A Specialized Mechanism of Translation Mediated by FXR1a-Associated MicroRNP in Cellular Quiescence

Molecular Cell

Volumn 61, Issue 5, 2016, Pages 760-773

  Bukhari, Syed I A ^a,b   Truesdell, Samuel S ^a,b   Lee, Sooncheol ^a,b   Kollu, Swapna ^a,b   Classon, Anthony ^a,b   Boukhali, Myriam ^a   Jain, Esha ^b   Mortensen, Richard D ^a,b,d   Yanagiya, Akiko ^c   Sadreyev, Ruslan I ^a   Haas, Wilhelm ^a   Vasudevan, Shobha ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; FXR1A PROTEIN; INITIATION FACTOR 4G; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MICRORNA; MICRORNA PROTEIN COMPLEX; POLYADENYLATED RNA; PROTEIN; PROTEIN P97; SHORT HAIRPIN RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; ARGONAUTE PROTEIN; CAPPED RNA; EIF2C2 PROTEIN, HUMAN; EIF4G2 PROTEIN, HUMAN; EXORIBONUCLEASE; FXR1 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; PAIP2 PROTEIN, HUMAN; POLY(A)-SPECIFIC RIBONUCLEASE; REPRESSOR PROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; TARGET OF RAPAMYCIN KINASE;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL CYCLE ARREST; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE ACTIVATION; GENE LOSS; GENE OVEREXPRESSION; GENE SILENCING; NEUROBLAST; NONHUMAN; OOCYTE; POLYSOME; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEOMICS; RNA BINDING; RNA TRANSLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; XENOPUS LAEVIS; ANIMAL; BINDING SITE; CELL AGING; CELL LINE; GENE EXPRESSION PROFILING; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; PROCEDURES; PROTEIN SYNTHESIS; RNA INTERFERENCE;

3' UNTRANSLATED REGIONS; ANIMALS; ARGONAUTE PROTEINS; BINDING SITES; CELL AGING; CELL LINE; EUKARYOTIC INITIATION FACTOR-4G; EXORIBONUCLEASES; GENE EXPRESSION PROFILING; HUMANS; MICRORNAS; OOCYTES; PROTEIN BIOSYNTHESIS; PROTEOMICS; REPRESSOR PROTEINS; RIBONUCLEOPROTEINS; RNA CAPS; RNA INTERFERENCE; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSFECTION; XENOPUS LAEVIS;

EID: 84959545844     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.02.013     Document Type: Article

References (39)

