303:844-8.
14. Tovar C, Rosinski J, Filipovic Z, et al. Small-molecule MDM2 antagonists reveal aberrant p53 signaling in cancer: implications for therapy. Proc Natl Acad Sci U S A 2006;103:1888-93.
15. Coll-Mulet L, Iglesias-Serret D, Santidrian AF, et al. MDM2 antagonists activate p53 and synergize with genotoxic drugs in B-cell chronic lymphocytic leukemia cells. Blood 2006;107:4109-14.
16. Thompson T, Tovar C, Yang H, et al. Phosphorylation of p53 on key serines is dispensable for transcriptional activation and apoptosis. J Biol Chem 2004;279:53015-22.
17. LaRusch GA, Jackson MW, Dunbar JD, Warren RS, Donner DB, Mayo LD. Nutlin3 blocks vascular endothelial growth factor induction by preventing the interaction between hypoxia inducible factor 1α and Hdm2. Cancer Res 2007;67:450-4.
18. Ambrosini G, Sambol EB, Carvajal D, Vassilev LT, Singer S, Schwartz GK. Mouse double minute antagonist nutlin-3a enhances chemotherapy-induced apoptosis in cancer cells with mutant p53 by activating E2F1. Oncogene 2007;26:3473-81.
19. Staib F, Robles AI, Varticovski L, et al. The p53 tumor suppressor network is a key responder to microenvironmental components of chronic inflammatory stress. Cancer Res 2005;65:10255-64.
20. Robinson M, Jiang P, Cui J, et al. Global genechip profiling to identify genes responsive to p53-induced growth arrest and apoptosis in human lung carcinoma cells. Cancer Biol Ther 2003;2:406-15.
21. Mirza A, Wu Q, Wang L, et al. Global transcriptional program of p53 target genes during the process of apoptosis and cell cycle progression. Oncogene 2003;2:3645-54.
22. Shelton DN, Chang E, Whittier PS, Choi D, Funk WD. Microarray analysis of replicative senescence. Curr Biol 1999;9:939-45.
23. Komarova EA, Diatchenko L, Rokhlin OW, et al. Stress-induced secretion of growth inhibitors: a novel tumor suppressor function of p53. Oncogene 1998;17:1089-96.
24. He L, He X, Lim LP, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007;447:1130-4.
25. Raver-Shapira N, Marciano E, Meiri E, et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 2007;26:731-43.
26. Chang TC, Wentzel EA, Kent OA, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007;26:745-52.
27. Tarasov V, Jung P, Verdoodt B, et al. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G(1)-arrest. Cell Cycle 2007;6:1586-93.
28. He GH, Helbing CC, Wagner MJ, Sensen CW, Riabowol K. Phylogenetic analysis of the ING family of PHD finger proteins. Mol Biol Evol 2005;22:104-16.
29. Nagashima M, Shiseki M, Miura K, et al. DNA damage-inducible gene p33ING2 negatively regulates cell proliferation through acetylation of p53. Proc Natl Acad Sci U S A 2001;98:9671-6.
30. Doyon Y, Cayrou C, Ullah M, et al. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 2006;21:51-64.
31. Pena PV, Davrazou F, Shi X, et al. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 2006;442:100-3.
32. Shi X, Hong T, Walter KL, et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 2006;442:96-9.
33. Ruthenburg AJ, Allis CD, Wysocka J. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell 2007;25:15-30.
34. Santos-Rosa H, Schneider R, Bannister AJ, et al. Active genes are tri-methylated at K4 of histone H3. Nature 2002;419:407-11.
35. Bernstein BE, Kamal M, Lindblad-Toh K, et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005;120:169-81.
36. Han X, Berardi P, Riabowol K. Chromatin modification and senescence: linkage by tumor suppressors? Rejuvenation Res 2006;9:69-76.
37. Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995;92:9363-7.
38. Sakaguchi K, Saito S, Higashimoto Y, Roy S, Anderson CW, Appella E. Damage-mediated phosphorylation of human p53 threonine 18 through a cascade mediated by a casein 1-like kinase. Effect on Mdm2 binding. J Biol Chem 2000;275:9278-83.
39. Craig AL, Burch L, Vojtesek B, Mikutowska J, Thompson A, Hupp TR. Novel phosphorylation sites of human tumour suppressor protein p53 at Ser20 and Thr18 that disrupt the binding of mdm2 (mouse double minute 2) protein are modified in human cancers. Biochem J 1999;342:133-41.
40. Sengupta S, Shimamoto A, Koshiji M, et al. Tumor suppressor p53 represses transcription of RECQ4 helicase. Oncogene 2005;24:1738-48.
41. Kanaya T, Kyo S, Hamada K, et al. Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription. Clin Cancer Res 2000;6:1239-47.
42. Ohlsson C, Kley N, Werner H, LeRoith D. p53 regulates insulin-like growth factor-I (IGF-I) receptor expression and IGF-I-induced tyrosine phosphorylation in an osteosarcoma cell line: interaction between p53 and Sp1. Endocrinology 1998;139:1101-7.
43. Li B, Lee MY. Transcriptional regulation of the human DNA polymerase δ catalytic subunit gene POLD1 by p53 tumor suppressor and Sp1. J Biol Chem 2001;276:29729-39.
44. Murphy M, Ahn J, Walker KK, et al. Transcriptional repression by wild-type p53 utilizes histone deacetylases, mediated by interaction with mSin3a. Genes Dev 1999;13:2490-501.
45. Pedeux R, Sengupta S, Shen JC, et al. ING2 regulates the onset of replicative senescence by induction of p300-dependent p53 acetylation. Mol Cell Biol 2005;25:6639-48.
46. Efeyan A, Ortega-Molina A, Velasco-Miguel S, Herranz D, Vassilev LT, Serrano M. Induction of p53-dependent senescence by the MDM2 antagonist nutlin-3a in mouse cells of fibroblast origin. Cancer Res 2007;67:7350-7.
47. Kataoka H, Bonnefin P, Vieyra D, et al. ING1 represses transcription by direct DNA binding and through effects on p53. Cancer Res 2003;63:5785-92.
48. Jackson MW, Agarwal MK, Agarwal ML, et al. Limited role of N-terminal phosphoserine residues in the activation of transcription by p53. Oncogene 2004;23:4477-87.
49. Kortlever RM, Higgins PJ, Bernards R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat Cell Biol 2006;8:877-84.
50. Ho J, Benchimol S. Transcriptional repression mediated by the p53 tumour suppressor. Cell Death Differ 2003;10:404-8.
51. Han EK, Ng SC, Arber N, Begemann M, Weinstein IB. Roles of cyclin D1 and related genes in growth inhibition, senescence and apoptosis. Apoptosis 1999;4:213-9.
52. Fukami J, Anno K, Ueda K, Takahashi T, Ide T. Enhanced expression of cyclin D1 in senescent human fibroblasts. Mech Ageing Dev 1995;81:139-57.
53. Atadja P, Wong H, Veillete C, Riabowol K. Overexpression of cyclin D1 blocks proliferation of normal diploid fibroblasts. Exp Cell Res 1995;217:205-16.