Allele-specific binding of ZFP57 in the epigenetic regulation of imprinted and non-imprinted monoallelic expression

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Strogantsev, Ruslan ^a,b   Krueger, Felix ^b   Yamazawa, Kazuki ^a   Shi, Hui ^a   Gould, Poppy ^a   Goldman Roberts, Megan ^a   McEwen, Kirsten ^a   Sun, Bowen ^a   Pedersen, Roger ^a   Ferguson Smith, Anne C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ZFP57; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; DNA BINDING PROTEIN; KRUPPEL LIKE FACTOR; REPRESSOR PROTEIN; ZFP-57 PROTEIN, MOUSE;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; FKBP6 GENE; GENE; GENE EXPRESSION; GENETIC REGULATION; GENETIC VARIABILITY; GENOME IMPRINTING; GERM LINE; HISTONE METHYLATION; MALE; MOUSE; NONHUMAN; PROTEIN BINDING; ANIMAL; C57BL MOUSE; CELL LINE; GENETIC VARIATION; HISTONE CODE; METABOLISM;

ANIMALIA; MUS;

ALLELES; ANIMALS; BINDING SITES; CELL LINE; DNA METHYLATION; DNA-BINDING PROTEINS; GENETIC VARIATION; GENOMIC IMPRINTING; HISTONE CODE; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C57BL; REPRESSOR PROTEINS;

EID: 84938910089     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0672-7     Document Type: Article

References (65)

