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L1 Regulation in Mouse and Human Germ Cells

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Abstract

One of the most illuminating discoveries emerging from genome sequencing is the abundance of transposable elements in mammalian genomes. The single largest group by mass in the human and mouse genomes is the long interspersed element type 1 (LINE-1, or L1). Among different groups of transposable elements, L1s are unique in that not only do they possess all of the machinery necessary to mobilize themselves, but they are also still actively replicating in the human genome. In order to survive, L1s must pass new insertions to future generations through the germline. Meanwhile, germ cells have evolved elaborate mechanisms to suppress excessive L1 activities. In the past decade, following the initial discovery of mammalian Piwi-interacting RNAs (piRNAs) in 2006, remarkable progress has been made in our understanding of L1 regulation during germ cell development. This review will focus on retrotransposons, especially L1s, and how they are regulated in the mouse and human germlines. We will summarize recent insights into transcriptional and posttranscriptional regulatory mechanisms, including fetal and pachytene piRNAs, DNA methylation, and histone modifications, and provide a synopsis of the interplay between L1s and the host during germ cell development.

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References

  • Abyzov A, Iskow R, Gokcumen O, Radke DW, Balasubramanian S, Pei B, Habegger L, Genomes Project C, Lee C, Gerstein M (2013) Analysis of variable retroduplications in human populations suggests coupling of retrotransposition to cell division. Genome Res 23(12):2042–2052. doi:10.1101/gr.154625.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alzohairy AM, Gyulai G, Jansen RK, Bahieldin A (2013) Transposable elements domesticated and neofunctionalized by eukaryotic genomes. Plasmid 69(1):1–15. doi:10.1016/j.plasmid.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  • An W, Han JS, Schrum CM, Maitra A, Koentgen F, Boeke JD (2008) Conditional activation of a single-copy L1 transgene in mice by Cre. Genesis 46(7):373–383. doi:10.1002/dvg.20407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ancelin K, Lange UC, Hajkova P, Schneider R, Bannister AJ, Kouzarides T, Surani MA (2006) Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8(6):623–630. doi:10.1038/ncb1413

    Article  CAS  PubMed  Google Scholar 

  • 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 (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442(7099):203–207. doi:10.1038/nature04916

    CAS  PubMed  Google Scholar 

  • 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(6):785–799. doi:10.1016/j.molcel.2008.09.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316(5825):744–747. doi:10.1126/science.1142612

    Article  CAS  PubMed  Google Scholar 

  • 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(12):e1000764. doi:10.1371/journal.pgen.1000764

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baltus AE, Menke DB, Hu YC, Goodheart ML, Carpenter AE, de Rooij DG, Page DC (2006) In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet 38(12):1430–1434. doi:10.1038/ng1919

    Article  CAS  PubMed  Google Scholar 

  • Bao J, Yan W (2012) Male germline control of transposable elements. Biol Reprod 86(5):162. doi:10.1095/biolreprod.111.095463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beck CR, Collier P, Macfarlane C, Malig M, Kidd JM, Eichler EE, Badge RM, Moran JV (2010) LINE-1 retrotransposition activity in human genomes. Cell 141(7):1159–1170. doi:10.1016/j.cell.2010.05.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belgnaoui SM, Gosden RG, Semmes OJ, Haoudi A (2006) Human LINE-1 retrotransposon induces DNA damage and apoptosis in cancer cells. Cancer Cell Int 6:13. doi:10.1186/1475-2867-6-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bellve AR, Cavicchia JC, Millette CF, O’Brien DA, Bhatnagar YM, Dym M (1977) Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 74(1):68–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bestor TH (2003) Cytosine methylation mediates sexual conflict. Trends Genet 19(4):185–190. doi:10.1016/S0168-9525(03)00049-0

    Article  CAS  PubMed  Google Scholar 

  • Beyret E, Lin H (2011) Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse. Dev Biol 355(2):215–226. doi:10.1016/j.ydbio.2011.04.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S, Jacobsen SE (2007) UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317(5845):1760–1764. doi:10.1126/science.1147939

    Article  CAS  PubMed  Google Scholar 

  • Bourc’his D, Bestor TH (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431(7004):96–99. doi:10.1038/nature02886

    Article  PubMed  CAS  Google Scholar 

  • Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294(5551):2536–2539. doi:10.1126/science.1065848

    Article  PubMed  Google Scholar 

  • Branciforte D, Martin SL (1994) Developmental and cell type specificity of LINE-1 expression in mouse testis: implications for transposition. Mol Cell Biol 14(4):2584–2592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, Kazazian HH Jr (2003) Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci U S A 100(9):5280–5285. doi:10.1073/pnas.0831042100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulut-Karslioglu A, De La Rosa-Velazquez IA, Ramirez F, Barenboim M, Onishi-Seebacher M, Arand J, Galan C, Winter GE, Engist B, Gerle B, O’Sullivan RJ, Martens JH, Walter J, Manke T, Lachner M, Jenuwein T (2014) Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol Cell 55(2):277–290. doi:10.1016/j.molcel.2014.05.029

