Disruption of microRNA nuclear transport in human cancer

Seminars in Cancer Biology

Volumn 27, Issue , 2014, Pages 46-51

  Melo, Sonia A ^a,b   Esteller, Manel ^c,d,e  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF PORTO   (Portugal)

^c BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Exportin 5; Microrna biogenesis; MiRNA biogenesis impairment; Nuclear export pre miRNAs; Pre miRNAs

Indexed keywords

EXPORTIN 5; MICRORNA; MICRORNA PRECURSOR; RNA PRECURSOR; UNCLASSIFIED DRUG;

CANCER CELL LINE; CANCER GENETICS; CANCER GROWTH; CARCINOGENESIS; CARCINOGENICITY; CELL NUCLEUS; EPIGENETICS; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE MUTATION; GENE SILENCING; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; ONCOGENE; PROTEIN EXPRESSION; PROTEIN FAMILY; REVIEW; RNA PROCESSING; RNA SYNTHESIS; RNA TRANSPORT; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; ACTIVE TRANSPORT; GENETICS; METABOLISM; NEOPLASM;

ACTIVE TRANSPORT, CELL NUCLEUS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASMS;

EID: 84904461746     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.02.012     Document Type: Review

References (49)

1. Carthew R.W., Sontheimer E.J. Origins and mechanisms of miRNAs and siRNAs. Cell 2009, 136(4):642-655. 10.1016/j.cell.2009.01.035.
2. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466(7308):835-840. 10.1038/nature09267.
3. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136(2):215-233. 10.1016/j.cell.2009.01.002.
4. Kim V.N., Han J., Siomi M.C. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009, 10(2):126-139. 10.1038/nrm2632.
5. Melo S.A., Ropero S., Moutinho C., Aaltonen L.A., Yamamoto H., Calin G.A., et al. A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nat Genet 2009, 41(3):365-370. 10.1038/ng.317.
6. Czech B., Hannon G.J. Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 2011, 12(1):19-31. 10.1038/nrg2916.
7. Doyle M., Badertscher L., Jaskiewicz L., Guttinger S., Jurado S., Hugenschmidt T., et al. The double-stranded RNA binding domain of human Dicer functions as a nuclear localization signal. RNA 2013, 19(9):1238-1252. 10.1261/rna.039255.113.
8. Diederichs S., Haber D.A. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007, 131(6):1097-1108. 10.1016/j.cell.2007.10.032.
9. Cifuentes D., Xue H., Taylor D.W., Patnode H., Mishima Y., Cheloufi S., et al. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 2010, 328(5986):1694-1698. 10.1126/science.1190809.
10. Bohnsack J.F., Whiting A.A., Martinez G., Jones N., Adderson E.E., Detrick S., et al. Serotype III Streptococcus agalactiae from bovine milk and human neonatal infections. Emerg Infect Dis 2004, 10(8):1412-1419. 10.3201/eid1008.030917.
11. Mattaj I.W., Englmeier L. Nucleocytoplasmic transport: the soluble phase. Annu Rev Biochem 1998, 67:265-306. 10.1146/annurev.biochem.67.1.265.
12. Bohnsack M.T., Czaplinski K., Gorlich D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 2004, 10(2):185-191.
13. Lund E., Guttinger S., Calado A., Dahlberg J.E., Kutay U. Nuclear export of microRNA precursors. Science 2004, 303(5654):95-98. 10.1126/science.1090599.
14. Moore M.S., Blobel G. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 1993, 365(6447):661-663. 10.1038/365661a0.
15. Kohler A., Hurt E. Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 2007, 8(10):761-773. 10.1038/nrm2255.
16. Zeng Y., Cullen B.R. Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res 2004, 32(16):4776-4785. 10.1093/nar/gkh824.
17. Kim V.N. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 2005, 6(5):376-385. 10.1038/nrm1644.
18. Mayr C., Bartel D.P. Widespread shortening of 3'UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 2009, 138(4):673-684. 10.1016/j.cell.2009.06.016.
19. Lopez-Serra P., Esteller M. DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene 2012, 31(13):1609-1622. 10.1038/onc.2011.354.
20. Melo S.A., Moutinho C., Ropero S., Calin G.A., Rossi S., Spizzo R., et al. A genetic defect in exportin-5 traps precursor microRNAs in the nucleus of cancer cells. Cancer Cell 2010, 18(4):303-315. 10.1016/j.ccr.2010.09.007.
21. Hill D.A., Ivanovich J., Priest J.R., Gurnett C.A., Dehner L.P., Desruisseau D., et al. DICER1 mutations in familial pleuropulmonary blastoma. Science 2009, 325(5943):965. 10.1126/science.1174334.
22. Kumar M.S., Pester R.E., Chen C.Y., Lane K., Chin C., Lu J., et al. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 2009, 23(23):2700-2704. 10.1101/gad.1848209.
23. De Vito C., Riggi N., Cornaz S., Suva M.L., Baumer K., Provero P., et al. A TARBP2-dependent miRNA expression profile underlies cancer stem cell properties and provides candidate therapeutic reagents in Ewing sarcoma. Cancer Cell 2012, 21(6):807-821. 10.1016/j.ccr.2012.04.023.
