Human UPF1 participates in small RNA-induced mRNA downregulation

Molecular and Cellular Biology

Volumn 29, Issue 21, 2009, Pages 5789-5799

  Jin, Hua ^a   Mi, Ra Suh ^a   Han, Jinju ^a   Yeom, Kyu Hyeon ^a   Lee, Yoontae ^a   Heo, Inha ^a   Ha, Minju ^a   Hyun, Seogang ^a   Kim, V Narry ^a  

^a Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; ARGONAUTE 2 PROTEIN; MICRORNA; PROTEIN UPF1; REGULATOR PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; DOWN REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA DEGRADATION;

CYTOPLASMIC STRUCTURES; DOWN-REGULATION; EUKARYOTIC INITIATION FACTOR-2; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HELA CELLS; HUMANS; MICRORNAS; MODELS, BIOLOGICAL; MOLECULAR MIMICRY; PROTEIN BINDING; PROTEIN TRANSPORT; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-INDUCED SILENCING COMPLEX; SUBCELLULAR FRACTIONS; TRANS-ACTIVATORS;

EID: 70350547778     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00653-09     Document Type: Article

References (74)

1. Arciga-Reyes, L., L. Wootton, M. Kieffer, and B. Davies. 2006. UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J. 47:480-489. (Pubitemid 44036415)
2. Baek, D., J. Villen, C. Shin, F. D. Camargo, S. P. Gygi, and D. P. Bartel. 2008. The impact of microRNAs on protein output. Nature 455:64-71.
3. Bagga, S., J. Bracht, S. Hunter, K. Massirer, J. Holtz, R. Eachus, and A. E. Pasquinelli. 2005. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122:553-563. (Pubitemid 41191154)
4. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
5. Behm-Ansmant, I., J. Rehwinkel, T. Doerks, A. Stark, P. Bork, and E. Izaurralde. 2006. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20:1885-1898. (Pubitemid 44079326)
6. Beitzinger, M., L. Peters, J. Y. Zhu, E. Kremmer, and G. Meister. 2007. Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol. 4:76-84.
7. Birmingham, A., E. M. Anderson, A. Reynolds, D. Ilsley-Tyree, D. Leake, Y. Fedorov, S. Baskerville, E. Maksimova, K. Robinson, J. Karpilow, W. S. Marshall, and A. Khvorova. 2006. 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Methods 3:199-204.
8. Chendrimada, T. P., K. J. Finn, X. Ji, D. Baillat, R. I. Gregory, S. A. Liebhaber, A. E. Pasquinelli, and R. Shiekhattar. 2007. MicroRNA silencing through RISC recruitment of eIF6. Nature 447:823-828.
9. Coller, J., and R. Parker. 2005. General translational repression by activators of mRNA decapping. Cell 122:875-886. (Pubitemid 41345205)
10. Ding, L., A. Spencer, K. Morita, and M. Han. 2005. The developmental timing regulator AIN-1 interacts with miRISCs and may target the argonaute protein ALG-1 to cytoplasmic P bodies in C. elegans. Mol. Cell 19:437-447. (Pubitemid 41140002)
11. Doench, J. G., C. P. Petersen, and P. A. Sharp. 2003. siRNAs can function as miRNAs. Genes Dev. 17:438-442.
12. Doi, N., S. Zenno, R. Ueda, H. Ohki-Hamazaki, K. Ui-Tei, and K. Saigo. 2003. Short-interfering-RNA-mediated gene silencing in mammalian cells requires Dicer and eIF2C translation initiation factors. Curr. Biol. 13:41-46.
13. Domeier, M. E., D. P. Morse, S. W. Knight, M. Portereiko, B. L. Bass, and S. E. Mango. 2000. A link between RNA interference and nonsense-mediated decay in Caenorhabditis elegans. Science 289:1928-1931.
14. Eberle, A. B., S. Lykke-Andersen, O. Muhlemann, and T. H. Jensen. 2009. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16:49-55.
15. Eulalio, A., I. Behm-Ansmant, and E. Izaurralde. 2007. P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8:9-22.
16. Eulalio, A., E. Huntzinger, and E. Izaurralde. 2008. GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat. Struct. Mol. Biol. 15:346-353.
17. Eulalio, A., E. Huntzinger, T. Nishihara, J. Rehwinkel, M. Fauser, and E. Izaurralde. 2009. Deadenylation is a widespread effect of miRNA regulation. RNA 15:21-32.
18. Eulalio, A., J. Rehwinkel, M. Stricker, E. Huntzinger, S. F. Yang, T. Doerks, S. Dorner, P. Bork, M. Boutros, and E. Izaurralde. 2007. Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev. 21:2558-2570. (Pubitemid 47607667)
19. Filipowicz, W., S. N. Bhattacharyya, and N. Sonenberg. 2008. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9:102-114.
