Gene expression networks: Competing mRNA decay pathways in mammalian cells

Biochemical Society Transactions

Volumn 37, Issue 6, 2009, Pages 1287-1292

  Maquat, Lynne E ^a   Gong, Chenguang ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Eukaryotic initiation factor 4E (eIF4E); Exon junction complex (EJC); Homoeostatic control of genes; Myogenesis; Nonsense mediated mRNA decay (NMD); Staufen1

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE;

3' UNTRANSLATED REGION; BINDING AFFINITY; BINDING SITE; CELL DIFFERENTIATION; CODON; DOWN REGULATION; EUKARYOTIC CELL; EXON; GENE FUNCTION; GENE REGULATORY NETWORK; HUMAN; MYOBLAST; MYOTUBE; NONHUMAN; NONSENSE MUTATION; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; RNA TRANSLATION; TRANSCRIPTION REGULATION; TRANSLATION INITIATION; TRANSPOSON; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; GENE REGULATORY NETWORKS; HUMANS; MODELS, GENETIC; RNA STABILITY; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EUKARYOTA; MAMMALIA;

EID: 70450182086     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0371287     Document Type: Review

References (65)

1. Houseley, J. and Tollervey, D. (2009) The many pathways of RNA degradation. Cell 136, 763-776
2. Moore, M.J. and Proudfoot, N.J. (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688-700
3. Behm-Ansmant, I., Kashima, I., Rehwinkel, J., Sauliere, J., Wittkopp, N. and Izaurralde, E. (2007) mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett. 581, 2845-2853
4. Chang, Y.F., Imam, J.S. and Wilkinson, M.F. (2007) The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76, 51-74
5. Isken, O. and Maquat, L.E. (2007) Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21, 1833-1856
6. Isken, O. and Maquat, L.E. (2008) The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat. Rev. Genet. 9, 699-712
7. McGlincy, N.J. and Smith, C.W. (2008) Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends Biochem. Sci. 33, 385-393
8. Mühlemann, O., Eberle, A.B., Stalder, L. and Zamudio Orozco, R. (2008) Recognition and elimination of nonsense mRNA. Biochim. Biophys. Acta 1779, 538-549
9. Neu-Yilik, G. and Kulozik, A.E. (2008) NMD: multitasking between mRNA surveillance and modulation of gene expression. Adv. Genet. 62, 185-243
10. Sánchez-Sánchez, F. and Mittnacht, S. (2008) Nonsense-mediated decay: paving the road for genome diversification. BioEssays 30, 926-928
11. Shyu, A.B., Wilkinson, M.F. and van Hoof, A. (2008) Messenger RNA regulation: to translate or to degrade. EMBO J. 27, 471-481
12. Silva, A.L. and Romäo, L. (2009) The mammalian nonsense-mediated mRNA decay pathway: to decay or not to decay! Which players make the decision? FEBS Lett. 583, 499-505
13. Stalder, L. and Mühlemann, O. (2008) The meaning of nonsense. Trends Cell Biol. 18, 315-321
14. Rebbapragada, I. and Lykke-Andersen, J. (2009) Execution of nonsense-mediated mRNA decay: what defines a substrate? Curr. Opin. Cell Biol. 21, 394-402
15. Lewis, B.P., Green, R.E. and Brenner, S.E. (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. U.S.A. 100, 189-192
16. Pan, Q., Saltzman, A.L., Kim, Y.K., Misquitta, C., Shai, O., Maquat, L.E., Frey, B.J. and Blencowe, B.J. (2006) Quantitative microarray profiling provides evidence against widespread coupling of alternative splicing with nonsense-mediated mRNA decay to control gene expression. Genes Dev. 20, 153-158
17. Mendell, J.T., Sharifi, N.A., Meyers, J.L., Martinez-Murillo, F. and Dietz, H.C. (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36, 1073-1078
18. Weischenfeldt, J., Damgaard, I., Bryder, D., Theilgaard-Monch, K., Thoren, L.A., Nielsen, F.C., Jacobsen, S.E., Nerlov, C. and Porse, B.T. (2008) NMD is essential for hematopoietic stem and progenitor cells and for eliminating by-products of programmed DNA rearrangements. Genes Dev. 22, 1381-1396
