Nonsense-mediated mRNA decay occurs during eIF4F-dependent translation in human cells

Nature Structural and Molecular Biology

Volumn 20, Issue 6, 2013, Pages 702-709

  Durand, Sébastien ^a   Lykke Andersen, Jens ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAP BINDING PROTEIN; INITIATION FACTOR 4F; MESSENGER RNA; PUROMYCIN;

ARTICLE; CELL ACTIVITY; HUMAN; HUMAN CELL; NONSENSE MEDIATED MRNA DECAY; PRIORITY JOURNAL; PROTEIN STABILITY; RNA DEGRADATION; RNA TRANSLATION; TRANSLATION REGULATION;

BLOTTING, NORTHERN; EUKARYOTIC INITIATION FACTOR-4F; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; NONSENSE MEDIATED MRNA DECAY; PROTEIN BIOSYNTHESIS; RNA CAP-BINDING PROTEINS;

EID: 84878945009     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2575     Document Type: Article

References (61)

1. Houseley, J. & Tollervey, D. The many pathways of RNA degradation. Cell 136, 763-776 (2009).
2. Chang, Y.F., Imam, J.S. & Wilkinson, M.F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76, 51-74 (2007).
3. Mühlemann, O., Eberle, A.B., Stalder, L. & Zamudio Orozco, R. Recognition and elimination of nonsense mRNA. Biochim. Biophys. Acta 1779, 538-549 (2008).
4. He, F. et al. Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5? to 3? mRNA decay pathways in yeast. Mol. Cell 12, 1439-1452 (2003). (Pubitemid 38037013)
5. Mendell, J.T., Sharifi, N.A., Meyers, J.L., Martinez-Murillo, F. & Dietz, H.C. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36, 1073-1078 (2004). (Pubitemid 41184468)
6. Rehwinkel, J., Letunic, I., Raes, J., Bork, P. & Izaurralde, E. Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 11, 1530-1544 (2005). (Pubitemid 41396923)
7. Kervestin, S. & Jacobson, A. NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell Biol. 13, 700-712 (2012).
8. Nicholson, P. et al. Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond quality control and the double-life of NMD factors. Cell Mol. Life Sci. 67, 677-700 (2010).
9. Rebbapragada, I. & Lykke-Andersen, J. Execution of nonsense-mediated mRNA decay: what defines a substrate? Curr. Opin. Cell Biol. 21, 394-402 (2009).
10. Le Hir, H., Moore, M.J. & Maquat, L.E. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 14, 1098-1108 (2000). (Pubitemid 30324423)
11. Saulière, J. et al. CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex. Nat. Struct. Mol. Biol. 19, 1124-1131 (2012).
12. Singh, G. et al. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151, 750-764 (2012).
13. Kim, V.N., Kataoka, N. & Dreyfuss, G. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293, 1832-1836 (2001). (Pubitemid 32845781)
14. Le Hir, H., Gatfield, D., Izaurralde, E. & Moore, M.J. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 20, 4987-4997 (2001). (Pubitemid 32848650)
15. Lykke-Andersen, J., Shu, M.D. & Steitz, J.A. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293, 1836-1839 (2001). (Pubitemid 32845782)
16. Amrani, N. et al. A faux 3?-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432, 112-118 (2004). (Pubitemid 39490837)
17. Behm-Ansmant, I., Gatfield, D., Rehwinkel, J., Hilgers, V. & Izaurralde, E. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J. 26, 1591-1601 (2007). (Pubitemid 46480926)
18. Eberle, A.B., Stalder, L., Mathys, H., Orozco, R.Z. & Muhlemann, O. Posttranscriptional gene regulation by spatial rearrangement of the 3? untranslated region. PLoS Biol. 6, e92 (2008).
