The Rhino-Deadlock-Cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila

Cell

Volumn 157, Issue 6, 2014, Pages 1364-1379

  Mohn, Fabio ^a   Sienski, Grzegorz ^a   Handler, Dominik ^a   Brennecke, Julius ^a  

^a INSTITUTE OF MOLECULAR BIOTECHNOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; DOUBLE STRANDED RNA; HISTONE LYSINE METHYLTRANSFERASE; PIWI INTERACTING RNA; PIWI PROTEIN; PROTEIN; RHINO DEADLOCK CUTOFF COMPLEX PROTEIN; RNA POLYMERASE II; UNCLASSIFIED DRUG; CUTOFF PROTEIN; DEADLOCK PROTEIN; DUAL STRAND PIWI INTERACTING RNA; HEAT SHOCK PROTEIN 70; HETEROCHROMATIN PROTEIN 1; RHINO PROTEIN;

ARTICLE; CHROMATIN; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; FEEDBACK SYSTEM; GENE LOCUS; GENETIC ASSOCIATION; MOLECULAR BIOLOGY; NONHUMAN; OVARY; PRIORITY JOURNAL; RNA TRANSCRIPTION; TRANSCRIPTION TERMINATION; 3' UNTRANSLATED REGION; BIOGENESIS; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CHROMOSOME 3; CHROMOSOME 3R; CHROMOSOME 4; CONSTITUTIVE HETEROCHROMATIN; DNA FLANKING REGION; EUCHROMATIN; FLUORESCENCE IN SITU HYBRIDIZATION; GENOTYPE; NONCANONICAL TRANSCRIPTION; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; RNA METHYLATION; RNA SEQUENCE; WILD TYPE;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENOME-WIDE ASSOCIATION STUDY; MICROTUBULE-ASSOCIATED PROTEINS; OVARY; RNA POLYMERASE II; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; TRANSCRIPTION TERMINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84902108866     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.04.031     Document Type: Article

References (59)