    Article  CAS  PubMed  Google Scholar 

  • 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(4):503–514. doi:10.1016/j.devcel.2007.03.001

    Article  CAS  PubMed  Google Scholar 

  • Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B, Friedli M, Duc J, Jang SM, Turelli P, Trono D (2014) Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev 28(13):1397–1409. doi:10.1101/gad.241661.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, Glass JL, Attreed M, Avner P, Wutz A, Barillot E, Greally JM, Voinnet O, Heard E (2010) LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141(6):956–969. doi:10.1016/j.cell.2010.04.042

    Article  CAS  PubMed  Google Scholar 

  • Collins T, Stone JR, Williams AJ (2001) All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol Cell Biol 21(11):3609–3615. doi:10.1128/MCB.21.11.3609-3615.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36(6):653–659. doi:10.1038/ng1367

    Article  CAS  PubMed  Google Scholar 

  • Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, Morell M, O’Shea KS, Moran JV, Gage FH (2009) L1 retrotransposition in human neural progenitor cells. Nature 460(7259):1127–1131. doi:10.1038/nature08248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crichton JH, Playfoot CJ, Adams IR (2014) The role of chromatin modifications in progression through mouse meiotic prophase. J Genet Genomics 41(3):97–106. doi:10.1016/j.jgg.2014.01.003

    Article  CAS  PubMed  Google Scholar 

  • Czech B, Hannon GJ (2016) One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends Biochem Sci 41(4):324–337. doi:10.1016/j.tibs.2015.12.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai L, LaCava J, Taylor MS, Boeke JD (2014) Expression and detection of LINE-1 ORF-encoded proteins. Mob Genet elements 4:e29319. doi:10.4161/mge.29319

    Article  PubMed  PubMed Central  Google Scholar 

  • De Fazio S, Bartonicek N, Di Giacomo M, Abreu-Goodger C, Sankar A, Funaya C, Antony C, Moreira PN, Enright AJ, O’Carroll D (2011) The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 480(7376):259–263. doi:10.1038/nature10547

    Article  PubMed  CAS  Google Scholar 

  • de Rooij DG, Russell LD (2000) All you wanted to know about spermatogonia but were afraid to ask. J Androl 21(6):776–798

    PubMed  Google Scholar 

  • de Souza FS, Franchini LF, Rubinstein M (2013) Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Mol Biol Evol 30(6):1239–1251. doi:10.1093/molbev/mst045

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deguchi K, Nagamatsu G, Miyachi H, Kato Y, Morita S, Kimura H, Kitano S, Hatada I, Saga Y, Tachibana M, Shinkai Y (2013) Posttranscriptional regulation of histone lysine methyltransferase GLP in embryonic male mouse germ cells. Biol Reprod 88(2):36. doi:10.1095/biolreprod.112.103572

    Article  PubMed  CAS  Google Scholar 

  • Deng W, Lin H (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2(6):819–830

    Article  CAS  PubMed  Google Scholar 

  • 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(4):601–608. doi:10.1016/j.molcel.2013.04.026

    Article  PubMed  CAS  Google Scholar 

  • Di Giacomo M, Comazzetto S, Sampath SC, Sampath SC, O’Carroll D (2014) G9a co-suppresses LINE1 elements in spermatogonia. Epigenetics Chromatin 7:24. doi:10.1186/1756-8935-7-24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Donertas D, Sienski G, Brennecke J (2013) Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev 27(15):1693–1705. doi:10.1101/gad.221150.113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Drost JB, Lee WR (1995) Biological basis of germline mutation: comparisons of spontaneous germline mutation rates among drosophila, mouse, and human. Environ Mol Mutagen 25(Suppl 26):48–64

    Article  CAS  PubMed  Google Scholar 

  • Drumond AL, Meistrich ML, Chiarini-Garcia H (2011) Spermatogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach. Reproduction 142(1):145–155. doi:10.1530/REP-10-0431

    Article  CAS  PubMed  Google Scholar 

  • Ergun S, Buschmann C, Heukeshoven J, Dammann K, Schnieders F, Lauke H, Chalajour F, Kilic N, Stratling WH, Schumann GG (2004) Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues. J Biol Chem 279(26):27753–27763

    Article  PubMed  CAS  Google Scholar 

  • Esnault C, Maestre J, Heidmann T (2000) Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24(4):363–367. doi:10.1038/74184

    Article  CAS  PubMed  Google Scholar 

  • Feng Q, Moran JV, Kazazian HH Jr, Boeke JD (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87(5):905–916. doi:10.1016/S0092-8674(00)81997-2

  • 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 U S A 107(26):11847–11852. doi:10.1073/pnas.1007158107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furano AV (2000) The biological properties and evolutionary dynamics of mammalian LINE-1 retrotransposons. Prog Nucleic Acid Res Mol Biol 64:255–294

