Long Terminal Repeats: From Parasitic Elements to Building Blocks of the Transcriptional Regulatory Repertoire

Molecular Cell

Volumn 62, Issue 5, 2016, Pages 766-776

  Thompson, Peter J ^a,c   Macfarlan, Todd S ^b   Lorincz, Matthew C ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TRANSCRIPTION; DOCUMENTATION; ENDOGENOUS RETROVIRUS; HUMAN; LONG TERMINAL REPEAT; MAMMAL; REGULATORY SEQUENCE; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPLICATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; PROMOTER REGION; VIRUS REPLICATION;

LONG UNTRANSLATED RNA; RNA DIRECTED DNA POLYMERASE; RNA POLYMERASE II; VIRUS DNA;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPLICATION; DNA, VIRAL; ENDOGENOUS RETROVIRUSES; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; RNA, LONG NONCODING; RNA-DIRECTED DNA POLYMERASE; TERMINAL REPEAT SEQUENCES; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

EID: 84971455349     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.03.029     Document Type: Review

References (111)

1. Bassett A.R., Akhtar A., Barlow D.P., Bird A.P., Brockdorff N., Duboule D., Ephrussi A., Ferguson-Smith A.C., Gingeras T.R., Haerty W., et al. Considerations when investigating lncRNA function in vivo. eLife 2014, 3:e03058.
2. Belshaw R., Watson J., Katzourakis A., Howe A., Woolven-Allen J., Burt A., Tristem M. Rate of recombinational deletion among human endogenous retroviruses. J. Virol. 2007, 81:9437-9442.
3. Bourque G., Leong B., Vega V.B., Chen X., Lee Y.L., Srinivasan K.G., Chew J.L., Ruan Y., Wei C.L., Ng H.H., Liu E.T. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 2008, 18:1752-1762.
4. Britten R.J., Davidson E.H. Gene regulation for higher cells: a theory. Science 1969, 165:349-357.
5. Buzdin A., Kovalskaya-Alexandrova E., Gogvadze E., Sverdlov E. At least 50% of human-specific HERV-K (HML-2) long terminal repeats serve in vivo as active promoters for host nonrepetitive DNA transcription. J. Virol. 2006, 80:10752-10762.
6. Castro-Diaz N., Friedli M., Trono D. Drawing a fine line on endogenous retroelement activity. Mob. Genet. Elements 2015, 5:1-6.
7. Chuong E.B., Rumi M.A.K., Soares M.J., Baker J.C. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat. Genet. 2013, 45:325-329.
8. Chuong E.B., Elde N.C., Feschotte C. Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 2016, 351:1083-1087.
9. Cohen C.J., Lock W.M., Mager D.L. Endogenous retroviral LTRs as promoters for human genes: a critical assessment. Gene 2009, 448:105-114.
10. Cordaux R., Batzer M.A. The impact of retrotransposons on human genome evolution. Nat. Rev. Genet. 2009, 10:691-703.
11. Cowley M., Oakey R.J. Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet. 2013, 9:e1003234.
12. de Souza F.S., Franchini L.F., Rubinstein M. Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong?. Mol. Biol. Evol. 2013, 30:1239-1251.
13. del Rosario R.C.H., Rayan N.A., Prabhakar S. Noncoding origins of anthropoid traits and a new null model of transposon functionalization. Genome Res. 2014, 24:1469-1484.
14. Dunn C.A., Medstrand P., Mager D.L. An endogenous retroviral long terminal repeat is the dominant promoter for human beta1,3-galactosyltransferase 5 in the colon. Proc. Natl. Acad. Sci. USA 2003, 100:12841-12846.
15. Dunn C.A., van de Lagemaat L.N., Baillie G.J., Mager D.L. Endogenous retrovirus long terminal repeats as ready-to-use mobile promoters: the case of primate beta3GAL-T5. Gene 2005, 364:2-12.
16. Dunn C.A., Romanish M.T., Gutierrez L.E., van de Lagemaat L.N., Mager D.L. Transcription of two human genes from a bidirectional endogenous retrovirus promoter. Gene 2006, 366:335-342.
