The impact of post-transcriptional regulation in the p53 network

Briefings in Functional Genomics

Volumn 12, Issue 1, 2013, Pages 46-57

  Freeman, Justin A ^a   Espinosa, Joaquin M ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

MiRNA; P53; Post transcriptional regulation; RNA binding proteins

Indexed keywords

CASPASE 8; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1A; MESSENGER RNA; MICRORNA 34A; PROTEIN BAX; PROTEIN MDM2; PROTEIN MDMX; PROTEIN NOXA; PROTEIN P53; PUMA PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR SNAIL;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; CANCER GROWTH; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL TYPE; CORRELATION ANALYSIS; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; LIVER CELL CARCINOMA; METASTASIS; NASOPHARYNX CARCINOMA; NEUROBLASTOMA; OSTEOBLASTOMA; OSTEOSARCOMA; PHENOTYPE; PLEIOTROPY; PROSTATE CARCINOMA; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RETINOBLASTOMA; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; RNA STABILITY; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84872762772     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/els058     Document Type: Article

References (103)

1. Rivlin N, Brosh R, Oren M, et al. Mutations in the p53 tumor suppressor gene: important milestones at the various steps of tumorigenesis. Genes Cancer 2011;2: 466-12.
2. Brady CA, Jiang D, Mello SS, et al. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 2011;145: 571-83.
3. Li T, Kon N, Jiang L, et al. Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 2012;149: 1269-83.
4. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell 2009;137: 413-31.
5. Brown CJ, Lain S, Verma CS, et al. Awakening guardian angels: drugging the p53 pathway. Nat Rev Cancer 2009;9: 862-73.
6. 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 USA 2006;103: 1888-93.
7. Paris R, Henry RE, Stephens SJ, et al. Multiple p53-independent gene silencing mechanisms define the cellular response to p53 activation. Cell Cycle 2008;7: 2427-33.
8. Henry RE, Andrysik Z, Paris R, et al. A DR4: tBID axis drives the p53 apoptotic response by promoting oligomerization of poised BAX. EMBOJ 2012;31: 1266-78.
9. Sullivan KD, Padilla-Just N, Henry RE, et al. ATM and MET kinases are synthetic lethal with nongenotoxic activation of p53. Nat Chem Biol 2012;8(7): 646-54.
10. Zhao R, Gish K, Murphy M, etal. Analysis of p53-regulated gene expression patterns using oligonucleotide arrays. Genes Dev 2000;14: 981-93.
11. Wei CL, Wu Q, Vega VB, et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006;124: 207-19.
12. Donner AJ, Szostek S, Hoover JM, et al. CDK8 Is a stimulus-specific positive coregulator of p53 target genes. Mol Cell 2007;27: 121-33.
13. Espinosa JM, Emerson BM. Transcriptional regulation by p53 through intrinsic DNA/chromatin binding and site-directed cofactor recruitment. Mol Cell 2001;8: 57-69.
14. Espinosa JM, Verdun RE, Emerson BM. p53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol Cell 2003;12: 1015-27.
15. Gu W, Malik S, Ito M, et al. A novel human SRB/ MED-containing cofactor complex, SMCC, involved in transcription regulation. Mol Cell 1999;3: 97-108.
16. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136: 215-33.
17. El-Deiry WS, Tokino T, Velculescu VE, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75: 817-25.
18. El-Deiry WS, Harper JW, O'Connor PM, et al. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res 1994;54: 1169-74.
19. Harper JW, Adami GR, Wei N, et al. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 1993;75: 805-16.
20. Harper JW, Elledge SJ, Keyomarsi K, et al. Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell 1995;6: 387-400.