    Article  CAS  PubMed  Google Scholar 

  • Gasior SL, Wakeman TP, Xu B, Deininger PL (2006) The human LINE-1 retrotransposon creates DNA double-strand breaks. J Mol Biol 357(5):1383–1393. doi:10.1016/j.jmb.2006.01.089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Girard A, Sachidanandam R, Hannon GJ, Carmell MA (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442(7099):199–202. doi:10.1038/nature04917

    PubMed  Google Scholar 

  • Gkountela S, Zhang KX, Shafiq TA, Liao WW, Hargan-Calvopina J, Chen PY, Clark AT (2015) DNA demethylation dynamics in the human prenatal germline. Cell 161(6):1425–1436. doi:10.1016/j.cell.2015.05.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodier JL, Kazazian HH Jr (2008) Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135(1):23–35. doi:10.1016/j.cell.2008.09.022

    Article  CAS  PubMed  Google Scholar 

  • Goodier JL, Ostertag EM, Du K, Kazazian HH Jr (2001) A novel active L1 retrotransposon subfamily in the mouse. Genome Res 11(10):1677–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grandi FC, Rosser JM, Newkirk SJ, Yin J, Jiang X, Xing Z, Whitmore L, Bashir S, Ivics Z, Izsvak Z, Ye P, Yu YE, An W (2015) Retrotransposition creates sloping shores: a graded influence of hypomethylated CpG islands on flanking CpG sites. Genome Res 25(8):1135–1146. doi:10.1101/gr.185132.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grivna ST, Beyret E, Wang Z, Lin H (2006a) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20(13):1709–1714. doi:10.1101/gad.1434406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grivna ST, Pyhtila B, Lin H (2006b) MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci U S A 103(36):13415–13420. doi:10.1073/pnas.0605506103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruppi CM, Wolgemuth DJ (1993) HSP86 and HSP84 exhibit cellular specificity of expression and co-precipitate with an HSP70 family member in the murine testis. Dev Genet 14(2):119–126. doi:10.1002/dvg.1020140206

    Article  CAS  PubMed  Google Scholar 

  • Guo F, Yan L, Guo H, Li L, Hu B, Zhao Y, Yong J, Hu Y, Wang X, Wei Y, Wang W, Li R, Yan J, Zhi X, Zhang Y, Jin H, Zhang W, Hou Y, Zhu P, Li J, Zhang L, Liu S, Ren Y, Zhu X, Wen L, Gao YQ, Tang F, Qiao J (2015) The Transcriptome and DNA Methylome Landscapes of Human Primordial Germ Cells. Cell 161(6):1437–1452. doi:10.1016/j.cell.2015.05.015

    Article  CAS  PubMed  Google Scholar 

  • Ha H, Song J, Wang S, Kapusta A, Feschotte C, Chen KC, Xing J (2014) A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements. BMC Genomics 15:545. doi:10.1186/1471-2164-15-545

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hadziselimovic F, Hadziselimovic NO, Demougin P, Krey G, Oakeley E (2015) Piwi-pathway alteration induces LINE-1 transposon derepression and infertility development in cryptorchidism. Sex Dev 9(2):98–104. doi:10.1159/000375351

    Article  CAS  PubMed  Google Scholar 

  • 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(1-2):15–23, doi:S0925477302001818

    Google Scholar 

  • Hancks DC, Kazazian HH Jr (2016) Roles for retrotransposon insertions in human disease. Mob DNA 7:9. doi:10.1186/s13100-016-0065-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Hata K, Kusumi M, Yokomine T, Li E, Sasaki H (2006) Meiotic and epigenetic aberrations in Dnmt3L-deficient male germ cells. Mol Reprod Dev 73(1):116–122. doi:10.1002/mrd.20387

    Article  CAS  PubMed  Google Scholar 

  • Hata K, Okano M, Lei H, Li E (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129(8):1983–1993

    CAS  PubMed  Google Scholar 

  • Howlett SK, Reik W (1991) Methylation levels of maternal and paternal genomes during preimplantation development. Development 113(1):119–127

    CAS  PubMed  Google Scholar 

  • Ichiyanagi T, Ichiyanagi K, Ogawa A, Kuramochi-Miyagawa S, Nakano T, Chuma S, Sasaki H, Udono H (2014) HSP90alpha plays an important role in piRNA biogenesis and retrotransposon repression in mouse. Nucleic Acids Res 42(19):11903–11911. doi:10.1093/nar/gku881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwasaki YW, Siomi MC, Siomi H (2015) PIWI-interacting RNA: its biogenesis and functions. Annu Rev Biochem 84:405–433. doi:10.1146/annurev-biochem-060614-034258

    Article  CAS  PubMed  Google Scholar 

  • Jacobs FM, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S, Paten B, Salama SR, Haussler D (2014) An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature 516(7530):242–245. doi:10.1038/nature13760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429(6994):900–903. doi:10.1038/nature02633

