Retrotransposons shape species-specific embryonic stem cell gene expression

Retrovirology

Volumn 12, Issue 1, 2015, Pages

  Robbez Masson, Luisa ^a   Rowe, Helen M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 2; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNTRANSLATED RNA; RETROPOSON;

DNA BINDING; EMBRYONIC STEM CELL; ENDOGENOUS RETROVIRUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE REPRESSION; HUMAN; LONG TERMINAL REPEAT; MOLECULAR EVOLUTION; NONHUMAN; OPEN READING FRAME; PROMOTER REGION; PROTEIN BINDING; PROTEIN CROSS LINKING; RETROPOSON; REVIEW; SPECIES DIFFERENCE; TISSUE SPECIFICITY; TRANSGENE; UBIQUITINATION; VARIABLE NUMBER OF TANDEM REPEAT; VIRUS GENOME; GENE EXPRESSION REGULATION; PHYSIOLOGY;

HUMAN ENDOGENOUS RETROVIRUS H;

EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HUMANS; RETROELEMENTS;

EID: 84930205085     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-015-0173-5     Document Type: Review

References (116)

1. de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7(12):e1002384. doi: 10.1371/journal.pgen.1002384.
2. Lamprecht B, Walter K, Kreher S, Kumar R, Hummel M, Lenze D et al (2010) Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat Med 16(5):571-579. doi: 10.1038/nm.2129(1p following 9) .
3. Nexo BA, Christensen T, Frederiksen J, Moller-Larsen A, Oturai AB, Villesen P et al (2011) The etiology of multiple sclerosis: genetic evidence for the involvement of the human endogenous retrovirus HERV-Fc1. PLoS One 6(2):e16652. doi: 10.1371/journal.pone.0016652.
4. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819):154-156
5. Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X et al (2010) Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 6(5):468-478. doi: 10.1016/j.stem.2010.03.015.
6. Marks H, Kalkan T, Menafra R, Denissov S, Jones K, Hofemeister H et al (2012) The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149(3):590-604. doi: 10.1016/j.cell.2012.03.026.
7. Nichols J, Smith A (2009) Naive and primed pluripotent states. Cell Stem Cell 4(6):487-492. doi: 10.1016/j.stem.2009.05.015.
8. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J et al (2008) The ground state of embryonic stem cell self-renewal. Nature 453(7194):519-523. doi: 10.1038/nature06968.
9. Nichols J, Smith A (2011) The origin and identity of embryonic stem cells. Development. 138(1):3-8. doi: 10.1242/dev.050831.
10. Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM, Bonanomi D et al (2012) Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487(7405):57-63. doi: 10.1038/nature11244.
11. Kigami D, Minami N, Takayama H, Imai H (2003) MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol Reprod 68(2):651-654
12. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL et al (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448(7150):196-199. doi: 10.1038/nature05972.
13. Gafni O, Weinberger L, Mansour AA, Manor YS, Chomsky E, Ben-Yosef D et al (2013) Derivation of novel human ground state naive pluripotent stem cells. Nature 504(7479):282-286. doi: 10.1038/nature12745.
14. Takashima Y, Guo G, Loos R, Nichols J, Ficz G, Krueger F et al (2014) Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158(6):1254-1269. doi: 10.1016/j.cell.2014.08.029.
15. Theunissen TW, Powell BE, Wang H, Mitalipova M, Faddah DA, Reddy J et al (2014) Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell 15(4):471-487. doi: 10.1016/j.stem.2014.07.002.
16. Hanna J, Cheng AW, Saha K, Kim J, Lengner CJ, Soldner F et al (2010) Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci 107(20):9222-9227. doi: 10.1073/pnas.1004584107.
17. Ohnuki M, Tanabe K, Sutou K, Teramoto I, Sawamura Y, Narita M et al (2014) Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential. Proc Natl Acad Sci 111(34):12426-12431. doi: 10.1073/pnas.1413299111.
18. Santoni FA, Guerra J, Luban J (2012) HERV-H RNA is abundant in human embryonic stem cells and a precise marker for pluripotency. Retrovirology 9:111. doi: 10.1186/1742-4690-9-111.
