Perispeckles are major assembly sites for the exon junction core complex

Molecular Biology of the Cell

Volumn 23, Issue 9, 2012, Pages 1765-1782

  Daguenet, Elisabeth ^a   Baguet, Aurélie ^a   Degot, Sébastien ^a,d   Schmidt, Ute ^b   Alpy, Fabien ^a   Wendling, Corinne ^a   Spiegelhalter, Coralie ^a   Kessler, Pascal ^a   Rio, Marie Christine ^a   Hir, Hervé Le ^c   Bertrand, Edouard ^b   Tomasetto, Catherine ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CNRS   (France)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d CYTOO SA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EXON JUNCTION COMPLEX; HISTONE H3; INITIATION FACTOR; MESSENGER RNA; MULTIPROTEIN COMPLEX; PROTEIN EIF4A3; PROTEIN MAGOH; PROTEIN MLN51; PROTEIN Y14; RNA POLYMERASE II; TETRAMER; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; MUTANT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STABILITY; RNA SPLICING; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; ULTRASTRUCTURE;

CELL NUCLEUS; DEAD-BOX RNA HELICASES; EXONS; HELA CELLS; HUMANS; MUTATION; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSFECTION;

EID: 84860378396     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-01-0040     Document Type: Article

References (93)

1. Andersen CB, Ballut L, Johansen JS, Chamieh H, Nielsen KH, Oliveira CL, Pedersen JS, Seraphin B, Le Hir H, Andersen GR (2006). Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 313, 1968-1972. (Pubitemid 44498005)
2. Ashton-Beaucage D et al. (2010). The exon junction complex controls the splicing of MAPK and other long intron-containing transcripts in Drosophila. Cell 143, 251-262.
3. Baguet A, Degot S, Cougot N, Bertrand E, Chenard MP, Wendling C, Kessler P, Le Hir H, Rio MC, Tomasetto C (2007). The exon-junction-complex-component metastatic lymph node 51 functions in stress-granule assembly. J Cell Sci 120, 2774-2784. (Pubitemid 47394252)
4. Ballut L, Marchadier B, Baguet A, Tomasetto C, Seraphin B, Le Hir H (2005). The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat Struct Mol Biol 12, 861-869. (Pubitemid 41486709)
5. Behm-Ansmant I, Izaurralde E (2006). Quality control of gene expression: a stepwise assembly pathway for the surveillance complex that triggers nonsense-mediated mRNA decay. Genes Dev 20, 391-398. (Pubitemid 43244392)
6. Bernard D et al. (2010). A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J 29, 3082-3093.
7. Bessonov S, Anokhina M, Will CL, Urlaub H, Luhrmann R (2008). Isolation of an active step I spliceosome and composition of its RNP core. Nature 452, 846-850. (Pubitemid 351550864)
8. Bono F, Ebert J, Lorentzen E, Conti E (2006). The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126, 713-725. (Pubitemid 44233638)
9. Bono F, Gehring N (2011). Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol 8, 24-29.
10. Brown JM et al. (2008). Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J Cell Biol 182, 1083-1097.
11. Buchwald G, Ebert J, Basquin C, Sauliere J, Jayachandran U, Bono F, Le Hir H, Conti E (2010). Insights into the recruitment of the NMD machinery from the crystal structure of a core EJC-UPF3b complex. Proc Natl Acad Sci USA 107, 10050-10055.
12. Carmo-Fonseca M, Tollervey D, Pepperkok R, Barabino SM, Merdes A, Brunner C, Zamore PD, Green MR, Hurt E, Lamond AI (1991). Mammalian nuclei contain foci which are highly enriched in components of the pre-mRNA splicing machinery. EMBO J 10, 195-206. (Pubitemid 21905282)
13. Carter KC, Bowman D, Carrington W, Fogarty K, McNeil JA, Fay FS, Lawrence JB (1993). A three-dimensional view of precursor messenger RNA metabolism within the mammalian nucleus. Science 259, 1330-1335. (Pubitemid 23100273)
14. 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.
15. Custodio N, Carvalho C, Condado I, Antoniou M, Blencowe BJ, Carmo- Fonseca M (2004). In vivo recruitment of exon junction complex proteins to transcription sites in mammalian cell nuclei. RNA 10, 622-633. (Pubitemid 38405941)
16. Daigle N, Ellenberg J (2007). LambdaN-GFP: an RNA reporter system for live-cell imaging. Nat Methods 4, 633-636. (Pubitemid 47202473)