21. Conkrite K, Sundby M, Mukai S, et al. miR-17_92 cooperates with RB pathway mutations to promote retinoblastoma. Genes Dev 2011;25: 1734-45.
22. Fontana L, Fiori ME, Albini S, et al. Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 2008;3: e2236.
23. Ivanovska I, Ball AS, Diaz RL, et al. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 2008;28: 2167-74.
24. Huang G, Nishimoto K, Zhou Z, et al. miR-20a encoded by the miR-17-92 cluster increases the metastatic potential of osteosarcoma cells by regulating Fas expression. Cancer Res 2012;72: 908-16.
25. Pan J, Hu H, Zhou Z, et al. Tumor-suppressive mir-663 gene induces mitotic catastrophe growth arrest in human gastric cancer cells. Oncol Rep 2010;24: 105-12.
26. Yi C, Wang Q, Wang L, et al. MiR-663, a microRNA targeting p21(WAF1/CIP1), promotes the proliferation and tumorigenesis of nasopharyngeal carcinoma. Oncogene 2012;31(41): 4421-33.
27. Gottwein E, Cullen BR. A human herpesvirus microRNA inhibits p21 expression and attenuates p21-mediated cell cycle arrest. JVirol 2010;84: 5229-37.
28. Jin Z, El-Deiry WS. Overview of cell death signaling pathways. Cancer BiolTher 2005;4: 139-63.
29. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001;7: 683-94.
30. Yu J, Zhang L, Hwang PM, et al. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 2001;7: 673-82.
31. Zhang C, Zhang J, Zhang A, et al. PUMA is a novel target of miR-221/222 in human epithelial cancers. Int J Oncol 2010;37: 1621-6.
32. Zhang CZ, Zhang JX, Zhang AL, et al. MiR-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Mol Cancer 2010;9: 229.
33. Garofalo M, Di Leva G, Romano G, et al. miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 2009;16: 498-509.
34. Lerner M, Haneklaus M, Harada M, et al. MiR-200c regulates Noxa expression and sensitivity to proteasomal inhibitors. PLoS One 2012;7: e36490.
35. Muller M, Wilder S, Bannasch D, et al. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J ExpMed 1998;188: 2033-45.
36. Wu GS, Burns TF, McDonald ER, III, et al. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet 1997;17: 141-3.
37. Liu X, Yue P, Khuri FR, et al. p53 upregulates death receptor 4 expression through an intronic p53 binding site. Cancer Res 2004;64: 5078-83.
38. Wang S, Tang Y, Cui H, et al. Let-7/miR-98 regulate Fas and Fas-mediated apoptosis. Genes Immun 2011;12: 149-54.
39. Momand J, Zambetti GP, Olson DC, et al. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992;69: 1237-45.
40. Oliner JD, Pietenpol JA, Thiagalingam S, etal. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 1993;362: 857-60.
41. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997;387: 299-303.
42. Tao W, Levine AJ. Nucleocytoplasmic shuttling of oncoprotein Hdm2 is required for Hdm2-mediated degradation of p53. Proc Natl Acad Sci USA 1999;96: 3077-80.
43. Xiao J, Lin H, Luo X, et al. miR-605 joins p53 network to form a p53: miR-605: Mdm2 positive feedback loop in response to stress. EMBOJ 2011;30: 524-32.
44. Zhang J, Sun Q, Zhang Z, et al. Loss of microRNA-143/145 disturbs cellular growth and apoptosis of human epithelial cancers by impairing the MDM2-p53 feedback loop. Oncogene 2012; doi: 10.1038/onc.2012.28 (Advance Access publication 13 February 2012).
45. Pichiorri F, Suh SS, Rocci A, et al. Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development. Cancer Cell 2010;18: 367-81.
46. Lujambio A, Lowe SW. The microcosmos of cancer. Nature 2012;482: 347-55.
47. Scoumanne A, Cho SJ, Zhang J, etal. The cyclin-dependent kinase inhibitor p21 is regulated by RNA-binding protein PCBP4 via mRNA stability. Nucleic Acids Res 2011;39: 213-24.
48. Battelli C, Nikopoulos CN, Mitchell JG, et al. The RNA-binding protein Musashi-1 regulates neural development through the translational repression of p21WAF-1. Mol Cell Neurosci 2006;31: 85-96.
