Gene-specific profiling of DNA methylation and mRNA expression in bovine oocytes derived from follicles of different size categories
F. Mattern A , J. Heinzmann B C D , D. Herrmann B , A. Lucas-Hahn B , T. Haaf A and H. Niemann B
+ Author Affiliations
- Author Affiliations
A Institute of Human Genetics, Julius Maximilians University, 97070 Würzburg, Germany.
B Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut, Federal Research Institute of Animal Health, Mariensee, 31535 Neustadt, Germany.
C Present address: Gynemed GmbH and CO. KG, 23738 Lensahn, Germany.
D Corresponding author. Email: heiner.niemann@fli.de
Reproduction, Fertility and Development 29(10) 2040-2051 https://doi.org/10.1071/RD16327
Submitted: 19 August 2016 Accepted: 14 December 2016 Published: 3 February 2017
Abstract
Epigenetic changes, such as DNA methylation, play an essential role in the acquisition of full developmental competence by mammalian oocytes during the late follicular growth phase. Here we used the bovine model to investigate the DNA methylation profiles of seven candidate genes (imprinted: bH19, bSNRPN; non-imprinted: bZAR1, bDNMT3A, bOCT4, bDNMT3 Lo and bDNMT3 Ls) and the mRNA expression of nine candidate genes (imprinted: bSNRPN, bPEG3, bIGF2R; non-imprinted: bPRDX1, bDNMT1B, bDNMT3A, bZAR1, bHSF1 and bNLRP9) in oocytes from antral follicles of three different size classes (≤2 mm, 3–5 mm, ≥6 mm) to unravel the epigenetic contribution to this process. We observed an increased number of aberrantly methylated alleles in bH19, bSNRPN and bDNMT3 Lo of oocytes from small antral follicles (≤2 mm), correlating with lower developmental competence. Furthermore, we detected an increased frequency of CpG sites with an unclear methylation status for DNMT3 Ls, specifically in oocytes from follicles ≥6 mm, predominantly at three CpG positions (CpG2, CpG7 and CpG8), of which CpG7 is a potential regulatory site. No major differences in mRNA expression were observed, indicating that the transcriptional machinery may not yet be active during the follicular growth phase. Our results support the notion that a follicle diameter of ~2 mm is a critical stage for establishing DNA methylation profiles and indicate a link between DNA methylation and the acquisition of oocyte developmental competence.
Additional keywords: abnormally methylated alleles, CpG sites, epigenetics, imprinted genes, limited dilution assay, pyro-sequencing.
References
Amor, D. J., and Halliday, J. (2008). A review of known imprinting syndromes and their association with assisted reproduction technologies. Hum. Reprod. 23, 2826–2834.| A review of known imprinting syndromes and their association with assisted reproduction technologies.Crossref | GoogleScholarGoogle Scholar |
Blondin, P., and Sirard, M. A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.
| Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsVagsrs%3D&md5=aeac839daffd86d3a147d5f9eecb4cfdCAS |
Bock, C., Reither, S., Mikeska, T., Paulsen, M., Walter, J., and Lengauer, T. (2005). BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 21, 4067–4068.
| BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCjt7bO&md5=f9e267e0137eee89280593dde74490d0CAS |
Cai, X., and Cullen, B. R. (2007). The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13, 313–316.
| The imprinted H19 noncoding RNA is a primary microRNA precursor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisFCks74%3D&md5=73df828c665ec5965d7011515269d4e7CAS |
Chen, T., and Li, E. (2006). Establishment and maintenance of DNA methylation patterns in mammals. Curr. Top. Microbiol. Immunol. 301, 179–201.
| Establishment and maintenance of DNA methylation patterns in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivFeqtb8%3D&md5=33395a16715b97d5e4f728b31bcc3764CAS |
Chen, Z., Robbins, K. M., Wells, K. D., and Rivera, R. M. (2013). Large offspring syndrome: a bovine model for the human loss-of-imprinting overgrowth syndrome Beckwith–Wiedemann. Epigenetics 8, 591–601.
