Epigenetic reprogramming: Preparing the epigenome for the next generation

Biochemical Society Transactions

Volumn 41, Issue 3, 2013, Pages 809-814

  Rose, Catherine M ^a   Van Den Driesche, Sander ^b   Meehan, Richard R ^c   Drake, Amanda J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

DNA methylation; Epigenetic reprogramming; Germline

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B;

CELL DIFFERENTIATION; CELL LINEAGE; CELL MIGRATION; CONFERENCE PAPER; DEAMINATION; DNA METHYLATION; DNA MODIFICATION; EMBRYO DEVELOPMENT; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GENOME IMPRINTING; GERM CELL; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; MITOSIS INHIBITION; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATION; PRIORITY JOURNAL; PROMOTER REGION; RETROPOSON; TRANSCRIPTION INITIATION;

ANIMALS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HUMANS; INHERITANCE PATTERNS; MALE; MICE; NUCLEAR REPROGRAMMING;

EID: 84878337055     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120356     Document Type: Conference Paper

References (63)

1. Hajkova, P., Erhardt, S., Lane, N., Haaf, T., El-Maarri, O., Reik, W., Walter, J. and Surani, M.A. (2002) Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117, 15-23
2. De Felici, M. (2011) Nuclear reprogramming in mouse primordial germ cells: epigenetic contribution. Stem Cells Int. 2011, 425863
3. Wu, S.C. and Zhang, Y. (2010) Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607-620
4. Choy, M.-K., Movassagh, M., Goh, H.-G., Bennett, M., Down, T. and Foo, R. (2010) Genome-wide conserved consensus transcription factor binding motifs are hyper-methylated. BMC Genomics 11, 519
5. Ng, H.-H., Zhang, Y., Hendrich, B., Johnson, C.A., Turner, B.M., Erdjument-Bromage, H., Tempst, P., Reinberg, D. and Bird, A. (1999) MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23, 58-61
6. Walsh, C.P., Chaillet, J.R. and Bestor, T.H. (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20, 116-117
7. Sado, T., Fenner, M.H., Tan, S.-S., Tam, P., Shioda, T. and Li, E. (2000) X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and random X inactivation. Dev. Biol. 225, 294-303
8. Hackett, J.A., Reddington, J., Nestor, C., Dunican, D.S., Branco, M., Reichmann, J., Reik, W., Surani, M.A., Adams, I.R. and Meehan, R.R. (2012) Promoter DNA methylation couples genome-defence mechanisms to epigenetic reprogramming in the mouse germline. Development 139, 3623-3632
9. Li, E., Bestor, T.H. and Jaenisch, R. (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926
10. Li, E., Beard, C. and Jaenisch, R. (1993) Role for DNA methylation in genomic imprinting. Nature 366, 362-365
11. Howell, C.Y., Bestor, T.H., Ding, F., Latham, K.E., Mertineit, C., Trasler, J.M. and Chaillet, J.R. (2001) Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104, 829-838
12. Mertineit, C., Yoder, J.A., Taketo, T., Laird, D.W., Trasler, J.M. and Bestor, T.H. (1998) Sex-specific exons control DNA methyltransferase in mammalian germ cells. Development 125, 889-897
13. Kaneda, M., Okano, M., Hata, K., Sado, T., Tsujimoto, N., Li, E. and Sasaki, H. (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429, 900-903
14. Kato, Y., Kaneda, M., Hata, K., Kumaki, K., Hisano, M., Kohara, Y., Okano, M., Li, E., Nozaki, M. and Sasaki, H. (2007) Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 16, 2272-2280
15. Gowher, H., Liebert, K., Hermann, A., Xu, G. and Jeltsch, A. (2005) Mechanism of stimulation of catalytic activity of Dnmt3A and Dnmt3B DNA-(cytosine-C5)-methyltransferases by Dnmt3L. J. Biol. Chem. 280, 13341-13348
16. Kaneda, M., Hirasawa, R., Chiba, H., Okano, M., Li, E. and Sasaki, H. (2010) Genetic evidence for Dnmt3a-dependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells 15, 169-179
17. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L.M., Liu, D.R., Aravind, L. and Rao, A. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935
18. Ito, S., D'Alessio, A.C., Taranova, O.V., Hong, K., Sowers, L.C. and Zhang, Y. (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133