17. Degot S, Le Hir H, Alpy F, Kedinger V, Stoll I, Wendling C, Seraphin B, Rio MC, Tomasetto C (2004). Association of the breast cancer protein MLN51 with the exon junction complex via its speckle localizer and RNA binding module. J Biol Chem 279, 33702-33715. (Pubitemid 39063020)
18. Degot S, Regnier CH, Wendling C, Chenard MP, Rio MC, Tomasetto C (2002). Metastatic Lymph Node 51, a novel nucleo-cytoplasmic protein overexpressed in breast cancer. Oncogene 21, 4422-4434. (Pubitemid 34774845)
19. Dias AP, Dufu K, Lei H, Reed R (2010). A role for TREX components in the release of spliced mRNA from nuclear speckle domains. Nat Commun 1, 97.
20. Diem MD, Chan CC, Younis I, Dreyfuss G (2007). PYM binds the cytoplasmic exon-junction complex and ribosomes to enhance translation of spliced mRNAs. Nat Struct Mol Biol 14, 1173-1179. (Pubitemid 350223330)
21. Dostie J, Dreyfuss G (2002). Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr Biol 12, 1060-1067. (Pubitemid 34766927)
22. Ellis JD, Lleres D, Denegri M, Lamond AI, Caceres JF (2008). Spatial mapping of splicing factor complexes involved in exon and intron definition. J Cell Biol 181, 921-934. (Pubitemid 351846826)
23. Fakan S (1994). Perichromatin fibrils are in situ forms of nascent transcripts. Trends Cell Biol 4, 86-90.
24. Fakan S, Leser G, Martin TE (1984). Ultrastructural distribution of nuclear ribonucleoproteins as visualized by immunocytochemistry on thin sections. J Cell Biol 98, 358-363. (Pubitemid 14221295)
25. Ferraiuolo MA, Lee CS, Ler LW, Hsu JL, Costa-Mattioli M, Luo MJ, Reed R, Sonenberg N (2004). A nuclear translation-like factor eIF4AIII is recruited to the mRNA during splicing and functions in nonsense-mediated decay. Proc Natl Acad Sci USA 101, 4118-4123. (Pubitemid 38405893)
26. Fribourg S, Gatfield D, Izaurralde E, Conti E (2003). A novel mode of RBD-protein recognition in the Y14-Mago complex. Nat Struct Biol 10, 433-439. (Pubitemid 36637640)
27. Gehring NH, Kunz JB, Neu-Yilik G, Breit S, Viegas MH, Hentze MW, Kulozik AE (2005). Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol Cell 20, 65-75. (Pubitemid 41396563)
28. Gehring NH, Lamprinaki S, Hentze MW, Kulozik AE (2009a). The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsense-mediated mRNA decay. PLoS Biol 7, e1000120.
29. Gehring NH, Lamprinaki S, Kulozik AE, Hentze MW (2009b). Disassembly of exon junction complexes by PYM. Cell 137, 536-548.
30. Giorgi C, Moore MJ (2007). The nuclear nurture and cytoplasmic nature of localized mRNPs. Semin Cell Dev Biol 18, 186-193. (Pubitemid 46756360)
31. Gordon GW, Berry G, Liang XH, Levine B, Herman B (1998). Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys J 74, 2702-2713. (Pubitemid 28225264)
32. Hall LL, Smith KP, Byron M, Lawrence JB (2006). Molecular anatomy of a speckle. Anat Rec A Discov Mol Cell Evol Biol 288, 664-675. (Pubitemid 44015467)
33. Han J, Xiong J, Wang D, Fu XD (2011). Pre-mRNA splicing: where and when in the nucleus. Trends Cell Biol 21, 336-343.
34. Herold N, Will CL, Wolf E, Kastner B, Urlaub H, Luhrmann R (2009). Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol Cell Biol 29, 281-301.
35. Hu Q et al. (2008). Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc Natl Acad Sci USA 105, 19199-19204.
36. Hu Y, Plutz M, Belmont AS (2010). Hsp70 gene association with nuclear speckles is Hsp70 promoter specific. J Cell Biol 191, 711-719.
37. Huang Y, Gattoni R, Stevenin J, Steitz JA (2003). SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol Cell 11, 837-843. (Pubitemid 36385134)
38. Isken O, Maquat LE (2008). The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat Rev Genet 9, 699-712.
39. Kataoka N, Yong J, Kim VN, Velazquez F, Perkinson RA, Wang F, 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.
40. Lamond AI, Spector DL (2003). Nuclear speckles: a model for nuclear organelles. Nat Rev Mol Cell Biol 4, 605-612. (Pubitemid 36934962)
41. Le Hir H, Andersen GR (2008). Structural insights into the exon junction complex. Curr Opin Struct Biol 18, 112-119.
42. Le Hir H, Gatfield D, Braun IC, Forler D, Izaurralde E (2001a). The protein Mago provides a link between splicing and mRNA localization. EMBO Rep 2, 1119-1124. (Pubitemid 34055959)
43. Le Hir H, Gatfield D, Izaurralde E, Moore MJ (2001b). 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. (Pubitemid 32848650)