| Large offspring syndrome: a bovine model for the human loss-of-imprinting overgrowth syndrome Beckwith–Wiedemann.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivFWksrw%3D&md5=40d154787ded8b59946afb6f3b3a1df6CAS |
Crozet, N., Ahmed-Ali, M., and Dubos, M. P. (1995). Developmental competence of goat oocytes from follicles of different size categories following maturation, fertilization and culture in vitro. J. Reprod. Fertil. 103, 293–298.
| Developmental competence of goat oocytes from follicles of different size categories following maturation, fertilization and culture in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlvV2rtLg%3D&md5=254ba845e3b5c9505bd7af708bfd9daeCAS |
De La Fuente, R. (2006). Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev. Biol. 292, 1–12.
| Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFGmtL4%3D&md5=3be358feade1bfc3e923b8ac94a93970CAS |
El Hajj, N., Trapphoff, T., Linke, M., May, A., Hansmann, T., Kuhtz, J., Reifenberg, K., Heinzmann, J., Niemann, H., Daser, A., Eichenlaub-Ritter, U., Zechner, U., and Haaf, T. (2011). Limiting dilution bisulfite (pyro)sequencing reveals parent-specific methylation patterns in single early mouse embryos and bovine oocytes. Epigenetics 6, 1176–1188.
| Limiting dilution bisulfite (pyro)sequencing reveals parent-specific methylation patterns in single early mouse embryos and bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFOntrs%3D&md5=a5a0c58020f9e0ca9cd2290362c3234aCAS |
Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–216.
| Follicular oocyte growth and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gtrw%3D&md5=5507a97506ca569f2f67a81e39e987a6CAS |
Fair, T., Hyttel, P., and Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437–442.
| Bovine oocyte diameter in relation to maturational competence and transcriptional activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVGisb4%3D&md5=e191dc47fe7cfc31725961e219f1f682CAS |
Favaedi, R., Shahhoseini, M., and Akhoond, M. R. (2012). Comparative epigenetic analysis of Oct4 regulatory region in RA-induced differentiated NT2 cells under adherent and non-adherent culture conditions. Mol. Cell. Biochem. 363, 129–134.
| Comparative epigenetic analysis of Oct4 regulatory region in RA-induced differentiated NT2 cells under adherent and non-adherent culture conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFKquro%3D&md5=95bc8b2b8d7315ac43e7909244118484CAS |
Goudet, G., Bezard, J., Duchamp, G., Gerard, N., and Palmer, E. (1997). Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment. Biol. Reprod. 57, 232–245.
| Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslWit7o%3D&md5=539ed268684c118cad563f7814dcdd96CAS |
Hagemann, L. J., Beaumont, S. E., Berg, M., Donnison, M. J., Ledgard, A., Peterson, A. J., Schurmann, A., and Tervit, H. R. (1999). Development during single IVP of bovine oocytes from dissected follicles: interactive effects of estrous cycle stage, follicle size and atresia. Mol. Reprod. Dev. 53, 451–458.
| Development during single IVP of bovine oocytes from dissected follicles: interactive effects of estrous cycle stage, follicle size and atresia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVOktro%3D&md5=731e187ca5af6ae68f651766b0b79b08CAS |
Hansmann, T., Heinzmann, J., Wrenzycki, C., Zechner, U., Niemann, H., and Haaf, T. (2011). Characterization of differentially methylated regions in 3 bovine imprinted genes: a model for studying human germ-cell and embryo development. Cytogenet. Genome Res. 132, 239–247.
| Characterization of differentially methylated regions in 3 bovine imprinted genes: a model for studying human germ-cell and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Sgs70%3D&md5=2747ec20f2e98a22412c8602a7cdf943CAS |
Hata, K., Okano, M., Lei, H., and Li, E. (2002). Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129, 1983–1993.