    Article  CAS  PubMed  Google Scholar 

  • Kano H, Godoy I, Courtney C, Vetter MR, Gerton GL, Ostertag EM, Kazazian HH Jr (2009) L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 23(11):1303–1312. doi:10.1101/gad.1803909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, Kohara Y, Okano M, Li E, Nozaki M, Sasaki H (2007) 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(19):2272–2280. doi:10.1093/hmg/ddm179

    Article  CAS  PubMed  Google Scholar 

  • Keam SP, Young PE, McCorkindale AL, Dang TH, Clancy JL, Humphreys DT, Preiss T, Hutvagner G, Martin DI, Cropley JE, Suter CM (2014) The human Piwi protein Hiwi2 associates with tRNA-derived piRNAs in somatic cells. Nucleic Acids Res 42(14):8984–8995. doi:10.1093/nar/gku620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan H, Smit A, Boissinot S (2006) Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res 16(1):78–87. doi:10.1101/gr.4001406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Gunesdogan U, Zylicz JJ, Hackett JA, Cougot D, Bao S, Lee C, Dietmann S, Allen GE, Sengupta R, Surani MA (2014) PRMT5 protects genomic integrity during global DNA demethylation in primordial germ cells and preimplantation embryos. Mol Cell 56(4):564–579. doi:10.1016/j.molcel.2014.10.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirino Y, Kim N, de Planell-Saguer M, Khandros E, Chiorean S, Klein PS, Rigoutsos I, Jongens TA, Mourelatos Z (2009) Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat Cell Biol 11(5):652–658. doi:10.1038/ncb1872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolosha VO, Martin SL (2003) High-affinity, non-sequence-specific RNA binding by the open reading frame 1 (ORF1) protein from long interspersed nuclear element 1 (LINE-1). J Biol Chem 278(10):8112–8117. doi:10.1074/jbc.M210487200

    Article  CAS  PubMed  Google Scholar 

  • Kubo S, Seleme MC, Soifer HS, Perez JL, Moran JV, Kazazian HH Jr, Kasahara N (2006) L1 retrotransposition in nondividing and primary human somatic cells. Proc Natl Acad Sci U S A 103(21):8036–8041. doi:10.1073/pnas.0601954103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131(4):839–849. doi:10.1242/dev.00973

    Article  CAS  PubMed  Google Scholar 

  • 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(1-2):121–133

    Article  CAS  PubMed  Google Scholar 

  • Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, Hata K, Li E, Matsuda Y, Kimura T, Okabe M, Sakaki Y, Sasaki H, Nakano T (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22(7):908–917. doi:10.1101/gad.1640708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • La Salle S, Oakes CC, Neaga OR, Bourc’his D, Bestor TH, Trasler JM (2007) Loss of spermatogonia and wide-spread DNA methylation defects in newborn male mice deficient in DNMT3L. BMC Dev Biol 7:104. doi:10.1186/1471-213X-7-104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann N, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blocker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowski J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ (2001) Initial sequencing and analysis of the human genome. Nature 409(6822):860–921. doi:10.1038/35057062

    Article  CAS  PubMed  Google Scholar 

  • Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, Reik W (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35(2):88–93. doi:10.1002/gene.10168

    Article  CAS  PubMed  Google Scholar 

  • 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(5785):363–367. doi:10.1126/science.1130164

    Article  CAS  PubMed  Google Scholar 

  • Lees-Murdock DJ, De Felici M, Walsh CP (2003) Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics 82(2):230–237, doi:S0888754303001058

    Google Scholar 

  • Leung DC, Lorincz MC (2012) Silencing of endogenous retroviruses: when and why do histone marks predominate? Trends Biochem Sci 37(4):127–133. doi:10.1016/j.tibs.2011.11.006

    Article  CAS  PubMed  Google Scholar 

  • Li E, Bestor TH, Jaenisch R (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69(6):915–926

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Dai H, Martos SN, Xu B, Gao Y, Li T, Zhu G, Schones DE, Wang Z (2015a) Distinct roles of DNMT1-dependent and DNMT1-independent methylation patterns in the genome of mouse embryonic stem cells. Genome Biol 16:115. doi:10.1186/s13059-015-0685-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Z, Yu J, Hosohama L, Nee K, Gkountela S, Chaudhari S, Cass AA, Xiao X, Clark AT (2015b) The Sm protein methyltransferase PRMT5 is not required for primordial germ cell specification in mice. EMBO J 34(6):748–758. doi:10.15252/embj.201489319

    Article  CAS  PubMed  Google Scholar 

  • Lim AK, Lorthongpanich C, Chew TG, Tan CW, Shue YT, Balu S, Gounko N, Kuramochi-Miyagawa S, Matzuk MM, Chuma S, Messerschmidt DM, Solter D, Knowles BB (2013) The nuage mediates retrotransposon silencing in mouse primordial ovarian follicles. Development 140(18):3819–3825. doi:10.1242/dev.099184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Brind’Amour J, Karimi MM, Shirane K, Bogutz A, Lefebvre L, Sasaki H, Shinkai Y, Lorincz MC (2014) Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells. Genes Dev 28(18):2041–2055. doi:10.1101/gad.244848.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macfarlan TS, Gifford WD, Agarwal S, Driscoll S, Lettieri K, Wang J, Andrews SE, Franco L, Rosenfeld MG, Ren B, Pfaff SL (2011) Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev 25(6):594–607. doi:10.1101/gad.2008511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magiorkinis G, Blanco-Melo D, Belshaw R (2015) The decline of human endogenous retroviruses: extinction and survival. Retrovirology 12:8. doi:10.1186/s12977-015-0136-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maksakova IA, Romanish MT, Gagnier L, Dunn CA, van de Lagemaat LN, Mager DL (2006) Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet 2(1):e2. doi:10.1371/journal.pgen.0020002

