Evolutionally dynamic L1 regulation in embryonic stem cells

Genes and Development

Volumn 28, Issue 13, 2014, Pages 1397-1409

  Castro Diaz, Nathaly ^a   Ecco, Gabriela ^a   Coluccio, Andrea ^a   Kapopoulou, Adamandia ^a   Yazdanpanah, Benyamin ^a   Friedli, Marc ^a   Duc, Julien ^a   Jang, Suk Min ^a   Turelli, Priscilla ^a   Trono, Didier ^a  

^a EPFL   (Switzerland)

Author keywords

DNA methylation; Embryonic stem cells; Evolution; KAP1; KRAB ZFPs; LINE1

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HISTONE METHYLTRANSFERASE; REPRESSOR PROTEIN; SHORT HAIRPIN RNA; ZINC FINGER PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EMBRYONIC STEM CELL; ENDOGENOUS RETROVIRUS; GENE; GENE EXPRESSION; GENE SILENCING; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN GENOME; KRUPPEL ASSOCIATED BOX DOMAIN ASSOCIATED PROTEIN 1 GENE; LONG INTERSPERSED ELEMENT 1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FAMILY; QUANTITATIVE ANALYSIS; RETROPOSON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSPOSON; UPREGULATION;

DNA METHYLATION; EMBRYONIC STEM CELLS; EVOLUTION; KAP1; KRAB-ZFPS; LINE1;

ANIMALS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EMBRYONIC STEM CELLS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MICE; REPRESSOR PROTEINS;

EID: 84903782130     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.241661.114     Document Type: Article

References (55)

