Splicing enhances translation in mammalian cells: An additional function of the exon junction complex

Genes and Development

Volumn 18, Issue 2, 2004, Pages 210-222

  Nott, Ajit ^a   Le Hir, Hervé ^a,b   Moore, Melissa J ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

Author keywords

Exon junction complex; Gene expression; Polysome; Splicing; Translation

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; NONSENSE MEDIATED DECAY FACTOR; PROTEIN MAGOH; PROTEIN RNPS1; PROTEIN UPF1; PROTEIN UPF2; PROTEIN UPF3B; PROTEIN Y14; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOPLASM; DNA REPLICATION; EXON; EXON JUNCTION COMPLEX; MOLECULAR DYNAMICS; NONHUMAN; OPEN READING FRAME; POLYSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUANTITATIVE ASSAY; RNA SPLICING; RNA TRANSLATION;

ANIMALS; GENES, REPORTER; HELA CELLS; HUMANS; MACROMOLECULAR SUBSTANCES; PROTEIN BIOSYNTHESIS; RECEPTORS, ANTIGEN, T-CELL; RNA SPLICE SITES; RNA SPLICING; RNA, MESSENGER; XENOPUS;

ANIMALIA; MAMMALIA;

EID: 0942268832     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1163204     Document Type: Article

References (73)

