Multiple LINEs of retrotransposon silencing mechanisms in the mammalian germline

Seminars in Cell and Developmental Biology

Volumn 59, Issue , 2016, Pages 118-125

  Yang, Fang ^a   Wang, P Jeremy ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

Author keywords

Germline; LINE1; Mouse; Retrotransposon; Spermatogenesis

Indexed keywords

DNA; HISTONE; PIWI INTERACTING RNA;

DNA METHYLATION; EPIGENETICS; FETUS CELL; GENE SILENCING; GERM CELL; HISTONE MODIFICATION; HUMAN; NONHUMAN; OOCYTE; RETROPOSON; RETROPOSON LINE1; REVIEW; SPERMATOGENESIS; ANIMAL; GENETICS; LONG INTERSPERSED REPEAT; MAMMAL; METABOLISM;

ANIMALS; DNA METHYLATION; GENE SILENCING; GERM CELLS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MAMMALS; OOCYTES; SPERMATOGENESIS;

EID: 84961266888     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2016.03.001     Document Type: Review

References (109)

1. [1] Goodier, J.L., Kazazian, H.H. Jr., Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135 (2008), 23–35.
2. [2] Levin, H.L., Moran, J.V., Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12 (2011), 615–627.
3. [3] DeBerardinis, R.J., Goodier, J.L., Ostertag, E.M., Kazazian, H.H. Jr., Rapid amplification of a retrotransposon subfamily is evolving the mouse genome. Nat. Genet. 20 (1998), 288–290.
4. [4] Sassaman, D.M., Dombroski, B.A., Moran, J.V., Kimberland, M.L., Naas, T.P., DeBerardinis, R.J., et al. Many human L1 elements are capable of retrotransposition. Nat. Genet. 16 (1997), 37–43.
5. [5] Mandal, P.K., Kazazian, H.H. Jr., SnapShot: vertebrate transposons. Cell, 135, 2008, 192 e1.
6. [6] Martin, S.L., Cruceanu, M., Branciforte, D., Wai-Lun Li, P., Kwok, S.C., Hodges, R.S., et al. LINE-1 retrotransposition requires the nucleic acid chaperone activity of the ORF1 protein. J. Mol. Biol. 348 (2005), 549–561.
7. [7] Feng, Q., Moran, J.V., Kazazian, H.H. Jr., Boeke, J.D., Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87 (1996), 905–916.
8. [8] Mathias, S.L., Scott, A.F., Kazazian, H.H. Jr., Boeke, J.D., Gabriel, A., Reverse transcriptase encoded by a human transposable element. Science 254 (1991), 1808–1810.
9. [9] Smallwood, S.A., Kelsey, G., De novo DNA methylation: a germ cell perspective. Trends Genet. 28 (2012), 33–42.
10. [10] Kato, Y., Kaneda, M., Hata, K., Kumaki, K., Hisano, M., Kohara, Y., et al. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 16 (2007), 2272–2280.
11. [11] Bourc'his, D., Bestor, T.H., Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431 (2004), 96–99.
12. [12] Ooi, S.K., Qiu, C., Bernstein, E., Li, K., Jia, D., Yang, Z., et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448 (2007), 714–717.
13. [13] Leitch, H.G., Tang, W.W., Surani, M.A., Primordial germ-cell development and epigenetic reprogramming in mammals. Curr. Top. Dev. Biol. 104 (2013), 149–187.
14. [14] Hackett, J.A., Zylicz, J.J., Surani, M.A., Parallel mechanisms of epigenetic reprogramming in the germline. Trends Genet. 28 (2012), 164–174.
15. [15] Siomi, M.C., Sato, K., Pezic, D., Aravin, A.A., PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12 (2011), 246–258.
16. [16] Thomson, T., Lin, H., The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 25 (2009), 355–376.
17. [17] Pillai, R.S., Chuma, S., piRNAs and their involvement in male germline development in mice. Dev. Growth Differ. 54 (2012), 78–92.
