piRNA-guided slicing of transposon transcripts enforces their transcriptional silencing via specifying the nuclear piRNA repertoire

Genes and Development

Volumn 29, Issue 16, 2015, Pages 1747-1762

  Senti, Kirsten André ^a   Jurczak, Daniel ^a   Sachidanandam, Ravi ^b   Brennecke, Julius ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila oogenesis; piRNA biogenesis; Piwi pathway; Transposon silencing

Indexed keywords

AGO3 PROTEIN; AUBERGINE PROTEIN; PIWI INTERACTING RNA; PROTEIN; UNCLASSIFIED DRUG; AGO3 PROTEIN, DROSOPHILA; ARGONAUTE PROTEIN; AUBERGINE PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; INITIATION FACTOR; SMALL INTERFERING RNA; TRANSPOSON;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOGENESIS; CONTROLLED STUDY; CYTOPLASM; FEMALE; GENE SILENCING; GERM CELL; GERMLINE CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OOCYTE DEVELOPMENT; OVARY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; RNA ANALYSIS; RNA CLEAVAGE; RNA INTERFERENCE; RNA PROCESSING; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TRANSPOSON; ANIMAL; BIOSYNTHESIS; CELL NUCLEUS; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ANIMALIA; CUCURBITA PEPO VAR. MELOPEPO;

ANIMALS; ARGONAUTE PROTEINS; CELL NUCLEUS; CYTOPLASM; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; GERM CELLS; OVARY; PEPTIDE INITIATION FACTORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL INTERFERING;

EID: 84940099987     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.267252.115     Document Type: Article

References (53)