1. Aravind, L. and Koonin, E.V. 2000. Eukaryote-specific domains in translation initiation factors: Implicaticns for translation regulation and evolution of the translation system. Genome Res. 10: 1172-1184.
2. Badolato, J., Gardiner, E., Morrison, N., and Eisman, J. 1995. Identification and characterization of a novel human RNA-binding protein. Gene 166: 323-327.
3. Bonneau, A.M., Darveau, A., and Sonenberg, N. 1985. Effect of viral infection on host protein synthesis and mRNA association with the cytoplasmic cytoskeletal structure. J. Cell Biol. 100: 1209-1218.
4. Bouvet, P. and Wolffe, A.P. 1994. A role for transcription and FRGY2 in masking maternal mRNA within Xenopus oocytes. Cell 77: 931-941.
5. Braddock, M., Muckenthaler, M., White, M.R., Thorburn, A.M., Sommerville, J., Kingsman, A.J., and Kingsman, S.M. 1994. Intron-less RNA injected into the nucleus of Xenopus oocytes accesses a regulated translation control pathway. Nucleic Acids Res. 22: 5255-5264.
6. Craig, A.W., Haghighat, A., Yu, A.T., and Sonenberg, N. 1998. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 392: 520-523.
7. Cui, Y., Gonzalez, C.I., Kinzy, T.G., Dinman, J.D., and Peltz, S.W. 1999. Mutations in the MOF2/SUI1 gene affect both translation and nonsense-mediated mRNA decay. RNA 5: 794-804.
8. Czaplinski, K., Ruiz-Echevarria, M.J., Paushkin, S.V., Han, X., Weng, Y., Perlick, H.A., Dietz, H.C., Ter-Avanesyan, M.D., and Peltz, S.W. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes & Dev. 12: 1665-1677.
9. Dostie, J. and Dreyfuss, G. 2002. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr. Biol. 12: 1060-1067.
10. Dreyfuss, G., Kim, V.N., and Kataoka, N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell. Biol. 3: 195-205.
11. Fribourg, S., Gatfield, D., Izaurralde, E., and Conti, E. 2003. A novel mode of RBD-protein recognition in the Y14-Mago complex. Nat. Struct. Biol. 10: 433-439.
12. Garfield, D. and Izaurralde, E. 2002. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J. Cell Biol. 159: 579-588.
13. Gatfield, D., Le Hir, H., Schmitt, C., Braun, I.C., Kocher, T., Wilm, M., and Izaurralde, E. 2001. The DExH/D box protein HEL/UAP56 is essential for mRNA nuclear export in Drosophila. Curr. Biol. 11: 1716-1721.
14. Gebauer, F. and Richter, J.D. 1996. Mouse cytoplasmic polyadenylylation element binding protein: An evolutionarily conserved protein that interacts with the cytoplasmic polyadenylylation elements of c-mos mRNA. Proc. Natl. Acad. Sci. 93: 14602-14607.
15. Gehring, N.H., Neu-Yilik, G., Schell, T., Hentze, M.W., and Kulozik, A.E. 2003. Y14 and hUpf3b form an NMD-activating complex. Mol. Cell 11: 939-949.
16. Gingras, A.C., Raught, B., and Sonenberg, N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68: 913-963.
17. Hachet, O. and Ephrussi, A. 2001. Drosophila Y14 shuttles to the posterior of the oocyte and is required for oskar mRNA transport. Curr. Biol. 11: 1666-1674.
18. He, F. and Jacobson, A. 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.
19. Herbert, T.P. and Hecht, N.B. 1999. The mouse Y-box protein, MSY2, is associated with a kinase on non-polysomal mouse testicular mRNAs. Nucleic Acids Res. 27: 1747-1753.
20. Hilleren, P. and Parker, R. 1999. mRNA surveillance in eukaryotes: Kinetic proofreading of proper translation termination as assessed by mRNP domain organization? RNA 5: 711-719.
21. Hovland, R., Hesketh, J.E., and Pryme, I.F. 1996. The compartmentalization of protein synthesis: importance of cytoskeleton and role in mRNA targeting. Int. J. Biochem. Cell Biol. 28: 1089-1105.
22. Jarmolowski, A., Boelens, W.C., Izaurralde, E., and Mattaj, I.W. 1994. Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol. 124: 627-635.
23. Johannes, G. and Sarnow, P. 1998. Cap-independent polysomal association of natural mRNAs encoding c-myc, BiP, and eIF4G conferred by internal ribosome entry sites. RNA 4: 1500-1513.
24. Kataoka, N., Yong, J., Kim, V.N., Velazquez, F., Perkinson, R.A., Wang, F., and Dreyfuss, G. 2000. Pre-mRNA splicing imprints mRNA in the nucleus with a novel RNA-binding protein that persists in the cytoplasm. Mol. Cell 6: 673-682.
25. Kataoka, N., Diem, M.D., Kim, V.N., Yong, J., and Dreyfuss, G. 2001. Magoh, a human homolog of Drosophila mago nashi protein, is a component of the splicing-dependent exon-exon junction complex. EMBO J. 20: 6424-6433.
26. Kim, V.N., Kataoka, N., and Dreyfuss, G. 2001. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293: 1832-1836.
27. Le Hir, H., Izaurralde, E., Maquat, L.E., and Moore, M.J. 2000a. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19: 6860-6869.
28. Le Hir, H., Moore, M.J., and Maquat, L.E. 2000b. Pre-mRNA splicing alters mRNP composition: Evidence for stable association of proteins at exon-exon junctions. Genes & Dev. 14: 1098-1108.
29. Le Hir, H., Gatfield, D., Izaurralde, E., and Moore, M.J. 2001. 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.
30. Le Hir, H., Nott, A., and Moore, M.J. 2003. How introns influence and enhance eukaryotic gene expression. Trends Biochem. Sci. 28: 215-220.
31. 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.
32. Loyer, P., Trembley, J.H., Lahti, J.M., and Kidd, V.J. 1998. The RNP protein, RNPS1, associates with specific isoforms of the p34cdc2-related PITSLRE protein kinase in vivo. J. Cell Sci. 111 (Pt 11): 1495-1506.
33. Lu, S. and Cullen, B.R. 2003. Analysis of the stimulatory effect of splicing on mRNA production and utilization in mammalian cells. RNA 9: 618-630.
34. Luo, M.J. and Reed, R. 1999. Splicing is required for rapid and efficient mRNA export in metazoans. Proc. Natl. Acad. Sci. 96: 14937-14942.
35. Luo, M.L., Zhou, Z., Magni, K., Christoforides, C., Rappsilber, J., Mann, M., and Reed, R. 2001. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413: 644-647.
36. Lykke-Andersen, J., Shu, M.D., and Steitz, J.A. 2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103: 1121-1131.
37. -. 2001. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293: 1836-1839.
