RNF17 blocks promiscuous activity of PIWI proteins in mouse testes

Genes and Development

Volumn 29, Issue 13, 2015, Pages 1403-1415

  Wasik, Kaja A ^a,b   Tam, Oliver H ^a   Knott, Simon R ^a,b   Falciatori, Ilaria ^a,b   Hammell, Molly ^a   Vagin, Vasily V ^a,b   Hannon, Gregory J ^a,b,c  

^a WATSON SCHOOL OF BIOLOGICAL SCIENCES   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Germ cells; piRNAs; PIWI proteins; Spermatogenesis; Transposons

Indexed keywords

LONG UNTRANSLATED RNA; PEPTIDES AND PROTEINS; PIWI INTERACTING RNA; PIWI PROTEIN; RNF17 PROTEIN; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; RNF17 PROTEIN, MOUSE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSPOSON;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELL MATURATION; DNA METHYLATION; ENZYME KINETICS; GERM CELL; MALE; MALE STERILITY; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ANALYSIS; RNA SEQUENCE; RNA SYNTHESIS; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SYSTEMATIC REVIEW; TESTIS DEVELOPMENT; TRANSPOSON; ANIMAL; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; MEIOSIS; METABOLISM; MUTATION; PATHOPHYSIOLOGY; TESTIS;

MAMMALIA;

ANIMALS; ARGONAUTE PROTEINS; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; MALE; MEIOSIS; MICE; MUTATION; RNA, SMALL INTERFERING; TESTIS; TRANSCRIPTION FACTORS;

EID: 84936992227     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.265215.115     Document Type: Article

References (61)