1. Beilharz T.H., Humphreys D.T., Clancy J.L., Thermann R., Martin D.I., Hentze M.W., Preiss T. microRNA-mediated messenger RNA deadenylation contributes to translational repression in mammalian cells. PLoS ONE 2009, 4:e6783.
2. Bhattacharyya S.N., Habermacher R., Martine U., Closs E.I., Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006, 125:1111-1124.
3. Coller H.A., Sang L., Roberts J.M. A new description of cellular quiescence. PLoS Biol. 2006, 4:e83.
4. Friedman Y., Linial M. miRror2.0: a platform for assessing the joint action of microRNAs in cell regulation. J. Bioinform. Comput. Biol. 2013, 11:1343012.
5. 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.
6. Fu S., Fan J., Blanco J., Gimenez-Cassina A., Danial N.N., Watkins S.M., Hotamisligil G.S. Polysome profiling in liver identifies dynamic regulation of endoplasmic reticulum translatome by obesity and fasting. PLoS Genet. 2012, 8:e1002902.
7. Gandin V., Sikström K., Alain T., Morita M., McLaughlan S., Larsson O., Topisirovic I. Polysome fractionation and analysis of mammalian translatomes on a genome-wide scale. J. Vis. Exp. 2014, 87. 10.3791/51455.
8. Gingras A.C., Gygi S.P., Raught B., Polakiewicz R.D., Abraham R.T., Hoekstra M.F., Aebersold R., Sonenberg N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 1999, 13:1422-1437.
9. He S.L., Green R. Polysome analysis of mammalian cells. Methods Enzymol. 2013, 530:183-192.
10. Iwasaki S., Tomari Y. Argonaute-mediated translational repression (and activation). Fly (Austin) 2009, 3:204-206.
11. Jonas S., Izaurralde E. Towards a molecular understanding of microRNA-mediated gene silencing. Nat. Rev. Genet. 2015, 16:421-433.
12. Jopling C.L., Yi M., Lancaster A.M., Lemon S.M., Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005, 309:1577-1581.
13. Kim J.H., Richter J.D. RINGO/cdk1 and CPEB mediate poly(A) tail stabilization and translational regulation by ePAB. Genes Dev. 2007, 21:2571-2579.
14. Körner C.G., Wormington M., Muckenthaler M., Schneider S., Dehlin E., Wahle E. The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. EMBO J. 1998, 17:5427-5437.
15. Lee S., Truesdell S.S., Bukhari S.I., Lee J.H., LeTonqueze O., Vasudevan S. Upregulation of eIF5B controls cell-cycle arrest and specific developmental stages. Proc. Natl. Acad. Sci. USA 2014, 111:E4315-E4322.
16. Levy-Strumpf N., Deiss L.P., Berissi H., Kimchi A. DAP-5, a novel homolog of eukaryotic translation initiation factor 4G isolated as a putative modulator of gamma interferon-induced programmed cell death. Mol. Cell. Biol. 1997, 17:1615-1625.
17. Lin C.C., Liu L.Z., Addison J.B., Wonderlin W.F., Ivanov A.V., Ruppert J.M. A KLF4-miRNA-206 autoregulatory feedback loop can promote or inhibit protein translation depending upon cell context. Mol. Cell. Biol. 2011, 31:2513-2527.
18. Loayza-Puch F., Drost J., Rooijers K., Lopes R., Elkon R., Agami R. p53 induces transcriptional and translational programs to suppress cell proliferation and growth. Genome Biol. 2013, 14:R32.
19. Marzluff W.F., Wagner E.J., Duronio R.J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 2008, 9:843-854.
20. Meijer H.A., Kong Y.W., Lu W.T., Wilczynska A., Spriggs R.V., Robinson S.W., Godfrey J.D., Willis A.E., Bushell M. Translational repression and eIF4A2 activity are critical for microRNA-mediated gene regulation. Science 2013, 340:82-85.
21. Moon K.H., Zhao X., Yu Y.T. Pre-mRNA splicing in the nuclei of Xenopus oocytes. Methods Mol. Biol. 2006, 322:149-163.
22. Moretti F., Kaiser C., Zdanowicz-Specht A., Hentze M.W. PABP and the poly(A) tail augment microRNA repression by facilitated miRISC binding. Nat. Struct. Mol. Biol. 2012, 19:603-608.
23. Mortensen R.D., Serra M., Steitz J.A., Vasudevan S. Posttranscriptional activation of gene expression in Xenopus laevis oocytes by microRNA-protein complexes (microRNPs). Proc. Natl. Acad. Sci. USA 2011, 108:8281-8286.
24. Nilsson P., Henriksson N., Niedzwiecka A., Balatsos N.A., Kokkoris K., Eriksson J., Virtanen A. A multifunctional RNA recognition motif in poly(A)-specific ribonuclease with cap and poly(A) binding properties. J. Biol. Chem. 2007, 282:32902-32911.
25. Preiss T., Baron-Benhamou J., Ansorge W., Hentze M.W. Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat. Struct. Biol. 2003, 10:1039-1047.
26. Radford H.E., Meijer H.A., de Moor C.H. Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim. Biophys. Acta 2008, 1779:217-229.
27. Ren Y.G., Martínez J., Virtanen A. Identification of the active site of poly(A)-specific ribonuclease by site-directed mutagenesis and Fe(2+)-mediated cleavage. J. Biol. Chem. 2002, 277:5982-5987.
28. Sachs A.B., Bond M.W., Kornberg R.D. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 1986, 45:827-835.
29. Seal R., Temperley R., Wilusz J., Lightowlers R.N., Chrzanowska-Lightowlers Z.M. Serum-deprivation stimulates cap-binding by PARN at the expense of eIF4E, consistent with the observed decrease in mRNA stability. Nucleic Acids Res. 2005, 33:376-387.
30. Sun X., Gao L., Chien H.Y., Li W.C., Zhao J. The regulation and function of the NUAK family. J. Mol. Endocrinol. 2013, 51:R15-R22.
31. Tahmasebi S., Alain T., Rajasekhar V.K., Zhang J.P., Prager-Khoutorsky M., Khoutorsky A., Dogan Y., Gkogkas C.G., Petroulakis E., Sylvestre A., et al. Multifaceted regulation of somatic cell reprogramming by mRNA translational control. Cell Stem Cell 2014, 14:606-616.
32. Thoreen C.C., Chantranupong L., Keys H.R., Wang T., Gray N.S., Sabatini D.M. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 2012, 485:109-113.
33. Truesdell S.S., Mortensen R.D., Seo M., Schroeder J.C., Lee J.H., LeTonqueze O., Vasudevan S. MicroRNA-mediated mRNA translation activation in quiescent cells and oocytes involves recruitment of a nuclear microRNP. Sci. Rep. 2012, 2:842.
34. Tserel L., Runnel T., Kisand K., Pihlap M., Bakhoff L., Kolde R., Peterson H., Vilo J., Peterson P., Rebane A. MicroRNA expression profiles of human blood monocyte-derived dendritic cells and macrophages reveal miR-511 as putative positive regulator of Toll-like receptor 4. J. Biol. Chem. 2011, 286:26487-26495.
35. Vasudevan S., Steitz J.A. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 2007, 128:1105-1118.
36. Vasudevan S., Tong Y., Steitz J.A. Switching from repression to activation: microRNAs can up-regulate translation. Science 2007, 318:1931-1934.
37. Voeltz G.K., Ongkasuwan J., Standart N., Steitz J.A. A novel embryonic poly(A) binding protein, ePAB, regulates mRNA deadenylation in Xenopus egg extracts. Genes Dev. 2001, 15:774-788.
38. Yanagiya A., Delbes G., Svitkin Y.V., Robaire B., Sonenberg N. The poly(A)-binding protein partner Paip2a controls translation during late spermiogenesis in mice. J. Clin. Invest. 2010, 120:3389-3400.
39. Zhang X., Zuo X., Yang B., Li Z., Xue Y., Zhou Y., Huang J., Zhao X., Zhou J., Yan Y., et al. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 2014, 158:607-619.