Differential association of microRNAs with polysomes reflects distinct strengths of interactions with their mRNA targets

RNA

Volumn 18, Issue 9, 2012, Pages 1612-1623

  Molotski, Natali ^a   Soen, Yoav ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Free energy; High throughput analysis; Human embryonic stem cells; microRNA; Polysomes occupancy of microRNAs

Indexed keywords

DOUBLE STRANDED RNA; MESSENGER RNA; MICRORNA;

ARTICLE; EMBRYONIC STEM CELL; ENERGY; FIBROBLAST; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; POLYSOME; PREPUCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA BINDING; RNA ISOLATION; RNA PURIFICATION; RNA STRUCTURE; RNA TRANSLATION;

CELL LINE; EMBRYONIC STEM CELLS; GENE EXPRESSION; HUMANS; MICRORNAS; POLYRIBOSOMES; PROTEIN BINDING; RNA, MESSENGER;

EID: 84865137034     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.033142.112     Document Type: Article

References (39)

1. Ambros V. 2004. The functions of animal microRNAs. Nature 431: 350-355. (Pubitemid 39265675)
2. Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, Herschlag D. 2003. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci 100: 3889-3894. (Pubitemid 36418127)
3. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
4. Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, Pasquinelli AE. 2005. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122: 553-563. (Pubitemid 41191154)
5. Bartel DP, Chen CZ. 2004. Micromanagers of gene expression: The potentially widespread influence of metazoan microRNAs. Nat Rev Genet 5: 396-400. (Pubitemid 38529411)
6. Brennecke J, Stark A, Russell R, Cohen S. 2005. Principles of microRNA-target recognition. PLoS Biol 3: e85. doi: 10.1371/journal.pbio. 0030085.
7. Carthew RW. 2006. Gene regulation by microRNAs. Curr Opin Genet Dev 16: 203-208. (Pubitemid 43376069)
8. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, et al. 2005. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33: e179. doi: 10.1093/nar/gni178.
9. Doench J, Sharp P. 2004. Specificity of microRNA target selection in translational repression. Genes Dev 18: 504-511. (Pubitemid 38372808)
10. Farh KK, Grimson A, Jan C, Lewis BP, Johnston WK, Lim LP, Burge CB, Bartel DP. 2005. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 310: 1817-1821. (Pubitemid 41814382)
11. Filipowicz W, Bhattacharyya SN, Sonenberg N. 2008. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 9: 102-114.
12. Griffiths-Jones S. 2006. miRBase: The microRNA sequence database. Methods Mol Biol 342: 129-138.
13. Griffiths-Jones S. 2007. Annotating noncoding RNA genes. Annu Rev Genomics Hum Genet 8: 279-298.
14. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. 2008. miRBase: Tools for microRNA genomics. Nucleic Acids Res 36: D154-D158. (Pubitemid 351149713)
15. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. 2007. MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Mol Cell 27: 91-105. (Pubitemid 46991392)
16. Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840.
17. Hendrickson DG, Hogan DJ, McCullough HL, Myers JW, Herschlag D, Ferrell JE, Brown PO. 2009. Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol 7: e1000238. doi: 10.1371/journal.pbio. 1000238.
18. Jackson RJ, Standart N. 2007. How do microRNAs regulate gene expression? Sci STKE 2007: re1. doi: 10.1126/stke.3672007re1.
19. Jannot G, Bajan S, Giguere NJ, Bouasker S, Banville IH, Piquet S, Hutvagner G, Simard MJ. 2011. The ribosomal protein RACK1 is required for microRNA function in both C. elegans and humans. EMBO Rep 12: 581-586.
20. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. 2007. The role of site accessibility in microRNA target recognition. Nat Genet 39: 1278-1284. (Pubitemid 47482690)
21. Kim J, Krichevsky A, Grad Y, Hayes GD, Kosik KS, Church GM, Ruvkun G. 2004. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci 101: 360-365. (Pubitemid 38084255)
22. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773. (Pubitemid 40292988)
23. Maroney PA, Yu Y, Fisher J, Nilsen TW. 2006. Evidence that microRNAs are associated with translating messenger RNAs in human cells. Nat Struct Mol Biol 13: 1102-1107. (Pubitemid 44885921)
24. Meister G. 2007. miRNAs get an early start on translational silencing. Cell 131: 25-28. (Pubitemid 47498539)
25. Melamed D, Eliyahu E, Arava Y. 2009. Exploring translation regulation by global analysis of ribosomal association. Methods 48: 301-305.
26. Mishima Y, Abreu-Goodger C, Staton AA, Stahlhut C, Shou C, Cheng C, Gerstein M, Enright AJ, Giraldez AJ. 2009. Zebrafish miR-1 and miR-133 shape muscle gene expression and regulate sarcomeric actin organization. Genes Dev 23: 619-632.
27. Nelson PT, Hatzigeorgiou AG, Mourelatos Z. 2004. miRNP:mRNA association in polyribosomes in a human neuronal cell line. RNA 10: 387-394. (Pubitemid 38240999)
28. Nielsen CB, Shomron N, Sandberg R, Hornstein E, Kitzman J, Burge CB. 2007. Determinants of targeting by endogenous and exogenous microRNAs and siRNAs. RNA 13: 1894-1910. (Pubitemid 350005216)
29. Nilsen TW. 2007. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet 23: 243-249. (Pubitemid 46628981)
30. Nottrott S, Simard MJ, Richter JD. 2006. Human let-7a miRNA blocks protein production on actively translating polyribosomes. Nat Struct Mol Biol 13: 1108-1114. (Pubitemid 44885922)
31. Olsen PH, Ambros V. 1999. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 216: 671-680. (Pubitemid 30013313)
32. Otsuka M, Takata A, Yoshikawa T, Kojima K, Kishikawa T, Shibata C, Takekawa M, Yoshida H, Omata M, Koike K. 2011. Receptor for activated protein kinase C: Requirement for efficient microRNA function and reduced expression in hepatocellular carcinoma. PLoS ONE 6: e24359. doi: 10.1371/journal.pone.0024359.
33. Petersen CP, Bordeleau ME, Pelletier J, Sharp PA. 2006. Short RNAs repress translation after initiation in mammalian cells. Mol Cell 21: 533-542. (Pubitemid 43228008)
34. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W. 2005. Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309: 1573-1576. (Pubitemid 41266485)
35. Raught B, Gingras A, Sonenberg N. 2001. The target of rapamycin (TOR) proteins. Proc Natl Acad Sci 98: 7037-7044. (Pubitemid 32567899)
36. SelbachM, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
37. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. 2005. Animal microRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 123: 1133-1146. (Pubitemid 41785426)
38. Terada N, Patel H, Takase K, Kohno K, Nairn A, Gelfand E. 1994. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc Natl Acad Sci 91: 11477-11481. (Pubitemid 24356367)
39. Wang B, Yanez A, Novina CD. 2008. MicroRNA-repressed mRNAs contain 40S but not 60S components. Proc Natl Acad Sci 105: 5343-5348. (Pubitemid 351753865)