| 1:CAS:528:DC%2BD38XjslSls70%3D&md5=2720bdb7f6f137e0bcf0d6bf210cada4CAS |
Heinzmann, J., Hansmann, T., Herrmann, D., Wrenzycki, C., Zechner, U., Haaf, T., and Niemann, H. (2011). Epigenetic profile of developmentally important genes in bovine oocytes. Mol. Reprod. Dev. 78, 188–201.
| Epigenetic profile of developmentally important genes in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVKmsL8%3D&md5=ceda4ca68f6096f6889a60f69688c730CAS |
Heinzmann, J., Mattern, F., Aldag, P., Bernal-Ulloa, S. M., Schneider, T., Haaf, T., and Niemann, H. (2015). Extended in vitro maturation affects gene expression and DNA methylation in bovine oocytes. Mol. Hum. Reprod. 21, 770–782.
| Extended in vitro maturation affects gene expression and DNA methylation in bovine oocytes.Crossref | GoogleScholarGoogle Scholar |
Hiura, H., Obata, Y., Komiyama, J., Shirai, M., and Kono, T. (2006). Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11, 353–361.
| Oocyte growth-dependent progression of maternal imprinting in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1Gktr8%3D&md5=7a8aa026ece20b2c2d942154a17137f3CAS |
Ideraabdullah, F. Y., Vigneau, S., and Bartolomei, M. S. (2008). Genomic imprinting mechanisms in mammals. Mutat. Res. 647, 77–85.
| Genomic imprinting mechanisms in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlyks7bN&md5=43debb88d7c98272e55d6222721852adCAS |
Jia, D., Jurkowska, R. Z., Zhang, X., Jeltsch, A., and Cheng, X. (2007). Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248–251.
| Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVagtbrF&md5=3b44e5aa69b41377a2033b4a4946b234CAS |
Kanitz, W. (2003). Follicular dynamic and ovulation in cattle—a review. Arch. Tierz. Dummerstorf 46, 187–198.
| 1:CAS:528:DC%2BD3sXivFaitL4%3D&md5=346242c552c6e65570e304c8fa17cd24CAS |
Kuhtz, J., Romero, S., De Vos, M., Smitz, J., Haaf, T., and Anckaert, E. (2014). Human in vitro oocyte maturation is not associated with increased imprinting error rates at LIT1, SNRPN, PEG3 and GTL2. Hum. Reprod. 29, 1995–2005.
| Human in vitro oocyte maturation is not associated with increased imprinting error rates at LIT1, SNRPN, PEG3 and GTL2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtl2gtb3J&md5=78e35892635fa6fe6a5e4a2b70bb71a4CAS |
Kurosaka, S., Eckardt, S., and McLaughlin, K. J. (2004). Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Biol. Reprod. 71, 1578–1582.
| Pluripotent lineage definition in bovine embryos by Oct4 transcript localization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1yisb0%3D&md5=95da1b0822fcfcfc7ebd983ef7ec3e88CAS |
Lequarre, A. S., Traverso, J. M., Marchandise, J., and Donnay, I. (2004). Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors. Biol. Reprod. 71, 425–431.
| Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgtLo%3D&md5=a09b86ed8bb8bbe04a8492fb76ef1c92CAS |
Lequarre, A. S., Vigneron, C., Ribaucour, F., Holm, P., Donnay, I., Dalbies-Tran, R., Callesen, H., and Mermillod, P. (2005). Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology 63, 841–859.
| Influence of antral follicle size on oocyte characteristics and embryo development in the bovine.Crossref | GoogleScholarGoogle Scholar |
Lonergan, P., Monaghan, P., Rizos, D., Boland, M. P., and Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48–53.
| Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7ns1Wltw%3D%3D&md5=7a2c452b61c0d42d1528fef5993382d3CAS |
Lucifero, D., Suzuki, J., Bordignon, V., Martel, J., Vigneault, C., Therrien, J., Filion, F., Smith, L. C., and Trasler, J. M. (2006). Bovine SNRPN methylation imprint in oocytes and day 17 in vitro-produced and somatic cell nuclear transfer embryos. Biol. Reprod. 75, 531–538.
| Bovine SNRPN methylation imprint in oocytes and day 17 in vitro-produced and somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCgs73P&md5=cd3cd5ddf6743377989af47f2075a2b0CAS |
Mattern, F., Herrmann, D., Heinzmann, J., Hadeler, K. G., Bernal-Ulloa, S. M., Haaf, T., and Niemann, H. (2016). DNA methylation and mRNA expression of developmentally important genes in bovine oocytes collected from donors of different age categories. Mol. Reprod. Dev. 83, 802–814.
| DNA methylation and mRNA expression of developmentally important genes in bovine oocytes collected from donors of different age categories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVWjtLvM&md5=a092a5a8ca75921da6df40834b3295daCAS |
McGee, E. A., and Hsueh, A. J. (2000). Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 21, 200–214.
| 1:STN:280:DC%2BD3c3ksVahsw%3D%3D&md5=51e65021c74621e9a293592c686510c8CAS |
McGrath, J., and Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179–183.
| Completion of mouse embryogenesis requires both the maternal and paternal genomes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3gsFKguw%3D%3D&md5=82cfc021e756b036a3678837ffc026c2CAS |
Memili, E., Dominko, T., and First, N. L. (1998). Onset of transcription in bovine oocytes and preimplantation embryos. Mol. Reprod. Dev. 51, 36–41.
| Onset of transcription in bovine oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVGltbc%3D&md5=049802930963064ab32aa26b00a7e782CAS |
Ménézo, Y. J., and Hérubel, F. (2002). Mouse and bovine models for human IVF. Reprod. Biomed. Online 4, 170–175.
| Mouse and bovine models for human IVF.Crossref | GoogleScholarGoogle Scholar |
Monk, D. (2015). Germline-derived DNA methylation and early embryo epigenetic reprogramming: the selected survival of imprints. Int. J. Biochem. Cell Biol. 67, 128–138.
| Germline-derived DNA methylation and early embryo epigenetic reprogramming: the selected survival of imprints.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotlGmsbs%3D&md5=705d21bc7050b3f9ca91800416c6851dCAS |
Mortusewicz, O., Schermelleh, L., Walter, J., Cardoso, M. C., and Leonhardt, H. (2005). Recruitment of DNA methyltransferase I to DNA repair sites. Proc. Natl. Acad. Sci. USA 102, 8905–8909.
| Recruitment of DNA methyltransferase I to DNA repair sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvF2qurY%3D&md5=6a7800a319f68c068c94dfe472b224a2CAS |
Motlik, J., Crozet, N., and Fulka, J. (1984). Meiotic competence in vitro of pig oocytes isolated from early antral follicles. J. Reprod. Fertil. 72, 323–328.
| Meiotic competence in vitro of pig oocytes isolated from early antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M%2Fot1yitg%3D%3D&md5=508d1946c0fac6564995d5e8969197b7CAS |
Mourot, M., Dufort, I., Gravel, C., Algriany, O., Dieleman, S., and Sirard, M. A. (2006). The influence of follicle size, FSH-enriched maturation medium, and early cleavage on bovine oocyte maternal mRNA levels. Mol. Reprod. Dev. 73, 1367–1379.
| The influence of follicle size, FSH-enriched maturation medium, and early cleavage on bovine oocyte maternal mRNA levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVSksb7K&md5=bc540586e77b14b86dfc3fd3df204ceaCAS |
Niemann, H., Carnwath, J. W., Herrmann, D., Wieczorek, G., Lemme, E., Lucas-Hahn, A., and Olek, S. (2010). DNA methylation patterns reflect epigenetic reprogramming in bovine embryos. Cell. Reprogram. 12, 33–42.