19. Nestor, C.E., Ottaviano, R., Reddington, J., Sproul, D., Reinhardt, D., Dunican, D., Katz, E., Dixon, J.M., Harrison, D.J. and Meehan, R.R. (2012) Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res. 22, 467-477
20. Williams, K., Christensen, J., Terndrup Pedersen, M., Johansen, J.V., Cloos, P.A.C., Rappsilber, J. and Helin, K. (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473, 343-348
21. Ficz, G., Branco, M.R., Seisenberger, S., Santos, F., Krueger, F., Hore, T.A., Marques, C.J., Andrews, S. and Reik, W. (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398-402
22. Ito, S., Shen, L., Dai, Q., Wu, S.C., Collins, L.B., Swenberg, J.A., He, C. and Zhang, Y. (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303
23. He, Y.F., Li, B.-Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L. et al. (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307
24. Inoue, A., Shen, L., Dai, Q., He, C. and Zhang, Y. (2011) Generation and replication-dependent dilution of 5fC and 5caC during mouse preimplantation development. Cell Res. 21, 1670-1676
25. Raiber, E.-A., Beraldi, D., Ficz, G., Burgess, H., Branco, M., Murat, P., Oxley, D., Booth, M., Reik, W. and Balasubramanian, S. (2012) Genome-wide distribution of 5-formylcytosine in ES cells is associated with transcription and depends on thymine DNA glycosylase. Genome Biol. 13, R69
26. Hashimoto, H., Liu, Y., Upadhyay, A.K., Chang, Y., Howerton, S.B., Vertino, P.M., Zhang, X. and Cheng, X. (2012) Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res. 40, 4841-4849
27. Nabel, C.S., Jia, H., Ye, Y., Shen, L., Goldschmidt, H.L., Stivers, J.T., Zhang, Y. and Kohli, R.M. (2012) AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat. Chem. Biol. 8, 751-758
28. Hackett, J.A., Zylicz, J.J. and Surani, M.A. (2012) Parallel mechanisms of epigenetic reprogramming in the germline. Trends Genet. 28, 164-174
29. Popp, C., Dean, W., Feng, S., Cokus, S.J., Andrews, S., Pellegrini, M., Jacobsen, S.E. and Reik, W. (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105
30. Inoue, A. and Zhang, Y. (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334, 194
31. Valinluck, V. and Sowers, L.C. (2007) Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res. 67, 946-950
32. Wossidlo, M., Arand, J., Sebastiano, V., Lepikhov, K., Boiani, M., Reinhardt, R., Scholer, H. and Walter, J. (2010) Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J. 29, 1877-1888
33. Hajkova, P., Jeffries, S.J., Lee, C., Miller, N., Jackson, S.P. and Surani, M.A. (2010) Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329, 78-82
34. Nestor, C., Ruzov, A., Meehan, R.R. and Dunican, D.S. (2010) Enzymatic approaches and bisulfite sequencing cannot distinguish between 5-methylcytosine and 5-hydroxymethylcytosine in DNA. BioTechniques 48, 317-319
35. Ginsburg, M., Snow, M.H. and McLaren, A. (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110, 521-528
36. Molyneaux, K.A., Stallock, J., Schaible, K. and Wylie, C. (2001) Time-lapse analysis of living mouse germ cell migration. Dev. Biol. 240, 488-498
37. Shovlin, T.C., Durcova-Hills, G., Surani, A. and McLaren, A. (2008) Heterogeneity in imprinted methylation patterns of pluripotent embryonic germ cells derived from pre-migratory mouse germ cells. Dev. Biol. 313, 674-681
38. Lee, J., Inoue, K., Ono, R., Ogonuki, N., Kohda, T., Kaneko-Ishino, T., Ogura, A. and Ishino, F. (2002) Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 129, 1807-1817
39. Yamazaki, Y., Mann, M.R.W., Lee, S.S., Marh, J., McCarrey, J.R., Yanagimachi, R. and Bartolomei, M.S. (2003) Reprogramming of primordial germ cells begins before migration into the genital ridge, making these cells inadequate donors for reproductive cloning. Proc. Natl. Acad. Sci. U.S.A. 100, 12207-12212
40. Sato, S., Yoshimizu, T., Sato, E. and Matsui, Y. (2003) Erasure of methylation imprinting of Igf2r during mouse primordial germ-cell development. Mol. Reprod. Dev. 65, 41-50
41. Guibert, S., Forné, T. and Weber, M. (2012) Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 22, 633-641
