Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern

Cell

Volumn 153, Issue 4, 2013, Pages 759-772

  Potok, Magdalena E ^a,b   Nix, David A ^b   Parnell, Timothy J ^a,b   Cairns, Bradley R ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; ENZYME INHIBITION; FERTILIZATION; GAMETE; GENE; GENE ACTIVITY; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; GENOME; GERM CELL; HISTONE MODIFICATION; HOX GENE; MUSCLE; NONHUMAN; OOCYTE; PIWIL1 GENE; PRIORITY JOURNAL; SPERM; ZEBRA FISH; ZYGOTE;

EID: 84877711740     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.04.030     Document Type: Article

References (53)

1. R.D. Almeida, M. Loose, V. Sottile, E. Matsa, C. Denning, L. Young, A.D. Johnson, M. Gering, and A. Ruzov 5-hydroxymethyl-cytosine enrichment of non-committed cells is not a universal feature of vertebrate development Epigenetics 7 2012 383 389
2. I.S. Andersen, A.H. Reiner, H. Aanes, P. Aleström, and P. Collas Developmental features of DNA methylation during activation of the embryonic zebrafish genome Genome Biol. 13 2012 R65
3. A. Arpanahi, M. Brinkworth, D. Iles, S.A. Krawetz, A. Paradowska, A.E. Platts, M. Saida, K. Steger, P. Tedder, and D. Miller Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences Genome Res. 19 2009 1338 1349
4. O. Bogdanovic, S.W. Long, S.J. van Heeringen, A.B. Brinkman, J.L. Gómez-Skarmeta, H.G. Stunnenberg, P.L. Jones, and G.J. Veenstra Temporal uncoupling of the DNA methylome and transcriptional repression during embryogenesis Genome Res. 21 2011 1313 1327
5. O. Bogdanovic, A. Fernandez-Miñán, J.J. Tena, E. de la Calle-Mustienes, C. Hidalgo, I. van Kruysbergen, S.J. van Heeringen, G.J. Veenstra, and J.L. Gómez-Skarmeta Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis Genome Res. 22 2012 2043 2053
6. J. Borgel, S. Guibert, Y. Li, H. Chiba, D. Schübeler, H. Sasaki, T. Forné, and M. Weber Targets and dynamics of promoter DNA methylation during early mouse development Nat. Genet. 42 2010 1093 1100
7. P. Braude, V. Bolton, and S. Moore Human gene expression first occurs between the four- and eight-cell stages of preimplantation development Nature 332 1988 459 461
8. U. Brykczynska, M. Hisano, S. Erkek, L. Ramos, E.J. Oakeley, T.C. Roloff, C. Beisel, D. Schübeler, M.B. Stadler, and A.H. Peters Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa Nat. Struct. Mol. Biol. 17 2010 679 687
9. S.J. Cokus, S. Feng, X. Zhang, Z. Chen, B. Merriman, C.D. Haudenschild, S. Pradhan, S.F. Nelson, M. Pellegrini, and S.E. Jacobsen Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning Nature 452 2008 215 219
10. C.R. Farthing, G. Ficz, R.K. Ng, C.F. Chan, S. Andrews, W. Dean, M. Hemberger, and W. Reik Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes PLoS Genet. 4 2008 e1000116
11. G. Flach, M.H. Johnson, P.R. Braude, R.A. Taylor, and V.N. Bolton The transition from maternal to embryonic control in the 2-cell mouse embryo EMBO J. 1 1982 681 686
12. M.G. Goll, and M.E. Halpern DNA methylation in zebrafish Prog. Mol. Biol. Transl. Sci. 101 2011 193 218
13. T.P. Gu, F. Guo, H. Yang, H.P. Wu, G.F. Xu, W. Liu, Z.G. Xie, L. Shi, X. He, and S.G. Jin The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes Nature 477 2011 606 610
14. P. Hajkova, K. Ancelin, T. Waldmann, N. Lacoste, U.C. Lange, F. Cesari, C. Lee, G. Almouzni, R. Schneider, and M.A. Surani Chromatin dynamics during epigenetic reprogramming in the mouse germ line Nature 452 2008 877 881
