The Exon Junction Complex Controls the Splicing of mapk and Other Long Intron-Containing Transcripts in Drosophila

Cell

Volumn 143, Issue 2, 2010, Pages 251-262

  Ashton Beaucage, Dariel ^a   Udell, Christian M ^a   Lavoie, Hugo ^a   Baril, Caroline ^a   Lefrançois, Martin ^a   Chagnon, Pierre ^a   Gendron, Patrick ^a   Caron Lizotte, Olivier ^a   Bonneil, Éric ^a   Thibault, Pierre ^a,b   Therrien, Marc ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

RNA; Signaling

Indexed keywords

EXON JUNCTION COMPLEX PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEAR FACTOR; RAS PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; RNA PRECURSOR;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; EXON; INTRON; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; RNA SPLICING;

ANIMALS; CELL LINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXONS; INTRONS; MITOGEN-ACTIVATED PROTEIN KINASES; RNA PRECURSORS; RNA SPLICING; SIGNAL TRANSDUCTION;

EID: 77957766928     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.09.014     Document Type: Article

References (72)

1. Baker N.E., Rubin G.M. Effect on eye development of dominant mutations in Drosophila homologue of the EGF receptor. Nature 1989, 340:150-153.
2. Ballut L., Marchadier B., Baguet A., Tomasetto C., Seraphin B., Le Hir H. The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat. Struct. Mol. Biol. 2005, 12:861-869.
3. Berghella L., Dimitri P. The heterochromatic rolled gene of Drosophila melanogaster is extensively polytenized and transcriptionally active in the salivary gland chromocenter. Genetics 1996, 144:117-125.
4. Bessonov S., Anokhina M., Will C.L., Urlaub H., Luhrmann R. Isolation of an active step I spliceosome and composition of its RNP core. Nature 2008, 452:846-850.
5. Blencowe B.J., Issner R., Nickerson J.A., Sharp P.A. A coactivator of pre-mRNAcsplicing. Genes Dev. 1998, 12:996-1009.
6. Boswell R.E., Prout M.E., Steichen J.C. Mutations in a newly identified Drosophila melanogaster gene, mago nashi, disrupt germ cell formation and result in the formation of mirror-image symmetrical double abdomen embryos. Development 1991, 113:373-384.
7. Budagyan, B., and Loraine, A. (2004). Gene length and alternative transcription in fruit fly. Computational Systems Bioinformatics Conference, 2004: 2004, Stanford, CA, USA: Proceedings, 515 - 516.
8. Chang Y.F., Imam J.S., Wilkinson M.F. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 2007, 76:51-74.
9. Cheng C., Sharp P.A. Regulation of CD44 alternative splicing by SRm160 and its potential role in tumor cell invasion. Mol. Cell. Biol. 2006, 26:362-370.
10. Cheng C., Yaffe M.B., Sharp P.A. A positive feedback loop couples Ras activation and CD44 alternative splicing. Genes Dev. 2006, 20:1715-1720.
11. Degot S. Association of the breast cancer protein MLN51 with the exon junction complex via its speckle localizer and RNA binding module. J. Biol. Chem. 2004, 279:33702-33715.
12. Diem M.D., Chan C.C., Younis I., Dreyfuss G. PYM binds the cytoplasmic exon-junction complex and ribosomes to enhance translation of spliced mRNAs. Nat. Struct. Mol. Biol. 2007, 14:1173-1179.
13. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
14. Dougherty M.K., Muller J., Ritt D.A., Zhou M., Zhou X.Z., Copeland T.D., Conrads T.P., Veenstra T.D., Lu K.P., Morrison D.K. Regulation of Raf-1 by direct feedback phosphorylation. Mol. Cell 2005, 17:215-224.
15. Douziech M., Roy F., Laberge G., Lefrancois M., Armengod A.V., Therrien M. Bimodal regulation of RAF by CNK in Drosophila. EMBO J. 2003, 22:5068-5078.
16. Ebisuya M., Kondoh K., Nishida E. The duration, magnitude and compartmentalization of ERK MAP kinase activity: mechanisms for providing signaling specificity. J. Cell Sci. 2005, 118:2997-3002.
17. Eldridge A.G., Li Y., Sharp P.A., Blencowe B.J. The SRm160/300 splicing coactivator is required for exon-enhancer function. Proc. Natl. Acad. Sci. USA 1999, 96:6125-6130.
18. Fortini M.E., Simon M.A., Rubin G.M. Signalling by the sevenless protein tyrosine kinase is mimicked by Ras1 activation. Nature 1992, 355:559-561.