1. Bartolomei MS, Ferguson-Smith AC. Mammalian genomic imprinting. Cold Spring Harb Perspect Biol. 2011;3:1-17.
2. Ferguson-Smith AC. Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet. 2011;12:565-75.
3. Li Y, Sasaki H. Genomic imprinting in mammals: its life cycle, molecular mechanisms and reprogramming. Cell Res. 2011;21:466-73.
4. Williamson CM, Blake A, Thomas S, Beechey CV, Hancock J, Cattanach BM, et al. MRC Harwell, Oxfordshire: MouseBook: Imprinting resource; 2013. http://www.har.mrc.ac.uk/research/genomic_imprinting/ .
5. Morison IM, Paton CJ, Cleverley SD. The imprinted gene and parent-of-origin effect database. Nucleic Acids Res. 2001;29:275-6.
6. Charalambous M, Ferron SR, da Rocha ST, Murray AJ, Rowland T, Ito M, et al. Imprinted gene dosage is critical for the transition to independent life. Cell Metab. 2012;15:209-21.
7. Yamazawa K, Ogata T, Ferguson-Smith AC. Uniparental disomy and human disease: an overview. Am J Med Genet C Semin Med Genet. 2010;154C:329-34.
8. Tomizawa S, Sasaki H. Genomic imprinting and its relevance to congenital disease, infertility, molar pregnancy and induced pluripotent stem cell. J Hum Genet. 2012;57:84-91.
9. Buiting K. Prader-Willi syndrome and Angelman syndrome. Am J Med Genet C Semin Med Genet. 2010;154C:365-76.
10. Cassidy SB, Schwartz S, Miller JL, Driscoll DJ. Prader-Willi syndrome. Genet Med. 2012;14:10-26.
11. Hirasawa R, Feil R. Genomic imprinting and human disease. Essays Biochem. 2010;48:187-200.
12. Wutz A, Smrzka OW, Schweifer N, Schellander K, Wagner EF, Barlow DP. Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature. 1997;389:745-9.
13. Thorvaldsen JL, Duran KL, Bartolomei MS. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 1998;12:3693-702.
14. Williamson CM, Turner MD, Ball ST, Nottingham WT, Glenister P, Fray M, et al. Identification of an imprinting control region affecting the expression of all transcripts in the Gnas cluster. Nat Genet. 2006;38:350-5.
15. Yang T, Adamson TE, Resnick JL, Leff S, Wevrick R, Francke U, et al. A mouse model for Prader-Willi syndrome imprinting-centre mutations. Nat Genet. 1998;19:25-31.
16. Fitzpatrick GV, Soloway PD, Higgins MJ. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat Genet. 2002;32:426-31.
17. Lin S-P, Youngson N, Takada S, Seitz H, Reik W, Paulsen M, et al. Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat Genet. 2003;35:97-102.
18. Strogantsev R, Ferguson-Smith AC. Proteins involved in establishment and maintenance of imprinted methylation marks. Brief Funct Genomics. 2012;11:227-39.
19. 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;15:547-57.
20. Mackay DJG, Callaway JLA, 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;40:949-51.
21. 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;44:361-72.
22. Zuo X, Sheng J, Lau H-T, McDonald CM, Andrade M, Cullen DE, et al. Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain. J Biol Chem. 2012;287:2107-18.
23. 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. 2012;335:1499-502.
24. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B, et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature. 2011;477:289-94.
25. Guberman JM, Ai J, Arnaiz O, Baran J, Blake A, Baldock R, et al. BioMart Central Portal: an open database network for the biological community. Database (Oxford). 2011;2011:bar041.
26. O'Geen H, Squazzo SL, Iyengar S, Blahnik K, Rinn JL, Chang HY, et al. Genome-wide analysis of KAP1 binding suggests autoregulation of KRAB-ZNFs. PLoS Genet. 2007;3, e89.
27. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, et al. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature. 2010;463:237-40.
28. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 2007;448:553-60.
29. Henckel A, Nakabayashi K, Sanz LA, Feil R, Hata K, Arnaud P. Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum Mol Genet. 2009;18:3375-83.
30. Singh P, Wu X, Lee D-H, Li AX, Rauch TA, Pfeifer GP, et al. Chromosome-wide analysis of parental allele-specific chromatin and DNA methylation. Mol Cell Biol. 2011;31:1757-70.
31. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature. 2008;454:766-70.
32. Smallwood SA, Tomizawa S-I, Krueger F, Ruf N, Carli N, Segonds-Pichon A, et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011;43:1-5.
33. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, et al. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 2012;8, e1002440.
34. Tomizawa S, Kobayashi H, Watanabe T, Andrews S, Hata K, Kelsey G, et al. Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development. 2011;138:811-20.
35. Sato S, Yoshida W, Soejima H, Nakabayashi K, Hata K. Methylation dynamics of IG-DMR and Gtl2-DMR during murine embryonic and placental development. Genomics. 2011;98:120-7.
36. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, et al. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature. 2012;0-7.
