Hide and seek: How chromatin-based pathways silence retroelements in the mammalian germline

Current Opinion in Genetics and Development

Volumn 37, Issue , 2016, Pages 51-58

  Molaro, Antoine ^a   Malik, Harmit S ^a,b  

^a USA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DNA METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; KZNF PROTEIN; PIWI INTERACTING RNA; UNCLASSIFIED DRUG; CHROMATIN; HISTONE; RETROPOSON;

CHROMATIN; EVOLUTIONARY ADAPTATION; GENE; GENE CONTROL; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENE INSERTION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GENOME ANALYSIS; GERM LINE; MIWI2 GENE; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RETROPOSON; REVIEW; ANIMAL; GENETICS; GERM CELL; MAMMAL; SIGNAL TRANSDUCTION;

ANIMALS; CHROMATIN; DNA-BINDING PROTEINS; GENE SILENCING; GERM CELLS; HISTONES; MAMMALS; RETROELEMENTS; SIGNAL TRANSDUCTION;

EID: 84955475665     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2015.12.001     Document Type: Review

References (71)

1. Consortium E.P. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
2. Reik W., Dean W., Walter J. Epigenetic reprogramming in mammalian development. Science 2001, 293:1089-1093.
3. Surani M.A., Hayashi K., Hajkova P. Genetic and epigenetic regulators of pluripotency. Cell 2007, 128:747-762.
4. Brulet P., Kaghad M., Xu Y.S., Croissant O., Jacob F. Early differential tissue expression of transposon-like repetitive DNA sequences of the mouse. Proc Natl Acad Sci U S A 1983, 80:5641-5645.
5. Kigami D., Minami N., Takayama H., Imai H. MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol Reprod 2003, 68:651-654.
6. 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.
7. Branciforte D., Martin S.L. Developmental and cell type specificity of LINE-1 expression in mouse testis: implications for transposition. Mol Cell Biol 1994, 14:2584-2592.
8. Dupressoir A., Heidmann T. Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol Cell Biol 1996, 16:4495-4503.
9. Seisenberger S., Andrews S., Krueger F., Arand J., Walter J., Santos F., Popp C., Thienpont B., Dean W., Reik W. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 2012, 48:849-862.
10. Tang W.W., Dietmann S., Irie N., Leitch H.G., Floros V.I., Bradshaw C.R., Hackett J.A., Chinnery P.F., Surani M.A. A unique gene regulatory network resets the human germline epigenome for development. Cell 2015, 161:1453-1467.
11. Goke 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.
12. Kelley D., Rinn J. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol 2012, 13:R107.
13. Lu X., Sachs F., Ramsay L., Jacques P.E., Goke 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.
14. 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.
15. Wang J., Xie G., Singh M., Ghanbarian A.T., Rasko 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.
16. Malki S., van der Heijden G.W., O'Donnell K.A., Martin S.L., Bortvin A. A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev Cell 2014, 29:521-533.
17. Zamudio N., Barau J., Teissandier A., Walter M., Borsos M., Servant N., Bourc'his D. DNA methylation restrains transposons from adopting a chromatin signature permissive for meiotic recombination. Genes Dev 2015, 29:1256-1270.
18. Friedli M., Turelli P., Kapopoulou A., Rauwel B., Castro-Diaz N., Rowe H.M., Ecco G., Unzu C., Planet E., Lombardo A., et al. Loss of transcriptional control over endogenous retroelements during reprogramming to pluripotency. Genome Res 2014, 24:1251-1259.
19. 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., et al. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 2008, 18:1752-1762.
20. 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.
21. Schmidt D., Schwalie P.C., Wilson M.D., Ballester B., Goncalves A., Kutter C., Brown G.D., Marshall A., Flicek P., Odom D.T. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 2012, 148:335-348.
22. 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.
23. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 2008, 31:785-799.
24. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Totoki Y., Toyoda A., Ikawa M., Asada N., Kojima K., Yamaguchi Y., Ijiri T.W., et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 2008, 22:908-917.
25. Carmell M.A., Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., Hannon G.J. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 2007, 12:503-514.