| DNA methylation patterns reflect epigenetic reprogramming in bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOju7o%3D&md5=e99b858b8f5fd97ea331905df97b8c96CAS |
Nordhoff, V., Hubner, K., Bauer, A., Orlova, I., Malapetsa, A., and Scholer, H. R. (2001). Comparative analysis of human, bovine, and murine Oct-4 upstream promoter sequences. Mamm. Genome 12, 309–317.
| Comparative analysis of human, bovine, and murine Oct-4 upstream promoter sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis12jsL8%3D&md5=4426f6bc486378f4d07e0491958794cdCAS |
O’Doherty, A. M., Rutledge, C. E., Sato, S., Thakur, A., Lees-Murdock, D. J., Hata, K., and Walsh, C. P. (2011). DNA methylation plays an important role in promoter choice and protein production at the mouse Dnmt3L locus. Dev. Biol. 356, 411–420.
| DNA methylation plays an important role in promoter choice and protein production at the mouse Dnmt3L locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlCntr4%3D&md5=9b05e3a9cbfbc36c72df266a45aa71deCAS |
O’Doherty, A. M., O’Shea, L. C., and Fair, T. (2012). Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol. Reprod. 86, 67.
| Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins.Crossref | GoogleScholarGoogle Scholar |
Oliveri, R. S., Kalisz, M., Schjerling, C. K., Andersen, C. Y., Borup, R., and Byskov, A. G. (2007). Evaluation in mammalian oocytes of gene transcripts linked to epigenetic reprogramming. Reproduction 134, 549–558.
| Evaluation in mammalian oocytes of gene transcripts linked to epigenetic reprogramming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Knur3J&md5=76f784dd908666ba7d2bbd8539dd3335CAS |
Pavlok, A., Lucas-Hahn, A., and Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–67.
| Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383it1Gqtw%3D%3D&md5=c29cfb38025a99800fac9698f76f8583CAS |
Pesce, M., and Scholer, H. R. (2001). Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 19, 271–278.
| Oct-4: gatekeeper in the beginnings of mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFKktL4%3D&md5=8ad7b9823961002b8e5ca8481d75ba34CAS |
Racedo, S. E., Branzini, M. C., Salamone, D., Wojcik, C., Rawe, V. Y., and Niemann, H. (2009). Dynamics of microtubules, motor proteins and 20S proteasomes during bovine oocyte IVM 5. Reprod. Fertil. Dev. 21, 304–312.
| Dynamics of microtubules, motor proteins and 20S proteasomes during bovine oocyte IVM 5.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVensLc%3D&md5=e516c85d7f903138fb585506f0eb1b74CAS |
Reik, W., and Walter, J. (2001). Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21–32.
| Genomic imprinting: parental influence on the genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisVGjs70%3D&md5=24777ac171a7df4c57766ab517ac55c7CAS |
Robbins, K. M., Chen, Z., Wells, K. D., and Rivera, R. M. (2012). Expression of KCNQ1OT1, CDKN1C, H19, and PLAGL1 and the methylation patterns at the KvDMR1 and H19/IGF2 imprinting control regions is conserved between human and bovine. J. Biomed. Sci. 19, 95.
| Expression of KCNQ1OT1, CDKN1C, H19, and PLAGL1 and the methylation patterns at the KvDMR1 and H19/IGF2 imprinting control regions is conserved between human and bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFWqs7c%3D&md5=0abcc2f60eccddab1f38807f30252bb7CAS |
Saitou, M., Kagiwada, S., and Kurimoto, K. (2012). Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139, 15–31.
| Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFKgtb4%3D&md5=44afb4c9ac195107c67c7bc41a6e1934CAS |
Schöler, H. R. (1991). Octamania: the POU factors in murine development. Trends Genet. 7, 323–329.
