Yb integrates piRNA intermediates and processing factors into perinuclear bodies to enhance piRISC assembly

Cell Reports

Volumn 8, Issue 1, 2014, Pages 103-113

  Murota, Yukiko ^a,b   Ishizu, Hirotsugu ^c   Nakagawa, Shinichi ^d   Iwasaki, Yuka W ^b   Shibata, Shinsuke ^b   Kamatani, Miharu K ^b   Saito, Kuniaki ^b   Okano, Hideyuki ^b   Siomi, Haruhiko ^b   Siomi, Mikiko C ^c  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARMITAGE; CELL PROTEIN; PIWI INTERACTING RNA; RNA HELICASE; UNCLASSIFIED DRUG; YB PROTEIN; ARGONAUTE PROTEIN; ARMI PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; FEMALE STERILE (1) YB PROTEIN, DROSOPHILA; PIWI PROTEIN, DROSOPHILA; PROTEIN BINDING; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; DNA; PIWI PROTEIN; RNA;

5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BIOGENESIS; CELL NUCLEUS INCLUSION BODY; CYTOPLASM; ELECTRON MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE LOCUS; GENE SILENCING; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PERINUCLEAR BODY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RNA BINDING; RNA INTERFERENCE; SOMATIC CELL; ANIMAL; CELL CULTURE; CYTOLOGY; DROSOPHILA; FEMALE; GENETICS; METABOLISM; CELL ORGANELLE; CONTROLLED STUDY; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; NORTHERN BLOTTING; PLASMID; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; SCREENING; WESTERN BLOTTING; YB BODY;

ANIMALS; ARGONAUTE PROTEINS; CELLS, CULTURED; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; OVARY; PROTEIN BINDING; RNA HELICASES; RNA, SMALL INTERFERING; RNA-INDUCED SILENCING COMPLEX;

EID: 84904034861     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.05.043     Document Type: Article

References (37)