38. Maderazo, A.B., He, F., Mangus, D.A., and Jacobson, A. 2000. Upf1p control of nonsense mRNA translation is regulated by Nmd2p and Upf3p. Mol. Cell. Biol. 20: 4591-4603.
39. Maniatis, T. and Reed, R. 2002. An extensive network of coupling among gene expression machines. Nature 416: 499-506.
40. Maquat, L.E. and Carmichael, G.G. 2001. Quality control of mRNA function. Cell 104: 173-176.
41. Matsumoto, K., Wassarman, K.M., and Wolffe, A.P. 1998. Nuclear history of a pre-mRNA determines the translational activity of cytoplasmic mRNA. EMBO J. 17: 2107-2121.
42. Mayeda, A., Badolato, J., Kobayashi, R., Zhang, M.Q., Gardiner, E.M., and Krainer, A.R. 1999. Purification and characterization of human RNPS1: A general activator of pre-mRNA splicing. EMBO J. 18: 4560-4570.
43. McCracken, S., Lambermon, M., and Blencowe, B.J. 2002. SRm160 splicing coactivator promotes transcript 3′-end cleavage. Mol. Cell. Biol. 22: 148-160.
44. McCracken, S., Longman, D., Johnstone, I.L., Caceres, J.F., and Blencowe, B.J. 2003. An evolutionarily conserved role for SRm160 in 3′-end formation that functions independently of exon junction complex formation. J. Biol. Chem. 278: 44153-44160.
45. 7 guanosine cap. Mol. Cell. Biol. 21: 3632-3641.
46. Mendell, J.T., Medghalchi, S.M., Lake, R.G., Noensie, E.N., and Dietz, H.C. 2000. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol. 20: 8944-8957.
47. Mendez, R. and Richter, J.D. 2001. Translational control by CPEB: A means to the end. Nat. Rev. Mol. Cell. Biol. 2: 521-529.
48. Minich, W.B. and Ovchinnikov, L.P. 1992. Role of cytoplasmic mRNP proteins in translation. Biochimie 74: 477-483.
49. Mohr, S.E., Dillon, S.T., and Boswell, R.E. 2001. The RNA-binding protein Tsunagi interacts with Mago Nashi to establish polarity and localize oskar mRNA during Drosophila oogenesis. Genes & Dev. 15: 2886-2899.
50. Negrutskii, B.S., Stapulionis, R., and Deutscher, M.P. 1994. Supramolecular organization of the mammalian translation system. Proc. Natl. Acad. Sci. 91: 964-968.
51. Nott, A., Meislin, S.H., and Moore, M.J. 2003. A quantitative analysis of intron effects on mammalian gene expression. RNA 9: 607-617.
52. Orphanides, G. and Reinberg, D. 2002. A unified theory of gene expression. Cell 108: 439-451.
53. Pisarev, A.V., Skabkin, M.A., Thomas, A.A., Merrick, W.C., Ovchinnikov, L.P., and Shatsky, I.N. 2002. Positive and negative effects of the major mammalian messenger ribonucleoprotein p50 on binding of 40 S ribosomal subunits to the initiation codon of β-globin mRNA. J. Biol. Chem. 277: 15445-15451.
54. Ponting, C.P. 2000. Novel eIF4G domain homologues linking mRNA translation with nonsense-mediated mRNA decay. Trends Biochem. Sci. 25: 423-426.
55. Proudfoot, N.J., Furger, A., and Dye, M.J. 2002. Integrating mRNA processing with transcription. Cell 108: 501-512.
56. Rafiq, M., Suen, C.K., Choudhury, N., Joannou, C.L., White, K.N., and Evans, R.W. 1997. Expression of recombinant human ceruloplasmin - An absolute requirement for splicing signals in the expression cassette. FEBS Lett. 407: 132-136.
57. Reichert, V.L., Le Hir, H., Jurica, M.S., and Moore, M.J. 2002. 5′ exon interactions within the human spliceosome establish a framework for exon junction complex structure and assembly. Genes & Dev 16: 2778-2791.
58. Ruan, H., Brown, C.Y., and Morris, D.R. 1997. Analysis of ribosome loading onto mRNA species: Implications for translation control. In mRNA formation and function (ed. J.D. Richter), pp. 305-321. Academic Press, San Diego.
59. Ryu, W.S. and Mertz, J.E. 1989. Simian virus 40 late transcripts lacking excisable intervening sequences are defective in both stability in the nucleus and transport to the cytoplasm. J. Virol. 63: 4386-4394.
60. Schell, T., Kulozik, A.E., and Hentze, M.W. 2002. Integration of splicing, transport and translation to achieve mRNA quality control by the nonsense-mediated decay pathway. Genome Biol. 3: REVIEWS1006.
61. Schwer, B. 2001. A new twist on RNA helicases: DExH/D box proteins as RNPases. Nat. Struct. Biol. 8: 113-116.
62. Sonenberg, N. 1996. mRNA 5′ cap-binding protein eIF4E and control of cell growth. In Translational control (eds. J.W.B. Hershey et al.), pp. 245-269. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
63. Spirin, A.S. 1996. Masked and translatable messenger ribonucleoproteins in higher eukaryotes. In Translational control (eds. J.W.B. Hershey et al.), pp. 319-334. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
64. Stapulionis, R., Kolli, S., and Deutscher, M.P. 1997. Efficient mammalian protein synthesis requires an intact F-actin system. J. Biol. Chem. 272: 24980-24986.
65. Trembley, J.H., Hu, D., Hsu, L.C., Yeung, C.Y., Slaughter, C., Lahti, J.M., and Kidd, V.J. 2002. PITSLRE p110 protein kinases associate with transcription complexes and affect their activity. J. Biol. Chem. 277: 2589-2596.
66. Wang, W., Czaplinski, K., Rao, Y., and Peltz, S.W. 2001. The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J. 20: 880-890.
67. Welch, E.M. and Jacobson, A. 1999. An internal open reading frame triggers nonsense-mediated decay of the yeast SPT10 mRNA. EMBO J. 18: 6134-6145.
68. Wiegand, H.L., Lu, S., and Cullen, B.R. 2002. Exon junction complexes mediate the enhancing effect of splicing on mRNA expression. Proc. Natl. Acad. Sci. 100: 11327-11332.
69. Wilkinson, M.F. and Shyu, A.B. 2002. RNA surveillance by nuclear scanning? Nat. Cell Biol. 4: E144-E147.
70. Will, C.L. and Luhrmann, R. 2001. Molecular biology. RNP remodeling with DExH/D boxes. Science 291: 1916-1917.
71. Wilusz, C.J., Wang, W., and Peltz, S.W. 2001. Curbing the nonsense: The activation and regulation of mRNA surveillance. Genes & Dev. 15: 2781-2785.
72. Zhou, Z., Luo, M.J., Straesser, K., Katahira, J., Hurt, E., and Reed, R. 2000. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 407: 401-405.
73. Zong, Q., Schummer, M., Hood, L., and Morris, D.R. 1999. Messenger RNA translation state: The second dimension of high-throughput expression screening. Proc. Natl. Acad. Sci. 96: 10632-10636.