MicroRNA-Dependent Transcriptional Silencing of Transposable Elements in Drosophila Follicle Cells

PLoS Genetics

Volumn 11, Issue 5, 2015, Pages

  Mugat, Bruno ^a   Akkouche, Abdou ^a   Serrano, Vincent ^a   Armenise, Claudia ^a,c   Li, Blaise ^a   Brun, Christine ^a   Fulga, Tudor A ^b,d   Van Vactor, David ^b   Pélisson, Alain ^a   Chambeyron, Séverine ^a  

^a CNRS   (France)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Quartz Bio   (Switzerland)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; MICRORNA; MICRORNA 14; MICRORNA 34; PIWI INTERACTING RNA; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MIRN14 MICRORNA, DROSOPHILA; MIRN34 MICRORNA, DROSOPHILA; SMALL INTERFERING RNA; TRANSPOSON;

3' UNTRANSLATED REGION; ADULT; AGO1 GENE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; DROSOPHILA; GAWKY GENE; GENE; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GENETIC STABILITY; LOSS OF FUNCTION MUTATION; NONHUMAN; OVARY FOLLICLE CELL; PHENOTYPE; TRANSCRIPTION REGULATION; TRANSPOSON; ANIMAL; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OVARY FOLLICLE; RNA INTERFERENCE;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; MICRORNAS; OVARIAN FOLLICLE; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84930814149     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005194     Document Type: Article

References (72)