1. Anders S, HuberW. 2010. Differential expression analysis for sequence count data. Genome Biol 11: R106.
2. Anders S, Pyl PT, Huber W. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169.
3. Aravin AA, Hannon GJ. 2008. Small RNA silencing pathways in germ and stem cells. Cold Spring Harb Symp Quant Biol 73: 283-290.
4. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, et al. 2006. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442: 203-207.
5. Aravin AA, Hannon GJ, Brennecke J. 2007. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764.
6. 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.
7. Armour CD, Castle JC, Chen R, Babak T, Loerch P, Jackson S, Shah JK, Dey J, Rohl CA, Johnson JM, et al. 2009. Digital transcriptome profiling using selective hexamer priming for cDNA synthesis. Nat Methods 6: 647-649.
8. Bao J, Yan W. 2012. Male germline control of transposable elements. Biol Reprod 86: 162, 161-114.
9. Bastos H, Lassalle B, Chicheportiche A, Riou L, Testart J, Allemand I, Fouchet P. 2005. Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry A 65: 40-49.
10. Beyret E, Liu N, Lin H. 2012. piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism. Cell Res 22: 1429-1439.
11. Bohgaki M, Bohgaki T, El Ghamrasni S, Srikumar T, Maire G, Panier S, Fradet-Turcotte A, Stewart GS, Raught B, Hakem A, et al. 2013. RNF168 ubiquitylates 53BP1 and controls its response to DNA double-strand breaks. Proc Natl Acad Sci 110: 20982-20987.
12. 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.
13. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG, Hannon GJ. 2007. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12: 503-514.
14. Castaneda J, Genzor P, Bortvin A. 2011. piRNAs, transposon silencing, and germline genome integrity. Mutat Res 714: 95-104.
15. Chen C, Nott TJ, Jin J, Pawson T. 2011. Deciphering arginine methylation: Tudor tells the tale. Nat Rev Mol Cell Biol 12: 629-642.
16. Chuma S, Nakano T. 2013. piRNA and spermatogenesis in mice. Philos Trans R Soc Lond B Biol Sci 368: 20110338.
17. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
18. DengW, Lin H. 2002. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830.
19. Di Giacomo M, Comazzetto S, Saini H, De Fazio S, Carrieri C, Morgan M, Vasiliauskaite L, Benes V, Enright AJ, O'Carroll D. 2013. Multiple epigenetic mechanisms and the piRNA pathway enforce LINE1 silencing during adult spermatogenesis. Mol Cell 50: 601-608.
20. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
21. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. 2006. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202.
22. Goh WS, Falciatori I, Tam OH, Burgess R, Meikar O, Kotaja N, Hammell M, Hannon GJ. 2015. piRNA-directed cleavage of meiotic transcripts regulates spermatogenesis. Genes Dev 29: 1032-1044.
23. Hirano T, Iwasaki YW, Lin ZY, Imamura M, Seki NM, Sasaki E, Saito K, Okano H, Siomi MC, Siomi H. 2014. Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate. RNA 20: 1223-1237.
24. Hosokawa M, Shoji M, Kitamura K, Tanaka T, Noce T, Chuma S, Nakatsuji N. 2007. Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice. Dev Biol 301: 38-52.
25. Karginov FV, Cheloufi S, Chong MM, Stark A, Smith AD, Hannon GJ. 2010. Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon microRNAs, Drosha, and additional nucleases. Mol Cell 38: 781-788.
26. Klattenhoff C, TheurkaufW. 2008. Biogenesis and germline functions of piRNAs. Development 135: 3-9.
27. Kota SK, Feil R. 2010. Epigenetic transitions in germ cell development and meiosis. Dev Cell 19: 675-686.
28. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, et al. 2004. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849.
29. Kuramochi-Miyagawa S, WatanabeT, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, et al. 2008. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908-917.
30. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
31. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE. 2006. Characterization of the piRNA complex from rat testes. Science 313: 363-367.
32. Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, Han BW, Xu J, Moore MJ, Schimenti JC, Weng Z, et al. 2013. An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol Cell 50: 67-81.
33. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
34. Liu W, Zhao Y, Cui P, Lin Q, Ding F, Xin C, Tan X, Song S, Yu J, Hu S. 2011. Thousands of novel transcripts identified in mouse cerebrum, testis, and ES cells based on ribo-minus RNA sequencing. Front Genet 2: 93.
35. (T)method. Methods 25: 402-408.
36. Malone CD, Hannon GJ. 2009. Small RNAs as guardians of the genome. Cell 136: 656-668.
37. Malone C, Brennecke J, Czech B, Aravin A, Hannon GJ. 2012. Preparation of small RNA libraries for high-throughput sequencing. Cold Spring Harb Protoc 2012: 1067-1077.
38. Mohn F, Handler D, Brennecke J. 2015. Noncoding RNA. piRNAguided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis. Science 348: 812-817.
39. Molaro A, Falciatori I, Hodges E, Aravin AA, Marran K, Rafii S, McCombie WR, Smith AD, Hannon GJ. 2014. Two waves of de novo methylation during mouse germ cell development. Genes Dev 28: 1544-1549.
40. Pan J, Goodheart M, Chuma S, Nakatsuji N, Page DC, Wang PJ. 2005. RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis. Development 132: 4029-4039.
41. Pillai RS, Chuma S. 2012. piRNAs and their involvement in male germline development in mice. Dev Growth Differ 54: 78-92.
42. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
43. 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.
44. Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM. 2007. Absence of tektin 4 causes asthenozoospermia and subfertility in male mice. FASEB J 21: 1013-1025.
45. Siomi MC, Mannen T, Siomi H. 2010. How does the royal family of Tudor rule the PIWI-interacting RNA pathway? Genes Dev 24: 636-646.
46. Siomi MC, Sato K, Pezic D, Aravin AA. 2011. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258.
47. Sookdeo A, Hepp CM, McClure MA, Boissinot S. 2013. Revisiting the evolution of mouse LINE-1 in the genomic era. Mob DNA 4: 3.
48. Soper SF, van der HeijdenGW, Hardiman TC, Goodheart M, Martin SL, de Boer P, Bortvin A. 2008. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev Cell 15: 285-297.
49. Sun J, Lin Y, Wu J. 2013. Long non-coding RNA expression profiling of mouse testis during postnatal development. PLoS One 8: e75750.
50. Tanaka T, Hosokawa M, Vagin VV, Reuter M, Hayashi E, Mochizuki AL, Kitamura K, Yamanaka H, Kondoh G, Okawa K, et al. 2011. Tudor domain containing 7 (Tdrd7) is essential for dynamic ribonucleoprotein (RNP) remodeling of chromatoid bodies during spermatogenesis. Proc Natl Acad Sci 108: 10579-10584.
51. Tsutsumi M, Kowa-Sugiyama H, Bolor H, Kogo H, Inagaki H, Ohye T, Yamada K, Taniguchi-Ikeda M, Toda T, Kurahashi H. 2012. Screening of genes involved in chromosome segregation during meiosis I: in vitro gene transfer to mouse fetal oocytes. J Hum Genet 57: 515-522.
52. Vagin VV, Wohlschlegel J, Qu J, Jonsson Z, Huang X, Chuma S, Girard A, Sachidanandam R, Hannon GJ, Aravin AA. 2009. Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 23: 1749-1762.
53. Vagin VV, Yu Y, Jankowska A, Luo Y, Wasik KA, Malone CD, Harrison E, Rosebrock A, Wakimoto BT, Fagegaltier D, et al. 2013. Minotaur is critical for primary piRNA biogenesis. RNA 19: 1064-1077.
54. Vasileva A, Tiedau D, Firooznia A, Muller-Reichert T, Jessberger R. 2009. Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression. Curr Biol 19: 630-639.
55. Vourekas A, Zheng Q, Alexiou P, Maragkakis M, Kirino Y, Gregory BD, Mourelatos Z. 2012. Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol 19: 773-781.
56. Vourekas A, Zheng K, Fu Q, Maragkakis M, Alexiou P, MaJ, Pillai RS, Mourelatos Z, Wang PJ. 2015. The RNA helicase MOV10L1 binds piRNA precursors to initiate piRNA processing. Genes Dev 29: 617-629.
57. Watanabe T, Cheng EC, Zhong M, Lin H. 2015. Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline. Genome Res 25: 368-380.
58. Xu M, You Y, Hunsicker P, Hori T, Small C, Griswold MD, Hecht NB. 2008. Mice deficient for a small cluster of Piwi-interacting RNAs implicate Piwi-interacting RNAs in transposon control. Biol Reprod 79: 51-57.
59. 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.
60. Zhang Z, Koppetsch BS, Wang J, Tipping C, Weng Z, Theurkauf WE, Zamore PD. 2014. Antisense piRNA amplification, but not piRNA production or nuage assembly, requires the Tudor-domain protein Qin. EMBO J 33: 536-539.
61. Zhang P, Kang JY, Gou LT, Wang J, Xue Y, Skogerboe G, Dai P, HuangDW, Chen R, Fu XD, et al. 2015. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res 25: 193-207.