19. Ivanov, P.V., Gehring, N.H., Kunz, J.B., Hentze, M.W. & Kulozik, A.E. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27, 736-747 (2008). (Pubitemid 351506680)
20. Silva, A.L., Ribeiro, P., Inacio, A., Liebhaber, S.A. & Romao, L. Proximity of the poly(A)-binding protein to a premature termination codon inhibits mammalian nonsense-mediated mRNA decay. RNA 14, 563-576 (2008). (Pubitemid 351397821)
21. Singh, G., Rebbapragada, I. & Lykke-Andersen, J. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 6, e111 (2008).
22. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y. & Ohno, S. Human SMG-1, a novel phosphatidylinositol-3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15, 2215-2228 (2001). (Pubitemid 32843834)
23. Cho, H., Kim, K.M. & Kim, Y.K. Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol. Cell 33, 75-86 (2009).
24. Eberle, A.B., Lykke-Andersen, S., Muhlemann, O. & Jensen, T.H. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16, 49-55 (2009).
25. Huntzinger, E., Kashima, I., Fauser, M., Sauliere, J. & Izaurralde, E. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14, 2609-2617 (2008).
26. Unterholzner, L. & Izaurralde, E. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16, 587-596 (2004). (Pubitemid 39531881)
27. Franks, T.M., Singh, G. & Lykke-Andersen, J. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143, 938-950 (2010).
28. Chiu, S.Y., Serin, G., Ohara, O. & Maquat, L.E. Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA 9, 77-87 (2003). (Pubitemid 36206304)
29. Ohnishi, T. et al. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell 12, 1187-1200 (2003). (Pubitemid 37487927)
30. Chiu, S.Y., Lejeune, F., Ranganathan, A.C. & Maquat, L.E. The pioneer translation initiation complex is functionally distinct from but structurally overlaps with the steady-state translation initiation complex. Genes Dev. 18, 745-754 (2004). (Pubitemid 38480887)
31. Ishigaki, Y., Li, X., Serin, G. & Maquat, L.E. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106, 607-617 (2001). (Pubitemid 32879322)
32. Görlich, D. et al. Importin provides a link between nuclear protein import and U snRNA export. Cell 87, 21-32 (1996). (Pubitemid 26337387)
33. Sato, H. & Maquat, L.E. Remodeling of the pioneer translation initiation complex involves translation and the karyopherin importin-?. Genes Dev. 23, 2537-2550 (2009).
34. Sonenberg, N. & Dever, T.E. Eukaryotic translation initiation factors and regulators. Curr. Opin. Struct. Biol. 13, 56-63 (2003). (Pubitemid 36170255)
35. Fortes, P. et al. The yeast nuclear cap binding complex can interact with translation factor eIF4G and mediate translation initiation. Mol. Cell 6, 191-196 (2000).
36. Kim, K.M. et al. A new MIF4G domain-containing protein, CTIF, directs nuclear cap-binding protein CBP80/20-dependent translation. Genes Dev. 23, 2033-2045 (2009).
37. Hosoda, N., Kim, Y.K., Lejeune, F. & Maquat, L.E. CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 12, 893-901 (2005). (Pubitemid 41486713)
38. Lejeune, F., Ishigaki, Y., Li, X. & Maquat, L.E. The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodeling. EMBO J. 21, 3536-3545 (2002). (Pubitemid 34760583)
39. Lejeune, F., Ranganathan, A.C. & Maquat, L.E. eIF4G is required for the pioneer round of translation in mammalian cells. Nat. Struct. Mol. Biol. 11, 992-1000 (2004). (Pubitemid 39315304)
40. Dzikiewicz-Krawczyk, A., Piontek, P., Szweykowska-Kulinska, Z. & Jarmolowski, A. The nuclear cap-binding protein complex is not essential for nonsense-mediated mRNA decay (NMD) in plants. Acta Biochim. Pol. 55, 825-828 (2008).
