Splicing-independent loading of TREX on nascent RNA is required for efficient expression of dual-strand piRNA clusters in drosophila

Genes and Development

Volumn 30, Issue 7, 2016, Pages 840-855

  Hur, Junho K ^a   Luo, Yicheng ^a   Moon, Sungjin ^b,c   Ninova, Maria ^a   Marinov, Georgi K ^a   Chung, Yun D ^b   Aravin, Alexei A ^a  

^a California Institute of Technology   (United States)

^b University of Seoul   (South Korea)

^c GEOPHYSICAL LABORATORY   (United States)

Author keywords

MRNA loading; PiRNA biogenesis; Thoc5; Transcriptional regulation; TREX

Indexed keywords

MULTIPROTEIN COMPLEX; PIWI INTERACTING RNA; RNA; THOC5 PROTEIN; UNCLASSIFIED DRUG; CUTOFF PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; NUCLEAR PROTEIN; RNA BINDING PROTEIN; RNA PRECURSOR; SMALL INTERFERING RNA; THOC5 PROTEIN, DROSOPHILA;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL MATURATION; DROSOPHILA; EMBRYO PATTERN FORMATION; FEMALE; FEMALE FERTILITY; GAMETOGENESIS; GENE EXPRESSION; GERM CELL; GERMLINE MUTATION; IN VITRO STUDY; INSECT GENETICS; MALE; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; RNA SPLICING; RNA TRANSCRIPTION; TRANSPOSON; ANIMAL; BIOSYNTHESIS; CELL NUCLEUS; DROSOPHILA MELANOGASTER; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORPHOGENESIS; MUTATION; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; BODY PATTERNING; CELL NUCLEUS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; FERTILITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MULTIPROTEIN COMPLEXES; MUTATION; NUCLEAR PROTEINS; PROTEIN TRANSPORT; RNA PRECURSORS; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 84962381499     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.276030.115     Document Type: Article

References (55)

