MRNA Destabilization Is the dominant effect of mammalian microRNAs by the time substantial repression ensues

Molecular Cell

Volumn 56, Issue 1, 2014, Pages 104-115

  Eichhorn, Stephen W ^a,b   Guo, Huili ^a,b,c,d,e   McGeary, Sean E ^a,b   Rodriguez Mias, Ricard A ^f   Shin, Chanseok ^a,b,g   Baek, Daehyun ^a,b,h,i   Hsu, Shu hao ^j   Ghoshal, Kalpana ^j   Villén, Judit ^f   Bartel, David P ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^f UNIVERSITY OF WASHINGTON   (United States)

^g Seoul National University   (South Korea)

^h Institute for Basic Science   (South Korea)

ⁱ Seoul National University   (South Korea)

^j OHIO STATE UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA;

ARTICLE; CELL GROWTH; CELLS BY BODY ANATOMY; DOMINANT GENE; DYNAMICS; HIGH THROUGHPUT SEQUENCING; MAMMAL; OPEN READING FRAME; PROTEOMICS; RNA DEGRADATION; RNA SEQUENCE; STEADY STATE; TIME; TRANSLATION INITIATION; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; RNA STABILITY;

MAMMALIA;

GENE EXPRESSION REGULATION; MICRORNAS; MODELS, GENETIC; RNA STABILITY; RNA, MESSENGER;

EID: 84922394487     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.08.028     Document Type: Article

References (58)

1. Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P. The impact of microRNAs on protein output. Nature 2008, 455:64-71.
2. Bagga S., Bracht J., Hunter S., Massirer K., Holtz J., Eachus R., Pasquinelli A.E. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 2005, 122:553-563.
3. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
4. Bazzini A.A., Lee M.T., Giraldez A.J. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 2012, 336:233-237.
5. Behm-Ansmant I., Rehwinkel J., Doerks T., Stark A., Bork P., Izaurralde E. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 2006, 20:1885-1898.
6. Béthune J., Artus-Revel C.G., Filipowicz W. Kinetic analysis reveals successive steps leading to miRNA-mediated silencing in mammalian cells. EMBO Rep. 2012, 13:716-723.
7. Braun J.E., Huntzinger E., Fauser M., Izaurralde E. GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol. Cell 2011, 44:120-133.
8. Braun J.E., Huntzinger E., Izaurralde E. A molecular link between miRISCs and deadenylases provides new insight into the mechanism of gene silencing by microRNAs. Cold Spring Harb. Perspect. Biol. 2012, 4:4.
9. Castilla-Llorente V., Spraggon L., Okamura M., Naseeruddin S., Adamow M., Qamar S., Liu J. Mammalian GW220/TNGW1 is essential for the formation of GW/P bodies containing miRISC. J.Cell Biol. 2012, 198:529-544.
10. Chekulaeva M., Mathys H., Zipprich J.T., Attig J., Colic M., Parker R., Filipowicz W. miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat. Struct. Mol. Biol. 2011, 18:1218-1226.
11. Chen J.F., Mandel E.M., Thomson J.M., Wu Q., Callis T.E., Hammond S.M., Conlon F.L., Wang D.Z. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 2006, 38:228-233.
12. Chen C.Y., Zheng D., Xia Z., Shyu A.B. Ago-TNRC6 triggers microRNA-mediated decay by promoting two deadenylation steps. Nat. Struct. Mol. Biol. 2009, 16:1160-1166.
13. Coccia E.M., Profita V., Fiorucci G., Romeo G., Affabris E., Testa U., Hentze M.W., Battistini A. Modulation of ferritin H-chain expression in Friend erythroleukemia cells: transcriptional and translational regulation by hemin. Mol. Cell. Biol. 1992, 12:3015-3022.
14. Cooke A., Prigge A., Wickens M. Translational repression by deadenylases. J.Biol. Chem. 2010, 285:28506-28513.
15. Deana A., Belasco J.G. Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev. 2005, 19:2526-2533.
16. Djuranovic S., Nahvi A., Green R. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 2012, 336:237-240.
17. Doench J.G., Sharp P.A. Specificity of microRNA target selection in translational repression. Genes Dev. 2004, 18:504-511.
18. Eulalio A., Rehwinkel J., Stricker M., Huntzinger E., Yang S.F., Doerks T., Dorner S., Bork P., Boutros M., Izaurralde E. Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev. 2007, 21:2558-2570.
19. Eulalio A., Huntzinger E., Izaurralde E. GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat. Struct. Mol. Biol. 2008, 15:346-353.
20. Eulalio A., Huntzinger E., Nishihara T., Rehwinkel J., Fauser M., Izaurralde E. Deadenylation is a widespread effect of miRNA regulation. RNA 2009, 15:21-32.
21. Fabian M.R., Mathonnet G., Sundermeier T., Mathys H., Zipprich J.T., Svitkin Y.V., Rivas F., Jinek M., Wohlschlegel J., Doudna J.A., et al. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol. Cell 2009, 35:868-880.
22. Friedman R.C., Farh K.K., Burge C.B., Bartel D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19:92-105.
23. Garcia D.M., Baek D., Shin C., Bell G.W., Grimson A., Bartel D.P. Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat. Struct. Mol. Biol. 2011, 18:1139-1146.
24. Giraldez A.J., Cinalli R.M., Glasner M.E., Enright A.J., Thomson J.M., Baskerville S., Hammond S.M., Bartel D.P., Schier A.F. MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308:833-838.
25. Giraldez A.J., Mishima Y., Rihel J., Grocock R.J., Van Dongen S., Inoue K., Enright A.J., Schier A.F. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312:75-79.
26. Grimson A., Farh K.K., Johnston W.K., Garrett-Engele P., Lim L.P., Bartel D.P. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 2007, 27:91-105.
27. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
28. Hendrickson D.G., Hogan D.J., McCullough H.L., Myers J.W., Herschlag D., Ferrell J.E., Brown P.O. Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol. 2009, 7:e1000238.
29. Hentze M.W., Rouault T.A., Caughman S.W., Dancis A., Harford J.B., Klausner R.D. A cis-acting element is necessary and sufficient for translational regulation of human ferritin expression in response to iron. Proc. Natl. Acad. Sci. USA 1987, 84:6730-6734.
30. Holtz J., Pasquinelli A.E. Uncoupling of lin-14 mRNA and protein repression by nutrient deprivation in Caenorhabditis elegans. RNA 2009, 15:400-405.
31. Huo Y., Iadevaia V., Yao Z., Kelly I., Cosulich S., Guichard S., Foster L.J., Proud C.G. Stable isotope-labelling analysis of the impact of inhibition of the mammalian target of rapamycin on protein synthesis. Biochem. J. 2012, 444:141-151.
32. Ingolia N.T., Ghaemmaghami S., Newman J.R., Weissman J.S. Genome-wide analysis invivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324:218-223.
33. Kim H.Y., LaVaute T., Iwai K., Klausner R.D., Rouault T.A. Identification of a conserved and functional iron-responsive element in the 5'-untranslated region of mammalian mitochondrial aconitase. J.Biol. Chem. 1996, 271:24226-24230.
34. Kiriakidou M., Nelson P.T., Kouranov A., Fitziev P., Bouyioukos C., Mourelatos Z., Hatzigeorgiou A. A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 2004, 18:1165-1178.
35. Krützfeldt J., Rajewsky N., Braich R., Rajeev K.G., Tuschl T., Manoharan M., Stoffel M. Silencing of microRNAs invivo with 'antagomirs'. Nature 2005, 438:685-689.
36. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
37. Melefors O., Goossen B., Johansson H.E., Stripecke R., Gray N.K., Hentze M.W. Translational control of 5-aminolevulinate synthase mRNA by iron-responsive elements in erythroid cells. J.Biol. Chem. 1993, 268:5974-5978.
38. Mishima Y., Giraldez A.J., Takeda Y., Fujiwara T., Sakamoto H., Schier A.F., Inoue K. Differential regulation of germline mRNAs in soma and germ cells by zebrafish miR-430. Curr. Biol. 2006, 16:2135-2142.
39. Muhlrad D., Decker C.J., Parker R. Turnover mechanisms of the stable yeast PGK1 mRNA. Mol. Cell. Biol. 1995, 15:2145-2156.
40. Nelson P.T., Hatzigeorgiou A.G., Mourelatos Z. miRNP:mRNA association in polyribosomes in a human neuronal cell line. RNA 2004, 10:387-394.
41. 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, 435:839-843.
42. Olsen P.H., Ambros V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 1999, 216:671-680.
43. Pillai R.S., Bhattacharyya S.N., Artus C.G., Zoller T., Cougot N., Basyuk E., Bertrand E., Filipowicz W. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 2005, 309:1573-1576.
44. Poy M.N., Eliasson L., Krutzfeldt J., Kuwajima S., Ma X., Macdonald P.E., Pfeffer S., Tuschl T., Rajewsky N., Rorsman P., Stoffel M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004, 432:226-230.
45. Rehwinkel J., Behm-Ansmant I., Gatfield D., Izaurralde E. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 2005, 11:1640-1647.
46. Rissland O.S., Hong S.J., Bartel D.P. MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell-cycle changes. Mol. Cell 2011, 43:993-1004.
47. Schwanhäusser B., Gossen M., Dittmar G., Selbach M. Global analysis of cellular protein translation by pulsed SILAC. Proteomics 2009, 9:205-209.
48. Schwartz D.C., Parker R. Mutations in translation initiation factors lead to increased rates of deadenylation and decapping of mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:5247-5256.
49. Seggerson K., Tang L., Moss E.G. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol. 2002, 243:215-225.
50. Selbach M., Schwanhäusser B., Thierfelder N., Fang Z., Khanin R., Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63.
51. Subtelny A.O., Eichhorn S.W., Chen G.R., Sive H., Bartel D.P. Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 2014, 508:66-71.
52. Thai T.H., Calado D.P., Casola S., Ansel K.M., Xiao C., Xue Y., Murphy A., Frendewey D., Valenzuela D., Kutok J.L., et al. Regulation of the germinal center response by microRNA-155. Science 2007, 316:604-608.
53. Wakiyama M., Takimoto K., Ohara O., Yokoyama S. Let-7 microRNA-mediated mRNA deadenylation and translational repression in a mammalian cell-free system. Genes Dev. 2007, 21:1857-1862.
54. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C.elegans. Cell 1993, 75:855-862.
55. Wu L., Fan J., Belasco J.G. MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. USA 2006, 103:4034-4039.
56. Yekta S., Shih I.H., Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
57. Zekri L., Kuzuoğlu-Öztürk D., Izaurralde E. GW182 proteins cause PABP dissociation from silenced miRNA targets in the absence of deadenylation. EMBO J. 2013, 32:1052-1065.
58. Zhao Y., Samal E., Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 2005, 436:214-220.