1. P.R. Andersen, M. Domanski, M.S. Kristiansen, H. Storvall, E. Ntini, C. Verheggen, A. Schein, J. Bunkenborg, I. Poser, and M. Hallais et al. The human cap-binding complex is functionally connected to the nuclear RNA exosome Nat. Struct. Mol. Biol. 20 2013 1367 1376
2. B.J. Beliveau, E.F. Joyce, N. Apostolopoulos, F. Yilmaz, C.Y. Fonseka, R.B. McCole, Y. Chang, J.B. Li, T.N. Senaratne, and B.R. Williams et al. Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes Proc. Natl. Acad. Sci. USA 109 2012 21301 21306
3. J. Brennecke, A.A. Aravin, A. Stark, M. Dus, M. Kellis, R. Sachidanandam, and G.J. Hannon Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila Cell 128 2007 1089 1103
4. J. Brennecke, C.D. Malone, A.A. Aravin, R. Sachidanandam, A. Stark, and G.J. Hannon An epigenetic role for maternally inherited piRNAs in transposon silencing Science 322 2008 1387 1392
5. B. Czech, J.B. Preall, J. McGinn, and G.J. Hannon A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway Mol. Cell 50 2013 749 761
6. A. de Vanssay, A.L. Bougé, A. Boivin, C. Hermant, L. Teysset, V. Delmarre, C. Antoniewski, and S. Ronsseray Paramutation in Drosophila linked to emergence of a piRNA-producing locus Nature 490 2012 112 115
7. S.I. Grewal RNAi-dependent formation of heterochromatin and its diverse functions Curr. Opin. Genet. Dev. 20 2010 134 141
8. E. Izaurralde, J. Lewis, C. McGuigan, M. Jankowska, E. Darzynkiewicz, and I.W. Mattaj A nuclear cap binding protein complex involved in pre-mRNA splicing Cell 78 1994 657 668
9. X. Jiao, S. Xiang, C. Oh, C.E. Martin, L. Tong, and M. Kiledjian Identification of a quality-control mechanism for mRNA 5′-end capping Nature 467 2010 608 611
10. X. Jiao, J.H. Chang, T. Kilic, L. Tong, and M. Kiledjian A mammalian pre-mRNA 5′ end capping quality control mechanism and an unexpected link of capping to pre-mRNA processing Mol. Cell 50 2013 104 115
11. C. Keller, R. Adaixo, R. Stunnenberg, K.J. Woolcock, S. Hiller, and M. Bühler HP1(Swi6) mediates the recognition and destruction of heterochromatic RNA transcripts Mol. Cell 47 2012 215 227
12. M. Kim, N.J. Krogan, L. Vasiljeva, O.J. Rando, E. Nedea, J.F. Greenblatt, and S. Buratowski The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II Nature 432 2004 517 522
13. C. Klattenhoff, H. Xi, C. Li, S. Lee, J. Xu, J.S. Khurana, F. Zhang, N. Schultz, B.S. Koppetsch, and A. Nowosielska et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters Cell 138 2009 1137 1149
14. N.C. Lau, N. Robine, R. Martin, W.J. Chung, Y. Niki, E. Berezikov, and E.C. Lai Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line Genome Res. 19 2009 1776 1785
15. A. Le Thomas, A.K. Rogers, A. Webster, G.K. Marinov, S.E. Liao, E.M. Perkins, J.K. Hur, A.A. Aravin, and K.F. Tóth Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state Genes Dev. 27 2013 390 399
16. X.Z. Li, C.K. Roy, X. Dong, E. Bolcun-Filas, J. Wang, B.W. Han, J. Xu, M.J. Moore, J.C. Schimenti, Z. Weng, and P.D. Zamore An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes Mol. Cell 50 2013 67 81
17. C.D. Malone, and G.J. Hannon Small RNAs as guardians of the genome Cell 136 2009 656 668
18. C.D. Malone, J. Brennecke, M. Dus, A. Stark, W.R. McCombie, R. Sachidanandam, and G.J. Hannon Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary Cell 137 2009 522 535
19. H.B. Megosh, D.N. Cox, C. Campbell, and H. Lin The role of PIWI and the miRNA machinery in Drosophila germline determination Curr. Biol. 16 2006 1884 1894
20. D. Moazed Small RNAs in transcriptional gene silencing and genome defence Nature 457 2009 413 420
21. F. Muerdter, I. Olovnikov, A. Molaro, N.V. Rozhkov, B. Czech, A. Gordon, G.J. Hannon, and A.A. Aravin Production of artificial piRNAs in flies and mice RNA 18 2012 42 52
22. A. Pane, P. Jiang, D.Y. Zhao, M. Singh, and T. Schüpbach The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline EMBO J. 30 2011 4601 4615
23. A. Raj, P. van den Bogaard, S.A. Rifkin, A. van Oudenaarden, and S. Tyagi Imaging individual mRNA molecules using multiple singly labeled probes Nat. Methods 5 2008 877 879
24. P. Rangan, C.D. Malone, C. Navarro, S.P. Newbold, P.S. Hayes, R. Sachidanandam, G.J. Hannon, and R. Lehmann piRNA production requires heterochromatin formation in Drosophila Curr. Biol. 21 2011 1373 1379
25. P. Richard, and J.L. Manley Transcription termination by nuclear RNA polymerases Genes Dev. 23 2009 1247 1269
26. N. Robine, N.C. Lau, S. Balla, Z. Jin, K. Okamura, S. Kuramochi-Miyagawa, M.D. Blower, and E.C. Lai A broadly conserved pathway generates 3'UTR-directed primary piRNAs Curr. Biol. 19 2009 2066 2076
27. N.V. Rozhkov, M. Hammell, and G.J. Hannon Multiple roles for Piwi in silencing Drosophila transposons Genes Dev. 27 2013 400 412
28. K.A. Senti, and J. Brennecke The piRNA pathway: a fly's perspective on the guardian of the genome Trends Genet. 26 2010 499 509