20. Fillman, C., and J. Lykke-Andersen. 2005. RNA decapping inside and outside of processing bodies. Curr. Opin. Cell Biol. 17:326-331.
21. Fukuhara, N., J. Ebert, L. Unterholzner, D. Lindner, E. Izaurralde, and E. Conti. 2005. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol. Cell 17:537-547. (Pubitemid 40269118)
22. Giraldez, A. J., Y. Mishima, J. Rihel, R. J. Grocock, S. Van Dongen, K. Inoue, A. J. Enright, and A. F. Schier. 2006. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312:75-79.
23. Gregory, R. I., T. P. Chendrimada, N. Cooch, and R. Shiekhattar. 2005. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123:631-640.
24. Haase, A. D., L. Jaskiewicz, H. Zhang, S. Laine, R. Sack, A. Gatignol, and W. Filipowicz. 2005. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6:961-967.
25. He, F., and A. Jacobson. 2001. Upf1p, Nmd2p, and Upf3p regulate the decapping and exonucleolytic degradation of both nonsense-containing mRNAs and wild-type mRNAs. Mol. Cell. Biol. 21:1515-1530.
26. Hock, J., L. Weinmann, C. Ender, S. Rudel, E. Kremmer, M. Raabe, H. Urlaub, and G. Meister. 2007. Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep. 8:1052-1060. (Pubitemid 350042341)
27. Hodgkin, J., A. Papp, R. Pulak, V. Ambros, and P. Anderson. 1989. A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123:301-313.
28. Holbrook, J. A., G. Neu-Yilik, M. W. Hentze, and A. E. Kulozik. 2004. Nonsense-mediated decay approaches the clinic. Nat. Genet. 36:801-808.
29. Huntzinger, E., I. Kashima, M. Fauser, J. Sauliere, and E. Izaurralde. 2008. SMG6 is the catalytic endonuclease that cleaves mRNAs containing non-sense codons in metazoans. RNA 14:2609-2617.
30. Ingelfinger, D., D. J. Arndt-Jovin, R. Luhrmann, and T. Achsel. 2002. The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8:1489-1501. (Pubitemid 36009020)
31. Isken, O., Y. K. Kim, N. Hosoda, G. L. Mayeur, J. W. Hershey, and L. E. Maquat. 2008. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133:314-327.
32. Isken, O., and L. E. Maquat. 2007. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21:1833-1856. (Pubitemid 47204924)
33. Ivanov, P. V., N. H. Gehring, J. B. Kunz, M. W. Hentze, and A. E. Kulozik. 2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27:736-747.
34. Jackson, A. L., S. R. Bartz, J. Schelter, S. V. Kobayashi, J. Burchard, M. Mao, B. Li, G. Cavet, and P. S. Linsley. 2003. Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21:635-637.
35. Kaygun, H., and W. F. Marzluff. 2005. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat. Struct. Mol. Biol. 12:794-800.
36. Kim, V. N. 2005. Small RNAs: classification, biogenesis, and function. Mol. Cells 19:1-15.
37. Kim, Y. K., L. Furic, L. Desgroseillers, and L. E. Maquat. 2005. Mammalian Staufen1 recruits Upf1 to specific mRNA 3′UTRs so as to elicit mRNA decay. Cell 120:195-208.
38. Kim, Y. K., L. Furic, M. Parisien, F. Major, L. DesGroseillers, and L. E. Maquat. 2007. Staufen1 regulates diverse classes of mammalian transcripts. EMBO J. 26:2670-2681.
39. Kim, Y. K., J. Yu, T. S. Han, S. Y. Park, B. Namkoong, D. H. Kim, K. Hur, M. W. Yoo, H. J. Lee, H. K. Yang, and V. N. Kim. 2009. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res. 37:1672-1681.
40. Lee, Y., C. Ahn, J. Han, H. Choi, J. Kim, J. Yim, J. Lee, P. Provost, O. Radmark, S. Kim, and V. N. Kim. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415-419. (Pubitemid 37187272)
41. Lee, Y., I. Hur, S. Y. Park, Y. K. Kim, M. R. Suh, and V. N. Kim. 2006. The role of PACT in the RNA silencing pathway. EMBO J. 25:522-532. (Pubitemid 43237659)
42. Lee, Y. S., and A. Dutta. 2007. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 21:1025-1030.
43. Leeds, P., S. W. Peltz, A. Jacobson, and M. R. Culbertson. 1991. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5:2303-2314. (Pubitemid 21905919)
44. Lejeune, F., X. Li, and L. E. Maquat. 2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12:675-687. (Pubitemid 37222488)
45. le Sage, C., R. Nagel, D. A. Egan, M. Schrier, E. Mesman, A. Mangiola, C. Anile, G. Maira, N. Mercatelli, S. A. Ciafre, M. G. Farace, and R. Agami. 2007. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J. 26:3699-3708.
46. Lim, L. P., N. C. Lau, P. Garrett-Engele, A. Grimson, J. M. Schelter, J. Castle, D. P. Bartel, P. S. Linsley, and J. M. Johnson. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769-773.
