The Effects of miR-20a on p21: Two Mechanisms Blocking Growth Arrest in TGF-β-Responsive Colon Carcinoma

Journal of Cellular Physiology

Volumn 230, Issue 12, 2015, Pages 3105-3114

  Sokolova, Viktorija ^a,b   Fiorino, Antonio ^b   Zoni, Eugenio ^a,b   Crippa, Elisabetta ^a,b   Reid, James F ^a,b   Gariboldi, Manuela ^a,b   Pierotti, Marco A ^b  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1A; MESSENGER RNA; MICRORNA; MICRORNA 17; MICRORNA 20A; MICRORNA 92; MYC PROTEIN; PROTEIN P21; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CDKN1A PROTEIN, HUMAN; MIRN20 MICRORNA, HUMAN; MYC PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ALLELE; ARTICLE; CANCER INHIBITION; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; COLON CARCINOMA; COLON MUCOSA; G1 PHASE CELL CYCLE CHECKPOINT; GENE CONTROL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; BINDING SITE; CACO 2 CELL LINE; CARCINOMA; CELL PROLIFERATION; COLON TUMOR; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; HT 29 CELL LINE; HUMAN; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

3' UNTRANSLATED REGIONS; BINDING SITES; CACO-2 CELLS; CARCINOMA; CELL PROLIFERATION; COLONIC NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HEK293 CELLS; HT29 CELLS; HUMANS; MICRORNAS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-MYC; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84939817596     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25051     Document Type: Article

References (60)

