The exon junction complex is required for definition and excision of neighboring introns in Drosophila

Genes and Development

Volumn 28, Issue 16, 2014, Pages 1772-1785

  Hayashi, Rippei ^a   Handler, Dominik ^a   Ish Horowicz, David ^b   Brennecke, Julius ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Exon junction complex; Intron definition; Piwi piRNA pathway; Splicing; SR proteins acinus and RnpS1; Transposon silencing

Indexed keywords

ARGONAUTE PROTEIN; PIWI INTERACTING RNA; PIWI PROTEIN; TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EXON; EXON JUNCTION COMPLEX; EXON SKIPPING; FLUORESCENCE IN SITU HYBRIDIZATION; GENE ISOLATION; GENE LOCUS; INTRON; INTRON RETENTION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; OVARY; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; RNA SEQUENCE; RNA SPLICING; TRANSPOSON;

EXON JUNCTION COMPLEX; INTRON DEFINITION; PIWI-PIRNA PATHWAY; SPLICING; SR PROTEINS ACINUS AND RNPS1; TRANSPOSON SILENCING;

ANIMALS; ARGONAUTE PROTEINS; CELLS, CULTURED; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; INTRONS; OVARY; RNA PRECURSORS; RNA SPLICING;

EID: 84906091347     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.245738.114     Document Type: Article

References (52)