1. Ghildiyal M, Zamore PD, Small silencing RNAs: an expanding universe. Nat Rev Genet. 2009;10: 94–108. doi: 10.1038/nrg2504 19148191
2. Czech B, Hannon GJ, Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet. 2011;12: 19–31. doi: 10.1038/nrg2916 21116305
3. Ketting RF, The many faces of RNAi. Dev Cell. 2011;20: 148–61. doi: 10.1016/j.devcel.2011.01.012 21316584
4. Rissland OS, Lai EC, RNA silencing in Monterey. Development. 2011;138: 3093–102. doi: 10.1242/dev.065284 21750025
5. Ambros V, Lee RC, Lavanway A, Williams PT, Jewell D, MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr Biol. 2003;13: 807–18. 12747828
6. Chawla G, Sokol NS, Kwang W, Jeon Chapter one—MicroRNAs in Drosophila Development. In: International Review of Cell and Molecular Biology. Academic Press; 2011. pp. 1–65. Available: http://www.sciencedirect.com/science/article/pii/B978012385859700001X doi: 10.1016/B978-0-12-386033-0.00001-3 22078958
7. Ding SW, Lu R, Virus-derived siRNAs and piRNAs in immunity and pathogenesis. Curr Opin Virol. 2011;1: 533–544. doi: 10.1016/j.coviro.2011.10.028 22180767
8. Guzzardo PM, Muerdter F, Hannon GJ, The piRNA pathway in flies: highlights and future directions. Curr Opin Genet Dev. 2013;23: 44–52. doi: 10.1016/j.gde.2012.12.003 23317515
9. Malone CD, Hannon GJ, Small RNAs as guardians of the genome. Cell. 2009;136: 656–68. doi: 10.1016/j.cell.2009.01.045 19239887
10. Obbard DJ, Gordon KH, Buck AH, Jiggins FM, The evolution of RNAi as a defence against viruses and transposable elements. Philos Trans R Soc Lond B Biol Sci. 2009;364: 99–115. doi: 10.1098/rstb.2008.0168 18926973
11. Siomi MC, Sato K, Pezic D, Aravin AA, PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol. 2011;12: 246–58. doi: 10.1038/nrm3089 21427766
12. Kim K, Lee YS, Carthew RW, Conversion of pre-RISC to holo-RISC by Ago2 during assembly of RNAi complexes. RNA. 2007;13: 22–9. doi: 10.1261/rna.283207 17123955
13. Nishida KM, Saito K, Mori T, Kawamura Y, Nagami-Okada T, Inagaki S, et al. Gene silencing mechanisms mediated by Aubergine—piRNA complexes in Drosophila male gonad. RNA. 2007;13: 1911–1922. doi: 10.1261/rna.744307 17872506
14. Chekulaeva M, Mathys H, Zipprich JT, Attig J, Colic M, Parker R, et al. miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat Struct Mol Biol. 2011;18. doi: 10.1038/nsmb.2166
15. Huntzinger E, Kuzuoglu-Öztürk D, Braun JE, Eulalio A, Wohlbold L, Izaurralde E, The interactions of GW182 proteins with PABP and deadenylases are required for both translational repression and degradation of miRNA targets. Nucleic Acids Res. 2013;41: 978–994. doi: 10.1093/nar/gks1078 23172285
16. Darricarrere N, Liu N, Watanabe T, Lin H, Function of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activity. Proc Natl Acad Sci U A. 2013;110: 1297–302. doi: 10.1073/pnas.1213283110 23297219
17. Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, et al. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev. 2010;24: 2493–8. doi: 10.1101/gad.1989510 20966047
18. Huang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin H, A major epigenetic programming mechanism guided by piRNAs. Dev Cell. 2013;24: 502–516. doi: 10.1016/j.devcel.2013.01.023 23434410
19. Klenov MS, Lavrov SA, Korbut AP, Stolyarenko AD, Yakushev EY, Reuter M, et al. Impact of nuclear Piwi elimination on chromatin state in Drosophila melanogaster ovaries. Nucleic Acids Res. 2014; gku268. doi: 10.1093/nar/gku268
20. Rozhkov NV, Hammell M, Hannon GJ, Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev. 2013;27: 400–412. doi: 10.1101/gad.209767.112 23392609
21. Sienski G, Donertas D, Brennecke J, Transcriptional silencing of transposons by piwi and maelstrom and its impact on chromatin state and gene expression. Cell. 2012;151: 964–80. doi: 10.1016/j.cell.2012.10.040 23159368
22. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 2013;27: 390–9. doi: 10.1101/gad.209841.112 23392610
23. Wang SH, Elgin SC, Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc Natl Acad Sci U A. 2011;108: 21164–9. doi: 10.1073/pnas.1107892109 22160707
24. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila. Cell. 2007;128: 1089–1103. doi: 10.1016/j.cell.2007.01.043 17346786
25. Robine N, Lau NC, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, et al. A broadly conserved pathway generates 3’UTR-directed primary piRNAs. Curr Biol. 2009;19: 2066–76. doi: 10.1016/j.cub.2009.11.064 20022248