1. Ando T, Sugai T, Habano W, Jiao YF, Suzuki K. 2005. Analysis of SMAD4/DPC4 gene alterations in multiploid colorectal carcinomas. J Gastroenterol 40:708-715.
2. Babar IA, Cheng CJ, Booth CJ, Liang X, Weidhaas JB, Saltzman WM, Slack FJ. 2012. Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc Natl Acad Sci USA 109:E1695-E1704.
3. Brattain MG, Levine AE, Chakrabarty S, Yeoman LC, Willson JK, Long B. 1984. Heterogeneity of human colon carcinoma. Cancer Metastasis Rev 3:177-191.
4. Buck A, Buchholz M, Wagner M, Adler G, Gress T, Ellenrieder V. 2006. The tumor suppressor KLF11 mediates a novel mechanism in transforming growth factor beta-induced growth inhibition that is inactivated in pancreatic cancer. Mol Cancer Res 4:861-872.
5. Buscemi G, Ricci C, Zannini L, Fontanella E, Plevani P, Delia D. 2014. Bimodal regulation of p21(waf1) protein as function of DNA damage levels. Cell Cycle 13:2901-2912.
6. Butz H, Racz K, Hunyady L, Patocs A. 2012. Crosstalk between TGF-beta signaling and the microRNA machinery. Trends Pharmacol Sci 33:382-393.
7. Chen CR, Kang Y, Siegel PM, Massague J. 2002. E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 110:19-32.
8. Claassen GF, Hann SR. 2000. A role for transcriptional repression of p21CIP1 by c-Myc in overcoming transforming growth factor beta-induced cell-cycle arrest. Proc Natl Acad Sci USA 97:9498-9503.
9. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. 1995. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 92:5545-5549.
10. Davis BN, Hilyard AC, Lagna G, Hata A. 2008. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454:56-61.
11. Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A. 2010. Smad proteins bind a conserved RNA sequence to promote microRNA maturation by Drosha. Mol Cell 39:373-384.
12. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. 1998. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. Embo J 17:3091-3100.
13. Dews M, Fox JL, Hultine S, Sundaram P, Wang W, Liu YY, Furth E, Enders GH, El-Deiry W, Schelter JM, Cleary MA, Thomas-Tikhonenko A. 2010. The myc-miR-17∼92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors. Cancer Res 70:8233-8246.
14. Engle SJ, Hoying JB, Boivin GP, Ormsby I, Gartside PS, Doetschman T. 1999. Transforming growth factor beta1 suppresses nonmetastatic colon cancer at an early stage of tumorigenesis. Cancer Res 59:3379-3386.
15. Fearon ER. 2011. Molecular genetics of colorectal cancer. Annu Rev Pathol 6:479-507.
16. Fearon ER, Vogelstein B. 1990. A genetic model for colorectal tumorigenesis. Cell 61:759-767.
17. Gartel AL, Tyner AL. 1999. Transcriptional regulation of the p21((WAF1/CIP1)) gene. Exp Cell Res 246:280-289.
18. Gayet J, Zhou XP, Duval A, Rolland S, Hoang JM, Cottu P, Hamelin R. 2001. Extensive characterization of genetic alterations in a series of human colorectal cancer cell lines. Oncogene 20:5025-5032.
19. Gong J, Ammanamanchi S, Ko TC, Brattain MG. 2003. Transforming growth factor beta 1 increases the stability of p21/WAF1/CIP1 protein and inhibits CDK2 kinase activity in human colon carcinoma FET cells. Cancer Res 63:3340-3346.
20. Grady WM, Myeroff LL, Swinler SE, Rajput A, Thiagalingam S, Lutterbaugh JD, Neumann A, Brattain MG, Chang J, Kim SJ, Kinzler KW, Vogelstein B, Willson JK, Markowitz S. 1999. Mutational inactivation of transforming growth factor beta receptor type II in microsatellite stable colon cancers. Cancer Res 59:320-324.
21. Grady WM, Rajput A, Myeroff L, Liu DF, Kwon K, Willis J, Markowitz S. 1998. Mutation of the type II transforming growth factor-beta receptor is coincident with the transformation of human colon adenomas to malignant carcinomas. Cancer Res 58:3101-3104.
22. Hannon GJ, Beach D. 1994. P15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature 371:257-261.
23. Hasegawa Y, Takanashi S, Kanehira Y, Tsushima T, Imai T, Okumura K. 2001. Transforming growth factor-beta1 level correlates with angiogenesis, tumor progression, and prognosis in patients with nonsmall cell lung carcinoma. Cancer 91:964-971.
24. Hong L, Lai M, Chen M, Xie C, Liao R, Kang YJ, Xiao C, Hu WY, Han J, Sun P. 2010. The miR-17-92 cluster of microRNAs confers tumorigenicity by inhibiting oncogene-induced senescence. Cancer Res 70:8547-8557.
25. Hsu S, Huang F, Hafez M, Winawer S, Friedman E. 1994. Colon carcinoma cells switch their response to transforming growth factor beta 1 with tumor progression. Cell Growth Differ 5:267-275.
26. Inomata M, Tagawa H, Guo YM, Kameoka Y, Takahashi N, Sawada K. 2009. MicroRNA- 17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood 113:396-402.
27. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. 2011. Global cancer statistics. CA Cancer J Clin 61:69-90.
28. Koutsodontis G, Moustakas A, Kardassis D. 2002. The role of Sp1 family members, the proximal GC-rich motifs, and the upstream enhancer region in the regulation of the human cell cycle inhibitor p21WAF-1/Cip1 gene promoter. Biochemistry 41:12771-12784.
29. Lao VV, Grady WM. 2011. Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol 8:686-700.
30. Lawrence MS, Stojanov P, Mermel CH, Robinson JT, Garraway LA, Golub TR, Meyerson M, Gabriel SB, Lander ES, Getz G. 2014. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 505:495-501.
31. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
32. Li L, Shi JY, Zhu GQ, Shi B. 2012. MiR-17-92 cluster regulates cell proliferation and collagen synthesis by targeting TGFB pathway in mouse palatal mesenchymal cells. J Cell Biochem 113:1235-1244.
33. Massague J. 2012. TGFbeta signalling in context. Nat Rev Mol Cell Biol 13:616-630.