19. Fox-Walsh K.L., Dou Y., Lam B.J., Hung S.P., Baldi P.F., Hertel K.J. The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc. Natl. Acad. Sci. USA 2005, 102:16176-16181.
20. Gatfield D., Izaurralde E. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J. Cell Biol. 2002, 159:579-588.
21. Gatfield D., Unterholzner L., Ciccarelli F.D., Bork P., Izaurralde E. Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J. 2003, 22:3960-3970.
22. Gehring N.H., Lamprinaki S., Hentze M.W., Kulozik A.E. The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsense-mediated mRNA decay. PLoS Biol. 2009, 7:e1000120.
23. Gehring N.H., Neu-Yilik G., Schell T., Hentze M.W., Kulozik A.E. Y14 and hUpf3b Form an NMD-Activating Complex. Mol. Cell 2003, 11:939-949.
24. Gygi S.P., Rochon Y., Franza B.R., Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 1999, 19:1720-1730.
25. Hachet O., Ephrussi A. Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 2004, 428:959-963.
26. Herold N., Will C.L., Wolf E., Kastner B., Urlaub H., Luhrmann R. Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol. Cell. Biol. 2009, 29:281-301.
27. House A.E., Lynch K.W. Regulation of alternative splicing: more than just the ABCs. J. Biol. Chem. 2008, 283:1217-1221.
28. Hurlbut G.D., Kankel M.W., Lake R.J., Artavanis-Tsakonas S. Crossing paths with Notch in the hyper-network. Curr. Opin. Cell Biol. 2007, 19:166-175.
29. Johnson S.M., Grosshans H., Shingara J., Byrom M., Jarvis R., Cheng A., Labourier E., Reinert K.L., Brown D., Slack F.J. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647.
30. Karim F.D., Chang H.C., Therrien M., Wassarman D.A., Laverty T., Rubin G.M. A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 1996, 143:315-329.
31. Kim E., Magen A., Ast G. Different levels of alternative splicing among eukaryotes. Nucleic Acids Res. 2007, 35:125-131.
32. Kolch W. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 2005, 6:827-837.
33. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
34. Le Hir H., Gatfield D., Braun I.C., Forler D., Izaurralde E. The protein Mago provides a link between splicing and mRNA localization. EMBO Rep. 2001, 2:1119-1124.
35. 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. 2001, 20:4987-4997.
36. Le Hir H., Izaurralde E., Maquat L.E., Moore M.J. The spliceosome deposits multiple proteins 20[ndash]24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 2000, 19:6860-6869.
37. Lee M.H., Hook B., Pan G., Kershner A.M., Merritt C., Seydoux G., Thomson J.A., Wickens M., Kimble J. Conserved regulation of MAP kinase expression by PUF RNA-binding proteins. PLoS Genet. 2007, 3:e233.
38. Long J.C., Caceres J.F. The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 2009, 417:15-27.
39. Longman D., Plasterk R.H.A., Johnstone I.L., Cáceres J.F. Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes Dev. 2007, 21:1075-1085.
40. 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 2001, 293:1836-1839.
41. Ma X.M., Yoon S.O., Richardson C.J., Julich K., Blenis J. SKAR links pre-mRNA splicing to mTOR/S6K1-mediated enhanced translation efficiency of spliced mRNAs. Cell 2008, 133:303-313.
42. Macchi P., Kroening S., Palacios I.M., Baldassa S., Grunewald B., Ambrosino C., Goetze B., Lupas A., St Johnston D., Kiebler M. Barentsz, a new component of the Staufen-containing ribonucleoprotein particles in mammalian cells, interacts with Staufen in an RNA-dependent manner. J. Neurosci. 2003, 23:5778-5788.
43. Mayeda A., Badolato J., Kobayashi R., Zhang M.Q., Gardiner E.M., Krainer A.R. Purification and characterization of human RNPS1: a general activator of pre-mRNA splicing. EMBO J. 1999, 18:4560-4570.
44. McCracken S., Lambermon M., Blencowe B.J. SRm160 splicing coactivator promotes transcript 3′-end cleavage. Mol. Cell. Biol. 2002, 22:148-160.
45. McCracken S., Longman D., Johnstone I.L., Cáceres J.F., Blencowe B.J. An Evolutionarily Conserved Role for SRm160 in 3′-End Processing That Functions Independently of Exon Junction Complex Formation. J. Biol. Chem. 2003, 278:44153-44160.