18. [18] Vagin, V.V., Wohlschlegel, J., Qu, J., Jonsson, Z., Huang, X., Chuma, S., et al. Proteomic analysis of murine piwi proteins reveals a role for arginine methylation in specifying interaction with tudor family members. Genes Dev. 23 (2009), 1749–1762.
19. [19] Chuma, S., Nakano, T., piRNA and spermatogenesis in mice. Philos. Trans. R. Soc. Lond. B Biol. Sci., 368, 2013, 20110338.
20. [20] Fu, Q., Wang, P.J., Mammalian piRNAs: biogenesis, function, and mysteries. Spermatogenesis, 4, 2014, e27889.
21. [21] Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T.W., Isobe, T., Asada, N., Fujita, Y., et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131 (2004), 839–849.
22. [22] Deng, W., Miwi, Lin H., a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2 (2002), 819–830.
23. [23] Carmell, M.A., Girard, A., van de Kant, H.J., Bourc'his, D., Bestor, T.H., de Rooij, D.G., et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12 (2007), 503–514.
24. [24] Zhang, P., Kang, J.Y., Gou, L.T., Wang, J., Xue, Y., Skogerboe, G., et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res. 25 (2015), 193–207.
25. [25] Gou, L.T., Dai, P., Yang, J.H., Xue, Y., Hu, Y.P., Zhou, Y., et al. Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis. Cell Res. 24 (2014), 680–700.
26. [26] Goh, W.S., Falciatori, I., Tam, O.H., Burgess, R., Meikar, O., Kotaja, N., et al. piRNA-directed cleavage of meiotic transcripts regulates spermatogenesis. Genes Dev. 29 (2015), 1032–1044.
27. [27] Shoji, M., Tanaka, T., Hosokawa, M., Reuter, M., Stark, A., Kato, Y., et al. The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev. Cell 17 (2009), 775–787.
28. [28] Pandey, R.R., Tokuzawa, Y., Yang, Z., Hayashi, E., Ichisaka, T., Kajita, S., et al. Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 16492–16497.
29. [29] Kirino, Y., Kim, N., de Planell-Saguer, M., Khandros, E., Chiorean, S., Klein, P.S., et al. Arginine methylation of piwi proteins catalysed by dPRMT5 is required for Ago3 and aub stability. Nat. Cell Biol. 11 (2009), 652–658.
30. [30] Kirino, Y., Vourekas, A., Sayed, N., de Lima Alves, F., Thomson, T., Lasko, P., et al. Arginine methylation of aubergine mediates tudor binding and germ plasm localization. RNA 16 (2010), 70–78.
31. [31] Reuter, M., Chuma, S., Tanaka, T., Franz, T., Stark, A., Pillai, R.S., Loss of the mili-interacting tudor domain-containing protein-1 activates transposons and alters the mili-associated small RNA profile. Nat. Struct. Mol. Biol. 16 (2009), 639–646.
32. [32] Chen, C., Jin, J., James, D.A., Adams-Cioaba, M.A., Park, J.G., Guo, Y., et al. Mouse piwi interactome identifies binding mechanism of tdrkh tudor domain to arginine methylated miwi. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 20336–20341.
33. [33] Pek, J.W., Anand, A., Kai, T., Tudor domain proteins in development. Development 139 (2012), 2255–2266.
34. [34] de Mateo, S., Sassone-Corsi, P., Regulation of spermatogenesis by small non-coding RNAs: role of the germ granule. Semin. Cell Dev. Biol. 29 (2014), 84–92.
35. [35] Li, X.Z., Roy, C.K., Dong, X., Bolcun-Filas, E., Wang, J., Han, B.W., et al. An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol. Cell 50 (2013), 67–81.
36. [36] Toscani, A., Mettus, R.V., Coupland, R., Simpkins, H., Litvin, J., Orth, J., et al. Arrest of spermatogenesis and defective breast development in mice lacking A-myb. Nature 386 (1997), 713–717.