19. Wang J, Xie G, Singh M, Ghanbarian AT, Rasko T, Szvetnik A et al (2014) Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells. Nature 516(7531):405-409. doi: 10.1038/nature13804.
20. Jacques PE, Jeyakani J, Bourque G (2013) The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 9(5):e1003504. doi: 10.1371/journal.pgen.1003504.
21. Garcia-Perez JL, Marchetto MC, Muotri AR, Coufal NG, Gage FH, O'Shea KS et al (2007) LINE-1 retrotransposition in human embryonic stem cells. Hum Mol Genet 16(13):1569-1577. doi: 10.1093/hmg/ddm105.
22. Narva E, Rahkonen N, Emani MR, Lund R, Pursiheimo JP, Nasti J et al (2012) RNA-binding protein L1TD1 interacts with LIN28 via RNA and is required for human embryonic stem cell self-renewal and cancer cell proliferation. Stem Cells 30(3):452-460. doi: 10.1002/stem.1013.
23. Martello G, Bertone P, Smith A (2013) Identification of the missing pluripotency mediator downstream of leukaemia inhibitory factor. EMBO J 32(19):2561-2574. doi: 10.1038/emboj.2013.177.
24. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS et al (2010) Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42(7):631-634. doi: 10.1038/ng.600.
25. Schmidt D, Schwalie PC, Wilson MD, Ballester B, Goncalves A, Kutter C et al (2012) Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148(1-2):335-348. doi: 10.1016/j.cell.2011.11.058.
26. Bourque G, Leong B, Vega VB, Chen X, Lee YL, Srinivasan KG et al (2008) Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18(11):1752-1762. doi: 10.1101/gr.080663.108.
27. Fort A, Hashimoto K, Yamada D, Salimullah M, Keya CA, Saxena A et al (2014) Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance. Nat Genet 46(6):558-566. doi: 10.1038/ng.2965.
28. Rowe HM, Kapopoulou A, Corsinotti A, Fasching L, Macfarlan TS, Tarabay Y et al (2013) TRIM28 repression of retrotransposon-based enhancers is necessary to preserve transcriptional dynamics in embryonic stem cells. Genome Res 23(3):452-461. doi: 10.1101/gr.147678.112.
29. Goke J, Lu X, Chan YS, Ng HH, Ly LH, Sachs F et al (2015) Dynamic transcription of distinct classes of endogenous retroviral elements marks specific populations of early human embryonic cells. Cell Stem Cell 16(2):135-141. doi: 10.1016/j.stem.2015.01.005.
30. Svoboda P, Stein P, Anger M, Bernstein E, Hannon GJ, Schultz RM et al (2004) RNAi and expression of retrotransposons MuERV-L and IAP in preimplantation mouse embryos. Dev Biol 269(1):276-285. doi: 10.1016/j.ydbio.2004.01.028.
31. Villar D, Berthelot C, Aldridge S, Rayner TF, Lukk M, Pignatelli M et al (2015) Enhancer evolution across 20 mammalian species. Cell 160(3):554-566. doi: 10.1016/j.cell.2015.01.006.
32. Lu X, Sachs F, Ramsay L, Jacques PE, Goke J, Bourque G et al (2014) The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat Struct Mol Biol 21(4):423-425. doi: 10.1038/nsmb.2799.
33. Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH et al (2010) Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42(12):1113-1117. doi: 10.1038/ng.710.
34. Ng SY, Johnson R, Stanton LW (2012) Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J 31(3):522-533. doi: 10.1038/emboj.2011.459.
35. Friedli M, Turelli P, Kapopoulou A, Rauwel B, Castro-Diaz N, Rowe HM et al (2014) Loss of transcriptional control over endogenous retroelements during reprogramming to pluripotency. Genome Res 24(8):1251-1259. doi: 10.1101/gr.172809.114.
36. Geisler S, Coller J (2013) RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nat Rev Mol Cell Biol 14(11):699-712. doi: 10.1038/nrm3679.