44. Le Hir H, Izaurralde E, Maquat LE, Moore MJ (2000). The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exonexon junctions. EMBO J 19, 6860-6869. (Pubitemid 32011679)
45. Le Hir H, Seraphin B (2008). EJCs at the heart of translational control. Cell 133, 213-216. (Pubitemid 351508309)
46. 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. (Pubitemid 34760583)
47. Luo ML, Zhou Z, Magni K, Christoforides C, Rappsilber J, Mann M, Reed R (2001). Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413, 644-647. (Pubitemid 32964065)
48. 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. (Pubitemid 32037398)
49. Ma XM, Yoon SO, Richardson CJ, Julich K, Blenis J (2008). SKAR links premRNA splicing to mTOR/S6K1-mediated enhanced translation efficiency of spliced mRNAs. Cell 133, 303-313. (Pubitemid 351508301)
50. Macchi P, Kroening S, Palacios IM, Baldassa S, Grunewald B, Ambrosino C, Goetze B, Lupas A, St Johnston D, Kiebler M (2003). Barentsz, a new component of the Staufen-containing ribonucleoprotein particles in mammalian cells, interacts with Staufen in an RNA-dependent manner. J Neurosci 23, 5778-5788. (Pubitemid 36807857)
51. Martin KC, Ephrussi A (2009). mRNA localization: gene expression in the spatial dimension. Cell 136, 719-730.
52. Matera AG, Izaguire-Sierra M, Praveen K, Rajendra TK (2009). Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Dev Cell 17, 639-647.
53. Mintz PJ, Spector DL (2000). Compartmentalization of RNA processing factors within nuclear speckles. J Struct Biol 129, 241-251. (Pubitemid 30481365)
54. Moog-Lutz C, Tomasetto C, Regnier CH, Wendling C, Lutz Y, Muller D, Chenard MP, Basset P, Rio MC (1997). MLN64 exhibits homology with the steroidogenic acute regulatory protein (STAR) and is over-expressed in human breast carcinomas. Int J Cancer 71, 183-191. (Pubitemid 27252988)
55. Moore MJ, Proudfoot NJ (2009). Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688-700.
56. Nott A, Le Hir H, Moore MJ (2004). Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev 18, 210-222. (Pubitemid 38141788)
57. Palacios IM, Gatfield D, St Johnston D, Izaurralde E (2004). An eIFS4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427, 753-757. (Pubitemid 38294596)
58. Phair RD, Misteli T (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609. (Pubitemid 30205058)
59. Puvion E, Puvion-Dutilleul F (1996). Ultrastructure of the nucleus in relation to transcription and splicing: roles of perichromatin fibrils and interchromatin granules. Exp Cell Res 229, 217-225. (Pubitemid 27026908)
60. Rebbapragada I, Lykke-Andersen J (2009). Execution of nonsense-mediated mRNA decay: what defines a substrate? Curr Opin Cell Biol 21, 394-402.
61. Reichert VL, Le Hir H, Jurica MS, Moore MJ (2002). 5′ exon interactions within the human spliceosome establish a framework for exon junction complex structure and assembly. Genes Dev 16, 2778-2791. (Pubitemid 35253146)
62. Roignant JY, Treisman JE (2010). Exon junction complex subunits are required to splice Drosophila MAP kinase, a large heterochromatic gene. Cell 143, 238-250.
63. Sacco-Bubulya P, Spector DL (2002). Disassembly of interchromatin granule clusters alters the coordination of transcription and pre-mRNA splicing. J Cell Biol 156, 425-436. (Pubitemid 34839892)
64. Saitoh N, Spahr CS, Patterson SD, Bubulya P, Neuwald AF, Spector DL (2004). Proteomic analysis of interchromatin granule clusters. Mol Biol Cell 15, 3876-3890. (Pubitemid 38989721)
65. Schmidt U, Basyuk E, Robert MC, Yoshida M, Villemin JP, Auboeuf D, Aitken S, Bertrand E (2011). Real-time imaging of cotranscriptional splicing reveals a kinetic model that reduces noise: implications for alternative splicing regulation. J Cell Biol 193, 819-829.
66. Schmidt U, Richter K, Berger AB, Lichter P (2006). In vivo BiFC analysis of Y14 and NXF1 mRNA export complexes: preferential localization within and around SC35 domains. J Cell Biol 172, 373-381. (Pubitemid 43187934)
67. Schwerk C, Prasad J, Degenhardt K, Erdjument-Bromage H, White E, Tempst P, Kidd VJ, Manley JL, Lahti JM, Reinberg D (2003). ASAP, a novel protein complex involved in RNA processing and apoptosis. Mol Cell Biol 23, 2981-2990. (Pubitemid 36403093)