1. Adelman K, Marr MT, Werner J, Saunders A, Ni Z, Andrulis ED, Lis JT. 2005. Efficient release from promoter-proximal stall sites requires transcript cleavage factor TFIIS. Mol Cell 17: 103-112.
2. Allen E, Xie Z, Gustafson AM, Carrington JC. 2005. microRNAdirected phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221.
3. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. 2007. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744-747.
4. 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.
5. Bagijn MP, Goldstein LD, Sapetschnig A, Weick EM, Bouasker S, Lehrbach NJ, Simard MJ, Miska EA. 2012. Function, targets, and evolution of Caenorhabditis elegans piRNAs. Science 337: 574-578.
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. Brennecke J, Malone CD, Aravin AA, SachidanandamR, Stark A, Hannon GJ. 2008. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322: 1387-1392.
8. Cox DN, Chao A, Lin H. 2000. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127: 503-514.
9. Creasey KM, Zhai J, Borges F, Van Ex F, Regulski M, Meyers BC, Martienssen RA. 2014. miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508: 411-415.
10. Gokcezade J, Sienski G, Duchek P. 2014. Efficient CRISPR/Cas9 plasmids for rapid and versatile genome editing in Drosophila. G3 4: 2279-2282.
11. GuW, Lee HC, Chaves D, Youngman EM, Pazour GJ, Conte D Jr, Mello CC. 2012. CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors. Cell 151: 1488-1500.
12. 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.
13. Haase AD, Fenoglio S, Muerdter F, Guzzardo PM, Czech B, Pappin DJ, Chen C, Gordon A, Hannon GJ. 2010. Probing the initiation and effector phases of the somatic piRNA pathway in Drosophila. Genes Dev 24: 2499-2504.
14. Han BW, Wang W, Li C, Weng Z, Zamore PD. 2015. Noncoding RNA. piRNA-guided transposon cleavage initiates Zucchinidependent, phased piRNA production. Science 348: 817-821.
15. Ipsaro JJ, Haase AD, Knott SR, Joshua-Tor L, Hannon GJ. 2012. The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis. Nature 491: 279-283.
16. Iwasaki YW, Siomi MC, Siomi H. 2015. PIWI-interacting RNA: its biogenesis and functions. Annu Rev Biochem 84: 405-433.
17. Jin Z, Flynt AS, Lai EC. 2013. Drosophila piwi mutants exhibit germline stem cell tumors that are sustained by elevated Dpp signaling. Curr Biol 23: 1442-1448.
18. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821.
19. Kadener S, Rodriguez J, Abruzzi KC, Khodor YL, Sugino K, Marr MT II, Nelson S, Rosbash M. 2009. Genome-wide identification of targets of the drosha-pasha/DGCR8 complex. RNA 15: 537-545.
20. Katsani KR, Karess RE, Dostatni N, Doye V. 2008. In vivo dynamics of Drosophila nuclear envelope components. Mol Biol Cell 19: 3652-3666.
21. Kazazian HH Jr. 2004. Mobile elements: drivers of genome evolution. Science 303: 1626-1632.
22. 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.
23. Lau NC, Robine N, Martin R, Chung WJ, Niki Y, Berezikov E, Lai EC. 2009. Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res 19: 1776-1785.
24. Lee TI, Johnstone SE, Young RA. 2006. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1: 729-748.
25. Lee HC, Gu W, Shirayama M, Youngman E, Conte D Jr, Mello CC. 2012. C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts. Cell 150: 78-87.
26. 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.
27. Li C, Vagin VV, Lee S, Xu J, MaS, Xi H, Seitz H, Horwich MD, Syrzycka M, Honda BM, et al. 2009. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137: 509-521.
28. Malone CD, Hannon GJ. 2009. Small RNAs as guardians of the genome. Cell 136: 656-668.
29. 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.
30. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N. 2008. Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 40: 476-483.
31. 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.
32. Mohn F, Handler D, Brennecke J. 2015. Noncoding RNA. piRNAguided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science 348: 812-817.
33. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, Yang-Zhou D, Shim HS, Tao R, Handler D, Karpowicz P, et al. 2011. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405-407.
34. Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, Bonnefond L, Matsumoto N, Nishizawa T, Nakanaga K, Aoki J, et al. 2012. Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491: 284-287.
35. 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.
36. Olivieri D, Senti KA, Subramanian S, Sachidanandam R, Brennecke J. 2012. The cochaperone shutdown defines a group of biogenesis factors essential for all piRNA populations in Drosophila. Mol Cell 47: 954-969.
37. Pane A, Wehr K, Schupbach T. 2007. zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev Cell 12: 851-862.
38. Pezic D, Manakov SA, Sachidanandam R, Aravin AA. 2014. piRNApathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev 28: 1410-1428.
39. Post C, Clark JP, Sytnikova YA, Chirn GW, Lau NC. 2014. The capacity of target silencing by Drosophila PIWI and piRNAs. RNA 20: 1977-1986.
40. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C, Antony C, SachidanandamR, Pillai RS. 2011. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480: 264-267.
41. Robine N, Lau NC, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, Blower MD, Lai EC. 2009. A broadly conserved pathway generates 3′UTR-directed primary piRNAs. Curr Biol 19: 2066-2076.
42. Rozhkov NV, Hammell M, Hannon GJ. 2013. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 27: 400-412.
43. 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.
44. 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.
45. Senti KA, Brennecke J. 2010. The piRNA pathway: a fly's perspective on the guardian of the genome. Trends Genet 26: 499-509.
46. Shpiz S, Olovnikov I, Sergeeva A, Lavrov S, Abramov Y, Savitsky M, Kalmykova A. 2011. Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res 39: 8703-8711.
47. Shpiz S, Ryazansky S, Olovnikov I, Abramov Y, Kalmykova A. 2014. Euchromatic transposon insertions trigger production of novel Pi-and endo-siRNAs at the target sites in the Drosophila germline. PLoS Genet 10: e1004138.
48. 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.
49. Slotkin RK, Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272-285.
50. 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.
51. Wang SH, Elgin SC. 2011. Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc Natl Acad Sci 108: 21164-21169.
52. Wang W, Yoshikawa M, Han BW, Izumi N, Tomari Y, Weng Z, Zamore PD. 2014. The initial uridine of primary piRNAs does not create the tenth adenine that is the hallmark of secondary piRNAs. Mol Cell 56: 708-716.
53. 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.