37. Wissing S, Munoz-Lopez M, Macia A, Yang Z, Montano M, Collins W et al (2012) Reprogramming somatic cells into iPS cells activates LINE-1 retroelement mobility. Hum Mol Genet 21(1):208-218. doi: 10.1093/hmg/ddr455.
38. Chuong EB, Rumi MA, Soares MJ, Baker JC (2013) Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat Genet 45(3):325-329. doi: 10.1038/ng.2553.
39. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB et al (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133(6):1106-1117. doi: 10.1016/j.cell.2008.04.043.
40. Cromack AS (1968) An electron microscope study of virus-like particles in chick embryo and L cell cultures. J Gen Virol 2(1):195-198
41. Calarco PG (1979) Intracisternal A particles in preimplantation embryos of feral mice (Mus musculus). Intervirology 11(6):321-325
42. Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis F et al (2015) Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci 112(5):E487-E496. doi: 10.1073/pnas.1417000112.
43. 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.
44. McLaughlin RN Jr, Young JM, Yang L, Neme R, Wichman HA, Malik HS et al (2014) Positive selection and multiple losses of the LINE-1-derived L1TD1 gene in mammals suggest a dual role in genome defense and pluripotency. PLoS Genet 10(9):e1004531. doi: 10.1371/journal.pgen.1004531.
45. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F et al (2011) Somatic retrotransposition alters the genetic landscape of the human brain. Nature 479(7374):534-537. doi: 10.1038/nature10531.
46. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT et al (2009) L1 retrotransposition in human neural progenitor cells. Nature 460(7259):1127-1131. doi: 10.1038/nature08248.
47. Evrony GD, Cai X, Lee E, Hills LB, Elhosary PC, Lehmann HS et al (2012) Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell 151(3):483-496. doi: 10.1016/j.cell.2012.09.035.
48. Muotri AR, Chu VT, Marchetto MC, Deng W, Moran JV, Gage FH et al (2005) Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435(7044):903-910. doi: 10.1038/nature03663.
49. Grow EJ, Flynn RA, Chavez SL, Bayless NL, Wossidlo M, Wesche DJ et al (2015) Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature. doi: 10.1038/nature14308.
50. Crichton JH, Dunican DS, Maclennan M, Meehan RR, Adams IR (2014) Defending the genome from the enemy within: mechanisms of retrotransposon suppression in the mouse germline. Cell Mol Life Sci 71(9):1581-1605. doi: 10.1007/s00018-013-1468-0.
51. Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B, Friedli M et al (2014) Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev 28(13):1397-1409. doi: 10.1101/gad.241661.114.
52. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H et al (2010) Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464(7290):927-931. doi: 10.1038/nature08858.
53. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T et al (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463(7278):237-240. doi: 10.1038/nature08674.
54. Turelli P, Castro-Diaz N, Marzetta F, Kapopoulou A, Raclot C, Duc J et al (2014) Interplay of TRIM28 and DNA methylation in controlling human endogenous retroelements. Genome Res 24(8):1260-1270. doi: 10.1101/gr.172833.114.
55. Wolf D, Goff SP (2007) TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 131(1):46-57. doi: 10.1016/j.cell.2007.07.026.
56. Wolf D, Goff SP (2009) Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 458(7242):1201-1204. doi: 10.1038/nature07844.
57. Leung DC, Lorincz MC (2011) 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.
58. Rowe HM, Trono D (2011) Dynamic control of endogenous retroviruses during development. Virology 411(2):273-287. doi: 10.1016/j.virol.2010.12.007.
59. Rowe HM, Friedli M, Offner S, Verp S, Mesnard D, Marquis J et al (2013) De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET. Development 140(3):519-529. doi: 10.1242/dev.087585.
60. Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, Tang JX et al (2011) DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8(6):676-687. doi: 10.1016/j.stem.2011.04.004.
61. Rebollo R, Karimi MM, Bilenky M, Gagnier L, Miceli-Royer K, Zhang Y et al (2011) Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms. PLoS Genet 7(9):e1002301. doi: 10.1371/journal.pgen.1002301.
62. Konkel MK, Batzer MA (2010) A mobile threat to genome stability: the impact of non-LTR retrotransposons upon the human genome. Semin Cancer Biol 20(4):211-221. doi: 10.1016/j.semcancer.2010.03.001.