37. [37] Bolcun-Filas, E., Bannister, L.A., Barash, A., Schimenti, K.J., Hartford, S.A., Eppig, J.J., et al. A-MYB (MYBL1) transcription factor is a master regulator of male meiosis. Development 138 (2011), 3319–3330.
38. [38] Zheng, K., Xiol, J., Reuter, M., Eckardt, S., Leu, N.A., McLaughlin, K.J., et al. 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. 107 (2010), 11841–11846.
39. [39] Zheng, K., Wang, P.J., Blockade of pachytene piRNA biogenesis reveals a novel requirement for maintaining post-meiotic germline genome integrity. PLoS Genet., 8, 2012, e1003038.
40. [40] Vourekas, A., Zheng, K., Fu, Q., Maragkakis, M., Alexiou, P., Ma, J., et al. The RNA helicase MOV10L1 binds piRNA precursors to initiate piRNA processing. Genes Dev. 29 (2015), 617–629.
41. [41] Castaneda, J., Genzor, P., van der Heijden, G.W., Sarkeshik, A., Yates, J.R. 3rd, Ingolia, N.T., et al. Reduced pachytene piRNAs and translation underlie spermiogenic arrest in maelstrom mutant mice. EMBO J. 33 (2014), 1999–2019.
42. [42] Chen, K.M., Campbell, E., Pandey, R.R., Yang, Z., McCarthy, A.A., Pillai, R.S., Metazoan maelstrom is an RNA-binding protein that has evolved from an ancient nuclease active in protists. RNA 21 (2015), 833–839.
43. [43] Genzor, P., Bortvin, A., A unique HMG-box domain of mouse maelstrom binds structured RNA but not double stranded DNA. PLoS One, 10, 2015, e0120268.
44. [44] Matsumoto, N., Sato, K., Nishimasu, H., Namba, Y., Miyakubi, K., Dohmae, N., et al. Crystal structure and activity of the endoribonuclease domain of the piRNA pathway factor maelstrom. Cell Rep. 11 (2015), 366–375.
45. [45] Voigt, F., Reuter, M., Kasaruho, A., Schulz, E.C., Pillai, R.S., Barabas, O., Crystal structure of the primary piRNA biogenesis factor zucchini reveals similarity to the bacterial PLD endonuclease nuc. RNA 18 (2012), 2128–2134.
46. [46] Nishimasu, H., Ishizu, H., Saito, K., Fukuhara, S., Kamatani, M.K., Bonnefond, L., et al. Structure and function of zucchini endoribonuclease in piRNA biogenesis. Nature 491 (2012), 284–287.
47. [47] Ipsaro, J.J., Haase, A.D., Knott, S.R., Joshua-Tor, L., Hannon, G.J., The structural biochemistry of zucchini implicates it as a nuclease in piRNA biogenesis. Nature 491 (2012), 279–283.
48. [48] Vourekas, A., Zheng, Q., Alexiou, P., Maragkakis, M., Kirino, Y., Gregory, B.D., et al. Mili and miwi target RNA repertoire reveals piRNA biogenesis and function of miwi in spermiogenesis. Nat. Struct. Mol. Biol. 19 (2012), 773–781.
49. [49] Kawaoka, S., Izumi, N., Katsuma, S., Tomari, Y., 3′ end formation of PIWI-interacting RNAs in vitro. Mol. Cell 43 (2011), 1015–1022.
50. [50] Saxe, J.P., Chen, M., Zhao, H., Lin, H., Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline. EMBO J. 32 (2013), 1869–1885.
51. [51] Gunawardane, L.S., Saito, K., Nishida, K.M., Miyoshi, K., Kawamura, Y., Nagami, T., et al. A slicer-mediated mechanism for repeat-associated siRNA 5’ end formation in drosophila. Science 315 (2007), 1587–1590.
52. [52] De Fazio, S., Bartonicek, N., Di Giacomo, M., Abreu-Goodger, C., Sankar, A., Funaya, C., et al. The endonuclease activity of mili fuels piRNA amplification that silences LINE1 elements. Nature 480 (2011), 259–263.
53. [53] Reuter, M., Berninger, P., Chuma, S., Shah, H., Hosokawa, M., Funaya, C., et al. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480 (2011), 264–267.
