MicroRNA-34a modulates MDM4 expression via a target site in the open reading frame

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Mandke, Pooja ^a   Wyatt, Nicholas ^a   Fraser, Jillian ^a   Bates, Benjamin ^a   Berberich, Steven J ^a   Markey, Michael P ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LUCIFERASE; MICRORNA 34A; PROTEIN MDMX;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXON; EXON 11; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN BLOOD LEVEL; REGULATORY MECHANISM; REPORTER GENE; RNA SYNTHESIS;

CELL LINE, TUMOR; DNA DAMAGE; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; NUCLEAR PROTEINS; OPEN READING FRAMES; PROTO-ONCOGENE PROTEINS; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINATION;

EID: 84864755975     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042034     Document Type: Article

References (54)

1. Mancini F, Moretti F, (2009) Mitochondrial MDM4 (MDMX): an unpredicted role in the p53-mediated intrinsic apoptotic pathway. Cell Cycle 8: 3854-3859.
2. Toledo F, Krummel KA, Lee CJ, Liu CW, Rodewald LW, et al. (2006) A mouse p53 mutant lacking the proline-rich domain rescues Mdm4 deficiency and provides insight into the Mdm2-Mdm4-p53 regulatory network. Cancer Cell 9: 273-285.
3. Rickman DS, Bobek MP, Misek DE, Kuick R, Blaivas M, et al. (2001) Distinctive molecular profiles of high-grade and low-grade gliomas based on oligonucleotide microarray analysis. Cancer Res 61: 6885-6891.
4. Riemenschneider MJ, Buschges R, Wolter M, Reifenberger J, Bostrom J, et al. (1999) Amplification and overexpression of the MDM4 (MDMX) gene from 1q32 in a subset of malignant gliomas without TP53 mutation or MDM2 amplification. Cancer Res 59: 6091-6096.
5. Riemenschneider MJ, Knobbe CB, Reifenberger G, (2003) Refined mapping of 1q32 amplicons in malignant gliomas confirms MDM4 as the main amplification target. Int J Cancer 104: 752-757.
6. Laurie NA, Donovan SL, Shih CS, Zhang J, Mills N, et al. (2006) Inactivation of the p53 pathway in retinoblastoma. Nature 444: 61-66.
7. Hu B, Gilkes DM, Farooqi B, Sebti SM, Chen J, (2006) MDMX overexpression prevents p53 activation by the MDM2 inhibitor Nutlin. J Biol Chem 281: 33030-33035.
8. Garcia D, Warr MR, Martins CP, Brown Swigart L, Passegue E, et al. (2011) Validation of MdmX as a therapeutic target for reactivating p53 in tumors. Genes Dev 25: 1746-1757.
9. Kawai H, Wiederschain D, Kitao H, Stuart J, Tsai KK, et al. (2003) DNA damage-induced MDMX degradation is mediated by MDM2. J Biol Chem 278: 45946-45953.
10. Pan Y, Chen J, (2003) MDM2 promotes ubiquitination and degradation of MDMX. Mol Cell Biol 23: 5113-5121.
11. Li C, Chen L, Chen J, (2002) DNA damage induces MDMX nuclear translocation by p53-dependent and-independent mechanisms. Mol Cell Biol 22: 7562-7571.
12. Ohtsubo C, Shiokawa D, Kodama M, Gaiddon C, Nakagama H, et al. (2009) Cytoplasmic tethering is involved in synergistic inhibition of p53 by Mdmx and Mdm2. Cancer Sci 100: 1291-1299.
13. Li M, Gu W, (2011) A critical role for noncoding 5S rRNA in regulating Mdmx stability. Mol Cell 43: 1023-1032.
14. Gilkes DM, Pan Y, Coppola D, Yeatman T, Reuther GW, et al. (2008) Regulation of MDMX expression by mitogenic signaling. Mol Cell Biol 28: 1999-2010.
15. Markey MP, (2011) Regulation of MDM4. Front Biosci 16: 1144-1156.
16. Phillips A, Teunisse A, Lam S, Lodder K, Darley M, et al. (2010) HDMX-L is expressed from a functional p53-responsive promoter in the first intron of the HDMX gene and participates in an autoregulatory feedback loop to control p53 activity. J Biol Chem 285: 29111-29127.
17. Markey M, Berberich SJ, (2008) Full-length hdmX transcripts decrease following genotoxic stress. Oncogene 27: 6657-6666.
18. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, et al. (2007) p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 17: 1298-1307.
19. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, et al. (2007) Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 26: 745-752.
20. He L, He X, Lim LP, de Stanchina E, Xuan Z, et al. (2007) A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134.
21. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, et al. (2007) Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 26: 731-743.
22. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, et al. (2007) Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6: 1586-1593.
23. He X, He L, Hannon GJ, (2007) The guardian's little helper: microRNAs in the p53 tumor suppressor network. Cancer Res 67: 11099-11101.
24. Hermeking H, (2010) The miR-34 family in cancer and apoptosis. Cell Death Differ 17: 193-199.