49. Nikpour P, Baygi ME, Steinhoff C, etal. The RNA binding protein Musashi1 regulates apoptosis, gene expression and stress granule formation in urothelial carcinoma cells. J Cell Mol Med 2011;15: 1210-24.
50. Sureban SM, May R, George RJ, et al. Knockdown of RNA binding protein musashi-1 leads to tumor regression in vivo. Gastroenterology 2008;134: 1448-58.
51. Wang W, Furneaux H, Cheng H, et al. HuR regulates p21 mRNA stabilization by UV light. Mol Cell Biol 2000;20: 760-9.
52. Mazan-Mamczarz K, Galban S, Lopez de Silanes I, et al. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc Natl Acad Sci USA 2003;100: 8354-9.
53. Lal A, Mazan-Mamczarz K, Kawai T, et al. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBOJ 2004;23: 3092-102.
54. Lal A, Abdelmohsen K, Pullmann R, et al. Posttranscriptional derepression of GADD45alpha by genotoxic stress. Mol Cell 2006;22: 117-28.
55. Riley T, Sontag E, Chen P, et al. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008;9: 402-12.
56. He L, He X, Lim LP, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007;447: 1130-4.
57. Hermeking H. p53 enters the microRNA world. Cancer Cell 2007;12: 414-8.
58. 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(5): 745-52.
59. 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.
60. 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(13): 1586-93.
61. Lodygin D, Tarasov V, Epanchintsev A, et al. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008;7: 2591-600.
62. Bommer GT, Gerin I, Feng Y, et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007;17: 1298-307.
63. Tanaka N, Toyooka S, Soh J, et al. Frequent methylation and oncogenic role of microRNA-34b/c in small-cell lung cancer. Lung Cancer 2012;76: 32-8.
64. Chim CS, Wong KY, Qi Y, et al. Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 2010;31: 745-50.
65. Yin D, Ogawa S, Kawamata N, etal. miR-34a functions as a tumor suppressor modulating EGFR in glioblastoma multiforme. Oncogene 2012; doi: 10.1038/onc.2012.132 (Advance Access publication 14 May 2012).
66. Sun F, Fu H, Liu Q, et al. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 2008;582: 1564-8.
67. Toyota M, Suzuki H, Sasaki Y, et al. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 2008;68: 4123-32.
68. Yan D, Zhou X, Chen X, et al. MicroRNA-34a inhibits uveal melanoma cell proliferation and migration through downregulation of c-Met. Invest Ophthalmol Vis Sci 2009; 50: 1559-65.
69. Migliore C, Petrelli A, Ghiso E, et al. MicroRNAs impair MET-mediated invasive growth. Cancer Res 2008;68: 10128-36.
70. Lal A, Thomas MP, Altschuler G, et al. Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet 2011;7: e1002363.
71. Wade M, Rodewald LW, Espinosa JM, et al. BH3 activation blocks Hdmx suppression of apoptosis and cooperates with Nutlin to induce cell death. Cell Cycle 2008;7: 1973-82.
72. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007;7: 415-28.
73. Siemens H, Jackstadt R, Hunten S, etal. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 2011;10: 4256-71.
74. Piovan C, Palmieri D, Di Leva G, et al. Oncosuppressive role of p53-induced miR-205 in triple negative breast cancer. Mol Oncol 2012;6(4): 458-72.
75. Gandellini P, Profumo V, Casamichele A, et al. miR-205 regulates basement membrane deposition in human prostate: implications for cancer development. Cell Death Differ 2012;19(11): 1750-60.
76. Hill L, Browne G, Tulchinsky E. ZEB/miR-200 feedback loop: at the crossroads ofsignal transduction in cancer. Int J cancer 2012; doi: 10.1002/ijc.27708 (Advance Access publication 2 July 2012).
77. Kim T, Veronese A, Pichiorri F, et al. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J ExpMed 2011;208: 875-83.
78. Cho SJ, Zhang J, Chen X. RNPC1 modulates the RNA-binding activity of, and cooperates with, HuR to regulate p21 mRNA stability. Nucleic Acids Res 2010;38: 2256-67.