42. Seki, Y., Hayashi, K., Itoh, K., Mizugaki, M., Saitou, M. and Matsui, Y. (2005) Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278, 440-458
43. Hackett, J.A., Sengupta, R., Zylicz, J.J., Murakami, K., Lee, C., Down, T.A. and Surani, M.A. (2013) Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339, 448-452
44. Seisenberger, S., Andrews, S., Krueger, F., Arand, J., Walter, J., Santos, F., Popp, C., Thienpont, B., Dean, W. and Reik, W. (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 48, 849-862
45. Lees-Murdock, D.J., De Felici, M. and Walsh, C.P. (2003) Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics 82, 230-237
46. Lane, N., Dean, W., Erhardt, S., Hajkova, P., Surani, A., Walter, J. and Reik, W. (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35, 88-93
47. Reichmann, J., Crichton, J.H., Madej, M.J., Taggart, M., Gautier, P., Garcia-Perez, J.L., Meehan, R.R. and Adams, I.R. (2012) Microarray analysis of LTR retrotransposon silencing identifies HDAC1 as a regulator of retrotransposon expression in mouse embryonic stem cells. PLoS Comput. Biol. 8, e1002486
48. Tachibana, M., Matsumura, Y., Fukuda, M., Kimura, H. and Shinkai, Y. (2008) G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription. EMBO J. 27, 2681-2690
49. Tachibana, M., Ueda, J., Fukuda, M., Takeda, N., Ohta, T., Iwanari, H., Sakihama, T., Kodama, T., Hamakubo, T. and Shinkai, Y. (2005) Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev. 19, 815-826
50. Li, J.-Y., Lees-Murdock, D.J., Xu, G.-L. and Walsh, C.P. (2004) Timing of establishment of paternal methylation imprints in the mouse. Genomics 84, 952-960
51. Davis, T.L., Yang, G.J., McCarrey, J.R. and Bartolomei, M.S. (2000) The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum. Mol. Genet. 9, 2885-2894
52. Lucifero, D., Mertineit, C., Clarke, H.J., Bestor, T.H. and Trasler, J.M. (2002) Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79, 530-538
53. Obata, Y. and Kono, T. (2002) Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J. Biol. Chem. 277, 5285-5289
54. Quenneville, S., Verde, G., Corsinotti, A., Kapopoulou, A., Jakobsson, J., Offner, S., Baglivo, I., Pedone, P.V., Grimaldi, G., Riccio, A. and Trono, D. (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
55. Lucifero, D., La Salle, S., Bourc'his, D., Martel, J., Bestor, T. and Trasler, J. (2007) Coordinate regulation of DNA methyltransferase expression during oogenesis. BMC Dev. Biol. 7, 36
56. Niles, K.M., Chan, D., La Salle, S., Oakes, C.C. and Trasler, J.M. (2011) Critical period of nonpromoter DNA methylation acquisition during prenatal male germ cell development. PLoS ONE 6, e24156
57. Bourc'his, D. and Bestor, T.H. (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99
58. La Salle, S., Mertineit, C., Taketo, T., Moens, P.B., Bestor, T.H. and Trasler, J.M. (2004) Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells. Dev. Biol. 268, 403-415
59. Hyldig, S., Croxall, N., Contreras, D., Thomsen, P. and Alberio, R. (2011) Epigenetic reprogramming in the porcine germ line. BMC Dev. Biol. 11, 11
60. Almstrup, K., Nielsen, J.E., Mlynarska, O., Jansen, M.T., Jorgensen, A., Skakkebak, N.E. and Rajpert-De Meyts, E. (2010) Carcinoma in situ testis displays permissive chromatin modifications similar to immature foetal germ cells. Br. J. Cancer 103, 1269-1276
61. Wermann, H., Stoop, H., Gillis, A.J.M., Honecker, F., van Gurp, R.J., Ammerpohl, O., Richter, J., Oosterhuis, J.W., Bokemeyer, C. and Looijenga, L.H.J. (2010) Global DNA methylation in fetal human germ cells and germ cell tumours: association with differentiation and cisplatin resistance. J. Pathol. 221, 433-442
62. Poplinski, A., Tüttelmann, F., Kanber, D., Horsthemke, B. and Gromoll, J. (2010) Idiopathic male infertility is strongly associated with aberrant methylation of MEST and IGF2/H19 ICR1. Int. J. Androl. 33, 642-649
63. Hammoud, S.S., Purwar, J., Pflueger, C., Cairns, B.R. and Carrell, D.T. (2010) Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil. Steril. 94, 1728-1733