19. Wittmann, J., Hol, E.M. and Jäck, H.M. (2006) hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol. Cell. Biol. 26, 1272-1287
20. Jumaa, H. and Nielsen, P.J. (1997) The splicing factor SRp20 modifies splicing of its own mRNA and ASF/SF2 antagonizes this regulation. EMBO J. 16, 5077-5085
21. Lareau, L.F., Inada, M., Green, R.E., Wengrod, J.C. and Brenner, S.E. (2007) Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446, 926-929
22. Lejeune, F., Cavaloc, Y. and Stévenin, J. (2001) Alternative splicing of intron 3 of the serine/arginine-rich protein 9G8 gene: identification of flanking exonic splicing enhancers and involvement of 9G8 as a trans-acting factor. J. Biol. Chem. 276, 7850-7858
23. Makeyev, E.V., Zhang, J., Carrasco, M.A. and Maniatis, T. (2007) The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27, 435-448
24. Ni, J.Z., Grate, L., Donohue, J.P., Preston, C., Nobida, N., O'Brien, G., Shiue, L., Clark, T.A., Blume, J.E. and Ares, Jr, M. (2007) Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev. 21, 708-718
25. Saltzman, A.L., Kim, Y.K., Pan, Q., Fagnani, M.M., Maquat, L.E. and Blencowe, B.J. (2008) Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol. Cell. Biol. 28, 4320-4330
26. Spellman, R., Llorian, M. and Smith, C.W. (2007) Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Mol. Cell 27, 420-434
27. Sureau, A., Gattoni, R., Dooghe, Y., Stévenin, J. and Soret, J. (2001) SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J. 20, 1785-1796
28. Wollerton, M.C., Gooding, C., Wagner, E.J., Garcia-Blanco, M.A. and Smith, C.W. (2004) Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell 13, 91-100
29. Medghalchi, S.M., Frischmeyer, P.A., Mendell, J.T., Kelly, A.G., Lawler, A.M. and Dietz, H.C. (2001) Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum. Mol. Genet. 10, 99-105
30. Bhattacharya, A., Czaplinski, K., Trifillis, P., He, F., Jacobson, A. and Peltz, S.W. (2000) Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. RNA 6, 1226-1235
31. Chamieh, H., Ballut, L., Bonneau, F. and Le Hir, H. (2008) NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat. Struct. Mol. Biol. 15, 85-93
32. Cheng, Z., Muhlrad, D., Lim, M.K., Parker, R. and Song, H. (2007) Structural and functional insights into the human Upf1 helicase core. EMBO J. 26, 253-264
33. Azzalin, C.M., Reichenbach, P., Khoriauli, L., Giulotto, E. and Lingner, J. (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318, 798-801
34. Gong, C., Kim, Y.K., Woeller, C.F., Tang, Y. and Maquat, L.E. (2009) SMD and NMD are competitive pathways that contribute to myogenesis: effects on PAX3 and myogenin mRNAs. Genes Dev. 23, 54-66
35. Chiu, S.Y., Lejeune, F., Ranganathan, A.C. and Maquat, L.E. (2004) The pioneer translation initiation complex is functionally distinct from but structurally overlaps with the steady-state translation initiation complex. Genes Dev. 18, 745-754
36. Hosoda, N., Kim, Y.K., Lejeune, F. and Maquat, L.E. (2005) CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 12, 893-901
37. Ishigaki, Y., Li, X., Serin, G. and Maquat, L.E. (2001) 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
38. Isken, O., Kim, Y.K., Hosoda, N., Mayeur, G.L., Hershey, J.W. and Maquat, L.E. (2008) Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133, 314-327
39. Kashima, I., Yamashita, A., Izumi, N., Kataoka, N., Morishita, R., Hoshino, S., Ohno, M., Dreyfuss, G. and Ohno, S. (2006) Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev. 20, 355-367
40. Lejeune, F., Ishigaki, Y., Li, X. and Maquat, L.E. (2002) 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
41. Lejeune, F., Ranganathan, A.C. and Maquat, L.E. (2004) eIF4G is required for the pioneer round of translation in mammalian cells. Nat. Struct. Mol. Biol. 11, 992-1000
42. Singh, G. and Lykke-Andersen, J. (2003) New insights into the formation of active nonsense-mediated decay complexes. Trends Biochem. Sci. 28, 464-466