37. Duffié R, Ajjan S, Greenberg MV, Zamudio N. Dynamic genomic imprinting in mammals the Gpr1/Zdbf2 locus provides new paradigms for transient and dynamic genomic imprinting in mammals. Genes Dev. 2014;28:463-78.
38. Kobayashi H, Sakurai T, Sato S, Nakabayashi K, Hata K, Kono T. Imprinted DNA methylation reprogramming during early mouse embryogenesis at the Gpr1-Zdbf2 locus is linked to long cis-intergenic transcription. FEBS Lett. 2012;2:1-7.
39. DeVeale B, van der Kooy D, Babak T. Critical evaluation of imprinted gene expression by RNA-Seq: a new perspective. PLoS Genet. 2012;8, e1002600.
40. Proudhon C, Duffié R, Ajjan S, Cowley M, Iranzo J, Carbajosa G, et al. Protection against de novo methylation is instrumental in maintaining parent-of-origin methylation inherited from the gametes. Mol Cell. 2012;47:1-12.
41. Gregg C, Zhang J, Weissbourd B, Luo S, Schroth GP, Haig D, et al. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science. 2010;329:643-8.
42. Hiura H, Sugawara A, Ogawa H, John RM, Miyauchi N, Miyanari Y, et al. A tripartite paternally methylated region within the Gpr1-Zdbf2 imprinted domain on mouse chromosome 1 identified by meDIP-on-chip. Nucleic Acids Res. 2010;38:4929-45.
43. Kobayashi H, Yamada K, Morita S, Hiura H, Fukuda A, Kagami M, et al. Identification of the mouse paternally expressed imprinted gene Zdbf2 on chromosome 1 and its imprinted human homolog ZDBF2 on chromosome 2. Genomics. 2009;93:461-72.
44. Crackower MA, Kolas NK, Noguchi J, Sarao R, Kikuchi K, Kaneko H, et al. Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science. 2003;300:1291-5.
45. Liu Y, Toh H, Sasaki H, Zhang X, Cheng X. An atomic model of Zfp57 recognition of CpG methylation within a specific DNA sequence. Genes Dev. 2012;26:2374-9.
46. McEwen KR, Ferguson-Smith AC. Distinguishing epigenetic marks of developmental and imprinting regulation. Epigenet Chromatin. 2010;3:2.
47. Rowe HM, Kapopoulou A, Corsinotti A, Fasching L, Macfarlan TS, Tarabay Y, et al. TRIM28 repression of retrotransposon-based enhancers is necessary to preserve transcriptional dynamics in embryonic stem cells. Genome Res. 2013;23:452-61.
48. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, et al. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol. 2007;9:64-71.
49. Lorthongpanich C, Cheow LF, Balu S, Quake SR, Knowles BB, Burkholder WF, et al. Single-cell DNA-methylation analysis reveals epigenetic chimerism in preimplantation embryos. Science. 2013;341:1110-2.
50. Xiol J, Cora E, Koglgruber R, Chuma S, Subramanian S, Hosokawa M, et al. A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol Cell. 2012;47:970-9.
51. Meng X, Lu X, Morris CA, Keating MT. A novel human gene FKBP6 is deleted in Williams syndrome. Genomics. 1998;52:130-7.
52. Pérez Jurado LA, Peoples R, Kaplan P, Hamel BC, Francke U. Molecular definition of the chromosome 7 deletion in Williams syndrome and parent-of-origin effects on growth. Am J Hum Genet. 1996;59:781-92.
53. Takikawa S, Wang X, Ray C, Vakulenko M, Bell FT, Li X. Human and mouse ZFP57 proteins are functionally interchangeable in maintaining genomic imprinting at multiple imprinted regions in mouse ES cells. Epigenetics. 2013;8:1-12.
54. Schalkwyk LC, Meaburn EL, Smith R, Dempster EL, Jeffries AR, Davies MN, et al. Allelic skewing of DNA methylation is widespread across the genome. Am J Hum Genet. 2010;86:196-212.
55. Xie W, Barr CL, Kim A, Yue F, Lee AY, Eubanks J, et al. Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell. 2012;148:816-31.
56. Shoemaker R, Deng J, Wang W, Zhang K. Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Res. 2010;20:883-9.
57. Schilling E, El Chartouni C, Rehli M. Allele-specific DNA methylation in mouse strains is mainly determined by cis-acting sequences. Genome Res. 2009;19:2028-35.
58. Majewski J, Pastinen T. The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet. 2011;27:72-9.
59. Goncalves A, Leigh-Brown S, Thybert D, Stefflova K, Turro E, Flicek P, et al. Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. Genome Res. 2012;22:2376-84.
60. Sun B, Ito M, Mendjan S, Ito Y, Brons IGM, Murrell A, et al. Status of genomic imprinting in epigenetically distinct pluripotent stem cells. Stem Cells. 2012;30:161-8.
61. Ying Q-L, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, et al. The ground state of embryonic stem cell self-renewal. Nature. 2008;453:519-23.
62. Ying Q-L, Stavridis M, Griffiths D, Li M, Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol. 2003;21:183-6.
63. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005;3, e283.
64. Litt MD, Simpson M, Recillas-Targa F, Prioleau MN, Felsenfeld G. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 2001;20:2224-35.
65. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-86.