Export of piRNA precursors by EJC triggers assembly of cytoplasmic Yb-body in Drosophila

Nature Communications

Volumn 7, Issue , 2016, Pages

  Dennis, Cynthia ^a   Brasset, Emilie ^a   Sarkar, Arpita ^a   Vaury, Chantal ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; FLAM PRECURSOR; NUCLEAR PROTEIN; NXF1 EXPORTIN; NXT1 EXPORTIN; PIWI INTERACTING RNA; RNA PRECURSOR; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MESSENGER RNA; SMALL INTERFERING RNA;

CYTOPLASM; FLY; GENE; MOLECULAR ANALYSIS; RNA;

ARTICLE; CYTOPLASM; DROSOPHILA; EXON; EXON JUNCTION COMPLEX; NONHUMAN; PROTEIN TRANSPORT; RNA PROCESSING; SOMATIC CELL; TRANSPOSON; YB BODY; ANIMAL; CELL NUCLEUS; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; OVARY FOLLICLE; RNA TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CYTOPLASM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXONS; FEMALE; OVARIAN FOLLICLE; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA TRANSPORT; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 85005959339     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13739     Document Type: Article

References (47)

1. Brennecke, J. et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128, 1089-1103 (2007).
2. Malone, C. D. et al. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137, 522-535 (2009).
3. Theron, E., Dennis, C., Brasset, E. & Vaury, C. Distinct features of the piRNA pathway in somatic and germ cells: from piRNA cluster transcription to piRNA processing and amplification. Mob. DNA 5, 28 (2014).
4. Goriaux, C., Theron, E., Brasset, E. & Vaury, C. History of the discovery of a master locus producing piRNAs: the flamenco/COM locus in Drosophila melanogaster. Front. Genet. 5, 257 (2014).
5. Goriaux, C., Desset, S., Renaud, Y., Vaury, C. & Brasset, E. Transcriptional properties and splicing of the flamenco piRNA cluster. EMBO Rep. 15, 411-418 (2014).
6. Sienski, G., Donertas, D. & Brennecke, J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151, 964-980 (2012).
7. Olivieri, D., Sykora, M. M., Sachidanandam, R., Mechtler, K. & Brennecke, J. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J. 29, 3301-3317 (2010).
8. Saito, K. et al. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 24, 2493-2498 (2010).
9. Ipsaro, J. J., Haase, A. D., Knott, S. R., Joshua-Tor, L. & Hannon, G. J. The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis. Nature 491, 279-283 (2012).
10. Mohn, F., Handler, D. & Brennecke, J. Noncoding RNA. piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science 348, 812-817 (2015).
11. Le Thomas, A. et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 27, 390-399 (2013).
12. Pezic, D., Manakov, S. A., Sachidanandam, R. & Aravin, A. A. piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev. 28, 1410-1428 (2014).
13. Shpiz, S. et al. Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res. 39, 8703-8711 (2011).
14. Wang, S. H. & Elgin, S. C. Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc. Natl Acad. Sci. USA 108, 21164-21169 (2011).
15. Senti, K. A., Jurczak, D., Sachidanandam, R. & Brennecke, J. piRNA-guided slicing of transposon transcripts enforces their transcriptional silencing via specifying the nuclear piRNA repertoire. Genes Dev. 29, 1747-1762 (2015).
16. Klenov, M. S. et al. Separation of stem cell maintenance and transposon silencing functions of Piwi protein. Proc. Natl Acad. Sci. USA 108, 18760-18765 (2011).
17. Dennis, C. et al. 'Dot COM', a nuclear transit center for the primary piRNA pathway in Drosophila. PLoS ONE 8, e72752 (2013).
18. Murota, Y. et al. Yb integrates piRNA intermediates and processing factors into perinuclear bodies to enhance piRISC assembly. Cell Rep. 8, 103-113 (2014).
19. Homolka, D. et al. PIWI slicing and RNA elements in precursors instruct directional primary piRNA biogenesis. Cell Rep. 12, 418-428 (2015).
20. Ishizu, H. et al. Somatic primary piRNA biogenesis driven by cis-acting RNA elements and trans-acting Yb. Cell Rep. 12, 429-440 (2015).