26. Saito K, Inagaki S, Mituyama T, Kawamura Y, Ono Y, Sakota E, et al. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature. 2009;461: 1296–9. doi: 10.1038/nature08501 19812547
27. Olivieri D, Sykora MM, 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. 2010;29: 3301–3317. doi: 10.1038/emboj.2010.212 20818334
28. 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. doi: 10.1016/j.molcel.2012.07.021 22902557
29. Handler D, Meixner K, Pizka M, Lauss K, Schmied C, Gruber FS, et al. The genetic makeup of the Drosophila piRNA pathway. Mol Cell. 2013;50: 762–777. doi: 10.1016/j.molcel.2013.04.031 23665231
30. Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, et al. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell. 2013;50: 736–748. doi: 10.1016/j.molcel.2013.04.006 23665228
31. Chalvet F, Teysset L, Terzian C, Prud’homme N, Santamaria P, Bucheton A, et al. Proviral amplification of the Gypsy endogenous retrovirus of Drosophila melanogaster involves env-independent invasion of the female germline. Embo J. 1999;18: 2659–69. doi: 10.1093/emboj/18.9.2659 10228177
32. Brasset E, Taddei AR, Arnaud F, Faye B, Fausto AM, Mazzini M, et al. Viral particles of the endogenous retrovirus ZAM from Drosophila melanogaster use a pre-existing endosome/exosome pathway for transfer to the oocyte. Retrovirology. 2006;3: 25. doi: 10.1186/1742-4690-3-25 16684341
33. Tanentzapf G, Devenport D, Godt D, Brown NH, Integrin-dependent anchoring of a stem-cell niche. Nat Cell Biol. 2007;9: 1413–8. doi: 10.1038/ncb1660 17982446
34. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL, Spatiotemporal rescue of memory dysfunction in Drosophila. Science. 2003;302: 1765–1768. doi: 10.1126/science.1089035 14657498
35. Desset S, Meignin C, Dastugue B, Vaury C, COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics. 2003;164: 501–509. 12807771
36. Han J, Lee Y, Yeom K-H, Kim Y-K, Jin H, Kim VN, The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004;18: 3016–3027. doi: 10.1101/gad.1262504 15574589
37. Han J, Pedersen JS, Kwon SC, Belair CD, Kim Y-K, Yeom K-H, et al. Posttranscriptional crossregulation between Drosha and DGCR8. Cell. 2009;136: 75–84. doi: 10.1016/j.cell.2008.10.053 19135890
38. Ni J-Q, Zhou R, Czech B, Liu L-P, Holderbaum L, Yang-Zhou D, et al. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods. 2011;8: 405–407. doi: 10.1038/nmeth.1592 21460824
39. Akkouche A, Rebollo R, Burlet N, Esnault C, Martinez S, Viginier B, et al. Tirant, a newly discovered active endogenous retrovirus in Drosophila simulans. J Virol. 2012; doi: 10.1128/JVI.07146-11
40. Dufourt J, Brasset E, Desset S, Pouchin P, Vaury C, Polycomb Group-Dependent, Heterochromatin Protein 1-Independent, Chromatin Structures Silence Retrotransposons in Somatic Tissues Outside Ovaries. DNA Res Int J Rapid Publ Rep Genes Genomes. 2011; doi: 10.1093/dnares/dsr031
41. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, et al. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell. 2009;137: 522–35. doi: 10.1016/j.cell.2009.03.040 19395010
42. Handler D, Olivieri D, Novatchkova M, Gruber FS, Meixner K, Mechtler K, et al. 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: 3977–93. doi: 10.1038/emboj.2011.308 21863019
43. Balcells I, Cirera S, Busk PK, Specific and sensitive quantitative RT-PCR of miRNAs with DNA primers. BMC Biotechnol. 2011;11: 70. doi: 10.1186/1472-6750-11-70 21702990
44. Bejarano F, Bortolamiol-Becet D, Dai Q, Sun K, Saj A, Chou Y-T, et al. A genome-wide transgenic resource for conditional expression of Drosophila microRNAs. Development. 2012;139: 2821–2831. doi: 10.1242/dev.079939 22745315
45. Loya CM, Lu CS, Van Vactor D, Fulga TA, Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat Methods. 2009;6: 897–903. doi: 10.1038/nmeth.1402 19915559
46. Hamada-Kawaguchi N, Nore BF, Kuwada Y, Smith CIE, Yamamoto D, Btk29A promotes Wnt4 signaling in the niche to terminate germ cell proliferation in Drosophila. Science. 2014;343: 294–297. doi: 10.1126/science.1244512 24436419
47. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP, The impact of microRNAs on protein output. Nature. 2008;455: 64–71. doi: 10.1038/nature07242 18668037
48. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N, Widespread changes in protein synthesis induced by microRNAs. Nature. 2008;455: 58–63. doi: 10.1038/nature07228 18668040
49. Haase AD, Fenoglio S, Muerdter F, Guzzardo PM, Czech B, Pappin DJ, et al. Probing the initiation and effector phases of the somatic piRNA pathway in Drosophila. Genes Dev. 2010;24: 2499–504. doi: 10.1101/gad.1968110 20966049