63. Hutnick LK, Huang X, Loo TC, Ma Z, Fan G (2010) Repression of retrotransposal elements in mouse embryonic stem cells is primarily mediated by a DNA methylation-independent mechanism. J Biol Chem 285(27):21082-21091. doi: 10.1074/jbc.M110.125674.
64. 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.
65. Fasching L, Kapopoulou A, Sachdeva R, Petri R, Jonsson ME, Manne C et al (2015) TRIM28 represses transcription of endogenous retroviruses in neural progenitor cells. Cell Rep. 10(1):20-28. doi: 10.1016/j.celrep.2014.12.004.
66. Teich NM, Weiss RA, Martin GR, Lowy DR (1977) Virus infection of murine teratocarcinoma stem cell lines. Cell 12(4):973-982 (pii:0092-8674(77)90162-3)
67. Barklis E, Mulligan RC, Jaenisch R (1986) Chromosomal position or virus mutation permits retrovirus expression in embryonal carcinoma cells. Cell 47(3):391-399 (pii:0092-8674(86)90596-9)
68. Colicelli J, Goff SP (1986) Isolation of a recombinant murine leukemia virus utilizing a new primer tRNA. J Virol 57(1):37-45
69. Schlesinger S, Goff SP (2013) Silencing of proviruses in embryonic cells: efficiency, stability and chromatin modifications. EMBO Rep 14(1):73-79. doi: 10.1038/embor.2012.182.
70. Schlesinger S, Lee AH, Wang GZ, Green L, Goff SP (2013) Proviral silencing in embryonic cells is regulated by Yin Yang 1. Cell Rep. 4(1):50-58. doi: 10.1016/j.celrep.2013.06.003.
71. Wang GZ, Wolf D, Goff SP (2014) EBP1, a novel host factor involved in primer binding site-dependent restriction of moloney murine leukemia virus in embryonic cells. J Virol 88(3):1825-1829. doi: 10.1128/JVI.02578-13.
72. Schlesinger S, Goff SP (2015) Retroviral transcriptional regulation and embryonic stem cells: war and peace. Mol Cell Biol 35(5):770-777. doi: 10.1128/MCB.01293-14.
73. Wolf G, Yang P, Fuchtbauer AC, Fuchtbauer EM, Silva AM, Park C et al (2015) The KRAB zinc finger protein ZFP809 is required to initiate epigenetic silencing of endogenous retroviruses. Genes Dev 29(5):538-554. doi: 10.1101/gad.252767.114.
74. Corsinotti A, Kapopoulou A, Gubelmann C, Imbeault M, Santoni de Sio FR, Rowe HM et al (2014) Global and stage specific patterns of Kruppel-associated-box zinc finger protein gene expression in murine early embryonic cells. PLoS One 8(2):e56721. doi: 10.1371/journal.pone.0056721.
75. Emerson RO, Thomas JH (2009) Adaptive evolution in zinc finger transcription factors. PLoS Genet 5(1):e1000325. doi: 10.1371/journal.pgen.1000325.
76. Liu H, Chang LH, Sun Y, Lu X, Stubbs L (2014) Deep vertebrate roots for mammalian zinc finger transcription factor subfamilies. Genome Biol Evol 6(3):510-525. doi: 10.1093/gbe/evu030.
77. Lukic S, Nicolas JC, Levine AJ (2014) The diversity of zinc-finger genes on human chromosome 19 provides an evolutionary mechanism for defense against inherited endogenous retroviruses. Cell Death Differ 21(3):381-387. doi: 10.1038/cdd.2013.150.
78. Thomas JH, Schneider S (2011) Coevolution of retroelements and tandem zinc finger genes. Genome Res 21(11):1800-1812. doi: 10.1101/gr.121749.111.
79. Hamilton AT, Huntley S, Tran-Gyamfi M, Baggott DM, Gordon L, Stubbs L (2006) Evolutionary expansion and divergence in the ZNF91 subfamily of primate-specific zinc finger genes. Genome Res 16(5):584-594. doi: 10.1101/gr.4843906.
