Is imprinting the result of “friendly fire” by the host defense system?

English version

Autoři: Miroslava Ondičová ^aff001; Rebecca J. Oakey ^aff002; Colum P. Walsh ^aff001
Působiště autorů: School of Biomedical Sciences, Ulster University, Coleraine, Northern Ireland, United Kingdom ^aff001; Department of Medical & Molecular Genetics, King’s College London, Guy’s Hospital, London, United Kingdom ^aff002
Vyšlo v časopise: Is imprinting the result of “friendly fire” by the host defense system?. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008599
Kategorie: Review
doi: https://doi.org/10.1371/journal.pgen.1008599

Souhrn

In 1993, Denise Barlow proposed that genomic imprinting might have arisen from a host defense mechanism designed to inactivate retrotransposons. Although there were few examples at hand, she suggested that there should be maternal-specific and paternal-specific factors involved, with cognate imprinting boxes that they recognized; furthermore, the system should build on conserved biochemical factors, including DNA methylation, and maternal control should predominate for imprints. Here, we revisit this hypothesis in the light of recent advances in our understanding of host defense and DNA methylation and in particular, the link with Krüppel-associated box–zinc finger (KRAB-ZF) proteins.

Klíčová slova:

DNA methylation – DNA transcription – DNA-binding proteins – Genetic loci – Genomic imprinting – Mammalian genomics – Oocytes – Retrotransposons

Zdroje

1. Barlow D, Stöger R, Herrmann B, Saito K, Schweifer N. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature. 1991;349: 84–87. doi: 10.1038/349084a0 1845916

2. Stöger R, Kubicka P, Liu C-G, Kafri T, Razin A, Cedar H, et al. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell. 1993;73: 61–71. doi: 10.1016/0092-8674(93)90160-r 8462104

3. Sleutels F, Zwart R, Barlow DP. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature. 2002;415: 810–813. doi: 10.1038/415810a 11845212

4. Barlow D. Methylation and imprinting: from host defence to gene regulation. Science (80-). 1993;260: 309–310. doi: 10.1126/science.8469984 8469984

5. Braidotti G, Baubec T, Pauler F, Seidl C, Smrzka O, Stricker S, et al. The Air noncoding RNA: An imprinted cis-silencing transcript. Cold Spring Harbor Symposia on Quantitative Biology. 2004;69: 55–66. doi: 10.1101/sqb.2004.69.55 16117633

6. Pauler FM, Koerner M V., Barlow DP. Silencing by imprinted noncoding RNAs: is transcription the answer? Trends Genet. 2007;23: 284–292. doi: 10.1016/j.tig.2007.03.018 17445943

7. Latos PA, Pauler FM, Koerner M V., Şenergin HB, Hudson QJ, Stocsits RR, et al. Airn transcriptional overlap, but not its lncRNA products, induces imprinted Igf2r silencing. Science (80-). 2012;338: 1469–1472. doi: 10.1126/science.1228110 23239737

8. Barlow DP, Bartolomei MS. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol. 2014;6: a018382. doi: 10.1101/cshperspect.a018382 24492710

9. Chaillet J, Vogt T, Beier D, Leder P. Parental-specific methylation of an imprinted transgene is established during gametogenesis and progressively changes during embryogeneis. Cell. 1991;66: 77–83. doi: 10.1016/0092-8674(91)90140-t 1649008

10. Jahner D, Stuhlmann H, Stewart CL, Harbers K, Lohler J, Simon I, et al. De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature. 1982;298: 623–8. doi: 10.1038/298623a0 6285203

11. Bestor TH. DNA methylation: evolution of a bacterial immune function into a regulator of gene expression and genome structure in higher eukaryotes. Philos Trans R Soc L B Biol Sci. 1990;326: 179.

12. Surani M. Genomic imprinting: developmental significance and molecular mechanism. Curr Opin Genet Dev. 1991;1: 241–246. doi: 10.1016/s0959-437x(05)80077-2 1822272

13. Jahner D, Jaenisch R. Chromosomal position and specific demethylation in enhancer sequences of germ line-transmitted retroviral genomes during mouse development. Mol Cell Biol. 1985;5: 2212–2220. doi: 10.1128/mcb.5.9.2212 3837187

14. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2: 21–32. doi: 10.1038/35047554 11253064

15. Ferguson-Smith AC. Genomic imprinting: The emergence of an epigenetic paradigm. Nature Reviews Genetics. 2011;12: 565–575. doi: 10.1038/nrg3032 21765458

16. Mackin S-J, Thakur A, Walsh CP. Imprint stability and plasticity during development. Reproduction. 2018;156: R43–R55. doi: 10.1530/REP-18-0051 29743259

