DPPA3 prevents cytosine hydroxymethylation of the maternal pronucleus and is required for normal development in bovine embryos

Epigenetics

Volumn 9, Issue 9, 2014, Pages 1271-1279

  Bakhtari, Azizollah ^a,b   Ross, Pablo J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ISFAHAN UNIVERSITY OF TECHNOLOGY   (Iran)

Author keywords

5 hydroxymethylcytosine; DPPA3; Epigenetic; Knockdown; Preimplantation; Reprogramming; TET; Zygote

Indexed keywords

COMPLEMENTARY DNA; CYTOSINE; MESSENGER RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR SOX2; PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATTLE; CONTROLLED STUDY; CYTOSINE HYDROXYMETHYLATION; DEVELOPMENTAL PLURIPOTENCY ASSOCIATED 3 GENE; DNA METHYLATION; EMBRYO DEVELOPMENT; EPIGENETICS; FERTILIZATION IN VITRO; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GENOME ACTIVATION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; METHYLATION; NONHUMAN; PARTHENOGENETIC ACTIVATION; PRONUCLEUS; QUANTITATIVE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; ANIMAL; BLASTOCYST; BOVINE; CELL NUCLEUS; FEMALE; GENETIC EPIGENESIS; GENETICS; METABOLISM; OOCYTE; ZYGOTE;

ANIMALS; BLASTOCYST; CATTLE; CELL NUCLEUS; CYTOSINE; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; FEMALE; GENE KNOCKDOWN TECHNIQUES; METHYLATION; OOCYTES; PROTEINS; RNA, SMALL INTERFERING; ZYGOTE;

EID: 84908221218     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.32087     Document Type: Article

References (32)