| Octamania: the POU factors in murine development.Crossref | GoogleScholarGoogle Scholar |
Schramm, R. D., Tennier, M. T., Boatman, D. E., and Bavister, B. D. (1993). Chromatin configurations and meiotic competence of oocytes are related to follicular diameter in nonstimulated rhesus monkeys. Biol. Reprod. 48, 349–356.
| Chromatin configurations and meiotic competence of oocytes are related to follicular diameter in nonstimulated rhesus monkeys.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7ns12jsQ%3D%3D&md5=73e66f842b7c15a34e2d4ba43ab30d1aCAS |
Suetake, I., Shinozaki, F., Miyagawa, J., Takeshima, H., and Tajima, S. (2004). DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J. Biol. Chem. 279, 27816–27823.
| DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvFGmsr8%3D&md5=b6ea8fd546692bc3dc0340f8de84e979CAS |
Szöllösi, D., Desmedt, V., Crozet, N., and Brender, C. (1988). In vitro maturation of sheep ovarian oocytes. Reprod. Nutr. Dev. 28, 1047–1080.
| In vitro maturation of sheep ovarian oocytes.Crossref | GoogleScholarGoogle Scholar |
Tomek, W., Torner, H., and Kanitz, W. (2002). Comparative analysis of protein synthesis, transcription and cytoplasmic polyadenylation of mRNA during maturation of bovine oocytes in vitro. Reprod. Domest. Anim. 37, 86–91.
| Comparative analysis of protein synthesis, transcription and cytoplasmic polyadenylation of mRNA during maturation of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xkt1Crt78%3D&md5=615fd604540b095c744b9211178c7d47CAS |
Tsuji, K., Sowa, M., and Nakano, R. (1985). Relationship between human oocyte maturation and different follicular sizes. Biol. Reprod. 32, 413–417.
| Relationship between human oocyte maturation and different follicular sizes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7nsFaqtg%3D%3D&md5=19220b975dd55aa16c706efb002ebbb9CAS |
Ulloa, S. M. B., Heinzmann, J., Herrmann, D., Timmermann, B., Baulain, U., Grossfeld, R., Diederich, M., Lucas-Hahn, A., and Niemann, H. (2015). Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote 23, 367–377.
| Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality.Crossref | GoogleScholarGoogle Scholar |
Uzbekova, S., Roy-Sabau, M., Dalbies-Tran, R., Perreau, C., Papillier, P., Mompart, F., Thelie, A., Pennetier, S., Cognie, J., Cadoret, V., Royere, D., Monget, P., and Mermillod, P. (2006). Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells. Reprod. Biol. Endocrinol. 4, 12.
| Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells.Crossref | GoogleScholarGoogle Scholar |
Warnecke, P. M., Stirzaker, C., Song, J., Grunau, C., Melki, J. R., and Clark, S. J. (2002). Identification and resolution of artefacts in bisulfite sequencing. Methods 27, 101–107.
| Identification and resolution of artefacts in bisulfite sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVShsbo%3D&md5=fbe0832971df5058757683a2b1bcb7f8CAS |
Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A., Sirisathien, S., Brackett, B., and Niemann, H. (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum. Reprod. 16, 893–901.
| Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Cqs74%3D&md5=d7ad9d18f0f6577d81c335f2eb243030CAS |
Wu, X., Viveiros, M. M., Eppig, J. J., Bai, Y., Fitzpatrick, S. L., and Matzuk, M. M. (2003a). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187–191.
| Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsFSktg%3D%3D&md5=f6023e8f719ccd73f1d93e70547b6fb6CAS |
Wu, X., Wang, P., Brown, C. A., Zilinski, C. A., and Matzuk, M. M. (2003b). Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol. Reprod. 69, 861–867.
| Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVeitLk%3D&md5=f9babbe7cbe2876fc90f038f148e774aCAS |