17. Durruthy-Durruthy J., Sebastiano V., Wossidlo M., Cepeda D., Cui J., Grow E.J., Davila J., Mall M., Wong W.H., Wysocka J., et al. The primate-specific noncoding RNA HPAT5 regulates pluripotency during human preimplantation development and nuclear reprogramming. Nat. Genet. 2016, 48:44-52.
18. Ecco G., Cassano M., Kauzlaric A., Duc J., Coluccio A., Offner S., Imbeault M., Rowe H.M., Turelli P., Trono D. Transposable elements and their KRAB-ZFP controllers regulate gene expression in adult tissues. Dev. Cell 2016, 36:611-623.
19. Emera D., Wagner G.P. Transformation of a transposon into a derived prolactin promoter with function during human pregnancy. Proc. Natl. Acad. Sci. USA 2012, 109:11246-11251.
20. Emera D., Wagner G.P. Transposable element recruitments in the mammalian placenta: impacts and mechanisms. Brief. Funct. Genomics 2012, 11:267-276.
21. Emera D., Casola C., Lynch V.J., Wildman D.E., Agnew D., Wagner G.P. Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 2012, 29:239-247.
22. Evsikov A.V., de Vries W.N., Peaston A.E., Radford E.E., Fancher K.S., Chen F.H., Blake J.A., Bult C.J., Latham K.E., Solter D., Knowles B.B. Systems biology of the 2-cell mouse embryo. Cytogenet. Genome Res. 2004, 105:240-250.
23. Faulkner G.J., Kimura Y., Daub C.O., Wani S., Plessy C., Irvine K.M., Schroder K., Cloonan N., Steptoe A.L., Lassmann T., et al. The regulated retrotransposon transcriptome of mammalian cells. Nat. Genet. 2009, 41:563-571.
24. Feschotte C., Gilbert C. Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 2012, 13:283-296.
25. Flemr M., Malik R., Franke V., Nejepinska J., Sedlacek R., Vlahovicek K., Svoboda P. A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 2013, 155:807-816.
26. Fort A., Hashimoto K., Yamada D., Salimullah M., Keya C.A., Saxena A., Bonetti A., Voineagu I., Bertin N., Kratz A., et al. Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance. Nat. Genet. 2014, 46:558-566. FANTOM Consortium.
27. Franchini L.F., López-Leal R., Nasif S., Beati P., Gelman D.M., Low M.J., de Souza F.J.S., Rubinstein M. Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons. Proc. Natl. Acad. Sci. USA 2011, 108:15270-15275.
28. Franchini L.F., de Souza F.S.J., Low M.J., Rubinstein M. Positive selection of co-opted mobile genetic elements in a mammalian gene: if you can't beat them, join them. Mob. Genet. Elements 2012, 2:106-109.
29. Friedli M., Trono D. The developmental control of transposable elements and the evolution of higher species. Annu. Rev. Cell Dev. Biol. 2015, 31:429-451.
30. Froberg J.E., Yang L., Lee J.T. Guided by RNAs: X-inactivation as a model for lncRNA function. J. Mol. Biol. 2013, 425:3698-3706.
31. Gemmell P., Hein J., Katzourakis A. Orthologous endogenous retroviruses exhibit directional selection since the chimp-human split. Retrovirology 2015, 12:52.
32. Gifford W.D., Pfaff S.L., Macfarlan T.S. Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol. 2013, 23:218-226.
33. Göke J., Lu X., Chan Y.S., Ng H.H., Ly L.H., Sachs F., Szczerbinska I. Dynamic transcription of distinct classes of endogenous retroviral elements marks specific populations of early human embryonic cells. Cell Stem Cell 2015, 16:135-141.
34. Grow E.J., Flynn R.A., Chavez S.L., Bayless N.L., Wossidlo M., Wesche D.J., Martin L., Ware C.B., Blish C.A., Chang H.Y., et al. Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature 2015, 522:221-225.
35. Hayashi M., Maehara K., Harada A., Semba Y., Kudo K., Takahashi H., Oki S., Meno C., Ichiyanagi K., Akashi K., Ohkawa Y. Chd5 regulates MuERV-L/MERVL expression in mouse embryonic stem cells via H3K27me3 modification and histone H3.1/H3.2. J. Cell. Biochem. 2016, 117:780-792.