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Malki S, van der Heijden GW, O’Donnell KA, Martin SL, Bortvin A (2014) A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev Cell 29(5):521–533. doi:10.1016/j.devcel.2014.04.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manakov SA, Pezic D, Marinov GK, Pastor WA, Sachidanandam R, Aravin AA (2015) MIWI2 and MILI have differential effects on piRNA biogenesis and DNA methylation. Cell Rep 12(8):1234–1243. doi:10.1016/j.celrep.2015.07.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin SL, Cruceanu M, Branciforte D, Wai-Lun Li P, Kwok SC, Hodges RS, Williams MC (2005) LINE-1 retrotransposition requires the nucleic acid chaperone activity of the ORF1 protein. J Mol Biol 348(3):549–561. doi:10.1016/j.jmb.2005.03.003

    Article  CAS  PubMed  Google Scholar 

  • Mathias SL, Scott AF, Kazazian HH Jr, Boeke JD, Gabriel A (1991) Reverse transcriptase encoded by a human transposable element. Science 254(5039):1808–1810

    Article  CAS  PubMed  Google Scholar 

  • McGee EA, Hsueh AJ (2000) Initial and cyclic recruitment of ovarian follicles. Endocr Rev 21(2):200–214. doi:10.1210/edrv.21.2.0394

    CAS  PubMed  Google Scholar 

  • McLaren A (2001) Mammalian germ cells: birth, sex, and immortality. Cell Struct Funct 26(3):119–122

    Article  CAS  PubMed  Google Scholar 

  • Medstrand P, van de Lagemaat LN, Mager DL (2002) Retroelement distributions in the human genome: variations associated with age and proximity to genes. Genome Res 12(10):1483–1495. doi:10.1101/gr.388902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messerschmidt DM, Knowles BB, Solter D (2014) DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos. Genes Dev 28(8):812–828. doi:10.1101/gad.234294.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(14):1544–1549. doi:10.1101/gad.244350.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran JV, DeBerardinis RJ, Kazazian HH Jr (1999) Exon shuffling by L1 retrotransposition. Science 283(5407):1530–1534

    Article  CAS  PubMed  Google Scholar 

  • Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH Jr (1996) High frequency retrotransposition in cultured mammalian cells. Cell 87(5):917–927. doi:10.1016/S0092-8674(00)81998-4

    Article  CAS  PubMed  Google Scholar 

  • Muerdter F, Guzzardo PM, Gillis J, Luo Y, Yu Y, Chen C, Fekete R, Hannon GJ (2013) A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in Drosophila. Mol Cell 50(5):736–748. doi:10.1016/j.molcel.2013.04.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K, Gage FH (2010) L1 retrotransposition in neurons is modulated by MeCP2. Nature 468(7322):443–446. doi:10.1038/nature09544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nebel BR, Amarose AP, Hacket EM (1961) Calendar of gametogenic development in the prepuberal male mouse. Science 134:832–833

    Article  CAS  PubMed  Google Scholar 

  • Nellaker C, Keane TM, Yalcin B, Wong K, Agam A, Belgard TG, Flint J, Adams DJ, Frankel WN, Ponting CP (2012) The genomic landscape shaped by selection on transposable elements across 18 mouse strains. Genome Biol 13(6):R45. doi:10.1186/gb-2012-13-6-r45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Donnell KA, An W, Schrum CT, Wheelan SJ, Boeke JD (2013) Controlled insertional mutagenesis using a LINE-1 (ORFeus) gene-trap mouse model. Proc Natl Acad Sci U S A 110(29):E2706–E2713. doi:10.1073/pnas.1302504110

    Article  PubMed  PubMed Central  Google Scholar 

  • Oakberg EF (1957) Duration of spermatogenesis in the mouse. Nature 180(4595):1137–1138

    Article  CAS  PubMed  Google Scholar 

  • Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM (2007) Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol 307(2):368–379. doi:10.1016/j.ydbio.2007.05.002

    Article  CAS  PubMed  Google Scholar 

  • Ohno R, Nakayama M, Naruse C, Okashita N, Takano O, Tachibana M, Asano M, Saitou M, Seki Y (2013) A replication-dependent passive mechanism modulates DNA demethylation in mouse primordial germ cells. Development 140(14):2892–2903. doi:10.1242/dev.093229