46. McGuire A., Pearson M., Neafsey D., Galagan J. Cross-kingdom patterns of alternative splicing and splice recognition. Genome Biol. 2008, 9:R50.
47. McKay M.M., Morrison D.K. Integrating signals from RTKs to ERK/MAPK. Oncogene 2007, 26:3113-3121.
48. Melnick M.B., Perkins L.A., Lee M., Ambrosio L., Perrimon N. Developmental and molecular characterization of mutations in the Drosophila-raf serine/threonine protein kinase. Development 1993, 118:127-138.
49. Merz C., Urlaub H., Will C.L., Luhrmann R. Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. RNA 2007, 13:116-128.
50. Mohr S.E., Dillon S.T., Boswell R.E. The RNA-binding protein Tsunagi interacts with Mago Nashi to establish polarity and localize oskar mRNA during Drosophila oogenesis. Genes Dev. 2001, 15:2886-2899.
51. Mount S.M., Burks C., Hertz G., Stormo G.D., White O., Fields C. Splicing signals in Drosophila: intron size, information content, and consensus sequences. Nucleic Acids Res. 1992, 20:4255-4262.
52. Nott A., Le Hir H., Moore M.J. Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev. 2004, 18:210-222.
53. Nykamp K., Lee M.H., Kimble J. C. elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis. RNA 2008, 14:1378-1389.
54. Palacios I.M., Gatfield D., St Johnston D., Izaurralde E. An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 2004, 427:753-757.
55. Perkins L.A., Johnson M.R., Melnick M.B., Perrimon N. The nonreceptor protein tyrosine phosphatase corkscrew functions in multiple receptor tyrosine kinase pathways in Drosophila. Dev. Biol. 1996, 180:63-81.
56. Perkins L.A., Larsen I., Perrimon N. corkscrew encodes a putative protein tyrosine phosphatase that functions to transduce the terminal signal from the receptor tyrosine kinase torso. Cell 1992, 70:225-236.
57. Roy M., Kim N., Xing Y., Lee C. The effect of intron length on exon creation ratios during the evolution of Mamm. Genomes. RNA 2008, 14:1-13.
58. Sakashita E., Tatsumi S., Werner D., Endo H., Mayeda A. Human RNPS1 and its associated factors: a versatile alternative pre-mRNA splicing regulator in vivo. Mol. Cell. Biol. 2004, 24:1174-1187.
59. Schubbert S., Shannon K., Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer 2007, 7:295-308.
60. Stamm S. Regulation of alternative splicing by reversible protein phosphorylation. J. Biol. Chem. 2008, 283:1223-1227.
61. Sterner D.A., Carlo T., Berget S.M. Architectural limits on split genes. Proc. Natl. Acad. Sci. USA 1996, 93:15081-15085.
62. Tange T.O., Nott A., Moore M.J. The ever-increasing complexities of the exon junction complex. Curr. Opin. Cell Biol. 2004, 16:279-284.
63. Therrien M., Morrison D.K., Wong A.M., Rubin G.M. A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics 2000, 156:1231-1242.
64. Trembley J.H., Tatsumi S., Sakashita E., Loyer P., Slaughter C.A., Suzuki H., Endo H., Kidd V.J., Mayeda A. Activation of pre-mRNA splicing by human RNPS1 is regulated by CK2 phosphorylation. Mol. Cell. Biol. 2005, 25:1446-1457.
65. Turjanski A.G., Vaque J.P., Gutkind J.S. MAP kinases and the control of nuclear events. Oncogene 2007, 26:3240-3253.
66. van Eeden F.J., Palacios I.M., Petronczki M., Weston M.J., St Johnston D. Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J. Cell Biol. 2001, 154:511-523.
67. Wassarman D.A., Therrien M., Rubin G.M. The Ras signaling pathway in Drosophila. Curr. Opin. Genet. Dev. 1995, 5:44-50.
68. Wen J., Brogna S. Splicing-dependent NMD does not require the EJC in Schizosaccharomyces pombe 2010, Embo J.
69. Wiegand H.L., Lu S., Cullen B.R. Exon junction complexes mediate the enhancing effect of splicing on mRNA expression. Proc. Natl. Acad. Sci. USA 2003, 100:11327-11332.
70. Xu T., Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993, 117:1223-1237.
71. Yu Y., Maroney P.A., Denker J.A., Zhang X.H., Dybkov O., Luhrmann R., Jankowsky E., Chasin L.A., Nilsen T.W. Dynamic regulation of alternative splicing by silencers that modulate 5′ splice site competition. Cell 2008, 135:1224-1236.
72. Zebisch A., Czernilofsky A.P., Keri G., Smigelskaite J., Sill H., Troppmair J. Signaling through RAS-RAF-MEK-ERK: from basics to bedside. Curr. Med. Chem. 2007, 14:601-623.