36. Herquel B., Ouararhni K., Martianov I., Le Gras S., Ye T., Keime C., Lerouge T., Jost B., Cammas F., Losson R., Davidson I. Trim24-repressed VL30 retrotransposons regulate gene expression by producing noncoding RNA. Nat. Struct. Mol. Biol. 2013, 20:339-346.
37. Hisada K., Sánchez C., Endo T.A., Endoh M., Román-Trufero M., Sharif J., Koseki H., Vidal M. RYBP represses endogenous retroviruses and preimplantation- and germ line-specific genes in mouse embryonic stem cells. Mol. Cell. Biol. 2012, 32:1139-1149.
38. Hon G.C., Rajagopal N., Shen Y., McCleary D.F., Yue F., Dang M.D., Ren B. Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat. Genet. 2013, 45:1198-1206.
39. Huarte M., Guttman M., Feldser D., Garber M., Koziol M.J., Kenzelmann-Broz D., Khalil A.M., Zuk O., Amit I., Rabani M., et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010, 142:409-419.
40. Isbel L., Whitelaw E. Endogenous retroviruses in mammals: an emerging picture of how ERVs modify expression of adjacent genes. BioEssays 2012, 34:734-738.
41. Isbel L., Srivastava R., Oey H., Spurling A., Daxinger L., Puthalakath H., Whitelaw E. Trim33 binds and silences a class of young endogenous retroviruses in the mouse testis; a novel component of the arms race between retrotransposons and the host genome. PLoS Genet. 2015, 11:e1005693.
42. Ishiuchi T., Enriquez-Gasca R., Mizutani E., Bošković A., Ziegler-Birling C., Rodriguez-Terrones D., Wakayama T., Vaquerizas J.M., Torres-Padilla M.-E. Early embryonic-like cells are induced by downregulating replication-dependent chromatin assembly. Nat. Struct. Mol. Biol. 2015, 22:662-671.
43. Jacques P.-E., Jeyakani J., Bourque G. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet. 2013, 9:e1003504.
44. Jern P., Coffin J.M. Effects of retroviruses on host genome function. Annu. Rev. Genet. 2008, 42:709-732.
45. Jjingo D., Conley A.B., Wang J., Mariño-Ramírez L., Lunyak V.V., Jordan I.K. Mammalian-wide interspersed repeat (MIR)-derived enhancers and the regulation of human gene expression. Mob. DNA 2014, 5:14.
46. Kannan S., Chernikova D., Rogozin I.B., Poliakov E., Managadze D., Koonin E.V., Milanesi L. Transposable element insertions in long intergenic non-coding RNA genes. Front. Bioeng. Biotechnol. 2015, 3:71.
47. Kapusta A., Feschotte C. Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications. Trends Genet. 2014, 30:439-452.
48. Kapusta A., Kronenberg Z., Lynch V.J., Zhuo X., Ramsay L., Bourque G., Yandell M., Feschotte C. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 2013, 9:e1003470.
49. Karimi M.M., Goyal P., Maksakova I.A., Bilenky M., Leung D., Tang J.X., Shinkai Y., Mager D.L., Jones S., Hirst M., Lorincz M.C. DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 2011, 8:676-687.
50. Kelley D., Rinn J. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol. 2012, 13:R107.
51. Kim T.-K., Hemberg M., Gray J.M. Enhancer RNAs: a class of long noncoding RNAs synthesized at enhancers. Cold Spring Harb. Perspect. Biol. 2015, 7:a018622.
52. Kunarso G., Chia N.Y., Jeyakani J., Hwang C., Lu X., Chan Y.S., Ng H.H., Bourque G. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 2010, 42:631-634.
53. Lam D.D., de Souza F.S.J., Nasif S., Yamashita M., López-Leal R., Otero-Corchon V., Meece K., Sampath H., Mercer A.J., Wardlaw S.L., et al. Partially redundant enhancers cooperatively maintain mammalian pomc expression above a critical functional threshold. PLoS Genet. 2015, 11:e1004935.