1. Ashton-Beaucage D., Therrien M. 2011. The exon junction complex: a splicing factor for long intron containing transcripts? Fly (Austin) 5: 224-233.
2. Ashton-Beaucage D., Udell CM, Lavoie H, Baril C, Lefrançois M, Chagnon P., Gendron P, Caron-Lizotte O, Bonneil E, Thibault P, 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. Bono F., Gehring NH. 2011. Assembly, disassembly and recycling: the dynamics of exon junction complexes. RNA Biol 8: 24-29.
4. Brennecke J., Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R., Hannon GJ. 2007. Discrete small RNAgenerating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
5. Clark F., Thanaraj TA. 2002. Categorization and characterization of transcript-confirmed constitutively and alternatively spliced introns and exons from human. Hum Mol Genet 11: 451-464.
6. Czech B., Preall JB, McGinn J, Hannon GJ. 2013. A transcriptomewide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell 50: 749-761.
7. De Conti L., Baralle M, Buratti E. 2013. Exon and intron definition in pre-mRNA splicing. Wiley Interdiscip Rev RNA 4: 49-60.
8. 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.
9. Dietzl G., Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B., Kinsey K, Oppel S, Scheiblauer S, et al. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
10. Fededa J. P, Petrillo E, Gelfand MS, Neverov AD, Kadener S, Nogues G., Pelisch F, Baralle FE, Muro AF, Kornblihtt AR. 2005. A polar mechanism coordinates different regions of alternative splicing within a single gene. Mol Cell 19: 393-404.
11. Fox-Walsh K. L, Dou Y, Lam BJ, Hung SP, Baldi PF, Hertel KJ. 2005. The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc Natl Acad Sci 102: 16176-16181.
12. Garg K., Green P. 2007. Differing patterns of selection in alternative and constitutive splice sites. Genome Res 17: 1015-1022.
13. Gehring N. H, Neu-Yilik G, Schell T, Hentze MW, Kulozik AE. 2003. Y14 and hUpf3b form an NMD-activating complex. Mol Cell 11: 939-949.
14. Gehring N. H, Lamprinaki S, Hentze MW, Kulozik AE. 2009. The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsensemediated mRNA decay. PLoS Biol 7: e1000120.
15. Gibson D. G, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343-345.
16. Glauser D. A, Johnson BE, Aldrich RW, Goodman MB. 2011. Intragenic alternative splicing coordination is essential for Caenorhabditis elegans slo-1 gene function. Proc Natl Acad Sci 108: 20790-20795.
17. Groth A. C, Fish M, Nusse R, Calos MP. 2004. Construction of transgenic Drosophila by using the site-specific integrase from phage uC31. Genetics 166: 1775-1782.
18. Guo M., Lo PC, Mount SM. 1993. Species-specific signals for the splicing of a short Drosophila intron in vitro. Mol Cell Biol 13: 1104-1118.
19. Handler D., Meixner K, Pizka M, Lauss K, Schmied C, Gruber FS, Brennecke J. 2013. The genetic makeup of the Drosophila piRNA pathway. Mol Cell 50: 762-777.
20. Kaida D., Berg MG, Younis I, Kasim M, Singh LN, Wan L, Dreyfuss G. 2010. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468: 664-668.
21. 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.
22. Khodor Y. L, Rodriguez J, Abruzzi KC, Tang CH, Marr MT 2nd, Rosbash M. 2011. Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila. Genes Dev 25: 2502-2512.
23. Lecuyer E., Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T., Hughes TR, Tomancak P, Krause HM. 2007. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187.
24. Le Hir H., Izaurralde E, Maquat LE, Moore MJ. 2000a. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J 19: 6860-6869.
25. Le Hir H., Moore MJ, Maquat LE. 2000b. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev 14: 1098-1108.
26. Li C., Lin RI, Lai MC, Ouyang P, Tarn WY. 2003. Nuclear Pnn/ DRS protein binds to spliced mRNPs and participates in mRNA processing and export via interaction with RNPS1. Mol Cell Biol 23: 7363-7376.
27. Luo M. L, 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.
28. Mayeda A., Badolato J, Kobayashi R, Zhang MQ, Gardiner EM, Krainer A.R. 1999. Purification and characterization of human RNPS1: a general activator of pre-mRNA splicing. EMBO J 18: 4560-4570.
29. Michelle L., Cloutier A, Toutant J, Shkreta L, Thibault P, Durand M, Garneau D., Gendron D, Lapointe E, Couture S, et al. 2012. Proteins associated with the exon junction complex also control the alternative splicing of apoptotic regulators. Mol Cell Biol 32: 954-967.
30. Muerdter F., Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, Fekete R, Hannon G.J. 2013. A genome-wideRNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell 50: 736-748.
31. Ni J. Q, Zhou R, Czech B, Liu LP, Holderbaum L, Yang-Zhou D, Shim H. S, Tao R, Handler D, Karpowicz P, et al. 2011. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405-407.
32. Niki Y., Yamaguchi T, Mahowald AP. 2006. Establishment of stable cell lines of Drosophila germ-line stem cells. Proc Natl Acad Sci 103: 16325-16330.
33. Olivieri D., Sykora MM, Sachidanandam R, Mechtler K, Brennecke J. 2010. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J 29: 3301-3317.
34. Roignant J. Y, Treisman JE. 2010. Exon junction complex subunits are required to splice Drosophila MAP kinase, a large heterochromatic gene. Cell 143: 238-250.
35. Saito K., Inagaki S, Mituyama T, Kawamura Y, Ono Y, Sakota E, Kotani H., Asai K, Siomi H, Siomi MC. 2009. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461: 1296-1299.
36. Saito K., Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, Siomi H., Siomi MC. 2010. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev 24: 2493-2498.
37. Sakashita E., Tatsumi S, Werner D, Endo H, Mayeda A. 2004. Human RNPS1 and its associated factors: a versatile alternative pre-mRNA splicing regulator in vivo. Mol Cell Biol 24: 1174-1187.
38. Sarot E., Payen-Groschene G, Bucheton A, Pelisson A. 2004. Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166: 1313-1321.
39. Schmittgen T. D, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
40. 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.
41. Senti K. A, Brennecke J. 2010. The piRNA pathway: a fly's perspective on the guardian of the genome. Trends Genet 26: 499-509.
42. Shibuya T., Tange TO, Sonenberg N, Moore MJ. 2004. eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat Struct Mol Biol 11: 346-351.
43. Sienski G., Donertas D, Brennecke J. 2012. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151: 964-980.
44. Singh G., Kucukural A, Cenik C, Leszyk JD, Shaffer SA, Weng Z, Moore M.J. 2012. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151: 750-764.
45. Siomi M. C, Sato K, Pezic D, Aravin AA. 2011. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258.
46. Szakmary A., Reedy M, Qi H, Lin H. 2009. The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. J Cell Biol 185: 613-627.
47. Tamura K., Subramanian S, Kumar S. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21: 36-44.
48. Tange T. O, Nott A, Moore MJ. 2004. The ever-increasing complexities of the exon junction complex. Curr Opin Cell Biol 16: 279-284.
49. Tange T. O, 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.
50. Zamore P. D, Patton JG, Green MR. 1992. Cloning and domain structure of the mammalian splicing factor U2AF. Nature 355: 609-614.
51. Zhang Y., Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D. 1997. Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 89: 357-364.
52. Zhang Z., Theurkauf WE, Weng Z, Zamore PD. 2012. Strandspecific libraries for high throughput RNA sequencing (RNA-seq) prepared without poly(A) selection. Silence 3: 9.