41. Gao, Q., Das, B., Sherman, F. & Maquat, L.E. Cap-binding protein 1-mediated and eukaryotic translation initiation factor 4E-mediated pioneer rounds of translation in yeast. Proc. Natl. Acad. Sci. USA 102, 4258-4263 (2005). (Pubitemid 40397099)
42. Kuperwasser, N., Brogna, S., Dower, K. & Rosbash, M. Nonsense-mediated decay does not occur within the yeast nucleus. RNA 10, 1907-1915 (2004). (Pubitemid 39557828)
43. Keeling, K.M. et al. Leaky termination at premature stop codons antagonizes nonsense-mediated mRNA decay in S. cerevisiae. RNA 10, 691-703 (2004). (Pubitemid 38405947)
44. Maderazo, A.B., Belk, J.P., He, F. & Jacobson, A. Nonsense-containing mRNAs that accumulate in the absence of a functional nonsense-mediated mRNA decay pathway are destabilized rapidly upon its restitution. Mol. Cell Biol. 23, 842-851 (2003). (Pubitemid 36133503)
45. Maquat, L.E., Hwang, J., Sato, H. & Tang, Y. CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter. Cold Spring Harb. Symp. Quant. Biol. 75, 127-134 (2010).
46. Pestka, S. Inhibitors of ribosome functions. Annu. Rev. Microbiol. 25, 487-562 (1971).
47. Yamashita, A. et al. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12, 1054-1063 (2005). (Pubitemid 41746775)
48. Moerke, N.J. et al. Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128, 257-267 (2007). (Pubitemid 46137991)
49. Holbrook, J.A., Neu-Yilik, G., Gehring, N.H., Kulozik, A.E. & Hentze, M.W. Internal ribosome entry sequence-mediated translation initiation triggers nonsense-mediated decay. EMBO Rep. 7, 722-726 (2006). (Pubitemid 43986270)
50. Woeller, C.F., Gaspari, M., Isken, O. & Maquat, L.E. NMD resulting from encephalomyocarditis virus IRES-directed translation initiation seems to be restricted to CBP80/20-bound mRNA. EMBO Rep. 9, 446-451 (2008). (Pubitemid 351627282)
51. Gingras, A.C., Raught, B. & Sonenberg, N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15, 807-826 (2001). (Pubitemid 32295062)
52. Gingras, A.C. et al. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 13, 1422-1437 (1999).
53. Moriarty, P.M., Reddy, C.C. & Maquat, L.E. Selenium deficiency reduces the abundance of mRNA for Se-dependent glutathione peroxidase 1 by a UGA-dependent mechanism likely to be nonsense codon-mediated decay of cytoplasmic mRNA. Mol. Cell Biol. 18, 2932-2939 (1998). (Pubitemid 28183462)
54. Hogg, J.R. & Goff, S.P. Upf1 senses 3? UTR length to potentiate mRNA decay. Cell 143, 379-389 (2010).
55. Gehring, N.H., Lamprinaki, S., Kulozik, A.E. & Hentze, M.W. Disassembly of exon junction complexes by PYM. Cell 137, 536-548 (2009).
56. Dostie, J. & Dreyfuss, G. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr. Biol. 12, 1060-1067 (2002). (Pubitemid 34766927)
57. Huang, L. et al. RNA homeostasis governed by cell type-specific and branched feedback loops acting on NMD. Mol. Cell 43, 950-961 (2011).
58. Yepiskoposyan, H., Aeschimann, F., Nilsson, D., Okoniewski, M. & Muhlemann, O. Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17, 2108-2118 (2011).
59. Giorgi, C. et al. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130, 179-191 (2007). (Pubitemid 47031322)
60. Duke, G.M., Hoffman, M.A. & Palmenberg, A.C. Sequence and structural elements that contribute to efficient encephalomyocarditis virus RNA translation. J. Virol. 66, 1602-1609 (1992).
61. Lykke-Andersen, J., Shu, M.D. & Steitz, J.A. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103, 1121-1131 (2000). (Pubitemid 32037398)