54. [54] Di Giacomo, M., Comazzetto, S., Saini, H., De Fazio, S., Carrieri, C., Morgan, M., et al. Multiple epigenetic mechanisms and the piRNA pathway enforce LINE1 silencing during adult spermatogenesis. Mol. Cell 50 (2013), 601–608.
55. [55] Zamudio, N., Barau, J., Teissandier, A., Walter, M., Borsos, M., Servant, N., et al. DNA methylation restrains transposons from adopting a chromatin signature permissive for meiotic recombination. Genes Dev. 29 (2015), 1256–1270.
56. [56] Walsh, C.P., Chaillet, J.R., Bestor, T.H., Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20 (1998), 116–117.
57. [57] Kuramochi-Miyagawa, S., Watanabe, T., Gotoh, K., Totoki, Y., Toyoda, A., Ikawa, M., et al. DNA methylation of retrotransposon genes is regulated by piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22 (2008), 908–917.
58. [58] Aravin, A.A., Sachidanandam, R., Bourc'his, D., Schaefer, C., Pezic, D., Toth, K.F., et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31 (2008), 785–799.
59. [59] Molaro, A., Falciatori, I., Hodges, E., Aravin, A.A., Marran, K., Rafii, S., et al. Two waves of de novo methylation during mouse germ cell development. Genes Dev. 28 (2014), 1544–1549.
60. [60] Tachibana, M., Nozaki, M., Takeda, N., Shinkai, Y., Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J. 26 (2007), 3346–3359.
61. [61] Tachibana, M., Sugimoto, K., Nozaki, M., Ueda, J., Ohta, T., Ohki, M., et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16 (2002), 1779–1791.
62. [62] Di Giacomo, M., Comazzetto, S., Sampath, S.C., Sampath, S.C., O'Carroll, D., G9a co-suppresses LINE1 elements in spermatogonia. Epigenet. Chromatin, 7, 2014 24-8935-7-24 eCollection.
63. [63] Sienski, G., Donertas, D., Brennecke, J., Transcriptional silencing of transposons by piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151 (2012), 964–980.
64. [64] Yu, Y., Gu, J., Jin, Y., Luo, Y., Preall, J.B., Ma, J., et al. Panoramix enforces piRNA-dependent cotranscriptional silencing. Science 350 (2015), 339–342.
65. [65] Sienski, G., Batki, J., Senti, K.A., Donertas, D., Tirian, L., Meixner, K., et al. Silencio/CG9754 connects the piwi-piRNA complex to the cellular heterochromatin machinery. Genes Dev. 29 (2015), 2258–2271.
66. [66] Le Thomas, A., Rogers, A.K., Webster, A., Marinov, G.K., Liao, S.E., Perkins, E.M., et al. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev. 27 (2013), 390–399.
67. [67] Pezic, D., Manakov, S.A., Sachidanandam, R., Aravin, A.A., piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev. 28 (2014), 1410–1428.
68. [68] Liu, S., Brind'Amour, J., Karimi, M.M., Shirane, K., Bogutz, A., Lefebvre, L., et al. Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells. Genes Dev. 28 (2014), 2041–2055.
69. [69] Watson, M.L., Zinn, A.R., Inoue, N., Hess, K.D., Cobb, J., Handel, M.A., et al. Identification of morc (microrchidia), a mutation that results in arrest of spermatogenesis at an early meiotic stage in the mouse. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 14361–14366.
70. [70] Inoue, N., Hess, K.D., Moreadith, R.W., Richardson, L.L., Handel, M.A., Watson, M.L., et al. New gene family defined by MORC, a nuclear protein required for mouse spermatogenesis. Hum. Mol. Genet. 8 (1999), 1201–1207.
71. [71] Moissiard, G., Cokus, S.J., Cary, J., Feng, S., Billi, A.C., Stroud, H., et al. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336 (2012), 1448–1451.
72. [72] Pastor, W.A., Stroud, H., Nee, K., Liu, W., Pezic, D., Manakov, S., et al. MORC1 represses transposable elements in the mouse male germline. Nat. Commun., 5, 2014, 5795.