34. Mestdagh P, Bostrom AK, Impens F, Fredlund E, Van Peer G, De Antonellis P, von Stedingk K, Ghesquiere B, Schulte S, Dews M, Thomas-Tikhonenko A, Schulte JH, Zollo M, Schramm A, Gevaert K, Axelson H, Speleman F, Vandesompele J. 2010. The miR-17-92 microRNA cluster regulates multiple components of the TGF-beta pathway in neuroblastoma. Mol Cell 40:762-773.
35. Mulder KM, Levine AE, Hernandez X, McKnight MK, Brattain DE, Brattain MG. 1988. Modulation of c-myc by transforming growth factor-beta in human colon carcinoma cells. Biochem Biophys Res Commun 150:711-716.
36. Mulder KM, Zhong Q, Choi HG, Humphrey LE, Brattain MG. 1990. Inhibitory effects of transforming growth factor beta 1 on mitogenic response, transforming growth factor alpha, and c-myc in quiescent, well-differentiated colon carcinoma cells. Cancer Res 50:7581-7586.
37. Network CGA. 2012. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487:330-337.
38. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. 2005. C-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839-843.
39. Ogino S, Nosho K, Irahara N, Shima K, Baba Y, Kirkner GJ, Meyerhardt JA, Fuchs CS. 2009. Prognostic significance and molecular associations of 18q loss of heterozygosity: A cohort study of microsatellite stable colorectal cancers. J Clin Oncol 27:4591-4598.
40. Okayama H, Schetter AJ, Harris CC. 2012. MicroRNAs and inflammation in the pathogenesis and progression of colon cancer. Dig Dis 30:9-15.
41. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, Iliopoulos D, Pilozzi E, Liu CG, Negrini M, Cavazzini L, Volinia S, Alder H, Ruco LP, Baldassarre G, Croce CM, Vecchione A. 2008. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer cell 13:272-286.
42. Reid JF, Gariboldi M, Sokolova V, Capobianco P, Lampis A, Perrone F, Signoroni S, Costa A, Leo E, Pilotti S, Pierotti MA. 2009. Integrative approach for prioritizing cancer genes in sporadic colon cancer. Genes Chromosomes Cancer 48:953-962.
43. Reid JF, Sokolova V, Zoni E, Lampis A, Pizzamiglio S, Bertan C, Zanutto S, Perrone F, Camerini T, Gallino G, Verderio P, Leo E, Pilotti S, Gariboldi M, Pierotti MA. 2012. MiRNA profiling in colorectal cancer highlights miR-1 involvement in MET-dependent proliferation. Mol Cancer Res 10:504-515.
44. Reynisdottir I, Polyak K, Iavarone A, Massague J. 1995. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev 9:1831-1845.
45. Rogler CE, Levoci L, Ader T, Massimi A, Tchaikovskaya T, Norel R, Rogler LE. 2009. MicroRNA-23b cluster microRNAs regulate transforming growth factor-beta/bone morphogenetic protein signaling and liver stem cell differentiation by targeting Smads. Hepatology 50:575-584.
46. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, Yuen ST, Chan TL, Kwong DL, Au GK, Liu CG, Calin GA, Croce CM, Harris CC. 2008. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 299:425-436.
47. Seoane J, Le HV, Massague J. 2002. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419:729-734.
48. Siegel PM, Massague J. 2003. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3:807-821.
49. Slaby O, Svoboda M, Michalek J, Vyzula R. 2009. MicroRNAs in colorectal cancer: Translation of molecular biology into clinical application. Mol Cancer 8:102.
50. Staller P, Peukert K, Kiermaier A, Seoane J, Lukas J, Karsunky H, Moroy T, Bartek J, Massague J, Hanel F, Eilers M. 2001. Repression of p15INK4b expression by Myc through association with Miz-1. Nat Cell Biol 3:392-399.
51. Stearns ME, Garcia FU, Fudge K, Rhim J, Wang M. 1999. Role of interleukin 10 and transforming growth factor beta1 in the angiogenesis and metastasis of human prostate primary tumor lines from orthotopic implants in severe combined immunodeficiency mice. Clin Cancer Res 5:711-720.
52. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, Ferbeyre G, Chartrand P. 2007. An E2F/miR-20a autoregulatory feedback loop. J Biol Chem 282:2135-2143.
53. Tili E, Michaille JJ, Liu CG, Alder H, Taccioli C, Volinia S, Calin GA, Croce CM. 2010. GAM/ZFp/ZNF512B is central to a gene sensor circuitry involving cell-cycle regulators, TGF{beta} effectors, Drosha and microRNAs with opposite oncogenic potentials. Nucleic Acids Res 38:7673-7688.
54. Trompeter HI, Abbad H, Iwaniuk KM, Hafner M, Renwick N, Tuschl T, Schira J, Muller HW, Wernet P. 2011. MicroRNAs MiR-17, MiR-20a, and MiR-106b act in concert to modulate E2F activity on cell cycle arrest during neuronal lineage differentiation of USSC. PLoS ONE 6:e16138.
55. Woods K, Thomson JM, Hammond SM. 2007. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 282:2130-2134.
56. Wu S, Huang S, Ding J, Zhao Y, Liang L, Liu T, Zhan R, He X. 2010. Multiple microRNAs modulate p21Cip1/Waf1 expression by directly targeting its 3′ untranslated region. Oncogene 29:2302-2308.
57. Wu SP, Theodorescu D, Kerbel RS, Willson JK, Mulder KM, Humphrey LE, Brattain MG. 1992. TGF-beta 1 is an autocrine-negative growth regulator of human colon carcinoma FET cells in vivo as revealed by transfection of an antisense expression vector. J Cell Biol 116:187-196.
58. Yagi K, Furuhashi M, Aoki H, Goto D, Kuwano H, Sugamura K, Miyazono K, Kato M. 2002. C-myc is a downstream target of the Smad pathway. J Biol Chem 277:854-861.
59. Ye SC, Foster JM, Li W, Liang J, Zborowska E, Venkateswarlu S, Gong J, Brattain MG, Willson JK. 1999. Contextual effects of transforming growth factor beta on the tumorigenicity of human colon carcinoma cells. Cancer Res 59:4725-4731.
60. Zhang JX, Song W, Chen ZH, Wei JH, Liao YJ, Lei J, Hu M, Chen GZ, Liao B, Lu J, Zhao HW, Chen W, He YL, Wang HY, Xie D, Luo JH. ( 2013). Prognostic and predictive value of a microRNA signature in stage II colon cancer: A microRNA expression analysis. Lancet Oncol 14, 1295-1306.