17. Walter J, Hutter B, Khare T, Paulsen M. Repetitive elements in imprinted genes. Cytogenet Genome Res. 2006;113: 109–115. doi: 10.1159/000090821 16575169

18. Cowley M, de Burca A, McCole RB, Chahal M, Saadat G, Oakey RJ, et al. Short Interspersed Element (SINE) Depletion and Long Interspersed Element (LINE) Abundance Are Not Features Universally Required for Imprinting. PLoS ONE. 2011;6: e18953. doi: 10.1371/journal.pone.0018953 21533089

19. Cowley M, Oakey RJ. Retrotransposition and genomic imprinting. Brief Funct Genomics. 2010;9: 340–346. doi: 10.1093/bfgp/elq015 20591835

20. Youngson NA, Kocialkowski S, Peel N, Ferguson-Smith AC. A small family of sushi-class retrotransposon-derived genes in mammals and their relation to genomic imprinting. J Mol Evol. 2005;61: 481–490. doi: 10.1007/s00239-004-0332-0 16155747

21. Wood AJ, Roberts RG, Monk D, Moore GE, Schulz R, Oakey RJ. A Screen for Retrotransposed Imprinted Genes Reveals an Association between X Chromosome Homology and Maternal Germ-Line Methylation. PLoS Genet. 2007;3: e20. doi: 10.1371/journal.pgen.0030020 17291163

22. Michaud EJ, van Vugt MJ, Bultman SJ, Sweet HO, Davisson MT, Woychik RP. Differential expression of a new dominant agouti allele (Aiapy) is correlated with methylation state and is influenced by parental lineage. Genes Dev. 1994;8: 1463–1472. doi: 10.1101/gad.8.12.1463 7926745

23. Neumann B, P. K, Barlow DP. Characteristics of imprinted genes. Nat Genet. 1995;9: 12–13. doi: 10.1038/ng0195-12 7704015

24. Mertineit C, Yoder JA, Taketo T, Laird DW, Trasler JM, Bestor TH. Sex-specific exons control DNA methyltransferase in mammalian germ cells. Development. 1998;125: 889–97. Available: http://www.cob.org.uk/Development/125/05/dev3790.html 9449671

25. Aapola U, Lyle R, Krohn K, Antonarakis SE, Peterson P. Isolation and initial characterization of the mouse Dnmt3l gene. Cytogenet Cell Genet. 2001;92: 122–6. doi: 10.1159/000056881 11306809

26. Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, Trasler JM, et al. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell. 2001;104: 829–38. doi: 10.1016/s0092-8674(01)00280-x 11290321

27. Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science (80-). 2001;294: 2536–9. doi: 10.1126/science.1065848 11719692

28. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A, et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011;43: 811–814. doi: 10.1038/ng.864 21706000

29. Shirane K, Toh H, Kobayashi H, Miura F, Chiba H, Ito T, et al. Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet. 2013;9: e1003439. doi: 10.1371/journal.pgen.1003439 23637617

30. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature. 2007;448: 714–717. doi: 10.1038/nature05987 17687327

31. Szabó PE, Pfeifer GP. H3K9me2 attracts PGC7 in the zygote to prevent Tet3-mediated oxidation of 5-methylcytosine. J Mol Cell Biol. 2012;4: 427–429. doi: 10.1093/jmcb/mjs038 22750790

32. Messerschmidt DM, de Vries W, Ito M, Solter D, Ferguson-Smith A, Knowles BB. Trim28 Is Required for Epigenetic Stability During Mouse Oocyte to Embryo Transition. Science (80-). 2012;335: 1499–1502. doi: 10.1126/science.1216154 22442485

33. Li X, Ito M, Zhou F, Youngson N, Zuo X, Leder P, et al. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev Cell. 2008;15: 547–557. doi: 10.1016/j.devcel.2008.08.014 18854139

34. Thomas JH, Schneider S. Coevolution of retroelements and tandem zinc finger genes. Genome Res. 2011;21: 1800–1812. doi: 10.1101/gr.121749.111 21784874

35. Yang P, Wang Y, Macfarlan TS. The Role of KRAB-ZFPs in Transposable Element Repression and Mammalian Evolution. Trends Genet. 2017;33(11): 871–881. doi: 10.1016/j.tig.2017.08.006 28935117

36. Helleboid P, Heusel M, Duc J, Piot C, Thorball CW, Coluccio A, et al. The interactome of KRAB zinc finger proteins reveals the evolutionary history of their functional diversification. EMBO J. 2019;38:e101220. doi: 10.15252/embj.2018101220 31403225