26. Kuramochi-Miyagawa S., Kimura T., Ijiri T.W., Isobe T., Asada N., Fujita Y., Ikawa M., Iwai N., Okabe M., Deng W., et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004, 131:839-849.
27. Kuramochi-Miyagawa S., Kimura T., Yomogida K., Kuroiwa A., Tadokoro Y., Fujita Y., Sato M., Matsuda Y., Nakano T. Two mouse piwi-related genes: miwi and mili. Mech Dev 2001, 108:121-133.
28. Aravin A.A., Sachidanandam R., Girard A., Fejes-Toth K., Hannon G.J. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007, 316:744-747.
29. Molaro A., Falciatori I., Hodges E., Aravin A.A., Marran K., Rafii S., McCombie W.R., Smith A.D., Hannon G.J. Two waves of de novo methylation during mouse germ cell development. Genes Dev 2014, 28:1544-1549.
30. Pezic D., Manakov S.A., Sachidanandam R., Aravin A.A. piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev 2014, 28:1410-1428.
31. Marchetto M.C., Narvaiza I., Denli A.M., Benner C., Lazzarini T.A., Nathanson J.L., Paquola A.C., Desai K.N., Herai R.H., Weitzman M.D., et al. Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 2013, 503:525-529.
32. Roovers E.F., Rosenkranz D., Mahdipour M., Han C.T., He N., Chuva de Sousa Lopes S.M., van der Westerlaken L.A., Zischler H., Butter F., Roelen B.A., et al. Piwi proteins and piRNAs in mammalian oocytes and early embryos. Cell Rep 2015, 10:2069-2082.
33. Khan H., Smit A., Boissinot S. Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res 2006, 16:78-87.
34. Mager D.L., Stoye J.P. Mammalian endogenous retroviruses. Microbiol Spectr 2015, 3. MDNA3-0009-2014.
35. Ivanov A.V., Peng H., Yurchenko V., Yap K.L., Negorev D.G., Schultz D.C., Psulkowski E., Fredericks W.J., White D.E., Maul G.G., et al. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 2007, 28:823-837.
36. Quenneville S., Verde G., Corsinotti A., Kapopoulou A., Jakobsson J., Offner S., Baglivo I., Pedone P.V., Grimaldi G., Riccio A., et al. In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol Cell 2011, 44:361-372.
37. Schultz D.C., Ayyanathan K., Negorev D., Maul G.G., Rauscher F.J. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 2002, 16:919-932.
38. Wolf D., Goff S.P. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 2009, 458:1201-1204.
39. Wolf G., Yang P., Fuchtbauer A.C., Fuchtbauer 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.
40. Corsinotti A., Kapopoulou A., Gubelmann C., Imbeault M., Santoni de Sio F.R., Rowe H.M., Mouscaz Y., Deplancke B., Trono D. Global and stage specific patterns of Kruppel-associated-box zinc finger protein gene expression in murine early embryonic cells. PLoS One 2013, 8:e56721.
41. Guallar D., Perez-Palacios R., Climent M., Martinez-Abadia I., Larraga A., Fernandez-Juan M., Vallejo C., Muniesa P., Schoorlemmer J. Expression of endogenous retroviruses is negatively regulated by the pluripotency marker Rex1/Zfp42. Nucleic Acids Res 2012, 40:8993-9007.
42. Jacobs F.M., Greenberg D., Nguyen N., Haeussler M., Ewing A.D., Katzman S., Paten B., Salama S.R., Haussler D. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature 2014, 516:242-245.
43. Najafabadi H.S., Mnaimneh S., Schmitges F.W., Garton M., Lam K.N., Yang A., Albu M., Weirauch M.T., Radovani E., Kim P.M., et al. C2H2 zinc finger proteins greatly expand the human regulatory lexicon. Nat Biotechnol 2015, 33:555-562.
44. Tan X., Xu X., Elkenani M., Smorag L., Zechner U., Nolte J., Engel W., Pantakani D.V. Zfp819, a novel KRAB-zinc finger protein, interacts with KAP1 and functions in genomic integrity maintenance of mouse embryonic stem cells. Stem Cell Res 2013, 11:1045-1059.
45. Thomas J.H., Schneider S. Coevolution of retroelements and tandem zinc finger genes. Genome Res 2011, 21:1800-1812.
46. Castro-Diaz N., Ecco G., Coluccio A., Kapopoulou A., Yazdanpanah B., Friedli M., Duc J., Jang S.M., Turelli P., Trono D. Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev 2014, 28:1397-1409.
47. 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.
48. Rowe H.M., Friedli M., Offner S., Verp S., Mesnard D., Marquis J., Aktas T., Trono D. De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET. Development 2013, 140:519-529.
49. 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.
50. 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.