43. Le Hir, H. and Andersen, G.R. (2008) Structural insights into the exon junction complex. Curr. Opin. Struct. Biol. 18, 112-119
44. Tange, T.O., Nott, A. and Moore, M.J. (2004) The ever-increasing complexities of the exon junction complex. Curr. Opin. Cell Biol. 16, 279-284
45. Matsuda, D., Hosoda, N., Kim, Y.K. and Maquat, L.E. (2007) Failsafe nonsense-mediated mRNA decay does not detectably target eIF4E-bound mRNA. Nat. Struct. Mol. Biol. 14, 974-979
46. Woeller, C.F., Gaspari, M., Isken, O. and Maquat, L.E. (2008) NMD resulting from encephalomyocarditis virus IRES-directed translation initiation seems to be restricted to CBP80/20-bound mRNA. EMBO Rep. 9, 446-451
47. Dostie, J. and Dreyfuss, G. (2002) Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr. Biol. 12, 1060-1067
48. Gehring, N.H., Lamprinaki, S., Kulozik, A.E. and Hentze, M.W. (2009) Disassembly of exon junction complexes by PYM. Cell 137, 536-548
49. Yamashita, A., Izumi, N., Kashima, I., Ohnishi, T., Saari, B., Katsuhata, Y., Muramatsu, R., Morita, T., Iwamatsu, A., Hachiya, T. et al. (2009) SMG-8 and SMG-9, two novel subunits of the SMG-1 complex, regulate remodeling of the mRNA surveillance complex during nonsense-mediated mRNA decay. Genes Dev. 23, 1091-1105
50. Lehner, B. and Sanderson, C.M. (2004) A protein interaction framework for human mRNA degradation. Genome Res. 14, 1315-1323
51. Le jeune, F., Li, X. and Maquat, L.E. (2003) Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12, 675-687
52. Lykke-Andersen, J. (2002) Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22, 8114-8121
53. Unterholzner, L. and Izaurralde, E. (2004) SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol. Cell 16, 587-596
54. Yamashita, A., Kashima, I. and Ohno, S. (2005) The role of SMG-1 in nonsense-mediated mRNA decay. Biochim. Biophys. Acta 1754, 305-315
55. Eberle, A.B., Lykke-Andersen, S., Mühlemann, O. and Jensen, T.H. (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. 16, 49-55
56. Glavan, F., Behm-Ansmant, I., Izaurralde, E. and Conti, E. (2006) Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J. 25, 5117-5125
57. Huntzinger, E., Kashima, I., Fauser, M., Sauliere, J. and Izaurralde, E. (2008) SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14, 2609-2617
58. Kim, Y.K., Furic, L., Desgroseillers, L. and Maquat, L.E. (2005) Mammalian Staufen1 recruits Upf1 to specific mRNA 3bUTRs so as to elicit mRNA decay. Cell 120, 195-208
59. Kim, Y.K., Furic, L., Parisien, M., Major, F., DesGroseillers, L. and Maquat, L.E. (2007) Staufen1 regulates diverse classes of mammalian transcripts. EMBO J. 26, 2670-2681
60. Vessey, J.P., Macchi, P., Stein, J.M., Mikl, M., Hawker, K.N., Vogelsang, P., Wieczorek, K., Vendra, G., Riefler, J., Tubing, F. et al. (2008) A loss of function allele for murine Staufen1 leads to impairment of dendritic Staufen1-RNP delivery and dendritic spine morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 16374-16379
61. Dugre-Brisson, S., Elvira, G., Boulay, K., Chatel-Chaix, L., Mouland, A.J. and DesGroseillers, L. (2005) Interaction of Staufen1 with the 5b end of mRNA facilitates translation of these RNAs. Nucleic Acids Res. 33, 4797-4812
62. Gautrey, H., McConnell, J., Lako, M., Hall, J. and Hesketh, J. (2008) Staufen1 is expressed in preimplantation mouse embryos and is required for embryonic stem cell differentiation. Biochim. Biophys. Acta 1783, 1935-1942
63. Epstein, J.A., Lam, P., Jepeal, L., Maas, R.L. and Shapiro, D.N. (1995) Pax3 inhibits myogenic differentiation of cultured myoblast cells. J. Biol. Chem. 270, 11719-11722
64. Wright, W.E., Sassoon, D.A. and Lin, V.K. (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56, 607-617
65. Gehring, N.H., Kunz, J.B., Neu-Yilik, G., Breit, S., Viegas, M.H., Hentze, M.W. and Kulozik, A.E. (2005) Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol. Cell 20, 65-75