    Article  CAS  PubMed  Google Scholar 

  • Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99(3):247–257

    Article  CAS  PubMed  Google Scholar 

  • Pepling ME (2006) From primordial germ cell to primordial follicle: mammalian female germ cell development. Genesis 44(12):622–632. doi:10.1002/dvg.20258

    Article  CAS  PubMed  Google Scholar 

  • Pepling ME, Spradling AC (2001) Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 234(2):339–351. doi:10.1006/dbio.2001.0269

    Article  CAS  PubMed  Google Scholar 

  • Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107(3):323–337, doi:S0092-8674(01)00542-6

    Google Scholar 

  • Peters H (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinol 62(1):98–116

    CAS  PubMed  Google Scholar 

  • Peters H (1970) Migration of gonocytes into the mammalian gonad and their differentiation. Philos Trans R Soc Lond B Biol Sci 259(828):91–101

    Article  CAS  PubMed  Google Scholar 

  • Pezic D, Manakov SA, Sachidanandam R, Aravin AA (2014) piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev 28(13):1410–1428. doi:10.1101/gad.240895.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puszyk W, Down T, Grimwade D, Chomienne C, Oakey RJ, Solomon E, Guidez F (2013) The epigenetic regulator PLZF represses L1 retrotransposition in germ and progenitor cells. EMBO J 32(13):1941–1952. doi:10.1038/emboj.2013.118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rebollo R, Karimi MM, Bilenky M, Gagnier L, Miceli-Royer K, Zhang Y, Goyal P, Keane TM, Jones S, Hirst M, Lorincz MC, Mager DL (2011) Retrotransposon-Induced Heterochromatin Spreading in the Mouse Revealed by Insertional Polymorphisms. PLoS Genet 7(9):e1002301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rebollo R, Romanish MT, Mager DL (2012) Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46:21–42. doi:10.1146/annurev-genet-110711-155621

    Article  CAS  PubMed  Google Scholar 

  • 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(7376):264–267. doi:10.1038/nature10672

    Article  CAS  PubMed  Google Scholar 

  • Roovers EF, Rosenkranz D, Mahdipour M, Han CT, He N, Chuva de Sousa Lopes SM, Van der Westerlaken LA, Zischler H, Butter F, Roelen BA, Ketting RF (2015) Piwi proteins and piRNAs in mammalian oocytes and early embryos. Cell Rep 10(12):2069–2082. doi:10.1016/j.celrep.2015.02.062

    Article  CAS  PubMed  Google Scholar 

  • Rosser JM, An W (2012) L1 expression and regulation in humans and rodents. Front Biosci (Elite Ed) 4:2203–2225

    Article  PubMed Central  Google Scholar 

  • Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, Spitz F, Constam DB, Trono D (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463(7278):237–240. doi:10.1038/nature08674

    Article  CAS  PubMed  Google Scholar 

  • Saitou M, Yamaji M (2012) Primordial germ cells in mice. Cold Spring Harb Perspect Biol 4(11):pii: a008375. doi:10.1101/cshperspect.a008375

    Article  CAS  Google Scholar 

  • Sanford JP, Clark HJ, Chapman VM, Rossant J (1987) Differences in DNA methylation during oogenesis and spermatogenesis and their persistence during early embryogenesis in the mouse. Genes Dev 1(10):1039–1046

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Shiohama A, Minoshima S, Shimizu N (2003) Identification of eight members of the Argonaute family in the human genome. Genomics 82(3):323–330

    Article  CAS  PubMed  Google Scholar 

  • Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, Popp C, Thienpont B, Dean W, Reik W (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48(6):849–862. doi:10.1016/j.molcel.2012.11.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y (2005) Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 278(2):440–458. doi:10.1016/j.ydbio.2004.11.025

    Article  CAS  PubMed  Google Scholar 

  • Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, Tajima S, Mitsuya K, Okano M, Koseki H (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450(7171):908–912. doi:10.1038/nature06397

    Article  CAS  PubMed  Google Scholar 

  • Shi X, Seluanov A, Gorbunova V (2007) Cell divisions are required for L1 retrotransposition. Mol Cell Biol 27(4):1264–1270. doi:10.1128/MCB.01888-06

    Article  CAS  PubMed  Google Scholar 

  • Smit AF (1999) Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr Opin Genet Dev 9(6):657–663, doi:S0959-437X(99)00031-3

    Article  CAS  PubMed  Google Scholar 

  • Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, Meissner A (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484(7394):339–344. doi:10.1038/nature10960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(2):285–297. doi:10.1016/j.devcel.2008.05.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szak ST, Pickeral OK, Makalowski W, Boguski MS, Landsman D, Boeke JD (2002) Molecular archeology of L1 insertions in the human genome. Genome Biol 3(10):research0052