24. Kim M.S., Oh J.E., Kim Y.R., Park S.W., Kang M.R., Kim S.S., et al. Somatic mutations and losses of expression of microRNA regulation-related genes AGO2 and TNRC6A in gastric and colorectal cancers. J Pathol 2010, 221(2):139-146. 10.1002/path.2683.
25. Yi R., Doehle B.P., Qin Y., Macara I.G., Cullen B.R. Overexpression of exportin 5 enhances RNA interference mediated by short hairpin RNAs and microRNAs. RNA 2005, 11(2):220-226. 10.1261/rna.7233305.
26. Lee E.J., Baek M., Gusev Y., Brackett D.J., Nuovo G.J., Schmittgen T.D. Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors. RNA 2008, 14(1):35-42. 10.1261/rna.804508.
27. Bussing I., Yang J.S., Lai E.C., Grosshans H. The nuclear export receptor XPO-1 supports primary miRNA processing in C. elegans and Drosophila. EMBO J 2010, 29(11):1830-1839. 10.1038/emboj.2010.82.
28. Yang J.S., Lai E.C. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 2011, 43(6):892-903. 10.1016/j.molcel.2011.07.024.
29. Wan G., Zhang X., Langley R.R., Liu Y., Hu X., Han C., et al. DNA-damage-induced nuclear export of precursor microRNAs is regulated by the ATM-AKT pathway. Cell Rep 2013, 3(6):2100-2112. 10.1016/j.celrep.2013.05.038.
30. Castanotto D., Lingeman R., Riggs A.D., Rossi J.J. CRM1 mediates nuclear-cytoplasmic shuttling of mature microRNAs. Proc Natl Acad Sci USA 2009, 106(51):21655-21659. 10.1073/pnas.0912384106.
31. Li Z.F., Liang Y.M., Lau P.N., Shen W., Wang D.K., Cheung W.T., et al. Dynamic localisation of mature microRNAs in Human nucleoli is influenced by exogenous genetic materials. PLoS ONE 2013, 8(8):e70869. 10.1371/journal.pone.0070869.
32. Hwang H.W., Wentzel E.A., Mendell J.T. A hexanucleotide element directs microRNA nuclear import. Science 2007, 315(5808):97-100. 10.1126/science.1136235.
33. Younger S.T., Corey D.R. Transcriptional gene silencing in mammalian cells by miRNA mimics that target gene promoters. Nucl Acids Res 2011, 39(13):5682-5691. 10.1093/nar/gkr155.
34. Huang V., Place R.F., Portnoy V., Wang J., Qi Z., Jia Z., et al. Upregulation of Cyclin B1 by miRNA and its implications in cancer. Nucl Acids Res 2012, 40(4):1695-1707. 10.1093/nar/gkr934.
35. Place R.F., Li L.C., Pookot D., Noonan E.J., Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci USA 2008, 105(5):1608-1613. 10.1073/pnas.0707594105.
36. Kim D.H., Saetrom P., Snove O., Rossi J.J. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci USA 2008, 105(42):16230-16235. 10.1073/pnas.0808830105.
37. Lu J., Getz G., Miska E.A., Alvarez-Saavedra E., Lamb J., Peck D., et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435(7043):834-838. 10.1038/nature03702.
38. He L., Thomson J.M., Hemann M.T., Hernando-Monge E., Mu D., Goodson S., et al. A microRNA polycistron as a potential human oncogene. Nature 2005, 435(7043):828-833. 10.1038/nature03552.
39. O'Donnell K.A., Wentzel E.A., Zeller K.I., Dang C.V., Mendell J.T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005, 435(7043):839-843. 10.1038/nature03677.
40. Li X., Cassidy J.J., Reinke C.A., Fischboeck S., Carthew R.W. A microRNA imparts robustness against environmental fluctuation during development. Cell 2009, 137(2):273-282. 10.1016/j.cell.2009.01.058.
41. Xu N., Papagiannakopoulos T., Pan G., Thomson J.A., Kosik K.S. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 2009, 137(4):647-658. 10.1016/j.cell.2009.02.038.
42. Suzuki H.I., Yamagata K., Sugimoto K., Iwamoto T., Kato S., Miyazono K. Modulation of microRNA processing by p53. Nature 2009, 460(7254):529-533. 10.1038/nature08199.
43. Davis B.N., Hilyard A.C., Lagna G., Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008, 454(7200):56-61. 10.1038/nature07086.
44. Wang X., Zhao X., Gao P., Wu M. c-Myc modulates microRNA processing via the transcriptional regulation of Drosha. Scientific reports 2013, 3:1942. 10.1038/srep01942.
45. Chang T.C., Yu D., Lee Y.S., Wentzel E.A., Arking D.E., West K.M., et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 2008, 40(1):43-50. 10.1038/ng.2007.30.
46. Shen J., Xia W., Khotskaya Y.B., Huo L., Nakanishi K., Lim S.O., et al. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 2013, 497(7449):383-387. 10.1038/nature12080.
47. Cawley K., Logue S.E., Gorman A.M., Zeng Q., Patterson J., Gupta S., et al. Disruption of microRNA biogenesis confers resistance to ER stress-induced cell death upstream of the mitochondrion. PLoS ONE 2013, 8(8):e73870. 10.1371/journal.pone.0073870.
48. Muqbil I., Bao B., Abou-Samra A.B., Mohammad R.M., Azmi A.S. Nuclear export mediated regulation of microRNAs: potential target for drug intervention. Curr Drug Targets 2013, 14(10):1094-1100.
49. Melo S., Villanueva A., Moutinho C., Davalos V., Spizzo R., Ivan C., et al. Small molecule enoxacin is a cancer-specific growth inhibitor that acts by enhancing TAR RNA-binding protein 2-mediated microRNA processing. Proc Natl Acad Sci USA 2011, 108(11):4394-4399. 10.1073/pnas.1014720108.