Distinct features of the piRNA pathway in somatic and germ cells: From piRNA cluster transcription to piRNA processing and amplification

Mobile DNA

Volumn 5, Issue 1, 2014, Pages

  Théron, Emmanuelle ^a,b,c   Dennis, Cynthia ^a,b,c   Brasset, Emilie ^a,b,c   Vaury, Chantal ^a,b,c  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b INSERM   (France)

^c CNRS   (France)

Author keywords

Germline protection; piRNA pathway; RNA silencing; Transposable elements

Indexed keywords

MITOCHONDRIAL PROTEIN; PIWI INTERACTING RNA; PIWI PROTEIN; RNA INDUCED SILENCING COMPLEX; RNA POLYMERASE II;

ALTERNATIVE RNA SPLICING; BIOGENESIS; DOWN REGULATION; DROSOPHILA MELANOGASTER; FEMALE STERILITY; GENE AMPLIFICATION; GENE REPRESSION; GERM CELL; NONHUMAN; NUCLEAR PORE; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; RETROPOSON; REVIEW; RNA PROCESSING; RNA TRANSCRIPTION; SOMATIC CELL; TRANSCRIPTION INITIATION SITE; TRANSPOSON;

EID: 84989177800     PISSN: None     EISSN: 17598753     Source Type: Journal    
DOI: 10.1186/s13100-014-0028-y     Document Type: Review

References (71)

1. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ: Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
2. Khurana JS, Wang J, Xu J, Koppetsch BS, Thomson TC, Nowosielska A, Li C, Zamore PD, Weng Z, Theurkauf WE: Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 2011, 147:1551-1563.
3. Zanni V, Eymery A, Coiffet M, Zytnicki M, Luyten I, Quesneville H, Vaury C, Jensen S: Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters. Proc Natl Acad Sci U S A 2013, 110:19842-19847.
4. Saito K, Inagaki S, Mituyama T, Kawamura Y, Ono Y, Sakota E, Kotani H, Asai K, Siomi H, Siomi MC: A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009, 461:1296-1299.
5. 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 2014, 5:257.
6. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T: A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006, 442:203-207.
7. Girard A, Sachidanandam R, Hannon GJ, Carmell MA: A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
8. Hirano T, Iwasaki YW, Lin ZY, Imamura M, Seki NM, Sasaki E, Saito K, Okano H, Siomi MC, Siomi H: Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate. RNA 2014, 20:1223-1237.
9. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE: Characterization of the piRNA complex from rat testes. Science 2006, 313:363-367.
10. Devor EJ, Huang L, Samollow PB: PiRNA-like RNAs in the marsupial Monodelphis domestica identify transcription clusters and likely marsupial transposon targets. Mamm Genome 2008, 19:581-586.
11. Shpiz S, Ryazansky S, Olovnikov I, Abramov Y, Kalmykova A: Euchromatic transposon insertions trigger production of novel Pi-And endo-siRNAs at the target sites in the Drosophila germline. PLoS Genet 2014, 10:e1004138.
12. Olovnikov I, Ryazansky S, Shpiz S, Lavrov S, Abramov Y, Vaury C, Jensen S, Kalmykova A: De novo piRNA cluster formation in the Drosophila germ line triggered by transgenes containing a transcribed transposon fragment. Nucleic Acids Res 2013, 41:5757-5768.
13. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP: Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 2006, 127:1193-1207.
14. Weick EM, Sarkies P, Silva N, Chen RA, Moss SM, Cording AC, Ahringer J, Martinez-Perez E, Miska EA: PRDE-1 is a nuclear factor essential for the biogenesis of Ruby motif-dependent piRNAs in C. elegans. Genes Dev 2014, 28:783-796.
15. 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.
16. Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, Han BW, Xu J, Moore MJ, Schimenti JC, Weng Z, Zamore PD: An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol Cell 2013, 50:67-81.
17. Grob S, Schmid MW, Grossniklaus U: Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol Cell 2014, 55:678-693.
18. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, Hannon GJ: Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 2009, 137:522-535.
19. 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, 151:964-980.
20. Murota Y, Ishizu H, Nakagawa S, Iwasaki YW, Shibata S, Kamatani MK, Saito K, Okano H, Siomi H, Siomi MC: Yb integrates piRNA intermediates and processing factors into perinuclear bodies to enhance piRISC assembly. Cell Rep 2014, 8:103-113.
21. Dennis C, Zanni V, Brasset E, Eymery A, Zhang L, Mteirek R, Jensen S, Rong YS, Vaury C: 'Dot COM', a nuclear transit center for the primary piRNA pathway in Drosophila. PLoS One 2013, 8:e72752.
22. Niki Y, Yamaguchi T, Mahowald AP: Establishment of stable cell lines of Drosophila germ-line stem cells. Proc Natl Acad Sci U S A 2006, 103:16325-16330.
23. Szakmary A, Reedy M, Qi H, Lin H: The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster. J Cell Biol 2009, 185:613-627.
24. Qi H, Watanabe T, Ku HY, 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.
25. Lau NC, Robine N, Martin R, Chung WJ, Niki Y, Berezikov E, Lai EC: Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res 2009, 19:1776-1785.
26. Ipsaro JJ, Haase AD, Knott SR, Joshua-Tor L, Hannon GJ: The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis. Nature 2012, 491:279-283.
27. Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, Bonnefond L, Matsumoto N, Nishizawa T, Nakanaga K, Aoki J, Ishitani R, Siomi H, Siomi MC, Nureki O: Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 2012, 491:284-287.
28. Handler D, Olivieri D, Novatchkova M, Gruber FS, 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.
29. Olivieri D, Senti KA, 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.
30. 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.
31. Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, Siomi H, Siomi MC: Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev 2010, 24:2493-2498.
32. Zamparini AL, Davis MY, Malone CD, Vieira E, Zavadil J, Sachidanandam R, Hannon GJ, Lehmann R: Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila. Development 2011, 138:4039-4050.
33. Preall JB, Czech B, Guzzardo PM, Muerdter F, Hannon GJ: shutdown is a component of the Drosophila piRNA biogenesis machinery. RNA 2012, 18:1446-1457.
34. Ma L, Buchold GM, Greenbaum MP, Roy A, Burns KH, Zhu H, Han DY, Harris RA, Coarfa C, Gunaratne PH, Yan W, Matzuk MM: GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet 2009, 5:e1000635.
35. Czech B, Preall JB, McGinn J, Hannon GJ: A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell 2013, 50:749-761.
36. Handler D, Meixner K, Pizka M, Lauss K, Schmied C, Gruber FS, Brennecke J: The genetic makeup of the Drosophila piRNA pathway. Mol Cell 2013, 50:762-777.
37. Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, Fekete R, Hannon GJ: A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell 2013, 50:736-748.
38. Pane A, Wehr K, Schupbach T: zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev Cell 2007, 12:851-862.