1. Romar R, De Santis T, Papillier P, Perreau C, Thélie A, Dell'Aquila ME, Mermillod P, Dalbiès- Tran R. Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age. Reprod Domest Anim 2011; 46:e23-30; PMID:20403124; http://dx.doi. org/10.1111/j.1439-0531.2010.01617.x
2. Thélie A, Papillier P, Pennetier S, Perreau C, Traverso JM, Uzbekova S, Mermillod P, Joly C, Humblot P, Dalbiès-Tran R. Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev Biol 2007; 7:125; PMID:17988387; http:// dx.doi.org/10.1186/1471-213X-7-125
3. Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA. Stella is a maternal effect gene required for normal early development in mice. Curr Biol 2003; 13:2110-7; PMID:14654002; http://dx.doi. org/10.1016/j.cub.2003.11.026
4. Sato M, Kimura T, Kurokawa K, Fujita Y, Abe K, Masuhara M, Yasunaga T, Ryo A, Yamamoto M, Nakano T. Identification of PGC7, a new gene expressed specifically in preimplantation embryos and germ cells. Mech Dev 2002; 113:91- 4; PMID:11900980; http://dx.doi.org/10.1016/ S0925-4773(02)00002-3
5. Saitou M, Payer B, Lange UC, Erhardt S, Barton SC, Surani MA. Specification of germ cell fate in mice. Philos Trans R Soc Lond B Biol Sci 2003; 358:1363- 70; PMID:14511483; http://dx.doi.org/10.1098/ rstb.2003.1324
6. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M, et al. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 2007; 9:64-71; PMID:17143267; http://dx.doi.org/10.1038/ncb1519
7. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010; 466:1129- 33; PMID:20639862; http://dx.doi.org/10.1038/ nature09303
8. Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG, et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 2011; 477:606-10; PMID:21892189; http:// dx.doi.org/10.1038/nature10443
9. Nakamura T, Liu YJ, Nakashima H, Umehara H, Inoue K, Matoba S, Tachibana M, Ogura A, Shinkai Y, Nakano T. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 2012; 486:415-9; PMID:22722204
10. Kocabas AM, Crosby J, Ross PJ, Otu HH, Beyhan Z, Can H, Tam WL, Rosa GJ, Halgren RG, Lim B, et al. The transcriptome of human oocytes. Proc Natl Acad Sci U S A 2006; 103:14027-32; PMID:16968779; http://dx.doi.org/10.1073/pnas.0603227103
11. Bian C, Yu X. PGC7 suppresses TET3 for protecting DNA methylation. Nucleic Acids Res 2014; 42:2893- 905; PMID:24322296; http://dx.doi.org/10.1093/ nar/gkt1261
12. Iqbal K, Jin SG, Pfeifer GP, Szabó PE. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci U S A 2011; 108:3642-7; PMID:21321204; http://dx.doi.org/10.1073/ pnas.1014033108
13. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, Boiani M, Arand J, Nakano T, Reik W, Walter J. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2011; 2:241; PMID:21407207; http://dx.doi.org/10.1038/ncomms1240
14. Bortvin A, Goodheart M, Liao M, Page DC. Dppa3 / Pgc7 / stella is a maternal factor and is not required for germ cell specification in mice. BMC Dev Biol 2004; 4:2; PMID:15018652; http://dx.doi. org/10.1186/1471-213X-4-2
15. Hayashi K, Lopes SM, Tang F, Surani MA. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 2008; 3:391-401; PMID:18940731; http://dx.doi.org/10.1016/j. stem.2008.07.027
16. Canovas S, Cibelli JB, Ross PJ. Jumonji domaincontaining protein 3 regulates histone 3 lysine 27 methylation during bovine preimplantation development. Proc Natl Acad Sci U S A 2012; 109:2400- 5; PMID:22308433; http://dx.doi.org/10.1073/ pnas.1119112109
17. Lee KB, Bettegowda A, Wee G, Ireland JJ, Smith GW. Molecular determinants of oocyte competence: potential functional role for maternal (oocytederived) follistatin in promoting bovine early embryogenesis. Endocrinology 2009; 150:2463- 71; PMID:19179440; http://dx.doi.org/10.1210/ en.2008-1574
18. Wu X, Li Y, Xue L, Wang L, Yue Y, Li K, Bou S, Li GP, Yu H. Multiple histone site epigenetic modifications in nuclear transfer and in vitro fertilized bovine embryos. Zygote 2011; 19:31-45; PMID:20609268; http://dx.doi.org/10.1017/S0967199410000328
19. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome. Nature 2000; 403:501-2; PMID:10676950; http:// dx.doi.org/10.1038/35000656
20. Beaujean N, Hartshorne G, Cavilla J, Taylor J, Gardner J, Wilmut I, Meehan R, Young L. Nonconservation of mammalian preimplantation methylation dynamics. Curr Biol 2004; 14:R266- 7; PMID:15062117; http://dx.doi.org/10.1016/j. cub.2004.03.019
21. Wilmut I, Beaujean N, de Sousa PA, Dinnyes A, King TJ, Paterson LA, Wells DN, Young LE. Somatic cell nuclear transfer. Nature 2002; 419:583- 6; PMID:12374931; http://dx.doi.org/10.1038/ nature01079
22. Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, Reik W. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci U S A 2001; 98:13734-8; PMID:11717434; http://dx.doi.org/10.1073/pnas.241522698
23. Pagé-Larivière F, Sirard MA. Spatiotemporal expression of DNA demethylation enzymes and histone demethylases in bovine embryos. Cell Reprogram 2014; 16:40-53; PMID:24459992; http://dx.doi. org/10.1089/cell.2013.0055
24. Liu YJ, Nakamura T, Nakano T. Essential role of DPPA3 for chromatin condensation in mouse oocytogenesis. Biol Reprod 2012; 86:40; PMID:22034526; http://dx.doi.org/10.1095/biolreprod.111.095018
25. Aravind L, Koonin EV. SAP - a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci 2000; 25:112-4; PMID:10694879; http://dx.doi.org/10.1016/S0968-0004(99)01537-6
26. Kono T, Sotomaru Y, Sato Y, Nakahara T. Development of androgenetic mouse embryos produced by in vitro fertilization of enucleated oocytes. Mol Reprod Dev 1993; 34:43-6; PMID:8418815; http://dx.doi.org/10.1002/mrd.1080340107
27. Kuijk EW, Du Puy L, Van Tol HT, Oei CH, Haagsman HP, Colenbrander B, Roelen BA. Differences in early lineage segregation between mammals. Dev Dyn 2008; 237:918-27; PMID:18330925; http://dx.doi. org/10.1002/dvdy.21480
28. Goissis MD, Cibelli JB. Functional characterization of SOX2 in bovine preimplantation embryos. Biol Reprod 2014; 90:30; PMID:24389873; http:// dx.doi.org/10.1095/biolreprod.113.111526
29. Wongtrakoongate P, Jones M, Gokhale PJ, Andrews PW. STELLA facilitates differentiation of germ cell and endodermal lineages of human embryonic stem cells. PLoS One 2013; 8:e56893; PMID:23457636; http://dx.doi.org/10.1371/journal.pone.0056893
30. Chitwood JL, Rincon G, Kaiser GG, Medrano JF, Ross PJ. RNA-seq analysis of single bovine blastocysts. BMC Genomics 2013; 14:350; PMID:23705625; http://dx.doi.org/10.1186/1471-2164-14-350
31. Iqbal K, Chitwood JL, Meyers-Brown GA, Roser JF, Ross PJ. RNA-seq transcriptome profiling of equine inner cell mass and trophectoderm. Biol Reprod 2014; 90:61; PMID:24478389; http://dx.doi.org/10.1095/ biolreprod.113.113928
32. Ross PJ, Beyhan Z, Iager AE, Yoon SY, Malcuit C, Schellander K, Fissore RA, Cibelli JB. Parthenogenetic activation of bovine oocytes using bovine and murine phospholipase C zeta. BMC Dev Biol 2008; 8:16; PMID:18284699; http://dx.doi. org/10.1186/1471-213X-8-16