50. Flynt AS, Lai EC, Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet. 2008;9: 831–842. doi: 10.1038/nrg2455 18852696
51. Kim HK, Lee YS, Sivaprasad U, Malhotra A, Dutta A, Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol. 2006;174: 677–687. doi: 10.1083/jcb.200603008 16923828
52. Azzam G, Smibert P, Lai EC, Liu JL, Drosophila Argonaute 1 and its miRNA biogenesis partners are required for oocyte formation and germline cell division. Dev Biol. 2012;365: 384–94. doi: 10.1016/j.ydbio.2012.03.005 22445511
53. Jin Z, Xie T, Dcr-1 Maintains Drosophila Ovarian Stem Cells. Curr Biol. 2007;17: 539–544. doi: 10.1016/j.cub.2007.01.050 17306537
54. Neumüller RA, Betschinger J, Fischer A, Bushati N, Poernbacher I, Mechtler K, et al. Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature. 2008;454: 241–245. doi: 10.1038/nature07014 18528333
55. Park JK, Liu X, Strauss TJ, McKearin DM, Liu Q, The miRNA Pathway Intrinsically Controls Self-Renewal of Drosophila Germline Stem Cells. Curr Biol. 2007;17: 533–538. doi: 10.1016/j.cub.2007.01.060 17320391
56. Poulton JS, Huang Y-C, Smith L, Sun J, Leake N, Schleede J, et al. The microRNA pathway regulates the temporal pattern of Notch signaling in Drosophila follicle cells. Development. 2011;138: 1737–1745. doi: 10.1242/dev.059352 21447549
57. Yang L, Chen D, Duan R, Xia L, Wang J, Qurashi A, et al. Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development. 2007;134: 4265–72. doi: 10.1242/dev.009159 17993467
58. Meignin C, Dastugue B, Vaury C, Intercellular communication between germ line and somatic line is utilized to control the transcription of ZAM, an endogenous retrovirus from Drosophila melanogaster. Nucleic Acids Res. 2004;32: 3799–3806. doi: 10.1093/nar/gkh708 15263061
59. Pelisson A, Song SU, Prud’homme N, Smith PA, Bucheton A, Corces VG, Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. Embo J. 1994;13: 4401–11. 7925283
60. Karginov FV, Cheloufi S, Chong MM, Stark A, Smith AD, Hannon GJ, Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon microRNAs, Drosha, and additional nucleases. Mol Cell. 2010;38: 781–8. doi: 10.1016/j.molcel.2010.06.001 20620951
61. Heras SR, Macias S, Plass M, Fernandez N, Cano D, Eyras E, et al. The Microprocessor controls the activity of mammalian retrotransposons. Nat Struct Mol Biol. 2013;20: 1173–1181. doi: 10.1038/nsmb.2658 23995758
62. Lin YT, Sullivan CS, Expanding the role of Drosha to the regulation of viral gene expression. Proc Natl Acad Sci U S A. 2011;108: 11229–34. doi: 10.1073/pnas.1105799108 21690333
63. Macias S, Plass M, Stajuda A, Michlewski G, Eyras E, Cáceres JF, DGCR8 HITS-CLIP reveals novel functions for the Microprocessor. Nat Struct Mol Biol. 2012;19: 760–766. doi: 10.1038/nsmb.2344 22796965
64. Bartel DP, MicroRNAs: target recognition and regulatory functions. Cell. 2009;136: 215–233. doi: 10.1016/j.cell.2009.01.002 19167326
65. Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, et al. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell. 2006;125: 887–901. doi: 10.1016/j.cell.2006.03.043 16751099
66. Livak KJ, Schmittgen TD, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25: 402–8. doi: 10.1006/meth.2001.1262 11846609
67. Grentzinger T, Armenise C, Brun C, Mugat B, Serrano V, Pelisson A, et al. piRNA-mediated transgenerational inheritance of an acquired trait. Genome Res. 2012;22: 1877–1888. doi: 10.1101/gr.136614.111 22555593
68. Grentzinger T, Chambeyron S, Siomi MC, Fast and Accurate Method to Purify Small Noncoding RNAs from Drosophila Ovaries. In: PIWI-Interacting RNAs. Humana Press; 2014. pp. 171–182. Available: http://link.springer.com/protocol/10.1007/978-1-62703-694-8_14
69. Celniker SE, Dillon LAL, Gerstein MB, Gunsalus KC, Henikoff S, Karpen GH, et al. Unlocking the secrets of the genome. Nature. 2009;459: 927–930. doi: 10.1038/459927a 19536255
70. Kozomara A, Griffiths-Jones S, miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011;39: D152–7. doi: 10.1093/nar/gkq1027 21037258
71. Kheradpour P, Stark A, Roy S, Kellis M, Reliable prediction of regulator targets using 12 Drosophila genomes. Genome Res. 2007;17: 1919–1931. doi: 10.1101/gr.7090407 17989251
72. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z, GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics. 2009;10: 48. doi: 10.1186/1471-2105-10-48 19192299