    Article  PubMed  PubMed Central  Google Scholar 

  • Tachibana M, Nozaki M, Takeda N, Shinkai Y (2007) Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J 26(14):3346–3359. doi:10.1038/sj.emboj.7601767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453(7194):534–538. doi:10.1038/nature06904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang WW, Dietmann S, Irie N, Leitch HG, Floros VI, Bradshaw CR, Hackett JA, Chinnery PF, Surani MA (2015) A unique gene regulatory network resets the human germline epigenome for development. Cell 161(6):1453–1467. doi:10.1016/j.cell.2015.04.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 U S A 92(5):1520–1524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turelli P, Castro-Diaz N, Marzetta F, Kapopoulou A, Raclot C, Duc J, Tieng V, Quenneville S, Trono D (2014) Interplay of TRIM28 and DNA methylation in controlling human endogenous retroelements. Genome Res 24(8):1260–1270. doi:10.1101/gr.172833.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unhavaithaya Y, Hao Y, Beyret E, Yin H, Kuramochi-Miyagawa S, Nakano T, Lin H (2009) MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J Biol Chem 284(10):6507–6519. doi:10.1074/jbc.M809104200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(15):1749–1762. doi:10.1101/gad.1814809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Meyenn F, Reik W (2015) Forget the parents: epigenetic reprogramming in human germ cells. Cell 161(6):1248–1251. doi:10.1016/j.cell.2015.05.039

    Article  CAS  Google Scholar 

  • Vourekas A, Zheng K, Fu Q, Maragkakis M, Alexiou P, Ma J, Pillai RS, Mourelatos Z, Wang PJ (2015) The RNA helicase MOV10L1 binds piRNA precursors to initiate piRNA processing. Genes Dev 29(6):617–629. doi:10.1101/gad.254631.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallace NA, Belancio VP, Deininger PL (2008) L1 mobile element expression causes multiple types of toxicity. Gene 419(1-2):75–81. doi:10.1016/j.gene.2008.04.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh CP, Chaillet JR, Bestor TH (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20(2):116–117. doi:10.1038/2413

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Zhu T, Li Q, Liu C, Han F, Chen M, Zhang L, Cui X, Qin Y, Bao S, Gao F (2015) Prmt5 is required for germ cell survival during spermatogenesis in mice. Sci Rep 5:11031. doi:10.1038/srep11031

    Article  PubMed  PubMed Central  Google Scholar 

  • 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: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 20(13):1732–1743. doi:10.1101/gad.1425706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, Surani MA, Sakaki Y, Sasaki H (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453(7194):539–543. doi:10.1038/nature06908

    Article  CAS  PubMed  Google Scholar 

  • Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P, Botcherby M, Bray N, Brent MR, Brown DG, Brown SD, Bult C, Burton J, Butler J, Campbell RD, Carninci P, Cawley S, Chiaromonte F, Chinwalla AT, Church DM, Clamp M, Clee C, Collins FS, Cook LL, Copley RR, Coulson A, Couronne O, Cuff J, Curwen V, Cutts T, Daly M, David R, Davies J, Delehaunty KD, Deri J, Dermitzakis ET, Dewey C, Dickens NJ, Diekhans M, Dodge S, Dubchak I, Dunn DM, Eddy SR, Elnitski L, Emes RD, Eswara P, Eyras E, Felsenfeld A, Fewell GA, Flicek P, Foley K, Frankel WN, Fulton LA, Fulton RS, Furey TS, Gage D, Gibbs RA, Glusman G, Gnerre S, Goldman N, Goodstadt L, Grafham D, Graves TA, Green ED, Gregory S, Guigo R, Guyer M, Hardison RC, Haussler D, Hayashizaki Y, Hillier LW, Hinrichs A, Hlavina W, Holzer T, Hsu F, Hua A, Hubbard T, Hunt A, Jackson I, Jaffe DB, Johnson LS, Jones M, Jones TA, Joy A, Kamal M, Karlsson EK, Karolchik D, Kasprzyk A, Kawai J, Keibler E, Kells C, Kent WJ, Kirby A, Kolbe DL, Korf I, Kucherlapati RS, Kulbokas EJ, Kulp D, Landers T, Leger JP, Leonard S, Letunic I, Levine R, Li J, Li M, Lloyd C, Lucas S, Ma B, Maglott DR, Mardis ER, Matthews L, Mauceli E, Mayer JH, McCarthy M, McCombie WR, McLaren S, McLay K, McPherson JD, Meldrim J, Meredith B, Mesirov JP, Miller W, Miner TL, Mongin E, Montgomery KT, Morgan M, Mott R, Mullikin JC, Muzny DM, Nash WE, Nelson JO, Nhan MN, Nicol R, Ning Z, Nusbaum C, O’Connor MJ, Okazaki Y, Oliver K, Overton-Larty E, Pachter L, Parra G, Pepin KH, Peterson J, Pevzner P, Plumb R, Pohl CS, Poliakov A, Ponce TC, Ponting CP, Potter S, Quail M, Reymond A, Roe BA, Roskin KM, Rubin EM, Rust AG, Santos R, Sapojnikov V, Schultz B, Schultz J, Schwartz MS, Schwartz S, Scott C, Seaman S, Searle S, Sharpe T, Sheridan A, Shownkeen R, Sims S, Singer JB, Slater G, Smit A, Smith DR, Spencer B, Stabenau A, Stange-Thomann N, Sugnet C, Suyama M, Tesler G, Thompson J, Torrents D, Trevaskis E, Tromp J, Ucla C, Ureta-Vidal A, Vinson JP, Von Niederhausern AC, Wade CM, Wall M, Weber RJ, Weiss RB, Wendl MC, West AP, Wetterstrand K, Wheeler R, Whelan S, Wierzbowski J, Willey D, Williams S, Wilson RK, Winter E, Worley KC, Wyman D, Yang S, Yang SP, Zdobnov EM, Zody MC, Lander ES (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420(6915):520–562. doi:10.1038/nature01262