54. Lamprecht B., Walter K., Kreher S., Kumar R., Hummel M., Lenze D., Köchert K., Bouhlel M.A., Richter J., Soler E., et al. Derepression of an endogenous long terminal repeat activates the CSF1R proto-oncogene in human lymphoma. Nat. Med. 2010, 16:571-579, 1p, 579.
55. Lin N., Chang K.Y., Li Z., Gates K., Rana Z.A., Dang J., Zhang D., Han T., Yang C.S., Cunningham T.J., et al. An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment. Mol. Cell 2014, 53:1005-1019.
56. Lipatov M., Lenkov K., Petrov D.A., Bergman C.M. Paucity of chimeric gene-transposable element transcripts in the Drosophila melanogaster genome. BMC Biol. 2005, 3:24.
57. Liu S., Brind'Amour J., Karimi M.M., Shirane K., Bogutz A., Lefebvre L., Sasaki H., Shinkai Y., Lorincz M.C. Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells. Genes Dev. 2014, 28:2041-2055.
58. Loewer S., Cabili M.N., Guttman M., Loh Y.-H., Thomas K., Park I.H., Garber M., Curran M., Onder T., Agarwal S., et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat. Genet. 2010, 42:1113-1117.
59. Lowe C.B., Bejerano G., Haussler D. Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc. Natl. Acad. Sci. USA 2007, 104:8005-8010.
60. Lu F., Liu Y., Jiang L., Yamaguchi S., Zhang Y. Role of Tet proteins in enhancer activity and telomere elongation. Genes Dev. 2014, 28:2103-2119.
61. Lu X., Sachs F., Ramsay L., Jacques P.-É., Göke J., Bourque G., Ng H.-H. The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat. Struct. Mol. Biol. 2014, 21:423-425.
62. Lynch V.J., Leclerc R.D., May G., Wagner G.P. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 2011, 43:1154-1159.
63. Lynch V.J., Nnamani M.C., Kapusta A., Brayer K., Plaza S.L., Mazur E.C., Emera D., Sheikh S.Z., Grützner F., Bauersachs S., et al. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 2015, 10:551-561.
64. Macfarlan T.S., Gifford W.D., Agarwal S., Driscoll S., Lettieri K., Wang J., Andrews S.E., Franco L., Rosenfeld M.G., Ren B., Pfaff S.L. Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev. 2011, 25:594-607.
65. Macfarlan T.S., Gifford W.D., Driscoll S., Lettieri K., Rowe H.M., Bonanomi D., Firth A., Singer O., Trono D., Pfaff S.L. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 2012, 487:57-63.
66. Mager D.L., Stoye J.P. Mammalian endogenous retroviruses. Microbiol. Spectr. 2015, 3:A3-A0009, 2014.
67. Magiorkinis G., Gifford R.J., Katzourakis A., De Ranter J., Belshaw R. Env-less endogenous retroviruses are genomic superspreaders. Proc. Natl. Acad. Sci. USA 2012, 109:7385-7390.
68. Mak K.S., Burdach J., Norton L.J., Pearson R.C.M., Crossley M., Funnell A.P.W. Repression of chimeric transcripts emanating from endogenous retrotransposons by a sequence-specific transcription factor. Genome Biol. 2014, 15:R58.
69. Maksakova I.A., Romanish M.T., Gagnier L., Dunn C.A., van de Lagemaat L.N., Mager D.L. Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet. 2006, 2:e2.
70. Maksakova I.A., Thompson P.J., Goyal P., Jones S.J., Singh P.B., Karimi M.M., Lorincz M.C. Distinct roles of KAP1, HP1 and G9a/GLP in silencing of the two-cell-specific retrotransposon MERVL in mouse ES cells. Epigenetics Chromatin 2013, 6:15.
71. Matsui T., Leung D., Miyashita H., Maksakova I.A., Miyachi H., Kimura H., Tachibana M., Lorincz M.C., Shinkai Y. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 2010, 464:927-931.
72. McClintock B. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA 1950, 36:344-355.
73. Medstrand P., van de Lagemaat L.N., Mager D.L. Retroelement distributions in the human genome: variations associated with age and proximity to genes. Genome Res. 2002, 12:1483-1495.