1. Aravin AA, Hannon GJ, Brennecke J. 2007. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764.
2. Babushok DV, Kazazian HH. 2007. Progress in understanding the biology of the human mutagen LINE-1. Hum Mutat 28: 527-539.
3. Barde I, Rauwel B, Marin-Florez RM, Corsinotti A, Laurenti E, Verp S, Offner S, Marquis J, Kapopoulou A, Vanicek J, et al. 2013. A KRAB/KAP1-miRNA cascade regulates erythropoiesis through stage-specific control of mitophagy. Science 340: 350-353.
4. Beck CR, Garcia-Perez JL, Badge RM, Moran JV. 2011. LINE-1 elements in structural variation and disease. Annu Rev Genomics Hum Genet 12: 187-215.
5. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, et al. 2010. The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28: 1045-1048.
6. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR. 2006. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci 103: 8780-8785.
7. Bourque G, Leong B, Vega VB, Chen X, Lee YL, Srinivasan KG, Chew JL, Ruan Y, Wei CL, Ng HH, et al. 2008. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18: 1752-1762.
8. 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 100: 5280-5285.
9. 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: 503-514.
10. Chiu YL, Greene WC. 2008. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol 26: 317-353.
11. Ciaudo C, Jay F, Okamoto I, Chen CJ, Sarazin A, Servant N, Barillot E, Heard E, Voinnet O. 2013. RNAi-dependent and independent control of LINE1 accumulation and mobility in mouse embryonic stem cells. PLoS Genet 9: e1003791.
12. Cordaux R, Batzer MA. 2009. The impact of retrotransposons on human genome evolution. Nat Rev Genet 10: 691-703.
13. Corsinotti A, Kapopoulou A, Gubelmann C, Imbeault M, Santoni de Sio FR, Rowe HM, Mouscaz Y, Deplancke B, Trono D. 2013. Global and stage specific patterns of Kruppelassociated-box zinc finger protein gene expression in murine early embryonic cells. PLoS ONE 8: e56721.
14. 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: 259-263.
15. Dewannieux M, Esnault C, Heidmann T. 2003. LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 35: 41-48.
16. Fadloun A, Le Gras S, Jost B, Ziegler-Birling C, Takahashi H, Gorab E, Carninci P, Torres-Padilla M-E. 2013. Chromatin signatures and retrotransposon profiling in mouse embryos reveal regulation of LINE-1 by RNA. Nat Struct Mol Biol 20: 332-338.
17. Faulkner GJ, Kimura Y, Daub CO, Wani S, Plessy C, Irvine KM, Schroder K, Cloonan N, Steptoe AL, Lassmann T, et al. 2009. The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41: 563-571.
18. Finnegan DJ. 2012. Retrotransposons. Curr Biol 22: R432-R437.
19. Furano AV, Boissinot S. 2008. Long interspersed nuclear elements (LINEs): evolution. eLS doi: 10.1002/9780470015902.a0005304. pub2.
20. Heras SR, Macias S, Plass M, Fernandez N, Cano D, Eyras E, Garcia-Perez JL, Cáceres JF. 2013. The Microprocessor controls the activity of mammalian retrotransposons. Nat Struct Mol Biol 20: 1173-1181.
21. Ivanov AV, Peng H, Yurchenko V, Yap KL, Negorev DG, Schultz DC, Psulkowski E, Fredericks WJ, White DE, Maul GG, et al. 2007. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 28: 823-837.
22. Iyengar S, Farnham PJ. 2011. KAP1 protein: an enigmatic master regulator of the genome. J Biol Chem 286: 26267-26276.
23. Iyengar S, Ivanov AV, Jin VX, Rauscher FJ 3rd, Farnham PJ. 2011. Functional analysis of KAP1 genomic recruitment. Mol Cell Biol 31: 1833-1847.
24. Jacques P-É, Jeyakani J, Bourque G. 2013. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 9: e1003504.
25. Khan H. 2005. Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res 16: 78-87.
26. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS, Ng HH, Bourque G. 2010. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42: 631-634.
27. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
28. Marchetto MCN, Narvaiza I, Denli AM, Benner C, Lazzarini TA, Nathanson JL, Paquola ACM, Desai KN, Herai RH, Weitzman MD, et al. 2013. Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 503: 525-529.
29. Matlik K, Redik K, Speek M. 2006. L1 antisense promoter drives tissue-specific transcription of human genes. J Biomed Biotechnol 2006: 71753.
30. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927-931.
31. Nigumann P, Redik K, Matlik K, Speek M. 2002. Many human genes are transcribed from the antisense promoter of L1 retrotransposon. Genomics 79: 628-634.
32. Quenneville S, Verde G, Corsinotti A, Kapopoulou A, Jakobsson J, Offner S, Baglivo I, Pedone PV, Grimaldi G, Riccio A, et al. 2011. In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol Cell 44: 361-372.
33. Quenneville S, Turelli P, Bojkowska K, Raclot C, Offner S, Kapopoulou A, Trono D. 2012. The KRAB-ZFP/KAP1 system contributes to the early embryonic establishment of sitespecific DNA methylation patterns maintained during development. Cell Reports 2: 766-773.
34. Rosser JM, An W. 2012. L1 expression and regulation in humans and rodents. in Front Biosci (Elite Ed) 4: 2203-2225.
35. Rowe HM, Trono D. 2011. Dynamic control of endogenous retroviruses during development. Virology 411: 273-287.
36. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, et al. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237-240.
37. Rowe HM, Friedli M, Offner S, Verp S, Mesnard D, Marquis J, Aktas T, Trono D. 2013a. De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET. Development 140: 519-529.
38. Rowe HM, Kapopoulou A, Corsinotti A, Fasching L, Macfarlan TS, Tarabay Y, Viville S, Jakobsson J, Pfaff SL, Trono D. 2013b. TRIM28 repression of retrotransposon-based enhancers is necessary to preserve transcriptional dynamics in embryonic stem cells. Genome Res 23: 452-461.
39. Santoni de Sio FR, Barde I, Offner S, Kapopoulou A, Corsinotti A, Bojkowska K, Genolet R, Thomas JH, Luescher IF, Pinschewer D et al. 2012. KAP1 regulates gene networks controlling T-cell development and responsiveness. FASEB J 26: 4561-4575.
40. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ. 2002. 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 16: 919-932.
41. Slotkin RK, Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272-285.
42. Smit AF, Tóth G, Riggs AD, Jurka J. 1995. Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences. J Mol Biol 246: 401-417.
43. Sookdeo A, Hepp CM, McClure MA, Boissinot S. 2013. Revisiting the evolution of mouse LINE-1 in the genomic era. Mob DNA 4: 3.
44. Speek M. 2001. Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes. Mol Cell Biol 21: 1973-1985.
45. Tan X, Xu X, Elkenani M, Smorag L, Zechner U, Nolte J, Engel W, Pantakani DV. 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: 1045-1059.
46. Thomas-Chollier M, Darbo E, Herrmann C, Defrance M, Thieffry D, van Helden J. 2012. A complete workflow for the analysis of full-size ChIP-seq (and similar) data sets using peak-motifs. Nat Protoc 7: 1551-1568.
47. 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 doi: 10.1101/ gr.172833.114.
48. Ward MC, Wilson MD, Barbosa-Morais NL, Schmidt D, Stark R, Pan Q, Schwalie PC, Menon S, Lukk M, Watt S, et al. 2013. Latent regulatory potential of human-specific repetitive elements. Mol Cell 49: 262-272.
49. Wissing S, Montano M, Garcia-Perez JL, Moran JV, Greene WC. 2011. Endogenous APOBEC3B restricts LINE-1 retrotransposition in transformed cells and human embryonic stem cells. J Biol Chem 286: 36427-36437.
50. Wolf D, Goff SP. 2007. TRIM28 mediates primer binding sitetargeted silencing of murine leukemia virus in embryonic cells. Cell 131: 46-57.
51. Wolf D, Goff SP. 2009. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 458: 1201-1204.
52. Xiong Z, Laird PW. 1997. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 25: 2532-2534.
53. Yahi H, Fritsch L, Philipot O, Guasconi V, Souidi M, Robin P, Polesskaya A, Losson R, Harel-Bellan A, Ait-Si-Ali S. 2008. Differential cooperation between heterochromatin protein HP1 isoforms and MyoD in myoblasts. J Biol Chem 283: 23692-23700.
54. Yang N, Kazazian HH Jr. 2006. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 13: 763-771.
55. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biol 9: R137.