Dynamic reprogramming of 5-hydroxymethylcytosine during early porcine embryogenesis

Theriogenology

Volumn 81, Issue 3, 2014, Pages 496-508

  Cao, Zubing ^a   Zhou, Naru ^b   Zhang, Yu ^b   Zhang, Yuanliang ^b   Wu, Ronghua ^b   Li, Yunsheng ^b   Zhang, Yunhai ^b   Li, Ning ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b ANHUI AGRICULTURAL UNIVERSITY   (China)

Author keywords

5 Hydroxymethylation; Active DNA demethylation; Embryo; Pig

Indexed keywords

SUIDAE; SUS;

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; 5-HYDROXYMETHYLCYTOSINE; CYTOSINE; DRUG DERIVATIVE;

5-HYDROXYMETHYLATION; ACTIVE DNA DEMETHYLATION; ANIMAL; ANIMAL DISEASE; ARTICLE; CELL NUCLEUS TRANSPLANTATION; DNA METHYLATION; EMBRYO; EMBRYO DEVELOPMENT; GENETICS; METABOLISM; PRENATAL DEVELOPMENT; SWINE;

5-HYDROXYMETHYLATION; ACTIVE DNA DEMETHYLATION; EMBRYO; PIG;

5-METHYLCYTOSINE; ANIMALS; CYTOSINE; DNA METHYLATION; EMBRYONIC DEVELOPMENT; NUCLEAR TRANSFER TECHNIQUES; SWINE;

EID: 84891633353     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2013.10.025     Document Type: Article

References (54)

1. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002, 16:6-21.
2. Chen T., Li E. Structure and function of eukaryotic DNA methyltransferases. Curr Top Dev Biol 2004, 60:55-89.
3. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 2010, 11:607-620.
4. Saitou M., Kagiwada S., Kurimoto K. Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 2012, 139:15-31.
5. Hajkova P., Erhardt S., Lane N., Haaf T., El-Maarri O., Reik W., et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002, 117:15-23.
6. Popp C., Dean W., Feng S., Cokus S.J., Andrews S., Pellegrini M., et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 2010, 463:1101-1105.
7. Monk M., Boubelik M., Lehnert S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 1987, 99:371-382.
8. Mayer W., Niveleau A., Walter J., Fundele R., Haaf T. Demethylation of the zygotic paternal genome. Nature 2000, 403:501-502.
9. Santos F., Hendrich B., Reik W., Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002, 241:172-182.
10. Oswald J., Engemann S., Lane N., Mayer W., Olek A., Fundele R., et al. Active demethylation of the paternal genome in the mouse zygote. Curr Biol 2000, 10:475-478.
11. Fulka J., Fulka H., Slavik T., Okada K., Fulka J. DNA methylation pattern in pig invivo produced embryos. Histochem Cell Biol 2006, 126:213-217.
12. Park J.S., Jeong Y.S., Shin S.T., Lee K.K., Kang Y.K. Dynamic DNA methylation reprogramming: active demethylation and immediate remethylation in the male pronucleus of bovine zygotes. Dev Dyn 2007, 236:2523-2533.
13. Xu Y., Zhang J.J., Grifo J.A., Krey L.C. DNA methylation patterns in human tripronucleate zygotes. Mol Hum Reprod 2005, 11:167-171.
14. Bhattacharya S.K., Ramchandani S., Cervoni N., Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 1999, 397:579-583.
15. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004, 73:39-85.
16. Barreto G., Schafer A., Marhold J., Stach D., Swaminathan S.K., Handa V., et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445:671-675.
17. Okada Y., Yamagata K., Hong K., Wakayama T., Zhang Y. A role for the elongator complex in zygotic paternal genome demethylation. Nature 2010, 463:554-558.
18. Cliffe L.J., Kieft R., Southern T., Birkeland S.R., Marshall M., Sweeney K., et al. JBP1 and JBP2 are two distinct thymidine hydroxylases involved in J biosynthesis in genomic DNA of African trypanosomes. Nucleic Acids Res 2009, 37:1452-1462.
19. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
20. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466:1129-1133.
21. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
22. Ko M., Huang Y., Jankowska A.M., Pape U.J., Tahiliani M., Bandukwala H.S., et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 2010, 468:839-843.
23. Iqbal K., Jin S.G., Pfeifer G.P., Szabo P.E. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci U S A 2011, 108:3642-3647.
24. Wossidlo M., Nakamura T., Lepikhov K., Marques C.J., Zakhartchenko V., Boiani M., et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2011, 2:241.
25. Gu T.P., Guo F., Yang H., Wu H.P., Xu G.F., Liu W., et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 2011, 477:606-610.
26. Dean W., Santos F., Stojkovic M., Zakhartchenko V., Walter J., Wolf E., et al. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci U S A 2001, 98:13734-13738.
27. Gioia L., Barboni B., Turriani M., Capacchietti G., Pistilli M.G., Berardinelli P., et al. The capability of reprogramming the male chromatin after fertilization is dependent on the quality of oocyte maturation. Reproduction 2005, 130:29-39.
28. Zhang Y., Li J., Villemoes K., Pedersen A.M., Purup S., Vajta G. An epigenetic modifier results in improved invitro blastocyst productionafter somatic cell nuclear transfer. Cloning Stem Cells 2007, 9:357-363.
29. Zhang K., Wei H.X., Zhang Y.H., Wang S.H., Li Y., Dai Y.P., et al. Effects of ghrelin on invitro development of porcine invitro fertilized and parthenogenetic embryos. J Reprod Dev 2007, 53:647-653.
30. Yoshioka K., Suzuki C., Tanaka A., Anas I.M., Iwamura S. Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol Reprod 2002, 66:112-119.
31. Gao Y., Hyttel P., Hall V.J. Regulation of H3K27me3 and H3K4me3 during early porcine embryonic development. Mol Reprod Dev 2010, 77:540-549.
32. Ross P.J., Ragina N.P., Rodriguez R.M., Iager A.E., Siripattarapravat K., Lopez-Corrales N., et al. Polycomb gene expression and histone H3 lysine 27 trimethylation changes during bovine preimplantation development. Reproduction 2008, 136:777-785.
33. Han X., Han J., Ding F., Cao S., Lim S.S., Dai Y., et al. Generation of induced pluripotent stem cells from bovine embryonic fibroblast cells. Cell Res 2011, 21:1509-1512.
34. Laurincik J., Rath D., Niemann H. Differences in pronucleus formation and first cleavage following invitro fertilization between pig oocytes matured invivo and invitro. J Reprod Fertil 1994, 102:277-284.
35. Miyamoto K., Hoshino Y., Minami N., Yamada M., Imai H. Effects of synchronization of donor cell cycle on embryonic development and DNA synthesis in porcine nuclear transfer embryos. J Reprod Dev 2007, 53:237-246.
36. Barnetová I., Okada K. Genome reprogramming during the first cell cycle in invitro produced porcine embryos. Czech J Anim Sci 2010, 55:49-57.
37. Jeong Y.S., Yeo S., Park J.S., Koo D.B., Chang W.K., Lee K.K., et al. DNA methylation state is preserved in the sperm-derived pronucleus of the pig zygote. Int J Dev Biol 2007, 51:707-714.
38. Jeong Y.S., Yeo S., Park J.S., Lee K.K., Kang Y.K. Gradual development of a genome-wide H3-K9 trimethylation pattern in paternally derived pig pronucleus. Dev Dyn 2007, 236:1509-1516.
39. He Y.F., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011, 333:1303-1307.
40. Inoue A., Zhang Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 2011, 334:194.
41. Hirasawa R., Chiba H., Kaneda M., Tajima S., Li E., Jaenisch R., et al. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 2008, 22:1607-1616.
42. Wrenzycki C., Niemann H. Epigenetic reprogramming in early embryonic development: effects of in-vitro production and somatic nuclear transfer. Reprod Biomed Online 2003, 7:649-656.
43. Ko Y.G., Nishino K., Hattori N., Arai Y., Tanaka S., Shiota K. Stage-by-stage change in DNA methylation status of Dnmt1 locus during mouse early development. J Biol Chem 2005, 280:9627-9634.
44. Jeong Y.S., Oh K.B., Park J.S., Kim J.S., Kang Y.K. Cytoplasmic localization of oocyte-specific variant of porcine DNA methyltransferase-1 during early development. Dev Dyn 2009, 238:1666-1673.
45. Deshmukh R.S., Ostrup O., Ostrup E., Vejlsted M., Niemann H., Lucas-Hahn A., et al. DNA methylation in porcine preimplantation embryos developed invivo and produced by invitro fertilization, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics 2011, 6:177-187.
46. Santos F., Zakhartchenko V., Stojkovic M., Peters A., Jenuwein T., Wolf E., et al. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol 2003, 13:1116-1121.
47. Santos F., Dean W. Epigenetic reprogramming during early development in mammals. Reproduction 2004, 127:643-651.
48. Santos F., Dean W. Using immunofluorescence to observe methylation changes in mammalian preimplantation embryos. Methods Mol Biol 2006, 325:129-137.
49. Fulka H., Mrazek M., Tepla O., Fulka J. DNA methylation pattern in human zygotes and developing embryos. Reproduction 2004, 128:703-708.
50. Yang J., Yang S., Beaujean N., Niu Y., He X., Xie Y., et al. Epigenetic marks in cloned rhesus monkey embryos: comparison with counterparts produced invitro. Biol Reprod 2007, 76:36-42.
51. Zhang P., Su L., Wang Z., Zhang S., Guan J., Chen Y., et al. The involvement of 5-hydroxymethylcytosine in active DNA demethylation in mice. Biol Reprod 2012, 86:104.
52. Xu Y., Wu F., Tan L., Kong L., Xiong L., Deng J., et al. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 2011, 42:451-464.
53. Kirchhof N., Carnwath J.W., Lemme E., Anastassiadis K., Scholer H., Niemann H. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 2000, 63:1698-1705.
54. Koh K.P., Yabuuchi A., Rao S., Huang Y., Cunniff K., Nardone J., et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011, 8:200-213.