68. Sharma A, Takata H, Shibahara K, Bubulya A, Bubulya PA (2010). Son is essential for nuclear speckle organization and cell cycle progression. Mol Biol Cell 21, 650-663.
69. Shibuya T, Tange TO, Stroupe ME, Moore MJ (2006). Mutational analysis of human eIF4AIII identifies regions necessary for exon junction complex formation and nonsense-mediated mRNA decay. RNA 12, 360-374. (Pubitemid 43290865)
70. Shopland LS, Johnson CV, Byron M, McNeil J, Lawrence JB (2003). Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods. J Cell Biol 162, 981-990. (Pubitemid 37179876)
71. Shyu AB, Wilkinson MF, van Hoof A (2008). Messenger RNA regulation: to translate or to degrade. EMBO J 27, 471-481. (Pubitemid 351225677)
72. Sleeman JE, Trinkle-Mulcahy L, Prescott AR, Ogg SC, Lamond AI (2003). Cajal body proteins SMN and Coilin show differential dynamic behaviour in vivo. J Cell Sci 116, 2039-2050. (Pubitemid 36622301)
73. Spector DL, Fu XD, Maniatis T (1991). Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J 10, 3467-3481. (Pubitemid 21905372)
74. Spector DL, Lamond AI (2011). Nuclear speckles. Cold Spring Harb Perspect Biol 3, a000646.
75. Spector DL, Schrier WH, Busch H (1983). Immunoelectron microscopic localization of snRNPs. Biol Cell 49, 1-10. (Pubitemid 14221581)
76. Spiegelhalter C, Tosch V, Hentsch D, Koch M, Kessler P, Schwab Y, Laporte J (2010). From dynamic live cell imaging to 3D ultrastructure: novel integrated methods for high pressure freezing and correlative light-electron microscopy. PLoS One 5, e9014.
77. Spiluttini B, Gu B, Belagal P, Smirnova AS, Nguyen VT, Hebert C, Schmidt U, Bertrand E, Darzacq X, Bensaude O (2010). Splicing-independent recruitment of U1 snRNP to a transcription unit in living cells. J Cell Sci 123, 2085-2093.
78. Stalder L, Muhlemann O (2008). The meaning of nonsense. Trends Cell Biol 18, 315-321.
79. Stroupe ME, Tange TO, Thomas DR, Moore MJ, Grigorieff N (2006). The three-dimensional architecture of the EJC core. J Mol Biol 360, 743-749.
80. Sutherland H, Bickmore WA (2009). Transcription factories: gene expression in unions? Nat Rev Genet 10, 457-466.
81. Tange TO, Nott A, Moore MJ (2004). The ever-increasing complexities of the exon junction complex. Curr Opin Cell Biol 16, 279-284. (Pubitemid 38610408)
82. Tange TO, Shibuya T, Jurica MS, Moore MJ (2005). Biochemical analysis of the EJC reveals two new factors and a stable tetrameric protein core. RNA 11, 1869-1883. (Pubitemid 41720036)
83. Thiry M (1995). The interchromatin granules. Histol Histopathol 10, 1035-1045.
84. Tripathi V et al. (2010). The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39, 925-938.
85. van Eeden FJ, Palacios IM, Petronczki M, Weston MJ, St Johnston D (2001). Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J Cell Biol 154, 511-523. (Pubitemid 34286158)
86. Vargas DY, Shah K, Batish M, Levandoski M, Sinha S, Marras SA, Schedl P, Tyagi S (2011). Single-molecule imaging of transcriptionally coupled and uncoupled splicing. Cell 147, 1054-1065.
87. Varnai P, Toth B, Toth DJ, Hunyady L, Balla T (2007). Visualization and manipulation of plasma membrane-endoplasmic reticulum contact sites indicates the presence of additional molecular components within the STIM1-Orai1 complex. J Biol Chem 282, 29678-29690. (Pubitemid 350043396)
88. Visa N, Puvion-Dutilleul F, Harper F, Bachellerie JP, Puvion E (1993). Intranuclear distribution of poly(A) RNA determined by electron microscope in situ hybridization. Exp Cell Res 208, 19-34. (Pubitemid 23274485)
89. Wouters FS, Verveer PJ, Bastiaens PI (2001). Imaging biochemistry inside cells. Trends Cell Biol 11, 203-211. (Pubitemid 32367877)
90. Xing Y, Johnson CV, Dobner PR, Lawrence JB (1993). Higher level organization of individual gene transcription and RNA splicing. Science 259, 1326-1330. (Pubitemid 23100272)
91. 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 USA 104, 11574-11579. (Pubitemid 47175054)
92. Zhong XY, Wang P, Han J, Rosenfeld MG, Fu XD (2009). SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol Cell 35, 1-10.
93. Zillmann M, Zapp ML, Berget SM (1988). Gel electrophoretic isolation of splicing complexes containing U1 small nuclear ribonucleoprotein particles. Mol Cell Biol 8, 814-821. (Pubitemid 18044886)