CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 75, Issue , 2010, Pages 127-134

  Maquat, L E ^a   Hwang, J ^a   Sato, H ^a   Tang, Y ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAP BINDING PROTEIN; CAP BINDING PROTEIN 80; INITIATION FACTOR 4E; RIBONUCLEOPROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CELL PROTEIN; HETERODIMER; KARYOPHERIN ALPHA; KARYOPHERIN BETA; MESSENGER RIBONUCLEOPROTEIN; MESSENGER RNA; PROTEIN; SMG1 PROTEIN; UPF1 PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; CODON; EXON; GENE EXPRESSION; IRON RESPONSIVE ELEMENT; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA PROCESSING; RNA SPLICING; STEADY STATE; TRANSLATION INITIATION; GENE CONTROL; GENE INTERACTION; GENE REARRANGEMENT; HUMAN; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; RNA TRANSLATION;

ANIMALS; CODON, NONSENSE; HUMANS; NUCLEAR CAP-BINDING PROTEIN COMPLEX; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEINS; RNA STABILITY;

EUKARYOTA; MAMMALIA;

EID: 80052411929     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2010.75.028     Document Type: Article

References (76)

1. Afonina E, Stauber R, Pavlakis GN. 1998. The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J Biol Chem 273: 13015-13021.
2. Bear DG, Fomproix N, Soop T, Bjorkroth B, Masich S, Daneholt B. 2003. Nuclear poly(A)-binding protein PABPN1 is associated with RNA polymerase II during transcription and accompanies the released transcript to the nuclear pore. Exp Cell Res 286: 332-344.
3. Cakmakçi NG, Lerner RS, Wagner EJ, Zheng L, Marzluff WF. 2008. SLIP1, a factor required for activation of histone mRNA translation by the stem-loop binding protein. Mol Cell Biol 28: 1182-1194.
4. 7GpppG binding to the nuclear cap-binding protein complex. Nat Struct Biol 9: 912-917.
5. Chamieh H, Ballut L, Bonneau F, 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.
6. Cheng H, Dufu K, Lee CS, Hsu JL, Dias A, Reed R. 2006. Human mRNA export machinery recruited to the 5' end of mRNA. Cell 127: 1389-1400.
7. Clerici M, Mourão A, Gutsche I, Gehring NH, Hentze MW, Ku-lozik A, Kadlec J, Sattler M, Cusack S. 2009. Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J 28: 2293-2306.
8. Chiu SY, Lejeune F, Ranganathan AC, Maquat LE. 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.
9. Derry MC, Yanagiya A, Martineau Y, Sonenberg N. 2006. Regulation of poly(A)-binding protein through PABP-interacting proteins. Cold Spring Harb Symp Quant Biol 71: 537-543.
10. Dias SM, Wilson KF, Rojas KS, Ambrosio AL, Cerione RA. 2009. The molecular basis for the regulation of the cap-binding complex by the importins. Nat Struct Mol Biol 16: 930-937.
11. Dostie J, Dreyfuss G. 2002. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr Biol 12: 1060-1067.
12. Eberle AB, Lykke-Andersen S, Mühlemann O, Jensen TH. 2009. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 16: 49-55.
13. Fortes P, Inada T, Preiss T, Hentze MW, Mattaj IW, Sachs AB. 2000. The yeast nuclear cap binding complex can interact with translation factor eIF4G and mediate translation initiation. Mol Cell 6: 191-196.
14. Franks TM, Singh G, Lykke-Andersen J. 2010. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143: 938-950.
15. Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW. 2009. Disassembly of exon junction complexes by PYM. Cell 137: 536-548.
16. Gong C, Kim YK, Woeller CF, Tang Y, Maquat LE. 2009. SMD and NMD are competitive pathways that contribute to myogenesis: Effects on PAX3 and myogenin mRNAs. Genes Dev 23: 54-66.
17. Görlich D, Kraft R, Kostka S, Vogel F, Hartmann E, Laskey RA, Mattaj IW, Izaurralde E. 1996. Importin provides a link between nuclear protein import and U snRNA export. Cell 87: 21-32.
18. Groft CM, Burley SK. 2002. Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol Cell 9: 1273-1283.
19. Gross JD, Moerke NJ, von der Haar T, Lugovskoy AA, Sachs AB, McCarthy JE, Wagner G. 2003. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115: 739-750.