79. Xu E, Zhang J, Chen X. MDM2 expression is repressed by the RNA-binding protein RNPC1 via mRNA stability. Oncogene 2012; doi: 10.1038/onc.2012.238 (Advance Access publication 18 June 2012).
80. Yan W, Zhang J, Zhang Y, et al. p73 expression is regulated by RNPC1, a target of the p53 family, via mRNA stability. Mol Cell Biol 2012;32: 2336-48.
81. Zhang J, Jun Cho S, Chen X. RNPC1, an RNA-binding protein and a target of the p53 family, regulates p63 expression through mRNA stability. Proc Natl Acad Sci USA 2010; 107: 9614-9.
82. Zhang J, Cho SJ, Shu L, etal. Translational repression of p53 by RNPC1, a p53 target overexpressed in lymphomas. Genes Dev 2011;25: 1528-43.
83. Hotte GJ, Linam-Lennon N, Reynolds JV, et al. Radiation sensitivity of esophageal adenocarcinoma: the contribution of the RNA-binding protein RNPC1 and p21-mediated cell cycle arrest to radioresistance. Radiation Res 2012;177: 272-9.
84. Chen AJ, Paik JH, Zhang H, et al. STAR RNA-binding protein Quaking suppresses cancer via stabilization of specific miRNA. Genes Dev 2012;26: 1459-72.
85. Wesolowska A, Kwiatkowska A, Slomnicki L, et al. Microglia-derived TGF-beta as an important regulator of glioblastoma invasion-an inhibition of TGF-betadependent effects by shRNA against human TGF-beta type II receptor. Oncogene 2008;27: 918-30.
86. Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995;55: 5187-90.
87. Hermeking H, Lengauer C, Polyak K, et al. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell 1997;1: 3-11.
88. Zhang L, Yu J, Park BH, etal. Role of BAX in the apoptotic response to anticancer agents. Science 2000;290: 989-92.
89. Sun A, Bagella L, Tutton S, et al. From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J Cell Biochem 2007;102: 1400-4.
90. Tazawa H, Tsuchiya N, Izumiya M, et al. Tumorsuppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci USA 2007;104: 15472-7.
91. De Wulf P, Montani F, Visintin R. Protein phosphatases take the mitotic stage. Curr Opin Cell Biol 2009;21: 806-15.
92. Peng CY, Graves PR, Thoma RS, et al. Worms, mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 1997;277: 1501-5.
93. Dalal SN, Schweitzer CM, Gan J, et al. Cytoplasmic localization of human cdc25C during interphase requires an intact 14-3-3 binding site. Mol Cell Biol 1999;19: 4465-79.
94. St Clair S, Giono L, Varmeh-Ziaie S, et al. DNA damageinduced downregulation of Cdc25C is mediated by p53 via two independent mechanisms: one involves direct binding to the cdc25C promoter. Mol Cell 2004;16: 725-36.
95. Maxwell CA, McCarthy J, Turley E. Cell-surface and mitotic-spindle RHAMM: moonlighting or dual oncogenic functions? J Cell Sci 2008;121: 925-32.
96. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003;4: 33-45.
97. Godar S, Ince TA, Bell GW, et al. Growth-inhibitory and tumor-suppressive functions of p53 depend on its repression of CD44 expression. Cell 2008;134: 62-73.
98. Sohr S, Engeland K. RHAMM is differentially expressed in the cell cycle and downregulated by the tumor suppressor p53. Cell Cycle 2008;7: 3448-60.
99. Liu C, Kelnar K, Liu B, et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 2011;17: 211-5.
100. Kuribayashi K, Finnberg N, Jeffers JR, et al. The relative contribution of pro-apoptotic p53-target genes in the triggering of apoptosis following DNA damage in vitro and in vivo. Cell Cycle 2011;10: 2380-9.
101. Li H, Zhu H, Xu CJ, et al. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998;94: 491-501.
102. Sax JK, Fei P, Murphy ME, et al. BID regulation by p53 contributes to chemosensitivity. Nat Cell Biol 2002;4: 842-9.
103. Wu Y, Mehew JW, Heckman CA, et al. Negative regulation of bcl-2 expression by p53 in hematopoietic cells. Oncogene 2001;20: 240-51.