1. Abruzzi KC, Lacadie S, Rosbash M. 2004. Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes. EMBO J 23: 2620–2631.
2. Aguilera A. 2005. Cotranscriptional mRNP assembly: from the DNA to the nuclear pore. Curr Opin Cell Biol 17: 242–250.
3. Alekseyenko AA, McElroy KA, Kang H, Zee BM, Kharchenko PV, Kuroda MI. 2015. BioTAP-XL: cross-linking/tandem affinity purification to study DNA targets, RNA, and protein components of chromatin-associated complexes. Curr Protoc Mol Biol 109: 21 30 21–21 30 32.
4. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11: R106.
5. Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. 2008. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785–799.
6. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089–1103.
7. Chavez S, Garcia-Rubio M, Prado F, Aguilera A. 2001. Hpr1 is preferentially required for transcription of either long or G+C-rich DNA sequences in Saccharomyces cerevisiae. Mol Cell Biol 21: 7054–7064.
8. Chen Y, Pane A, Schupbach T. 2007. Cutoff and aubergine mutations result in retrotransposon upregulation and checkpoint activation in Drosophila. Curr Biol 17: 637–642.
9. 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.
10. Chi B, Wang Q, Wu G, Tan M, Wang L, Shi M, Chang X, Cheng H. 2013. Aly and THO are required for assembly of the human TREX complex and association of TREX components with the spliced mRNA. Nucleic Acids Res 41: 1294–1306.
11. Chi B, Wang K, Du Y, Gui B, Chang X, Wang L, Fan J, Chen S, Wu X, Li G, et al. 2014. A Sub-Element in PRE enhances nuclear export of intronless mRNAs by recruiting the TREX complex via ZC3H18. Nucleic Acids Res 42: 7305–7318.
12. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, Perrimon N, Kellis M, Wohlschlegel JA, Sachidanandam R, et al. 2008. An endogenous small interfering RNA pathway in Drosophila. Nature 453: 798–802.
13. 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.
14. Dominguez-Sanchez MS, Barroso S, Gomez-Gonzalez B, Luna R, Aguilera A. 2011. Genome instability and transcription elongation impairment in human cells depleted of THO/TREX. PLoS Genet 7: e1002386.
15. Dreyfuss G, Kim VN, Kataoka N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3: 195–205.
16. Gatfield D, Izaurralde E. 2002. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J Cell Biol 159: 579–588.
17. Gatfield D, Le Hir H, Schmitt C, Braun IC, Kocher T, Wilm M, Izaurralde E. 2001. The DExH/D box protein HEL/UAP56 is essential for mRNA nuclear export in Drosophila. Curr Biol 11: 1716–1721.
18. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. 2007. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 315: 1587–1590.
19. Guria A, Tran DD, Ramachandran S, Koch A, El Bounkari O, Dutta P, Hauser H, Tamura T. 2011. Identification of mRNAs that are spliced but not exported to the cytoplasm in the absence of THOC5 in mouse embryo fibroblasts. RNA 17: 1048–1056.
20. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. 2005. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110: 462–467.
21. Katahira J. 2012. mRNA export and the TREX complex. Biochim Biophys Acta 1819: 507–513.
22. Katahira J, Inoue H, Hurt E, Yoneda Y. 2009. Adaptor Aly and coadaptor Thoc5 function in the Tap-p15-mediated nuclear export of HSP70 mRNA. EMBO J 28: 556–567.
23. Kent WJ, Zweig AS, Barber G, Hinrichs AS, Karolchik D. 2010. BigWig and BigBed: enabling browsing of large distributed datasets. Bioinformatics 26: 2204–2207.
24. Khodor YL, Rodriguez J, Abruzzi KC, Tang CH, Marr MT II, Rosbash M. 2011. Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila. Genes Dev 25: 2502–2512.
25. Kim H, Cho B, Moon S, Chung YD. 2011. The THO complex is required for stress tolerance and longevity in Drosophila. Genes Genomics 33: 291–297.
26. Klattenhoff C, Bratu DP, McGinnis-Schultz N, Koppetsch BS, Cook HA, Theurkauf WE. 2007. Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response. Dev Cell 12: 45–55.
27. Klattenhoff C, Xi H, Li C, Lee S, Xu J, Khurana JS, Zhang F, Schultz N, Koppetsch BS, Nowosielska A, et al. 2009. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138: 1137–1149.
28. Kopytova DV, Orlova AV, Krasnov AN, Gurskiy DY, Nikolenko JV, Nabirochkina EN, Shidlovskii YV, Georgieva SG. 2010. Multifunctional factor ENY2 is associated with the THO complex and promotes its recruitment onto nascent mRNA. Genes Dev 24: 86–96.
29. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
30. Lei EP, Krebber H, Silver PA. 2001. Messenger RNAsare recruited for nuclear export during transcription. Genes Dev 15: 1771–1782.
31. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, Hur JK, Aravin AA, Toth KF. 2013. Piwi induces piRNA- guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 27: 390–399.
32. Le Thomas A, Stuwe E, Li S, Du J, Marinov G, Rozhkov N, Chen YC, Luo Y, Sachidanandam R, Toth KF, et al. 2014. Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing. Genes Dev 28: 1667–1680.
33. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550.
34. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, Hannon GJ. 2009. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522–535.
35. Masuda S, Das R, Cheng H, Hurt E, Dorman N, Reed R. 2005. Recruitment of the human TREX complex to mRNA during splicing. Genes Dev 19: 1512–1517.
36. Mohn F, Sienski G, Handler D, Brennecke J. 2014. The Rhino–Deadlock–Cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 157: 1364–1379.
37. Moon S, Cho B, Min SH, Lee D, Chung YD. 2011. The THO complex is required for nucleolar integrity in Drosophila spermatocytes. Development 138: 3835–3845.
38. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628.
39. Nojima T, Hirose T, Kimura H, Hagiwara M. 2007. The interaction between cap-binding complex and RNA export factor is required for intronless mRNA export. J Biol Chem 282: 15645–15651.
40. Pane A, Jiang P, Zhao DY, Singh M, Schupbach T. 2011. The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline. EMBO J 30: 4601–4615.
41. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842.
42. Rehwinkel J, Herold A, Gari K, Kocher T, Rode M, Ciccarelli FL, Wilm M, Izaurralde E. 2004. Genome-wide analysis of mRNAs regulated by the THO complex in Drosophila melanogaster. Nat Struct Mol Biol 11: 558–566.
43. Rozhkov NV, Hammell M, Hannon GJ. 2013. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 27: 400–412.
44. Siomi MC, Sato K, Pezic D, Aravin AA. 2011. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246–258.
45. Strasser K, Hurt E. 2000. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J 19: 410–420.
46. Strasser K, Masuda S, Mason P, Pfannstiel J, Oppizzi M, Rodriguez- Navarro S, Rondon AG, Aguilera A, Struhl K, Reed R, et al. 2002. TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417: 304–308.
47. Stutz F, Bachi A, Doerks T, Braun IC, Seraphin B, Wilm M, Bork P, Izaurralde E. 2000. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 6: 638–650.
48. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320–324.
49. Viphakone N, Hautbergue GM, Walsh M, Chang CT, Holland A, Folco EG, Reed R, Wilson SA. 2012. TREX exposes the RNAbinding domain of Nxf1 to enable mRNA export. Nat Commun 3: 1006.
50. Voynov V, Verstrepen KJ, Jansen A, Runner VM, Buratowski S, Fink GR. 2006. Genes with internal repeats require the THO complex for transcription. Proc Natl Acad Sci 103: 14423–14428.
51. Yu B, Cassani M, Wang M, Liu M, Ma J, Li G, Zhang Z, Huang Y. 2015. Structural insights into Rhinomediated germline piRNA cluster formation. Cell Res 25: 525–528.
52. Zhang Z, Xu J, Koppetsch BS, Wang J, Tipping C, Ma S, Weng Z, Theurkauf WE, Zamore PD. 2011. Heterotypic piRNA Ping- Pong requires qin, a protein with both E3 ligase and Tudor domains. Mol Cell 44: 572–584.
53. Zhang F, Wang J, Xu J, Zhang Z, Koppetsch BS, Schultz N, Vreven T, Meignin C, Davis I, Zamore PD, et al. 2012. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 151: 871–884.
54. Zhang Z, Wang J, Schultz N, Zhang F, Parhad SS, Tu S, Vreven T, Zamore PD, Weng Z, Theurkauf WE. 2014. The HP1 homolog rhino anchors a nuclear complex that suppresses piRNA precursor splicing. Cell 157: 1353–1363.
55. Zhou Z, Luo MJ, Straesser K, Katahira J, Hurt E, Reed R. 2000. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature 407: 401–405.