20. Guo L, Allen EM, Miller WA. 2001. Base-pairing between untranslated regions facilitates translation of uncapped, non-polyadenylated viral RNA. Mol Cell 7: 1103-1109.
21. Haghighat A, Sonenberg N. 1997. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5'-cap structure. J Biol Chem 272: 21677-21680.
22. Herold J, Andino R. 2001. Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol Cell 7: 581-591.
23. Hoshino S, Imai M, Kobayashi T, Uchida N, Katada T. 1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3'-poly(A) tail of mRNA. Direct association of eRF3/GSPT with polyadenylate-binding protein. J Biol Chem 274: 16677-16680.
24. Hosoda N, Kim YK, Lejeune F, Maquat LE. 2005. CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat Struct Mol Biol 12: 893-901.
25. Hosoda N, Lejeune F, Maquat LE. 2006. Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol Cell Biol 26: 3085-3097.
26. Huntzinger E, Kashima I, Fauser M, Saulière J, Izaurralde E. 2008. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14: 2609-2617.
27. Hwang J, Sato H, Matsuda D, Tang Y, Maquat LE. 2010. UPF1 association with the cap-binding protein, CBP80, promotes nonsense-mediated mRNA decay at two distinct steps. Mol Cell 39: 396-409.
28. Ishigaki Y, Li X, Serin G, Maquat LE. 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.
29. Isken O, Maquat LE. 2007. Quality control of eukaryotic mRNA: Safeguarding cells from abnormal mRNA function. Genes Dev 21: 1833-1856.
30. Isken O, Maquat LE. 2008. The multiple lives of NMD factors: Balancing roles in gene and genome regulation. Nat Rev Genet 9: 699-712.
31. Isken O, Kim YK, Hosoda N, Mayeur GL, Hershey JW, Maquat LE. 2008. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133: 314-327.
32. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE. 2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J 27: 736-747.
33. Izaurralde E, Lewis J, McGuigan C, Jankowska M, Darzynkiewicz E, Mattaj IW. 1994. A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell 78: 657-668.
34. Jackson RJ, Hellen CU, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
35. Kashima I, Yamashita A, Izumi N, Kataoka N, Morishita R, Hoshino S, Ohno M, Dreyfuss G, 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.
36. Kim VN, Kataoka N, Dreyfuss G. 2001. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293: 1832-1836.
37. Kühn U, Wahle E. 2004. Structure and function of poly(A) binding proteins. Biochim Biophys Acta 1678: 67-84.
38. Le Hir H, Andersen GR. 2008. Structural insights into the exon junction complex. Curr Opin Struct Biol 18: 112-119.
39. Lehner B, Sanderson CM. 2004. A protein interaction framework for human mRNA degradation. Genome Res 14: 1315-1323.
40. Lejeune F, Ishigaki Y, Li X, Maquat LE. 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, Li X, Maquat LE. 2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol Cell 12: 675-687.
42. Lejeune F, Ranganathan AC, Maquat LE. 2004. eIF4G is required for the pioneer round of translation in mammalian cells. Nat Struct Mol Biol 11: 992-1000.
43. Lewis JD, Izaurralde E. 1997. The role of the cap structure in RNA processing and nuclear export. Eur J Biochem 247: 461-469.
44. Lykke-Andersen J. 2002. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 22: 8114-8121.
45. Lykke-Andersen J, Shu MD, Steitz JA. 2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103: 1121-1131.
46. Lykke-Andersen J, Shu MD, Steitz JA. 2001. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293: 1836-1839.
47. Maquat LE, Tarn WY, Isken O. 2010. The pioneer round of translation: Features and functions. Cell 142: 368-374.
48. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. 1997. Cocrystal structure of the messenger RNA 5' cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89: 951-961.
49. 7GDP and interaction with 4E-binding protein. Nat Struct Biol 4: 717-724.
50. Mazza C, Ohno M, Segref A, Mattaj IW, Cusack S. 2001. Crystal structure of the human nuclear cap binding complex. Mol Cell 8: 383-396.