73. [73] Roeder, G.S., Bailis, J.M., The pachytene checkpoint. Trends Genet. 16 (2000), 395–403.
74. [74] Soper, S.F., van der Heijden, G.W., Hardiman, T.C., Goodheart, M., Martin, S.L., de Boer, P., et al. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev. Cell 15 (2008), 285–297.
75. [75] Webster, K.E., O'Bryan, M.K., Fletcher, S., Crewther, P.E., Aapola, U., Craig, J., et al. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 4068–4073.
76. [76] Hayashi, K., Yoshida, K., Matsui, Y., A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438 (2005), 374–378.
77. [77] Smagulova, F., Gregoretti, I.V., Brick, K., Khil, P., Camerini-Otero, R.D., Petukhova, G.V., Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472 (2011), 375–378.
78. [78] Keeney, S., Giroux, C.N., Kleckner, N., Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88 (1997), 375–384.
79. [79] Shinohara, A., Ogawa, H., Ogawa, T., Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69 (1992), 457–470.
80. [80] Bishop, D.K., Park, D., Xu, L., Kleckner, N., DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69 (1992), 439–456.
81. [81] Iguchi, N., Xu, M., Hori, T., Hecht, N.B., Noncoding RNAs of the mammalian testis: the meiotic transcripts Nct1 and Nct2 encode piRNAs. Ann. N. Y. Acad. Sci. 1120 (2007), 84–94.
82. [82] Xu, M., You, Y., Hunsicker, P., Hori, T., Small, C., Griswold, M.D., et al. Mice deficient for a small cluster of piwi-interacting RNAs implicate piwi-interacting RNAs in transposon control. Biol. Reprod. 79 (2008), 51–57.
83. [83] Horwich, M.D., Li, C., Matranga, C., Vagin, V., Farley, G., Wang, P., et al. The drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr. Biol. 17 (2007), 1265–1272.
84. [84] Kirino, Y., Mourelatos, Z., The mouse homolog of HEN1 is a potential methylase for piwi-interacting RNAs. RNA 13 (2007), 1397–1401.
85. [85] Lim, S.L., Qu, Z.P., Kortschak, R.D., Lawrence, D.M., Geoghegan, J., Hempfling, A.L., et al. HENMT1 and piRNA stability are required for adult male germ cell transposon repression and to define the spermatogenic program in the mouse. PLoS Genet., 11, 2015, e1005620.
86. [86] Taylor, M.S., LaCava, J., Mita, P., Molloy, K.R., Huang, C.R., Li, D., et al. Affinity proteomics reveals human host factors implicated in discrete stages of LINE-1 retrotransposition. Cell 155 (2013), 1034–1048.
87. [87] Goodier, J.L., Cheung, L.E., Kazazian, H.H. Jr., Jr: Mapping the LINE1 ORF1 protein interactome reveals associated inhibitors of human retrotransposition. Nucleic Acids Res. 41 (2013), 7401–7419.
88. [88] Prak, E.T., Dodson, A.W., Farkash, E.A., Kazazian, H.H. Jr., Tracking an embryonic L1 retrotransposition event. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 1832–1837.
89. [89] Malki, S., van der Heijden, G.W., O'Donnell, K.A., Martin, S.L., Bortvin, A., A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev. Cell 29 (2014), 521–533.
90. [90] Chuma, S., LINE-1 of evidence for fetal oocyte attrition by retrotransposon. Dev. Cell 29 (2014), 501–502.
91. [91] Lim, A.K., Lorthongpanich, C., Chew, T.G., Tan, C.W., Shue, Y.T., Balu, S., et al. The nuage mediates retrotransposon silencing in mouse primordial ovarian follicles. Development 140 (2013), 3819–3825.
92. [92] Flemr, M., Malik, R., Franke, V., Nejepinska, J., Sedlacek, R., Vlahovicek, K., et al. A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 155 (2013), 807–816.