29. S. Shpiz, S. Ryazansky, I. Olovnikov, Y. Abramov, and A. Kalmykova Euchromatic transposon insertions trigger production of novel Pi- and endo-siRNAs at the target sites in the Drosophila germline PLoS Genet. 10 2014 e1004138
30. G. Sienski, D. Dönertas, and J. Brennecke Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression Cell 151 2012 964 980
31. M.C. Siomi, K. Sato, D. Pezic, and A.A. Aravin PIWI-interacting small RNAs: the vanguard of genome defence Nat. Rev. Mol. Cell Biol. 12 2011 246 258
32. R.K. Slotkin, and R. Martienssen Transposable elements and the epigenetic regulation of the genome Nat. Rev. Genet. 8 2007 272 285
33. J.F. Smothers, and S. Henikoff The HP1 chromo shadow domain binds a consensus peptide pentamer Curr. Biol. 10 2000 27 30
34. D. Vermaak, and H.S. Malik Multiple roles for heterochromatin protein 1 genes in Drosophila Annu. Rev. Genet. 43 2009 467 492
35. D. Vermaak, S. Henikoff, and H.S. Malik Positive selection drives the evolution of rhino, a member of the heterochromatin protein 1 family in Drosophila PLoS Genet. 1 2005 96 108
36. S.H. Wang, and S.C. Elgin Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line Proc. Natl. Acad. Sci. USA 108 2011 21164 21169
37. K. Wehr, A. Swan, and T. Schüpbach Deadlock, a novel protein of Drosophila, is required for germline maintenance, fusome morphogenesis and axial patterning in oogenesis and associates with centrosomes in the early embryo Dev. Biol. 294 2006 406 417
38. F. Zhang, J. Wang, J. Xu, Z. Zhang, B.S. Koppetsch, N. Schultz, T. Vreven, C. Meignin, I. Davis, and P.D. Zamore et al. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery Cell 151 2012 871 884
39. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, and J. Gentry et al. Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
40. A.C. Groth, M. Fish, R. Nusse, and M.P. Calos Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31 Genetics 166 2004 1775 1782
41. W. Gu, H.-C. Lee, D. Chaves, E.M. Youngman, G.J. Pazour, D. Conte Jr., and C.C. Mello CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors Cell 151 2012 1488 1500
42. D. Handler, K. Meixner, M. Pizka, K. Lauss, C. Schmied, F.S. Gruber, and J. Brennecke The genetic makeup of the Drosophila piRNA pathway Mol. Cell 50 2013 762 777
43. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
44. A.D. Jayaprakash, O. Jabado, B.D. Brown, and R. Sachidanandam Identification and remediation of biases in the activity of RNA ligases in small-RNA deep sequencing Nucleic Acids Res. 39 2011 e141-e141
45. J. Jurka, V.V. Kapitonov, A. Pavlicek, P. Klonowski, O. Kohany, and J. Walichiewicz Repbase Update, a database of eukaryotic repetitive elements Cytogenet. Genome Res. 110 2005 462 467
46. T.M. Keane, K. Wong, and D.J. Adams RetroSeq: transposable element discovery from next-generation sequencing data Bioinformatics 29 2013 389 390
47. W.J. Kent, C.W. Sugnet, T.S. Furey, K.M. Roskin, T.H. Pringle, A.M. Zahler, and D. Haussler The human genome browser at UCSC Genome Res. 12 2002 996 1006
48. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol. 10 2009 R25
49. E. Larschan, E.P. Bishop, P.V. Kharchenko, L.J. Core, J.T. Lis, P.J. Park, and M.I. Kuroda X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila Nature 471 2011 115 118
50. J.A. Law, J. Du, C.J. Hale, S. Feng, K. Krajewski, A.M.S. Palanca, B.D. Strahl, D.J. Patel, and S.E. Jacobsen Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1 Nature 498 2013 385 389
51. T.I. Lee, S.E. Johnstone, and R.A. Young Chromatin immunoprecipitation and microarray-based analysis of protein location Nat. Protoc. 1 2006 729 748
52. J. Miller, and I. Stagljar Using the yeast two-hybrid system to identify interacting proteins Methods Mol. Biol. 261 2004 247 262
53. S. Nechaev, D.C. Fargo, G. dos Santos, L. Liu, Y. Gao, and K. Adelman Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila Science 327 2010 335 338
54. J.-Q. Ni, R. Zhou, B. Czech, L.-P. Liu, L. Holderbaum, D. Yang-Zhou, H.-S. Shim, R. Tao, D. Handler, and P. Karpowicz et al. A genome-scale shRNA resource for transgenic RNAi in Drosophila Nat. Methods 8 2011 405 407
55. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
56. B.J. Raney, T.R. Dreszer, G.P. Barber, H. Clawson, P.A. Fujita, T. Wang, N. Nguyen, B. Paten, A.S. Zweig, and D. Karolchik et al. Track data hubs enable visualization of user-defined genome-wide annotations on the UCSC Genome Browser Bioinformatics 30 2014 1003 1005
57. E. Sarot, G. Payen-Groschêne, A. Bucheton, and A. Pélisson Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene Genetics 166 2004 1313 1321
58. S. Shpiz, and A. Kalmykova Analyses of piRNA-mediated transcriptional transposon silencing in Drosophila: nuclear run-on assay on ovaries Methods Mol. Biol. 1093 2014 149 159
59. Z. Zhang, W.E. Theurkauf, Z. Weng, and P.D. Zamore Strand-specific libraries for high throughput RNA sequencing (RNA-Seq) prepared without poly(A) selection Silence 3 2012 9