51. Bulut-Karslioglu A., De La Rosa-Velazquez I.A., Ramirez F., Barenboim M., Onishi-Seebacher M., Arand J., Galan C., Winter G.E., Engist B., Gerle B., et al. Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol Cell 2014, 55:277-290.
52. Di Giacomo M., Comazzetto S., Sampath S.C., Sampath S.C., O'Carroll D. G9a co-suppresses LINE1 elements in spermatogonia. Epigenetics Chromatin 2014, 7:24.
53. 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.
54. 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.
55. Elsasser S.J., Noh K.M., Diaz N., Allis C.D., Banaszynski L.A. Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells. Nature 2015, 522:240-244.
56. Jang C.W., Shibata Y., Starmer J., Yee D., Magnuson T. Histone H3.3 maintains genome integrity during mammalian development. Genes Dev 2015, 29:1377-1392.
57. Schlesinger S., Lee A.H., Wang G.Z., Green L., Goff S.P. Proviral silencing in embryonic cells is regulated by Yin Yang 1. Cell Rep 2013, 4:50-58.
58. Tchasovnikarova I.A., Timms R.T., Matheson N.J., Wals K., Antrobus R., Gottgens B., Dougan G., Dawson M.A., Lehner P.J. GENE SILENCING. Epigenetic silencing by the HUSH complex mediates position-effect variegation in human cells. Science 2015, 348:1481-1485.
59. Chang Y., Sun L., Kokura K., Horton J.R., Fukuda M., Espejo A., Izumi V., Koomen J.M., Bedford M.T., Zhang X., et al. MPP8 mediates the interactions between DNA methyltransferase Dnmt3a and H3K9 methyltransferase GLP/G9a. Nat Commun 2011, 2:533.
60. Harten S.K., Bruxner T.J., Bharti V., Blewitt M., Nguyen T.M., Whitelaw E., Epp T. The first mouse mutants of D14Abb1e (Fam208a) show that it is critical for early development. Mamm Genome 2014, 25:293-303.
61. Huh J.W., Kim T.H., Yi J.M., Park E.S., Kim W.Y., Sin H.S., Kim D.S., Min D.S., Kim S.S., Kim C.B., et al. Molecular evolution of the periphilin gene in relation to human endogenous retrovirus m element. J Mol Evol 2006, 62:730-737.
62. Murata K., Sato S., Haruta M., Goshima T., Chiba Y., Takahashi S., Sharif J., Koseki H., Nakanishi M., Shimada M. Physical interaction between MPP8 and PRC1 complex and its implication for regulation of spermatogenesis. Biochem Biophys Res Commun 2015, 458:470-475.
63. Poleshko A., Einarson M.B., Shalginskikh N., Zhang R., Adams P.D., Skalka A.M., Katz R.A. Identification of a functional network of human epigenetic silencing factors. J Biol Chem 2010, 285:422-433.
64. Poleshko A., Palagin I., Zhang R., Boimel P., Castagna C., Adams P.D., Skalka A.M., Katz R.A. Identification of cellular proteins that maintain retroviral epigenetic silencing: evidence for an antiviral response. J Virol 2008, 82:2313-2323.
65. Yang B.X., El Farran C.A., Guo H.C., Yu T., Fang H.T., Wang H.F., Schlesinger S., Seah Y.F., Goh G.Y., Neo S.P., et al. Systematic identification of factors for provirus silencing in embryonic stem cells. Cell 2015, 163:230-245.
66. Greger J.G., Katz R.A., Ishov A.M., Maul G.G., Skalka A.M. The cellular protein daxx interacts with avian sarcoma virus integrase and viral DNA to repress viral transcription. J Virol 2005, 79:4610-4618.
67. Brown J.P., Bullwinkel J., Baron-Luhr B., Billur M., Schneider P., Winking H., Singh P.B. HP1gamma function is required for male germ cell survival and spermatogenesis. Epigenetics Chromatin 2010, 3:9.
68. Sripathy S.P., Stevens J., Schultz D.C. The KAP1 corepressor functions to coordinate the assembly of de novo HP1-demarcated microenvironments of heterochromatin required for KRAB zinc finger protein-mediated transcriptional repression. Mol Cell Biol 2006, 26:8623-8638.
69. Shalginskikh N., Poleshko A., Skalka A.M., Katz R.A. Retroviral DNA methylation and epigenetic repression are mediated by the antiviral host protein Daxx. J Virol 2013, 87:2137-2150.
70. Kim S., Gunesdogan U., Zylicz J.J., Hackett J.A., Cougot D., Bao S., Lee C., Dietmann S., Allen G.E., Sengupta R., et al. PRMT5 protects genomic integrity during global DNA demethylation in primordial germ cells and preimplantation embryos. Mol Cell 2014, 56:564-579.
71. Yu W., McIntosh C., Lister R., Zhu I., Han Y., Ren J., Landsman D., Lee E., Briones V., Terashima M., et al. Genome-wide DNA methylation patterns in LSH mutant reveals de-repression of repeat elements and redundant epigenetic silencing pathways. Genome Res 2014, 24:1613-1623.