51. 7GpppG cap analogue by the human nuclear cap-binding complex. EMBO J 21: 5548-5557.
52. 7guanosine cap. Mol Cell Biol 21: 3632-3641.
53. Niedzwiecka A, Stepinski J, Darzynkiewicz E, Sonenberg N, Sto-larski R. 2002. Positive heat capacity change upon specific binding of translation initiation factor eIF4E to mRNA 5' cap. Biochemistry 41: 12140-12148.
54. Nicholson P, Yepiskoposyan H, Metze S, Orozco RZ, Kleinschmidt N, Mühlemann O. 2010. 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.
55. Ohnishi T, Yamashita A, Kashima I, Schell T, Anders KR, Grimson A, Hachiya T, Hentze MW, Anderson P, Ohno S. 2003. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol Cell 12: 1187-1200.
56. Rebbapragada I, Lykke-Andersen J. 2009. Execution of nonsense-mediated mRNA decay: What defines a substrate? Curr Opin Cell Biol 21: 394-402.
57. Sato H, Maquat LE. 2009. Remodeling of the pioneer translation initiation complex involves translation and the karyopherin im-portin β. Genes Dev 23: 2537-2550.
58. Sato H, Hosoda N, Maquat LE. 2008. Efficiency of the pioneer round of translation affects the cellular site of nonsense-mediated mRNA decay. Mol Cell 29: 255-262.
59. Silva AL, Romão 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.
60. Singh G, Jakob S, Kleedehn MG, Lykke-Andersen J. 2007. Communication with the exon-junction complex and activation of nonsense-mediated mRNA decay by human Upf proteins occur in the cytoplasm. Mol Cell 27: 780-792.
61. Singh G, Rebbapragada I, Lykke-Andersen J. 2008. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol 6: 860-871.
62. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136:731-745.
63. Steitz JA, Vasudevan S. 2009. miRNPs: Versatile regulators of gene expression in vertebrate cells. Biochem Soc Trans 37: 931-935.
64. Stephenson LS, Maquat LE. 1996. Cytoplasmic mRNA for human triosephosphate isomerase is immune to nonsense-mediated decay despite forming polysomes. Biochimie 78: 1043-1047.
65. 7GpppA)-bound human full-length eukaryotic initiation factor 4E: Biological importance of the C-terminal flexible region. Biochem J 362: 539-544.
66. Tran EJ, Zhou Y, Corbett AH, Wente SR. 2007. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol Cell 28: 850-859.
67. Tritschler F, Huntzinger E, Izaurralde E. 2010. Role of GW182 proteins and PABPC1 in the miRNA pathway: A sense of déjà vu. Nat Rev Mol Cell Biol 11: 379-384.
68. Unterholzner L, Izaurralde E. 2004. SMG7 acts as a molecular link between mRNA surveillance and mRNA decay. Mol Cell 16: 587-596.
69. Viegas MH, Gehring NH, Breit S, Hentze MW, Kulozik AE. 2007. The abundance of RNPS1, a protein component of the exon junction complex, can determine the variability in efficiency of the nonsense-mediated decay pathway. Nucleic Acids Res 35: 4542-4551.
70. Visa N, Izaurralde E, Ferreira J, Daneholt B, Mattaj IW. 1996. A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export. J Cell Biol 133: 5-14.
71. Wen Y, Shatkin AJ. 2000. Cap methyltransferase selective binding and methylation of GpppG-RNA are stimulated by importin-α. Genes Dev 14: 2944-2949.
72. Wittmann J, Hol EM, Jack HM. 2006. hUPF2 silencing identifies physiologic substrates of mammalian nonsense-mediated mRNA decay. Mol Cell Biol 26: 1272-1287.
73. Worch R, Niedzwiecka A, Stepinski J, Mazza C, Jankowska-Anyszka M, Darzynkiewicz E, Cusack S, Stolarski R. 2005. Specificity of recognition of mRNA 5' cap by human nuclear cap-binding complex. RNA 11: 1355-1363.
74. Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z, Chen CY, Shyu AB. 2005. Concerted action of poly(A) nucleases and de-capping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 12: 1054-1063.
75. 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.
76. Zhang Z, Krainer AR. 2007. Splicing remodels messenger ribonucleoprotein architecture via eIF4A3-dependent and -independent recruitment of exon junction complex components. Proc Natl Acad Sci 104: 11574-11579.