15. S.S. Hammoud, D.A. Nix, H. Zhang, J. Purwar, D.T. Carrell, and B.R. Cairns Distinctive chromatin in human sperm packages genes for embryo development Nature 460 2009 473 478
16. R.D. Hawkins, G.C. Hon, L.K. Lee, Q. Ngo, R. Lister, M. Pelizzola, L.E. Edsall, S. Kuan, Y. Luu, and S. Klugman Distinct epigenomic landscapes of pluripotent and lineage-committed human cells Cell Stem Cell 6 2010 479 491
17. T.L. Hoffman, A.L. Javier, S.A. Campeau, R.D. Knight, and T.F. Schilling Tfap2 transcription factors in zebrafish neural crest development and ectodermal evolution J. Exp. Zoolog. B Mol. Dev. Evol. 308 2007 679 691
18. S.K. Howlett, and W. Reik Methylation levels of maternal and paternal genomes during preimplantation development Development 113 1991 119 127
19. K. Iqbal, S.G. Jin, G.P. Pfeifer, and P.E. Szabó Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine Proc. Natl. Acad. Sci. USA 108 2011 3642 3647
20. D.A. Kane, and C.B. Kimmel The zebrafish midblastula transition Development 119 1993 447 456
21. H. Knaut, F. Pelegri, K. Bohmann, H. Schwarz, and C. Nüsslein- Volhard Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification J. Cell Biol. 149 2000 875 888
22. H. Kobayashi, T. Sakurai, M. Imai, N. Takahashi, A. Fukuda, O. Yayoi, S. Sato, K. Nakabayashi, K. Hata, and Y. Sotomaru Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks PLoS Genet. 8 2012 e1002440
23. L. Laurent, E. Wong, G. Li, T. Huynh, A. Tsirigos, C.T. Ong, H.M. Low, K.W. Kin Sung, I. Rigoutsos, J. Loring, and C.L. Wei Dynamic changes in the human methylome during differentiation Genome Res. 20 2010 320 331
24. L.C. Lindeman, I.S. Andersen, A.H. Reiner, N. Li, H. Aanes, O. Strup, C. Winata, S. Mathavan, F. Müller, P. Aleström, and P. Collas Prepatterning of developmental gene expression by modified histones before zygotic genome activation Dev. Cell 21 2011 993 1004
25. R. Lister, R.C. O'Malley, J. Tonti-Filippini, B.D. Gregory, C.C. Berry, A.H. Millar, and J.R. Ecker Highly integrated single-base resolution maps of the epigenome in Arabidopsis Cell 133 2008 523 536
26. R. Lister, M. Pelizzola, R.H. Dowen, R.D. Hawkins, G. Hon, J. Tonti-Filippini, J.R. Nery, L. Lee, Z. Ye, and Q.M. Ngo Human DNA methylomes at base resolution show widespread epigenomic differences Nature 462 2009 315 322
27. H.K. Long, D. Sims, A. Heger, N.P. Blackledge, C. Kutter, M.L. Wright, F. Grutzner, D.T. Odom, R. Patient, and C.P. Ponting Epigenetic conservation at gene regulatory elements revealed by non-methylated DNA profiling in seven vertebrates eLife 2 2013 e00348
28. D. Macleod, V.H. Clark, and A. Bird Absence of genome-wide changes in DNA methylation during development of the zebrafish Nat. Genet. 23 1999 139 140
29. C.C. Martin, L. Laforest, M.A. Akimenko, and M. Ekker A role for DNA methylation in gastrulation and somite patterning Dev. Biol. 206 1999 189 205
30. W. Mayer, A. Niveleau, J. Walter, R. Fundele, and T. Haaf Demethylation of the zygotic paternal genome Nature 403 2000 501 502
31. R.A. McGowan, and C.C. Martin DNA methylation and genome imprinting in the zebrafish, Danio rerio: some evolutionary ramifications Biochem. Cell Biol. 75 1997 499 506
32. A. Meissner, T.S. Mikkelsen, H. Gu, M. Wernig, J. Hanna, A. Sivachenko, X. Zhang, B.E. Bernstein, C. Nusbaum, and D.B. Jaffe Genome-scale DNA methylation maps of pluripotent and differentiated cells Nature 454 2008 766 770
33. A.A. Mhanni, and R.A. McGowan Global changes in genomic methylation levels during early development of the zebrafish embryo Dev. Genes Evol. 214 2004 412 417
