piRNA and spermatogenesis in mice

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1609, 2013, Pages

  Chuma, Shinichiro ^a,b   Nakano, Toru ^c  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

DNA methylation; Germ cells; piRNA; Piwi; Retrotransposon; Spermatogenesis

Indexed keywords

CYTOLOGY; DEFENSE MECHANISM; DEVELOPMENTAL BIOLOGY; FERTILITY; GENOMICS; GERM CELL; MUTATION; PHENOTYPE; PHYSIOLOGICAL RESPONSE; RNA; RODENT;

EID: 84869457050     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0338     Document Type: Review

References (91)

1. Gundry M, Vijg J. 2012 Direct mutation analysis by high-throughput sequencing: from germline to lowabundant, somatic variants. Mutat. Res. 729, 1-15. (doi:10.1016/j.mrfmmm.2011.10.001)
2. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. 2005 DNA repair and mutagenesis, 2nd edn. Washington, DC: ASM Press.
3. Kazazian Jr HH, 2004 Mobile elements: drivers of genome evolution. Science 303, 1626-1632. (doi:10.1126/science.1089670)
4. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y. 2010 Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464, 927-931. (doi:10.1038/nature08858)
5. Rowe HM et al. 2010 KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463, 237-240. (doi:10.1038/nature08674)
6. Carthew RW, Sontheimer EJ. 2009 Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655. (doi:10.1016/j.cell. 2009.01.035)
7. Aravin AA, Hannon GJ, Brennecke J. 2007 The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318, 761-764. (doi:10.1126/science. 1146484)
8. Aravin A et al. 2006 A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203-207. (doi:10.1038/nature04916)
9. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. 2006 A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442, 199-202. (doi:10.1038/nature04917)
10. Grivna ST, Beyret E, Wang Z, Lin H. 2006 A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20, 1709-1714. (doi:10.1101/gad.1434406)
11. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, Imai H. 2006 Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposonderived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 20, 1732-1743. (doi:10.1101/gad.1425706)
12. Kuramochi-Miyagawa S et al. 2010 MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 24, 887-892. (doi:10.1101/gad.1902110)
13. Wang J, Saxe JP, Tanaka T, Chuma S, Lin H. 2009 Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr. Biol. 19, 640-644. (doi:10.1016/j.cub.2009.02.061)
14. Reuter M, Chuma S, Tanaka T, Franz T, Stark A, Pillai RS. 2009 Loss of the Mili-interacting Tudor domaincontaining protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat. Struct. Mol. Biol. 16, 639-646. (doi:10.1038/nsmb.1615)
15. Vagin VV et al. 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. (doi:10. 1101/gad.1814809)
16. Saffman EE, Lasko P. 1999 Germline development in vertebrates and invertebrates. Cell Mol. Life Sci. 55, 1141-1163. (doi:10.1007/s000180050363)
17. Seydoux G, Braun RE. 2006 Pathway to totipotency: lessons from germ cells. Cell 127, 891-904. (doi:10.1016/j.cell.2006.11.016)
18. Strome S, Lehmann R. 2007 Germ versus soma decisions: lessons from flies and worms. Science 316, 392-393. (doi:10.1126/science.1140846)
19. McLaren A. 2003 Primordial germ cells in the mouse. Dev. Biol. 262, 1-15. (doi:10.1016/S0012-1606(03)00214-8)
20. Yoshida S. 2010 Stem cells in mammalian spermatogenesis. Dev. Growth Diff. 52, 311-317. (doi:10.1111/j.1440-169X.2010.01174.x)
21. Handel MA, Eppig JJ. 1998 Sexual dimorphism in the regulation of mammalian meiosis. Curr. Top. Dev. Biol. 37, 333-358. (doi:10.1016/S0070-2153(08)60179-9)
22. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani MA. 2002 Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117, 15-23. (doi:10.1016/S0925-4773(02)00181-8)
23. Schaefer CB, Ooi SK, Bestor TH, Bourc'his D. 2007 Epigenetic decisions in mammalian germ cells. Science 316, 398-399. (doi:10.1126/science.1137544)
24. Sasaki H, Matsui Y. 2008 Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat. Rev. Genet. 9, 129-140. (doi:10.1038/nrg2295)
25. Trelogan SA, Martin SL. 1995 Tightly regulated, developmentally specific expression of the first open reading frame from LINE-1 during mouse embryogenesis. Proc. Natl Acad. Sci. USA 92, 1520-1524. (doi:10.1073/pnas.92.5.1520)
26. Lander ES et al. 2001 Initial sequencing and analysis of the human genome. Nature 409, 860-921. (doi:10.1038/35057062)
27. Waterston RH et al. 2002 Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562. (doi:10.1038/nature01262)
28. Feschotte C, Pritham EJ. 2007 DNA transposons and the evolution of eukaryotic genomes. Annu. Rev. Genet. 41, 331-368. (doi:10.1146/annurev.genet. 40.110405.090448)
29. Ray DA, Feschotte C, Pagan HJ, Smith JD, Pritham EJ, Arensburger P, Atkinson PW, Craig NL. 2008 Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus. Genome Res. 18, 717-728. (doi:10.1101/gr.071886.107)
30. Jurka J, Kapitonov VV, Kohany O, Jurka MV. 2007 Repetitive sequences in complex genomes: structure and evolution. Annu. Rev. Genomics Hum. Genet. 8, 241-259. (doi:10.1146/annurev.genom.8. 080706.092416)
31. Deininger PL, Moran JV, Batzer MA, Kazazian Jr HH. 2003 Mobile elements and mammalian genome evolution. Curr. Opin. Genet. Dev. 13, 651-658. (doi:10.1016/j.gde.2003.10.013)
32. Kramerov DA, Vassetzky NS. 2005 Short retroposons in eukaryotic genomes. Int. Rev. Cytol. 247, 165-221. (doi:10.1016/S0074-7696(05)47004-7)
33. Farkash EA, Luning Prak ET. 2006 DNA damage and L1 retrotransposition. J. Biomed. Biotechnol. 2006, 37285. (doi:10.1155/JBB/2006/37285)
34. Li E, Bestor TH, Jaenisch R. 1992 Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926. (doi:10. 1016/0092-8674(92)90611-F)
35. Walsh CP, Chaillet JR, Bestor TH. 1998 Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20, 116-117. (doi:10.1038/2413)
36. Bourc'his D, Bestor TH. 2004 Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99. (doi:10.1038/nature02886)
37. Hutvagner G, Simard MJ. 2008 Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 9, 22-32. (doi:10.1038/nrm2321)
38. Tolia NH, Joshua-Tor L. 2007 Slicer and the argonautes. Nat. Chem. Biol. 3, 36-43. (doi:10. 1038/nchembio848)
39. Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H. 1998 A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell selfrenewal. Genes Dev. 12, 3715-3727. (doi:10.1101/gad.12.23.3715)
40. Deng W, Lin H. 2002 miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2, 819-830. (doi:10. 1016/S1534-5807(02)00165-X)
41. Kuramochi-Miyagawa S et al. 2004 Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131, 839-849. (doi:10.1242/dev.00973)
42. 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. (doi:10.1016/j.devcel.2007.03.001)
43. Kuramochi-Miyagawa S, Kimura T, Yomogida K, Kuroiwa A, Tadokoro Y, Fujita Y, Sato M, Matsuda Y, Nakano T. 2001 Two mouse piwi-related genes: miwi and mili. Mech. Dev. 108, 121-133. (doi:10. 1016/S0925-4773(01)00499-3)
44. 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. (doi:10.1016/j.molcel.2008.09.003)
45. Watanabe T et al. 2008 Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539-543. (doi:10. 1038/nature06908)
46. 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. (doi:10.1126/science.1142612)
47. Kuramochi-Miyagawa S 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. (doi:10.1101/gad.1640708)