    Article  CAS  PubMed  Google Scholar 

  • Webster KE, O’Bryan MK, Fletcher S, Crewther PE, Aapola U, Craig J, Harrison DK, Aung H, Phutikanit N, Lyle R, Meachem SJ, Antonarakis SE, de Kretser DM, Hedger MP, Peterson P, Carroll BJ, Scott HS (2005) Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc Natl Acad Sci U S A 102(11):4068–4073. doi:10.1073/pnas.0500702102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Western PS, Miles DC, van den Bergen JA, Burton M, Sinclair AH (2008) Dynamic regulation of mitotic arrest in fetal male germ cells. Stem Cells 26(2):339–347. doi:10.1634/stemcells.2007-0622

    Article  CAS  PubMed  Google Scholar 

  • Williams Z, Morozov P, Mihailovic A, Lin C, Puvvula PK, Juranek S, Rosenwaks Z, Tuschl T (2015) Discovery and characterization of piRNAs in the human fetal ovary. Cell Rep 13(4):854–863. doi:10.1016/j.celrep.2015.09.030

    Article  CAS  PubMed  Google Scholar 

  • Wolf G, Greenberg D, Macfarlan TS (2015) Spotting the enemy within: targeted silencing of foreign DNA in mammalian genomes by the Kruppel-associated box zinc finger protein family. Mob DNA 6:17. doi:10.1186/s13100-015-0050-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xie Y, Mates L, Ivics Z, Izsvak Z, Martin SL, An W (2013) Cell division promotes efficient retrotransposition in a stable L1 reporter cell line. Mob DNA 4(1):10. doi:10.1186/1759-8753-4-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Q, Hua J, Wang L, Xu B, Zhang H, Ye N, Zhang Z, Yu D, Cooke HJ, Zhang Y, Shi Q (2013) MicroRNA and piRNA profiles in normal human testis detected by next generation sequencing. PLoS One 8(6):e66809. doi:10.1371/journal.pone.0066809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, Nabeshima Y (2006) The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 133(8):1495–1505. doi:10.1242/dev.02316

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura T, Toyoda S, Kuramochi-Miyagawa S, Miyazaki T, Miyazaki S, Tashiro F, Yamato E, Nakano T, Miyazaki J (2009) 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(1):216–227. doi:10.1016/j.ydbio.2009.09.003

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Gu J, Jin Y, Luo Y, Preall JB, Ma J, Czech B, Hannon GJ (2015) Panoramix enforces piRNA-dependent cotranscriptional silencing. Science 350(6258):339–342. doi:10.1126/science.aab0700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zamudio N, Barau J, Teissandier A, Walter M, Borsos M, Servant N, Bourc’his D (2015) DNA methylation restrains transposons from adopting a chromatin signature permissive for meiotic recombination. Genes Dev 29(12):1256–1270. doi:10.1101/gad.257840.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zamudio N, Bourc’his D (2010) Transposable elements in the mammalian germline: a comfortable niche or a deadly trap? Heredity 105(1):92–104. doi:10.1038/hdy.2010.53

    Article  CAS  PubMed  Google Scholar 

  • Zemojtel T, Penzkofer T, Schultz J, Dandekar T, Badge R, Vingron M (2007) Exonization of active mouse L1s: a driver of transcriptome evolution? BMC Genomics 8:392. doi:10.1186/1471-2164-8-392

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng K, Wang PJ (2012) Blockade of pachytene piRNA biogenesis reveals a novel requirement for maintaining post-meiotic germline genome integrity. PLoS Genet 8(11), e1003038. doi:10.1371/journal.pgen.1003038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng K, Xiol J, Reuter M, Eckardt S, Leu NA, McLaughlin KJ, Stark A, Sachidanandam R, Pillai RS, Wang PJ (2010) 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(26):11841–11846. doi:10.1073/pnas.1003953107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Research in our laboratory is supported by the National Institutes of Health (NIH) grants R21OD017965, R21HD080143, and P50GM107632. SN was supported, in part, by NIH award T32GM008336. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

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Correspondence to Wenfeng An .

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Newkirk, S.J., An, W. (2017). L1 Regulation in Mouse and Human Germ Cells. In: Cristofari, G. (eds) Human Retrotransposons in Health and Disease. Springer, Cham. https://doi.org/10.1007/978-3-319-48344-3_2

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