37. Jacobs FMJ, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S, et al. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature. 2014;516: 242–245. doi: 10.1038/nature13760 25274305

38. Rowe HM, Friedli M, Offner S, Verp S, Mesnard D, Marquis J, et al. De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET. Development. 2013;140: 519–529. doi: 10.1242/dev.087585 23293284

39. Wolf G, Yang P, Füchtbauer AC, Füchtbauer EM, Silva AM, Park C, et al. The KRAB zinc finger protein ZFP809 is required to initiate epigenetic silencing of endogenous retroviruses. Genes Dev. 2015;29: 538–554. doi: 10.1101/gad.252767.114 25737282

40. Nishitsuji H, Sawada L, Sugiyama R, Takaku H. ZNF10 inhibits HIV-1 LTR activity through interaction with NF-κB and Sp1 binding motifs. FEBS Lett. 2015;589: 2019–2025. doi: 10.1016/j.febslet.2015.06.013 26096782

41. Quenneville S, Verde G, Corsinotti A, Kapopoulou A, Jakobsson J, Offner S, 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. doi: 10.1016/j.molcel.2011.08.032 22055183

42. Strogantsev R, Krueger F, Yamazawa K, Shi H, Gould P, Goldman-Roberts M, et al. Allele-specific binding of ZFP57 in the epigenetic regulation of imprinted and non-imprinted monoallelic expression. Genome Biol. 2015;16: 112. doi: 10.1186/s13059-015-0672-7 26025256

43. Moore T, Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. TIG. 1991;7: 45–49. doi: 10.1016/0168-9525(91)90230-N 2035190

44. Bartolomei MS, Ferguson-Smith AC. Mammalian genomic imprinting. Cold Spring Harb Perspect Biol. 2011;3: 1–17. doi: 10.1101/cshperspect.a002592 21576252

45. Mackay DJ, Callaway JL, Marks SM, White HE, Acerini CL, Boonen SE, et al. Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat Genet. 2008;40: 949–951. doi: 10.1038/ng.187 18622393

46. Mackay DJG, Temple IK. Human imprinting disorders: Principles, practice, problems and progress. Eur J Med Genet. 2017;60: 618–626. doi: 10.1016/j.ejmg.2017.08.014 28818477

47. Takahashi N, Coluccio A, Thorball CW, Planet E, Shi H, Offner S, et al. ZNF445 is a primary regulator of genomic imprinting. Genes Dev. 2019;33: 49–54. doi: 10.1101/gad.320069.118 30602440

48. Yang P, Wang Y, Hoang D, Tinkham M, Patel A, Sun M-A, et al. A placental growth factor is silenced in mouse embryos by the zinc finger protein ZFP568. Science (80-). 2017;356: 757–759. doi: 10.1126/science.aah6895 28522536

49. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally Regulated piRNA Clusters Implicate MILI in Transposon Control. Science (80-). 2007;316: 744–747. doi: 10.1126/science.1142612 17446352

50. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, 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. doi: 10.1101/gad.1640708 18381894

51. Bourc’his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature. 2004;431: 96–99. doi: 10.1038/nature02886 15318244

52. Walsh CPP, Chaillet JRR, Bestor THH. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet. 1998;20: 116–7. doi: 10.1038/2413 9771701

53. Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31: 785–799. doi: 10.1016/j.molcel.2008.09.003 18922463

54. Barau J, Teissandier A, Zamudio N, Roy S, Nalesso V, Hérault Y, et al. The DNA methyltransferase DNMT3C protects male germ cells from transposon activity. Science (80-). 2016;354: 909–912. doi: 10.1126/science.aah5143 27856912

55. Lees-Murdock DJJ, McLoughlin GAA, McDaid JRR, Quinn LMM, O’Doherty A, Hiripi L, et al. Identification of 11 pseudogenes in the DNA methyltransferase gene family in rodents and humans and implications for the functional loci. Genomics. 2004;84: 193–204. doi: 10.1016/j.ygeno.2004.02.004 15203217

56. Watanabe T, Tomizawa S -i., Mitsuya, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S, et al. Role for piRNAs and Noncoding RNA in de Novo DNA Methylation of the Imprinted Mouse Rasgrf1 Locus. Science (80-). 2011;332: 848–852. doi: 10.1126/science.1203919 21566194

57. Flemr M, Malik R, Franke V, Nejepinska J, Sedlacek R, Vlahovicek K, et al. A Retrotransposon-Driven Dicer Isoform Directs Endogenous Small Interfering RNA Production in Mouse Oocytes. Cell. 2013;155: 807–816. doi: 10.1016/j.cell.2013.10.001 24209619

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