25. Harris CC, Hollstein M, (1993) Clinical implications of the p53 tumor-suppressor gene. N Engl J Med 329: 1318-1327.
26. Danovi D, Meulmeester E, Pasini D, Migliorini D, Capra M, et al. (2004) Amplification of Mdmx (or Mdm4) directly contributes to tumor formation by inhibiting p53 tumor suppressor activity. Mol Cell Biol 24: 5835-5843.
27. Sun F, Fu H, Liu Q, Tie Y, Zhu J, et al. (2008) Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 582: 1564-1568.
28. Betel D, Koppal A, Agius P, Sander C, Leslie C, (2010) Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 11: R90.
29. Jan CH, Friedman RC, Ruby JG, Bartel DP, (2011) Formation, regulation and evolution of Caenorhabditis elegans 3′UTRs. Nature 469: 97-101.
30. Allende-Vega N, Sparks A, Lane DP, Saville MK, (2010) MdmX is a substrate for the deubiquitinating enzyme USP2a. Oncogene 29: 432-441.
31. Cummins JM, Rago C, Kohli M, Kinzler KW, Lengauer C,et al. (2004) Tumour suppression: disruption of HAUSP gene stabilizes p53. Nature 428: 1 p following 486.
32. Wynendaele J, Bohnke A, Leucci E, Nielsen SJ, Lambertz I, et al. (2010) An illegitimate microRNA target site within the 3′UTR of MDM4 affects ovarian cancer progression and chemosensitivity. Cancer Res 70: 9641-9649.
33. Ovcharenko D, Stolzel F, Poitz D, Fierro F, Schaich M, et al. (2011) miR-10a overexpression is associated with NPM1 mutations and MDM4 downregulation in intermediate-risk acute myeloid leukemia. Exp Hematol 39 (1030-1042): e1037.
34. Allende-Vega N, Dayal S, Agarwala U, Sparks A, Bourdon JC, et al. (2012) p53 is activated in response to disruption of the pre-mRNA splicing machinery. Oncogene.
35. Barak Y, Gottlieb E, Juven-Gershon T, Oren M, (1994) Regulation of mdm2 expression by p53: alternative promoters produce transcripts with nonidentical translation potential. Genes Dev 8: 1739-1749.
36. Duursma AM, Kedde M, Schrier M, le Sage C, Agami R, (2008) miR-148 targets human DNMT3b protein coding region. Rna 14: 872-877.
37. Chen X, (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303: 2022-2025.
38. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, et al. (2002) Prediction of plant microRNA targets. Cell 110: 513-520.
39. Takagi S, Nakajima M, Kida K, Yamaura Y, Fukami T, et al. (2010) MicroRNAs regulate human hepatocyte nuclear factor 4alpha, modulating the expression of metabolic enzymes and cell cycle. J Biol Chem 285: 4415-4422.
40. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105.
41. Fang Z, Rajewsky N, (2011) The impact of miRNA target sites in coding sequences and in 3′UTRs. PLoS One 6: e18067.
42. Giglio S, Mancini F, Gentiletti F, Sparaco G, Felicioni L, et al. (2005) Identification of an aberrantly spliced form of HDMX in human tumors: a new mechanism for HDM2 stabilization. Cancer Res 65: 9687-9694.
43. de Graaf P, Little NA, Ramos YF, Meulmeester E, Letteboer SJ, et al. (2003) Hdmx protein stability is regulated by the ubiquitin ligase activity of Mdm2. J Biol Chem 278: 38315-38324.
44. Chandler DS, Singh RK, Caldwell LC, Bitler JL, Lozano G, (2006) Genotoxic stress induces coordinately regulated alternative splicing of the p53 modulators MDM2 and MDM4. Cancer Res 66: 9502-9508.
45. Bartel F, Schulz J, Blumke K, Kappler M, Bache M, et al. (2004) [HDMX amplification and high levels of HDMX-S splice variant are correlated with a poor prognosis in soft tissue sarcomas]. Verh Dtsch Ges Pathol 88: 199-206.
46. Bartel F, Schulz J, Bohnke A, Blumke K, Kappler M, et al. (2005) Significance of HDMX-S (or MDM4) mRNA splice variant overexpression and HDMX gene amplification on primary soft tissue sarcoma prognosis. Int J Cancer 117: 469-475.
47. Consortium TGP, (2010) A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073.
48. Wirsing A, Senkel S, Klein-Hitpass L, Ryffel GU, (2011) A systematic analysis of the 3′UTR of HNF4A mRNA reveals an interplay of regulatory elements including miRNA target sites. PLoS One 6: e27438.
49. Yamakuchi M, Lowenstein CJ, (2009) MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle 8: 712-715.
50. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, et al. (2001) hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107: 149-159.
51. Lal A, Thomas MP, Altschuler G, Navarro F, O'Day E, et al. (2012) Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet 7: e1002363.
52. Rasband WS (2008) ImageJ. Bethesda, Maryland: U. S. National Institutes of Health.
53. Betel D, Wilson M, Gabow A, Marks DS, Sander C, (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36: D149-153.
54. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.