47. Liu, J., M. A. Carmell, F. V. Rivas, C. G. Marsden, J. M. Thomson, J. J. Song, S. M. Hammond, L. Joshua-Tor, and G. J. Hannon. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437-1441. (Pubitemid 39167657)
48. Liu, J., F. V. Rivas, J. Wohlschlegel, J. R. Yates III, R. Parker, and G. J. Hannon. 2005. A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7:1261-1266.
49. Liu, J., M. A. Valencia-Sanchez, G. J. Hannon, and R. Parker. 2005. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7:719-723.
50. Lykke-Andersen, J. 2002. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22:8114-8121.
51. Mayr, C., M. T. Hemann, and D. P. Bartel. 2007. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315:1576-1579. (Pubitemid 46449474)
52. Medghalchi, S. M., P. A. Frischmeyer, J. T. Mendell, A. G. Kelly, A. M. Lawler, and H. C. Dietz. 2001. Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet. 10:99-105.
53. Mishima, Y., A. J. Giraldez, Y. Takeda, T. Fujiwara, H. Sakamoto, A. F. Schier, and K. Inoue. 2006. Differential regulation of germline mRNAs in soma and germ cells by zebrafish miR-430. Curr. Biol. 16:2135-2142.
54. Mitchell, P., and D. Tollervey. 2003. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′→5′ degradation. Mol. Cell 11:1405-1413. (Pubitemid 36645158)
55. Nielsen, C. B., N. Shomron, R. Sandberg, E. Hornstein, J. Kitzman, and C. B. Burge. 2007. Determinants of targeting by endogenous and exogenous microRNAs and siRNAs. RNA 13:1894-1910.
56. Nottrott, S., M. J. Simard, and J. D. Richter. 2006. Human let-7a miRNA blocks protein production on actively translating polyribosomes. Nat. Struct. Mol. Biol. 13:1108-1114.
57. Parker, R., and H. Song. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11:121-127.
58. Petersen, C. P., M. E. Bordeleau, J. Pelletier, and P. A. Sharp. 2006. Short RNAs repress translation after initiation in mammalian cells. Mol. Cell 21:533-542.
59. Pillai, R. S. 2005. MicroRNA function: multiple mechanisms for a tiny RNA? RNA 11:1753-1761.
60. Pillai, R. S., S. N. Bhattacharyya, C. G. Artus, T. Zoller, N. Cougot, E. Basyuk, E. Bertrand, and W. Filipowicz. 2005. Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309:1573-1576.
61. Rehwinkel, J., I. Behm-Ansmant, D. Gatfield, and E. Izaurralde. 2005. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11:1640-1647. (Pubitemid 41505538)
62. Richter, J. D. 2008. Think you know how miRNAs work? Think again. Nat. Struct. Mol. Biol. 15:334-336.
63. Schmitter, D., J. Filkowski, A. Sewer, R. S. Pillai, E. J. Oakeley, M. Zavolan, P. Svoboda, and W. Filipowicz. 2006. Effects of Dicer and Argonaute downregulation on mRNA levels in human HEK293 cells. Nucleic Acids Res. 34:4801-4815. (Pubitemid 44605625)
64. Selbach, M., B. Schwanhausser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-63.
65. Sen, G. L., and H. M. Blau. 2005. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 7:633-636.
66. Sheth, U., and R. Parker. 2003. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300:805-808. (Pubitemid 36532117)
67. Singh, G., I. Rebbapragada, and J. Lykke-Andersen. 2008. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 6:e111. (Pubitemid 351649317)
68. Sun, X., H. A. Perlick, H. C. Dietz, and L. E. Maquat. 1998. A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense-containing mRNAs in mammalian cells. Proc. Natl. Acad. Sci. USA 95:10009-10014.
69. Tomari, Y., and P. D. Zamore. 2005. Perspective: machines for RNAi. Genes Dev. 19:517-529.
70. Unterholzner, L., and E. Izaurralde. 2004. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16:587-596. (Pubitemid 39531881)
71. Weinmann, L., J. Hock, T. Ivacevic, T. Ohrt, J. Mutze, P. Schwille, E. Kremmer, V. Benes, H. Urlaub, and G. Meister. 2009. Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 136:496-507.
72. Wu, L., and J. G. Belasco. 2005. Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol. Cell. Biol. 25:9198-9208.
73. Wu, L., J. Fan, and J. G. Belasco. 2006. MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. USA 103:4034-4039.
74. Zhang, J., X. Sun, Y. Qian, and L. E. Maquat. 1998. Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 4:801-815. (Pubitemid 28317828)