74. Nei M., Xu P., Glazko G. Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms. Proc. Natl. Acad. Sci. USA 2001, 98:2497-2502.
75. Ohnuki M., Tanabe K., Sutou K., Teramoto I., Sawamura Y., Narita M., Nakamura M., Tokunaga Y., Nakamura M., Watanabe A., et al. Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential. Proc. Natl. Acad. Sci. USA 2014, 111:12426-12431.
76. Okahara G., Matsubara S., Oda T., Sugimoto J., Jinno Y., Kanaya F. Expression analyses of human endogenous retroviruses (HERVs): tissue-specific and developmental stage-dependent expression of HERVs. Genomics 2004, 84:982-990.
77. Pavlicev M., Hiratsuka K., Swaggart K.A., Dunn C., Muglia L. Detecting endogenous retrovirus-driven tissue-specific gene transcription. Genome Biol. Evol. 2015, 7:1082-1097.
78. Peaston A.E., Evsikov A.V., Graber J.H., de Vries W.N., Holbrook A.E., Solter D., Knowles B.B. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 2004, 7:597-606.
79. Pi W., Zhu X., Wu M., Wang Y., Fulzele S., Eroglu A., Ling J., Tuan D. Long-range function of an intergenic retrotransposon. Proc. Natl. Acad. Sci. USA 2010, 107:12992-12997.
80. Plank J.L., Dean A. Enhancer function: mechanistic and genome-wide insights come together. Mol. Cell 2014, 55:5-14.
81. Rebollo R., Romanish M.T., Mager D.L. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu. Rev. Genet. 2012, 46:21-42.
82. Rebollo R., Zhang Y., Mager D.L. Transposable elements: not as quiet as a mouse. Genome Biol. 2012, 13:159.
83. Reiss D., Zhang Y., Mager D.L. Widely variable endogenous retroviral methylation levels in human placenta. Nucleic Acids Res. 2007, 35:4743-4754.
84. Rinn J.L., Kertesz M., Wang J.K., Squazzo S.L., Xu X., Brugmann S.A., Goodnough L.H., Helms J.A., Farnham P.J., Segal E., Chang H.Y. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323.
85. Robbez-Masson L., Rowe H.M. Retrotransposons shape species-specific embryonic stem cell gene expression. Retrovirology 2015, 12:45.
86. Romanish M.T., Lock W.M., van de Lagemaat L.N., Dunn C.A., Mager D.L. Repeated recruitment of LTR retrotransposons as promoters by the anti-apoptotic locus NAIP during mammalian evolution. PLoS Genet. 2007, 3:e10.
87. Rowe H.M., Jakobsson J., Mesnard D., Rougemont J., Reynard S., Aktas T., Maillard P.V., Layard-Liesching H., Verp S., Marquis J., et al. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 2010, 463:237-240.
88. Rowe H.M., Kapopoulou A., Corsinotti A., Fasching L., Macfarlan T.S., Tarabay Y., Viville S., Jakobsson J., Pfaff S.L., Trono D. TRIM28 repression of retrotransposon-based enhancers is necessary to preserve transcriptional dynamics in embryonic stem cells. Genome Res. 2013, 23:452-461.
89. Sadic D., Schmidt K., Groh S., Kondofersky I., Ellwart J., Fuchs C., Theis F.J., Schotta G. Atrx promotes heterochromatin formation at retrotransposons. EMBO Rep. 2015, 16:836-850.
90. Smit A.F. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr. Opin. Genet. Dev. 1999, 9:657-663.
91. Stocking C., Kozak C.A. Murine endogenous retroviruses. Cell. Mol. Life Sci. 2008, 65:3383-3398.
92. Sundaram V., Cheng Y., Ma Z., Li D., Xing X., Edge P., Snyder M.P., Wang T. Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res. 2014, 24:1963-1976.
93. Thompson P.J., Dulberg V., Moon K.M., Foster L.J., Chen C., Karimi M.M., Lorincz M.C. hnRNP K coordinates transcriptional silencing by SETDB1 in embryonic stem cells. PLoS Genet. 2015, 11:e1004933.