48. Siomi MC, Sato K, Pezic D, Aravin AA. 2011 PIWIinteracting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12, 246-258. (doi:10.1038/nrm3089)
49. De Fazio S et al. 2011 The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 480, 259-263. (doi:10.1038/nature10547)
50. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C, Antony C, Sachidanandam R, Pillai RS. 2011 Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480, 264-267. (doi:10.1038/nature10672)
51. Chuma S, Hosokawa M, Kitamura K, Kasai S, Fujioka M, Hiyoshi M, Takamune K, Noce T, Nakatsuji N. 2006 Tdrd1/Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice. Proc. Natl Acad. Sci. USA 103, 15 894-15 899. (doi:10.1073/pnas.0601878103)
52. Kojima K, Kuramochi-Miyagawa S, Chuma S, Tanaka T, Nakatsuji N, Kimura T, Nakano T. 2009 Associations between PIWI proteins and TDRD1/MTR-1 are critical for integrated subcellular localization in murine male germ cells. Genes Cells 14, 1155-1165. (doi:10.1111/j.1365-2443. 2009.01342.x)
53. Yabuta Y, Ohta H, Abe T, Kurimoto K, Chuma S, Saitou M. 2011 TDRD5 is required for retrotransposon silencing, chromatoid body assembly and spermiogenesis in mice. J. Cell Biol. 192, 781-795. (doi:10.1083/jcb.201009043)
54. Shoji M et al. 2009 The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev. Cell 17, 775-787. (doi:10.1016/j.devcel.2009.10.012)
55. Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui Y, Nakahara Y, Suzuki R, Yokoyama M, Noce T. 2000 The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14, 841-853.
56. Frost RJ, Hamra FK, Richardson JA, Qi X, Bassel-Duby R, Olson EN. 2010 MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proc. Natl Acad. Sci. USA 107, 11 847-11 852. (doi:10. 1073/pnas.1007158107)
57. Zheng K et al. 2010 Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc. Natl Acad. Sci. USA 107, 11 841-11 846. (doi:10. 1073/pnas.1003953107)
58. Soper SF, van der Heijden GW, 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. (doi:10.1016/j.devcel.2008.05.015)
59. Aravin AA, van der Heijden GW, Castaneda J, Vagin VV, Hannon GJ, Bortvin A. 2009 Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 5, e1000764. (doi:10.1371/journal.pgen.1000764)
60. Ma L et al. 2009 GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet. 5, e1000635. (doi:10.1371/journal.pgen.1000635)
61. Huang H, Gao Q, Peng X, Choi SY, Sarma K, Ren H, Morris AJ, Frohman MA. 2011 piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev. Cell 20, 376-387. (doi:10. 1016/j.devcel.2011.01.004)
62. Watanabe T et al. 2011 MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev. Cell 20, 364-375. (doi:10.1016/j.devcel.2011.01.005)
63. 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. (doi:10.1016/j.cell.2007.01.043)
64. Zhang X, Rossi JJ. 2011 Phylogenetic comparison of small RNA-triggered transcriptional gene silencing. J. Biol. Chem. 286, 29 443-29 448. (doi:10.1074/jbc.R111.276378)
65. Chuma S, Hiyoshi M, Yamamoto A, Hosokawa M, Takamune K, Nakatsuji N. 2003 Mouse Tudor Repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech. Dev. 120, 979-990. (doi:10.1016/S0925-4773(03)00181-3)
66. 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. (doi:10.1016/j.ydbio.2006.10.046)
67. 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. (doi:10.1016/j.cub.2009.02.047)
68. Chen C et al. 2009 Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi. Proc. Natl Acad. Sci. USA 106, 20 336-20 341. (doi:10.1073/pnas.0911640106)
69. Chen C, Nott TJ, Jin J, Pawson T. 2011 Deciphering arginine methylation: Tudor tells the tale. Nat. Rev. Mol. Cell Biol. 12, 629-642. (doi:10.1038/nrm3185)
70. Smith JM, Bowles J, Wilson M, Teasdale RD, Koopman P. 2004 Expression of the tudor-related gene Tdrd5 during development of the male germline in mice. Gene Expr. Patterns 4, 701-705. (doi:10.1016/j.modgep.2004.04.002)