80. Jacobs FM, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S et al (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.
81. Hancks DC, Kazazian HH Jr (2010) SVA retrotransposons: evolution and genetic instability. Semin Cancer Biol 20(4):234-245. doi: 10.1016/j.semcancer.2010.04.001.
82. Tan X, Xu X, Elkenani M, Smorag L, Zechner U, Nolte J et al (2013) Zfp819, a novel KRAB-zinc finger protein, interacts with KAP1 and functions in genomic integrity maintenance of mouse embryonic stem cells. Stem Cell Res. 11(3):1045-1059. doi: 10.1016/j.scr.2013.07.006.
83. Ratnam S, Engler P, Bozek G, Mao L, Podlutsky A, Austad S et al (2014) Identification of Ssm1b, a novel modifier of DNA methylation, and its expression during mouse embryogenesis. Development. 141(10):2024-2034. doi: 10.1242/dev.105726.
84. Najafabadi HS, Mnaimneh S, Schmitges FW, Garton M, Lam KN, Yang A et al (2015) C2H2 zinc finger proteins greatly expand the human regulatory lexicon. Nat Biotechnol. doi: 10.1038/nbt.3128.
85. Gifford WD, Pfaff SL, Macfarlan TS (2013) Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol 23(5):218-226. doi: 10.1016/j.tcb.2013.01.001.
86. Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, Matsuoka C et al (2006) Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11(7):805-814. doi: 10.1111/j.1365-2443.2006.00984.x.
87. Garcia-Perez JL, Morell M, Scheys JO, Kulpa DA, Morell S, Carter CC et al (2010) Epigenetic silencing of engineered L1 retrotransposition events in human embryonic carcinoma cells. Nature 466(7307):769-773. doi: 10.1038/nature09209.
88. Reichmann J, Crichton JH, Madej MJ, Taggart M, Gautier P, Garcia-Perez JL et al (2012) Microarray analysis of LTR retrotransposon silencing identifies Hdac1 as a regulator of retrotransposon expression in mouse embryonic stem cells. PLoS Comput Biol 8(4):e1002486. doi: 10.1371/journal.pcbi.1002486.
89. Leung D, Du T, Wagner U, Xie W, Lee AY, Goyal P et al (2014) Regulation of DNA methylation turnover at LTR retrotransposons and imprinted loci by the histone methyltransferase Setdb1. Proc Natl Acad Sci 111(18):6690-6695. doi: 10.1073/pnas.1322273111.
90. Macfarlan TS, Gifford WD, Agarwal S, Driscoll S, Lettieri K, Wang J et al (2011) Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev 25(6):594-607. doi: 10.1101/gad.2008511.
91. Leung DC, Dong KB, Maksakova IA, Goyal P, Appanah R, Lee S et al (2011) Lysine methyltransferase G9a is required for de novo DNA methylation and the establishment, but not the maintenance, of proviral silencing. Proc Natl Acad Sci 108(14):5718-5723. doi: 10.1073/pnas.1014660108.
92. Leeb M, Pasini D, Novatchkova M, Jaritz M, Helin K, Wutz A et al (2010) Polycomb complexes act redundantly to repress genomic repeats and genes. Genes Dev 24(3):265-276. doi: 10.1101/gad.544410.
93. Bulut-Karslioglu A, De La Rosa-Velazquez IA, Ramirez F, Barenboim M, Onishi-Seebacher M, Arand J et al (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.
94. di Caprio R, Ciano M, Montano G, Costanzo P, Cesaro E (2015) KAP1 is a novel substrate for the arginine methyltransferase PRMT5. Biology 4(1):41-49. doi: 10.3390/biology4010041.
95. Kim S, Gunesdogan U, Zylicz JJ, Hackett JA, Cougot D, Bao S et al (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.
96. Cammas F, Herzog M, Lerouge T, Chambon P, Losson R (2004) Association of the transcriptional corepressor TIF1beta with heterochromatin protein 1 (HP1): an essential role for progression through differentiation. Genes Dev 18(17):2147-2160. doi: 10.1101/gad.30290418/17/2147.