94. Tomizawa S., Kobayashi H., Watanabe T., Andrews S., Hata K., Kelsey G., Sasaki H. Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development 2011, 138:811-820.
95. Turelli P., Castro-Diaz N., Marzetta F., Kapopoulou A., Raclot C., Duc J., Tieng V., Quenneville S., Trono D. Interplay of TRIM28 and DNA methylation in controlling human endogenous retroelements. Genome Res. 2014, 24:1260-1270.
96. van de Lagemaat L.N., Landry J.-R., Mager D.L., Medstrand P. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet. 2003, 19:530-536.
97. Venter J.C., Adams M.D., Myers E.W., Li P.W., Mural R.J., Sutton G.G., Smith H.O., Yandell M., Evans C.A., Holt R.A., et al. The sequence of the human genome. Science 2001, 291:1304-1351.
98. Veselovska L., Smallwood S.A., Saadeh H., Stewart K.R., Krueger F., Maupetit-Méhouas S., Arnaud P., Tomizawa S., Andrews S., Kelsey G. Deep sequencing and de novo assembly of the mouse oocyte transcriptome define the contribution of transcription to the DNA methylation landscape. Genome Biol. 2015, 16:209.
99. Wang T., Zeng J., Lowe C.B., Sellers R.G., Salama S.R., Yang M., Burgess S.M., Brachmann R.K., Haussler D. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc. Natl. Acad. Sci. USA 2007, 104:18613-18618.
100. Wang J., Xie G., Singh M., Ghanbarian A.T., Raskó T., Szvetnik A., Cai H., Besser D., Prigione A., Fuchs N.V., et al. Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells. Nature 2014, 516:405-409.
101. Wang J., Vicente-García C., Seruggia D., Moltó E., Fernandez-Miñán A., Neto A., Lee E., Gómez-Skarmeta J.L., Montoliu L., Lunyak V.V., Jordan I.K. MIR retrotransposon sequences provide insulators to the human genome. Proc. Natl. Acad. Sci. USA 2015, 112:E4428-E4437.
102. Waterston R.H., Lindblad-Toh K., Birney E., Rogers J., Abril J.F., Agarwal P., Agarwala R., Ainscough R., Alexandersson M., An P., et al. Initial sequencing and comparative analysis of the mouse genome. Nature 2002, 420:520-562. Mouse Genome Sequencing Consortium.
103. Wolf D., Goff S.P. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 2009, 458:1201-1204.
104. Wolf G., Greenberg D., Macfarlan T.S. Spotting the enemy within: targeted silencing of foreign DNA in mammalian genomes by the Krüppel-associated box zinc finger protein family. Mob. DNA 2015, 6:17.
105. Wolf G., Yang P., Füchtbauer A.C., Füchtbauer E.-M., Silva A.M., Park C., Wu W., Nielsen A.L., Pedersen F.S., Macfarlan T.S. The KRAB zinc finger protein ZFP809 is required to initiate epigenetic silencing of endogenous retroviruses. Genes Dev. 2015, 29:538-554.
106. Wu X., Sharp P.A. Divergent transcription: a driving force for new gene origination?. Cell 2013, 155:990-996.
107. Xie D., Chen C.C., Ptaszek L.M., Xiao S., Cao X., Fang F., Ng H.H., Lewin H.A., Cowan C., Zhong S. Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res. 2010, 20:804-815.
108. Xie M., Hong C., Zhang B., Lowdon R.F., Xing X., Li D., Zhou X., Lee H.J., Maire C.L., Ligon K.L., et al. DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat. Genet. 2013, 45:836-841.
109. Yang L., Güell M., Niu D., George H., Lesha E., Grishin D., Aach J., Shrock E., Xu W., Poci J., et al. Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 2015, 350:1101-1104.
110. Zhang Q., Dan J., Wang H., Guo R., Mao J., Fu H., Wei X., Liu L. Tcstv1 and Tcstv3 elongate telomeres of mouse ES cells. Sci. Rep. 2016, 6:19852.
111. Ziller M.J., Gu H., Müller F., Donaghey J., Tsai L.T.-Y., Kohlbacher O., De Jager P.L., Rosen E.D., Bennett D.A., Bernstein B.E., et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 2013, 500:477-481.