21. Czech, B., Preall, J. B., McGinn, J. & Hannon, G. J. A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol. Cell 50, 749-761 (2013).
22. Handler, D. et al. The genetic makeup of the Drosophila piRNA pathway. Mol. Cell 50, 762-777 (2013).
23. Muerdter, F. et al. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol. Cell 50, 736-748 (2013).
24. Izaurralde, E. A novel family of nuclear transport receptors mediates the export of messenger RNA to the cytoplasm. Eur. J. Cell Biol. 81, 577-584 (2002).
25. Izaurralde, E. Nuclear export of messenger RNA. Results Probl. Cell Differ. 35, 133-150 (2002).
26. Tan, W., Zolotukhin, A. S., Bear, J., Patenaude, D. J. & Felber, B. K. The mRNA export in Caenorhabditis elegans is mediated by Ce-NXF-1, an ortholog of human TAP/NXF and Saccharomyces cerevisiae Mex67p. RNA 6, 1762-1772 (2000).
27. Wilkie, G. S. et al. Small bristles, the Drosophila ortholog of NXF-1, is essential for mRNA export throughout development. RNA 7, 1781-1792 (2001).
28. Levesque, L. et al. RNA export mediated by tap involves NXT1-dependent interactions with the nuclear pore complex. J. Biol. Chem. 276, 44953-44962 (2001).
29. Wiegand, H. L. et al. Formation of Tap/NXT1 heterodimers activates Tapdependent nuclear mRNA export by enhancing recruitment to nuclear pore complexes. Mol. Cell Biol. 22, 245-256 (2002).
30. 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. 20, 4987-4997 (2001).
31. Dostie, J. & Dreyfuss, G. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr. Biol. 12, 1060-1067 (2002).
32. Grant, R. P., Hurt, E., Neuhaus, D. & Stewart, M. Structure of the C-terminal FG-nucleoporin binding domain of Tap/NXF1. Nat. Struct. Biol. 9, 247-251 (2002).
33. Reed, R. & Hurt, E. A conserved mRNA export machinery coupled to premRNA splicing. Cell 108, 523-531 (2002).
34. Tange, T. O., Nott, A. & Moore, M. J. The ever-increasing complexities of the exon junction complex. Curr. Opin. Cell Biol. 16, 279-284 (2004).
35. Handler, D. et al. A systematic analysis of Drosophila TUDOR domaincontaining proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J. 30, 3977-3993 (2011).
36. Malone, C. D. et al. The exon junction complex controls transposable element activity by ensuring faithful splicing of the piwi transcript. Genes Dev. 28, 1786-1799 (2014).
37. Hayashi, R., Handler, D., Ish-Horowicz, D. & Brennecke, J. The exon junction complex is required for definition and excision of neighboring introns in Drosophila. Genes Dev. 28, 1772-1785 (2014).
38. Zhang, F. et al. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 151, 871-884 (2012).
39. Zhang, Z. et al. The HP1 homolog rhino anchors a nuclear complex that suppresses piRNA precursor splicing. Cell 157, 1353-1363 (2014).
40. Mevel-Ninio, M., Pelisson, A., Kinder, J., Campos, A. R. & Bucheton, A. The flamenco locus controls the gypsy and ZAM retroviruses and is required for Drosophila oogenesis. Genetics 175, 1615-1624 (2007).
41. Gatfield, D. & Izaurralde, E. REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. J. Cell Biol. 159, 579-588 (2002).
42. Jackson, B. R. et al. An interaction between KSHV ORF57 and UIF provides mRNA-adaptor redundancy in herpesvirus intronless mRNA export. PLoS Pathog. 7, e1002138 (2011).
43. Levesque, L. et al. Mutations in tap uncouple RNA export activity from translocation through the nuclear pore complex. Mol. Biol. Cell 17, 931-943 (2006).
44. Schwerk, C. et al. ASAP, a novel protein complex involved in RNA processing and apoptosis. Mol. Cell Biol. 23, 2981-2990 (2003).
45. Shen, H. UAP56- a key player with surprisingly diverse roles in pre-mRNA splicing and nuclear export. BMB Rep. 42, 185-188 (2009).
46. Klattenhoff, C. et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138, 1137-1149 (2009).
47. Mohn, F., Sienski, G., Handler, D. & Brennecke, J. The rhino-deadlock-cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 157, 1364-1379 (2014).