93. [93] Tam, O.H., Aravin, A.A., Stein, P., Girard, A., Murchison, E.P., Cheloufi, S., et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453 (2008), 534–538.
94. [94] Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453 (2008), 539–543.
95. [95] Stein, P., Rozhkov, N.V., Li, F., Cardenas, F.L., Davydenko, O., Vandivier, L.E., et al. Essential role for endogenous siRNAs during meiosis in mouse oocytes. PLoS Genet., 11, 2015, e1005013.
96. [96] Roovers, E.F., Rosenkranz, D., Mahdipour, M., Han, C.T., He, N., Chuva de Sousa Lopes SM, et al: Piwi proteins and piRNAs in mammalian oocytes and early embryos. Cell Rep. 10 (2015), 2069–2082.
97. [97] Williams, Z., Morozov, P., Mihailovic, A., Lin, C., Puvvula, P.K., Juranek, S., et al. Discovery and characterization of piRNAs in the human fetal ovary. Cell Rep. 13 (2015), 854–863.
98. [98] Aravin, A.A., Sachidanandam, R., Girard, A., Fejes-Toth, K., Hannon, G.J., Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316 (2007), 744–747.
99. [99] Frost, R.J., Hamra, F.K., Richardson, J.A., Qi, X., Bassel-Duby, R., Olson, E.N., MOV10L1 is necessary for protection of spermatocytes against retrotransposons by piwi-interacting RNAs. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 11847–11852.
100. [100] Kuramochi-Miyagawa, S., Watanabe, T., Gotoh, K., Takamatsu, K., Chuma, S., Kojima-Kita, K., et al. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 24 (2010), 887–892.
101. [101] Chuma, S., Hosokawa, M., Kitamura, K., Kasai, S., Fujioka, M., Hiyoshi, M., et al. 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. U. S. A. 103 (2006), 15894–15899.
102. [102] Yabuta, Y., Ohta, H., Abe, T., Kurimoto, K., Chuma, S., Saitou, M., TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice. J. Cell Biol. 192 (2011), 781–795.
103. [103] Watanabe, T., Chuma, S., Yamamoto, Y., Kuramochi-Miyagawa, S., Totoki, Y., Toyoda, A., et al. MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev. Cell 20 (2011), 364–375.
104. [104] Ma, L., Buchold, G.M., Greenbaum, M.P., Roy, A., Burns, K.H., Zhu, H., et al. GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet., 5, 2009, e1000635.
105. [105] Xiol, J., Cora, E., Koglgruber, R., Chuma, S., Subramanian, S., Hosokawa, M., et al. A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol. Cell 47 (2012), 970–979.
106. [106] Grad, I., Cederroth, C.R., Walicki, J., Grey, C., Barluenga, S., Winssinger, N., et al. The molecular chaperone Hsp90alpha is required for meiotic progression of spermatocytes beyond pachytene in the mouse. PLoS One, 5, 2010, e15770.
107. [107] Ichiyanagi, T., Ichiyanagi, K., Ogawa, A., Kuramochi-Miyagawa, S., Nakano, T., Chuma, S., et al. HSP90alpha plays an important role in piRNA biogenesis and retrotransposon repression in mouse. Nucleic Acids Res. 42 (2014), 11903–11911.
108. [108] Yoshimura, T., Toyoda, S., Kuramochi-Miyagawa, S., Miyazaki, T., Miyazaki, S., Tashiro, F., et al. Gtsf1/Cue110, a gene encoding a protein with two copies of a CHHC zn-finger motif, is involved in spermatogenesis and retrotransposon suppression in murine testes. Dev. Biol. 335 (2009), 216–227.
109. [109] Yang, Z., Chen, K.M., Pandey, R.R., Homolka, D., Reuter, M., Janeiro, B.K., et al. PIWI slicing and EXD1 drive biogenesis of nuclear piRNAs from cytosolic targets of the mouse piRNA pathway. Mol. Cell 61 (2016), 138–152.