34. F. Mohn, M. Weber, M. Rebhan, T.C. Roloff, J. Richter, M.B. Stadler, M. Bibel, and D. Schübeler Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors Mol. Cell 30 2008 755 766
35. Y. Okada, K. Yamagata, K. Hong, T. Wakayama, and Y. Zhang A role for the elongator complex in zygotic paternal genome demethylation Nature 463 2010 554 558
36. J. Oswald, S. Engemann, N. Lane, W. Mayer, A. Olek, R. Fundele, W. Dean, W. Reik, and J. Walter Active demethylation of the paternal genome in the mouse zygote Curr. Biol. 10 2000 475 478
37. S.A. Smallwood, S. Tomizawa, F. Krueger, N. Ruf, N. Carli, A. Segonds-Pichon, S. Sato, K. Hata, S.R. Andrews, and G. Kelsey Dynamic CpG island methylation landscape in oocytes and preimplantation embryos Nat. Genet. 43 2011 811 814
38. Z.D. Smith, M.M. Chan, T.S. Mikkelsen, H. Gu, A. Gnirke, A. Regev, and A. Meissner A unique regulatory phase of DNA methylation in the early mammalian embryo Nature 484 2012 339 344
39. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, and S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872
40. L. Tan, and Y.G. Shi Tet family proteins and 5-hydroxymethylcytosine in development and disease Development 139 2012 1895 1902
41. Thisse, B., Pflumio, S., Fürthauer, M., Loppin, B., Heyer, V., Degrave, A., Woehl, R., Lux, A., Steffan, T., Charbonnier, X.Q. and Thisse, C. (2001) Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission (http://zfin.org).
42. N.L. Vastenhouw, and A.F. Schier Bivalent histone modifications in early embryogenesis Curr. Opin. Cell Biol. 24 2012 374 386
43. N.L. Vastenhouw, Y. Zhang, I.G. Woods, F. Imam, A. Regev, X.S. Liu, J. Rinn, and A.F. Schier Chromatin signature of embryonic pluripotency is established during genome activation Nature 464 2010 922 926
44. M. Weber, I. Hellmann, M.B. Stadler, L. Ramos, S. Pääbo, M. Rebhan, and D. Schübeler Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome Nat. Genet. 39 2007 457 466
45. M. Westerfield The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio) 2000 University of Oregon Press Eugene, OR
46. S.F. Wu, H. Zhang, and B.R. Cairns Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm Genome Res. 21 2011 578 589
47. S.F. Wu, H. Zhang, S.S. Hammoud, M. Potok, D.A. Nix, D.A. Jones, and B.R. Cairns DNA methylation profiling in zebrafish Methods Cell Biol. 104 2011 327 339
48. V.W. Zhou, A. Goren, and B.E. Bernstein Charting histone modifications and the functional organization of mammalian genomes Nat. Rev. Genet. 12 2011 7 18
49. T.J. Dahlem, K. Hoshijima, M.J. Jurynec, D. Gunther, C.G. Starker, A.S. Locke, A.M. Weis, D.F. Voytas, and D.J. Grunwald Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome PLoS Genet. 8 2012 e1002861
50. S. Feng, S.J. Cokus, X. Zhang, P.Y. Chen, M. Bostick, M.G. Goll, J. Hetzel, J. Jain, S.H. Strauss, and M.E. Halpern Conservation and divergence of methylation patterning in plants and animals Proc. Natl. Acad. Sci. USA 107 2010 8689 8694
51. M. Gardiner-Garden, and M. Frommer CpG islands in vertebrate genomes J. Mol. Biol. 196 1987 261 282
52. D.A. Nix, T.L. Di Sera, B.K. Dalley, B.A. Milash, R.M. Cundick, K.S. Quinn, and S.J. Courdy Next generation tools for genomic data generation, distribution, and visualization BMC Bioinformatics 11 2010 455
53. A.R. Quinlan, and I.M. Hall BEDTools: a flexible suite of utilities for comparing genomic features Bioinformatics 26 2010 841 842