1. Aravin A.A., Hannon G.J., Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007, 318:761-764.
2. Banroques J., Doère M., Dreyfus M., Linder P., Tanner N.K. Motif III in superfamily 2 "helicases" helps convert the binding energy of ATP into a high-affinity RNA binding site in the yeast DEAD-box protein Ded1. J.Mol. Biol. 2010, 396:949-966.
3. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
4. Cherbas L., Willingham A., Zhang D., Yang L., Zou Y., Eads B.D., Carlson J.W., Landolin J.M., Kapranov P., Dumais J., et al. The transcriptional diversity of 25 Drosophila cell lines. Genome Res. 2011, 21:301-314.
5. Choi S.Y., Huang P., Jenkins G.M., Chan D.C., Schiller J., Frohman M.A. A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat. Cell Biol. 2006, 8:1255-1262.
6. Cook H.A., Koppetsch B.S., Wu J., Theurkauf W.E. The Drosophila SDE3 homolog armitage is required for oskar mRNA silencing and embryonic axis specification. Cell 2004, 116:817-829.
7. Dennis C., Zanni V., Brasset E., Eymery A., Zhang L., Mteirek R., Jensen S., Rong Y.S., Vaury C. "Dot COM", a nuclear transit center for the primary piRNA pathway in Drosophila. PLoS ONE 2013, 8:e72752.
8. Dönertas D., Sienski G., Brennecke J. Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev. 2013, 27:1693-1705.
9. Goriaux C., Desset S., Renaud Y., Vaury C., Brasset E. Transcriptional properties and splicing of the flamenco piRNA cluster. EMBO Rep. 2014, 15:411-418.
10. Gunawardane L.S., Saito K., Nishida K.M., Miyoshi K., Kawamura Y., Nagami T., Siomi H., Siomi M.C. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 2007, 315:1587-1590.
11. Haase A.D., Fenoglio S., Muerdter F., Guzzardo P.M., Czech B., Pappin D.J., Chen C., Gordon A., Hannon G.J. Probing the initiation and effector phases of the somatic piRNA pathway in Drosophila. Genes Dev. 2010, 24:2499-2504.
12. Handler D., Olivieri D., Novatchkova M., Gruber F.S., Meixner K., Mechtler K., Stark A., Sachidanandam R., Brennecke J. A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J. 2011, 30:3977-3993.
13. 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 2012, 491:279-283.
14. Ishizu H., Siomi H., Siomi M.C. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012, 26:2361-2373.
15. Jaskiewicz L., Bilen B., Hausser J., Zavolan M. ArgonauteCLIP-a method to identify invivo targets of miRNAs. Methods 2012, 58:106-112.
16. Juliano C., Wang J., Lin H. Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annu. Rev. Genet. 2011, 45:447-469.
17. Khurana J.S., Theurkauf W. piRNAs, transposon silencing, and Drosophila germline development. J.Cell Biol. 2010, 191:905-913.
18. Malone C.D., Brennecke J., Dus M., Stark A., McCombie W.R., Sachidanandam R., Hannon G.J. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 2009, 137:522-535.
19. Masumoto H., Sugimoto K., Okazaki T. Alphoid satellite DNAistightly associated with centromere antigens in human chromosomes throughout the cell cycle. Exp. Cell Res. 1989, 181:181-196.
20. Mével-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 2007, 175:1615-1624.
21. Miyoshi K., Tsukumo H., Nagami T., Siomi H., Siomi M.C. Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev. 2005, 19:2837-2848.
22. Muerdter F., Guzzardo P.M., Gillis J., Luo Y., Yu Y., Chen C., Fekete R., Hannon G.J. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol. Cell 2013, 50:736-748.
23. Nishimasu H., Ishizu H., Saito K., Fukuhara S., Kamatani M.K., Bonnefond L., Matsumoto N., Nishizawa T., Nakanaga K., Aoki J., et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 2012, 491:284-287.
24. Ohtani H., Iwasaki Y.W., Shibuya A., Siomi H., Siomi M.C., Saito K. DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev. 2013, 27:1656-1661.
25. Olivieri D., Sykora M.M., Sachidanandam R., Mechtler K., Brennecke J. An invivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J. 2010, 29:3301-3317.
26. Olivieri D., Senti K.A., Subramanian S., Sachidanandam R., Brennecke J. The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila. Mol. Cell 2012, 47:954-969.
27. Pillai R.S., Chuma S. piRNAs and their involvement in male germline development in mice. Dev. Growth Differ. 2012, 54:78-92.
28. Qi H., Watanabe T., Ku H.Y., Liu N., Zhong M., Lin H. The Yb body, a major site for Piwi-associated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. J.Biol. Chem. 2011, 286:3789-3797.
29. Robine N., Lau N.C., Balla S., Jin Z., Okamura K., Kuramochi-Miyagawa S., Blower M.D., Lai E.C. A broadly conserved pathway generates 3'UTR-directed primary piRNAs. Curr. Biol. 2009, 19:2066-2076.
30. Saito K., Inagaki S., Mituyama T., Kawamura Y., Ono Y., Sakota E., Kotani H., Asai K., Siomi H., Siomi M.C. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009, 461:1296-1299.
31. Saito K., Ishizu H., Komai M., Kotani H., Kawamura Y., Nishida K.M., Siomi H., Siomi M.C. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 2010, 24:2493-2498.
32. Sengoku T., Nureki O., Nakamura A., Kobayashi S., Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 2006, 125:287-300.
33. Sienski G., Dönertas D., Brennecke J. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 2012, 151:964-980.
34. Siomi M.C., Sato K., Pezic D., Aravin A.A. PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 2011, 12:246-258.
35. Sone M., Hayashi T., Tarui H., Agata K., Takeichi M., Nakagawa S. The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J.Cell Sci. 2007, 120:2498-2506.
36. Szakmary A., Reedy M., Qi H., Lin H. The Yb protein defines anovel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. J.Cell Biol. 2009, 185:613-627.
37. Zamparini A.L., Davis M.Y., Malone C.D., Vieira E., Zavadil J., Sachidanandam R., Hannon G.J., Lehmann R. Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila. Development 2011, 138:4039-4050.