71. Tanaka T et al. 2011 Tudor domain containing 7 (Tdrd7) is essential for dynamic ribonucleoprotein (RNP) remodeling of chromatoid bodies during spermatogenesis. Proc. Natl Acad. Sci. USA 108, 10 579-10 584. (doi:10.1073/pnas.1015447108)
72. Lachke SA et al. 2011 Mutations in the RNA granule component TDRD7 cause cataract and glaucoma. Science 331, 1571-1576. (doi:10.1126/science. 1195970)
73. Handler D, Olivieri D, Novatchkova M, Gruber FS, Meixner K, Mechtler K, Stark A, Sachidanandam R, Brennecke J. 2011 A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. Embo J. 30, 3977-3993. (doi:10.1038/emboj.2011.308)
74. 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. (doi:10.1101/gad.1899210)
75. Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M, Noce T. 1994 Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc. Natl Acad. Sci. USA 91, 12 258-12 262. (doi:10.1073/pnas.91.25.12258)
76. 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. (doi:10.1016/j.cell.2009.03.040)
77. Boswell RE, Mahowald AP. 1985 tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43, 97-104. (doi:10. 1016/0092-8674(85)90015-7)
78. Schupbach T, Wieschaus E. 1986 Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev. Biol. 113, 443-448. (doi:10.1016/0012-1606(86)90179-X)
79. Ephrussi A, Lehmann R. 1992 Induction of germ cell formation by oskar. Nature 358, 387-392. (doi:10. 1038/358387a0)
80. Zhang D, Xiong H, Shan J, Xia X, Trudeau VL. 2008 Functional insight into Maelstrom in the germline piRNA pathway: a unique domain homologous to the DnaQ-H 3-5exonuclease, its lineage-specific expansion/loss and evolutionarily active site switch. Biol. Direct. 3, 48. (doi:10.1186/1745-6150-3-48)
81. Choi SY, Huang P, Jenkins GM, Chan DC, Schiller J, Frohman MA. 2006 A common lipid links Mfnmediated mitochondrial fusion and SNAREregulated exocytosis. Nat. Cell Biol. 8, 1255-1262. (doi:10.1038/ncb1487)
82. Tam OH et al. 2008 Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534-538. (doi:10.1038/nature06904)
83. Saito K et al. 2009 A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461, 1296-1299. (doi:10.1038/nature08501)
84. Kawaoka S, Hayashi N, Suzuki Y, Abe H, Sugano S, Tomari Y, Shimada T, Katsuma S. 2009 The Bombyx ovary-derived cell line endogenously expresses PIWI/PIWI-interacting RNA complexes. RNA 15, 1258-1264. (doi:10.1261/rna.1452209)
85. Kawaoka S, Izumi N, Katsuma S, Tomari Y. 2011 3 end formation of PIWI-interacting RNAs in vitro. Mol. Cell 43, 1015-1022. (doi:10.1016/j.molcel. 2011.07.029)
86. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, Shinohara T. 2003 Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol. Reprod. 69, 612-616. (doi:10.1095/biolreprod.103.017012)
87. Eddy EM. 1975 Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43, 229-280. (doi:10.1016/S0074-7696(08)60070-4)
88. Chuma S, Hosokawa M, Tanaka T, Nakatsuji N. 2009 Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: germinal granules in mammals. Mol. Cell Endocrinol. 306, 17-23. (doi:10.1016/j. mce.2008.11.009)
89. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, Filipowicz W, Sassone-Corsi P. 2006 The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc. Natl Acad. Sci. USA 103, 2647-2652. (doi:10.1073/pnas. 0509333103)
90. Meikar O, Da Ros M, Liljenback H, Toppari J, Kotaja N. 2010 Accumulation of piRNAs in the chromatoid bodies purified by a novel isolation protocol. Exp. Cell Res. 316, 1567-1575. (doi:10.1016/j.yexcr. 2010.02.023)
91. Watanabe T et al. 2011 Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332, 848-852. (doi:10.1126/science.1203919)