97. Lechner MS, Begg GE, Speicher DW, Rauscher FJ 3rd (2000) Molecular determinants for targeting heterochromatin protein 1-mediated gene silencing: direct chromoshadow domain-KAP-1 corepressor interaction is essential. Mol Cell Biol 20(17):6449-6465
98. Wolf D, Cammas F, Losson R, Goff SP (2008) Primer binding site-dependent restriction of murine leukemia virus requires HP1 binding by TRIM28. J Virol 82(9):4675-4679. doi: 10.1128/JVI.02445-07.
99. Groner AC, Meylan S, Ciuffi A, Zangger N, Ambrosini G, Denervaud N et al (2010) KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet 6(3):e1000869. doi: 10.1371/journal.pgen.1000869.
100. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410(6824):116-120. doi: 10.1038/3506513235065132.
101. Kao TH, Liao HF, Wolf D, Tai KY, Chuang CY, Lee HS et al (2014) Ectopic DNMT3L triggers assembly of a repressive complex for retroviral silencing in somatic cells. J Virol 88(18):10680-10695. doi: 10.1128/JVI.01176-14.
102. Vlachogiannis G, Niederhuth CE, Tuna S, Stathopoulou A, Viiri K, de Rooij DG et al (2015) The Dnmt3L ADD domain controls cytosine methylation establishment during spermatogenesis. Cell Rep. doi: 10.1016/j.celrep.2015.01.021.
103. Thompson PJ, Dulberg V, Moon KM, Foster LJ, Chen C, Karimi MM et al (2015) hnRNP K coordinates transcriptional silencing by SETDB1 in embryonic stem cells. PLoS Genet 11(1):e1004933. doi: 10.1371/journal.pgen.1004933.
104. Guallar D, Perez-Palacios R, Climent M, Martinez-Abadia I, Larraga A, Fernandez-Juan M et al (2012) Expression of endogenous retroviruses is negatively regulated by the pluripotency marker Rex1/Zfp42. Nucleic Acids Res 40(18):8993-9007. doi: 10.1093/nar/gks686.
105. Schoorlemmer J, Perez-Palacios R, Climent M, Guallar D, Muniesa P (2014) Regulation of mouse retroelement MuERV-L/MERVL expression by REX1 and epigenetic control of stem cell potency. Front Oncol. 4:14. doi: 10.3389/fonc.2014.00014.
106. Van Meter M, Kashyap M, Rezazadeh S, Geneva AJ, Morello TD, Seluanov A et al (2014) SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age. Nat Commun. 5:5011. doi: 10.1038/ncomms6011.
107. Zhao K, Du J, Han X, Goodier JL, Li P, Zhou X et al (2013) Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutieres syndrome-related SAMHD1. Cell Rep. 4(6):1108-1115. doi: 10.1016/j.celrep.2013.08.019.
108. Dewannieux M, Heidmann T (2013) Endogenous retroviruses: acquisition, amplification and taming of genome invaders. Curr Opin Virol 3(6):646-656. doi: 10.1016/j.coviro.2013.08.005.
109. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF et al (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.
110. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M et al (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.
111. 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.
112. Marchetto MC, Narvaiza I, Denli AM, Benner C, Lazzarini TA, Nathanson JL et al (2013) Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 503(7477):525-529. doi: 10.1038/nature12686.
113. Fadloun A, Le Gras S, Jost B, Ziegler-Birling C, Takahashi H, Gorab E et al (2013) Chromatin signatures and retrotransposon profiling in mouse embryos reveal regulation of LINE-1 by RNA. Nat Struct Mol Biol 20(3):332-338. doi: 10.1038/nsmb.2495.
114. Ciaudo C, Jay F, Okamoto I, Chen CJ, Sarazin A, Servant N et al (2013) RNAi-dependent and independent control of LINE1 accumulation and mobility in mouse embryonic stem cells. PLoS Genet 9(11):e1003791. doi: 10.1371/journal.pgen.1003791.
115. Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13(4):283-296. doi: 10.1038/nrg3199.
116. Weiss RA, Stoye JP (2013) Virology. Our viral inheritance. Science 340(6134):820-821. doi: 10.1126/science.1235148