39. Ohtani H, Iwasaki YW, Shibuya A, Siomi H, Siomi MC, Saito K: DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev 2013, 27:1656-1661.
40. Lim AK, Kai T: Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc Natl Acad Sci U S A 2007, 104:6714-6719.
41. Anand A, Kai T: The tudor domain protein kumo is required to assemble the nuage and to generate germline piRNAs in Drosophila. EMBO J 2012, 31:870-882.
42. Zhang Z, Xu J, Koppetsch BS, Wang J, Tipping C, Ma S, Weng Z, Theurkauf WE, Zamore PD: Heterotypic piRNA Ping-Pong requires qin, a protein with both E3 ligase and Tudor domains. Mol Cell 2011, 44:572-584.
43. Patil VS, Kai T: Repression of retroelements in Drosophila germline via piRNA pathway by the Tudor domain protein Tejas. Curr Biol 2010, 20:724-730.
44. Liu L, Qi H, Wang J, Lin H: PAPI, a novel TUDOR-domain protein, complexes with AGO3, ME31B and TRAL in the nuage to silence transposition. Development 2011, 138:1863-1873.
45. Patil VS, Anand A, Chakrabarti A, Kai T: The Tudor domain protein Tapas, a homolog of the vertebrate Tdrd7, functions in piRNA pathway to regulate retrotransposons in germline of Drosophila melanogaster. BMC Biol 2014, 12:61.
46. Mendez DL, Mandt RE, Elgin SC: Heterochromatin Protein 1a (HP1a) partner specificity is determined by critical amino acids in the chromo shadow domain and C-Terminal extension. J Biol Chem2013, 288:22315-22323.
47. Donertas D, Sienski G, Brennecke J: Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev 2013, 27:1693-1705.
48. Kawaoka S, Izumi N, Katsuma S, Tomari Y: 3′ end formation of PIWIinteracting RNAs in vitro. Mol Cell 2011, 43:1015-1022.
49. Horwich MD, Li C, Matranga C, Vagin V, Farley G, Wang P, Zamore PD: The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 2007, 17:1265-1272.
50. Saito K, Sakaguchi Y, Suzuki T, Siomi H, Siomi MC: Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi-interacting RNAs at their 3′ ends. Genes Dev 2007, 21:1603-1608.
51. Watanabe T, Chuma S, Yamamoto Y, Kuramochi-Miyagawa S, Totoki Y, Toyoda A, Hoki Y, Fujiyama A, Shibata T, Sado T, Noce T, Nakano T, Nakatsuji N, Lin H, Sasaki H: MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev Cell 2011, 20:364-375.
52. Zheng K, Xiol J, Reuter M, Eckardt S, Leu NA, McLaughlin KJ, Stark A, Sachidanandam R, Pillai RS, Wang PJ: Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc Natl Acad Sci U S A 2010, 107:11841-11846.
53. Frost RJ, Hamra FK, Richardson JA, Qi X, Bassel-Duby R, Olson EN: MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proc Natl Acad Sci U S A 2010, 107:11847-11852.
54. Pandey RR, Tokuzawa Y, Yang Z, Hayashi E, Ichisaka T, Kajita S, Asano Y, Kunieda T, Sachidanandam R, Chuma S, Yamanaka S, Pillai RS: Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice. Proc Natl Acad Sci U S A 2013, 110:16492-16497.
55. Xiol J, Cora E, Koglgruber R, Chuma S, Subramanian S, Hosokawa M, Reuter M, Yang Z, Berninger P, Palencia A, Benes V, Penninger J, Sachidanandam R, Pillai RS: A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol Cell 2012, 47:970-979.
56. Crackower MA, Kolas NK, Noguchi J, Sarao R, Kikuchi K, Kaneko H, Kobayashi E, Kawai Y, Kozieradzki I, Landers R, Mo R, Hui CC, Nieves E, Cohen PE, Osborne LR, Wada T, Kunieda T, Moens PB, Penninger JM: Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 2003, 300:1291-1295.
57. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, Hur JK, Aravin AA, Toth KF: Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 2013, 27:390-399.
58. Rozhkov NV, Hammell M, Hannon GJ: Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 2013, 27:400-412.
59. 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.
60. Brower-Toland B, Findley SD, Jiang L, Liu L, Yin H, Dus M, Zhou P, Elgin SC, Lin H: Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 2007, 21:2300-2311.
61. Mohn F, Sienski G, Handler D, Brennecke J: The rhino-deadlock-cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 2014, 157:1364-1379.
62. Klattenhoff C, Xi H, Li C, Lee S, Xu J, Khurana JS, Zhang F, Schultz N, Koppetsch BS, Nowosielska A, Seitz H, Zamore PD, Weng Z, Theurkauf WE: The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 2009, 138:1137-1149.
63. Pane A, Jiang P, Zhao DY, Singh M, Schupbach T: The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline. EMBO J 2011, 30:4601-4615.
64. Zhang Z, Wang J, Schultz N, Zhang F, Parhad SS, Tu S, Vreven T, Zamore PD, Weng Z, Theurkauf WE: The HP1 homolog rhino anchors a nuclear complex that suppresses piRNA precursor splicing. Cell 2014, 157:1353-1363.
65. Zhang F, Wang J, Xu J, Zhang Z, Koppetsch BS, Schultz N, Vreven T, Meignin C, Davis I, Zamore PD, Weng Z, Theurkauf WE: UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 2012, 151:871-884.
66. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC: A slicer-mediated mechanism for repeat-Associated siRNA 5′ end formation in Drosophila. Science 2007, 315:1587-1590.
67. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD: A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006, 313:320-324.
68. Xiol J, Spinelli P, Laussmann MA, Homolka D, Yang Z, Cora E, Coute Y, Conn S, Kadlec J, Sachidanandam R, Pillai RS: RNA clamping by vasa assembles a piRNA amplifier complex on transposon transcripts. Cell 2014, 157:1698-1711.
69. Dufourt J, Dennis C, Boivin A, Gueguen N, Theron E, Goriaux C, Pouchin P, Ronsseray S, Brasset E, Vaury C: Spatio-Temporal requirements for transposable element piRNA-mediated silencing during Drosophila oogenesis. Nucleic Acids Res 2014, 42:2512-2524.
70. Le Thomas A, Stuwe E, Li S, Du J, Marinov G, Rozhkov N, Chen YC, Luo Y, Sachidanandam R, Toth KF, Patel D, Aravin AA: Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing. Genes Dev 2014, 28:1667-1680.
71. Simonelig M: piRNAs, master regulators of gene expression. Cell Res 2014, 24:779-780.