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DNA methylation pattern in mouse oocytes and their in vitro fertilized early embryos: effect of oocyte vitrification

Published online by Cambridge University Press:  31 October 2012

Ying Liang ,
Xiang-Wei Fu ,
Jun-Jie Li ,
Dian-Shuai Yuan  and
Shi-En Zhu
Ying Liang
Affiliation:
Laboratory of Animal Embryonic Biotechnology, College of Animal Science and Technology, and State Key Laboratories for Agrobiotechnology, China Agricultural University, Beijing 100193, People's Republic of China.
Xiang-Wei Fu
Affiliation:
Laboratory of Animal Embryonic Biotechnology, College of Animal Science and Technology, and State Key Laboratories for Agrobiotechnology, China Agricultural University, Beijing 100193, People's Republic of China.
Jun-Jie Li
Affiliation:
Laboratory of Animal Embryonic Biotechnology, College of Animal Science and Technology, and State Key Laboratories for Agrobiotechnology, China Agricultural University, Beijing 100193, People's Republic of China.
Dian-Shuai Yuan
Affiliation:
Laboratory of Animal Embryonic Biotechnology, College of Animal Science and Technology, and State Key Laboratories for Agrobiotechnology, China Agricultural University, Beijing 100193, People's Republic of China.
Shi-En Zhu*
Affiliation:
Laboratory of Animal Embryonic Biotechnology, College of Animal Science and Technology, and State Key Laboratories for Agrobiotechnology, China Agricultural University, Beijing 100193, People's Republic of China.
*
All correspondence to: Shi-En Zhu. Laboratory of Animal Embryonic Biotechnology, College of Animal Science and Technology, and State Key Laboratories for Agrobiotechnology, China Agricultural University, Beijing 100193, People's Republic of China. Tel: +86 10 62731767. e-mail: zhushien@cau.edu.cn
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Summary

This study was conducted to investigate the pattern of DNA methylation in vitrified–thawed mouse oocytes and their in vitro fertilized early embryos. Firstly, mouse oocytes at metaphase II (MII) stage of meiosis were allocated randomly into three groups: (1) untreated (control); (2) exposed to vitrification solution without being plunged into liquid nitrogen (toxicity); or (3) vitrified by open-pulled straw (OPS) method (vitrification). Oocytes from all three groups were fertilized subsequently in vitro. The level of DNA methylation in the MII oocytes and their early embryos was then examined by immunofluorescence using an anti-5-methylcytosine (anti-5-MeC) monoclonal antibody and fluorescein isothiocyanate (FITC)-conjugated goat anti-mouse IgG. Developmental rates to 2-cell embryos (62.28%) and blastocysts (43.68%) of the vitrified–thawed oocytes were lower (P < 0.01) than those of fresh oocytes (81.47%, 61.99%) and vitrification solution treated (79.20%, 60.04%) oocytes. DNA methylation (as reflected by 5-MeC fluorescence intensity) in the vitrification group was less (P < 0.01) for MII oocyte and 2- to 8-cell stages compared with that in the control and toxicity groups. Accordingly, a reduction in global genomic methylation due to vitrification of MII oocytes may result in compromised in vitro developmental potential in early mouse embryos.

Keywords

Early EmbryoDNA MethylationMouseOocyteOPS Vitrification
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 138 - 145
Copyright
Copyright © Cambridge University Press 2012 

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References

Anon. (2006). Vitrification devices affect developmental competence and biochemical properties of IVM ovine oocytes. Reprod. Fertil. Dev. 18, 163–3.Google Scholar
Aoki, F., Worrad, D.M. & Schultz, R.M. (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181, 296–307.Google Scholar
Baylin, S.B. (1997). Tying it all together: epigenetics, genetics, cell cycle, and cancer. Science 277, 1948–9.Google Scholar
Bird, A.P. & Wolffe, A.P. (1999). Methylation-induced repression—belts, braces, and chromatin. Cell 99, 451–4.Google Scholar
Carambula, S.F., Oliveira, L.J., & Hansen, P.J. (2009). Repression of induced apoptosis in the 2-cell bovine embryo involves DNA methylation and histone deacetylation. Biochem. Biophys. Res. Com. 388, 418–21.Google Scholar
Chen, S.U., Lien, Y.R., Cheng, Y.Y., Chen, H.F., Ho, H.N. & Yang, Y.S. (2001). Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids. Hum. Reprod. 16, 2350–6.Google Scholar
Dinnyes, A., Dai, Y.P., Jiang, S. & Yang, X.Z. (2000). High developmental rates of vitrified bovine oocytes following parthenogenetic activation, in vitro fertilization, and somatic cell nuclear transfer. Biol. Reprod. 63, 513–8.Google Scholar
Eden, S., Hashimshony, T., Keshet, I., Cedar, H. & Thorne, A.W. (1998). DNA methylation models histone acetylation. Nature 394, 842.Google Scholar
Fan, Z.Q., Li, X.W., Liu, Y., Meng, Q.G., Wang, Y.P., Hou, Y.P., Zhou, G.B. & Zhu, S.E. (2008). Piezo-assisted in vitro fertilization of mouse oocytes with spermatozoa retrieved from epididymides stored at 4 degree C. J. Reprod. Dev. 54, 107–12.Google Scholar
Holliday, R. & Pugh, J.E. (1975). DNA Modification mechanisms and gene activity during development. Science 187, 226–32.Google Scholar
Howlett, S.K. & Reik, W. (1991). Methylation levels of maternal and paternal genomes during preimplantation development. Development 113, 119–27.Google Scholar
Huang, J.Y.J., Chen, H.Y., Tan, S.L. & Chian, R.C. (2007). Effect of choline-supplemented sodium-depleted slow freezing versus vitrification on mouse oocyte meiotic spindles and chromosome abnormalities. Fertil. Steril. 88, 1093–1100.Google Scholar
Issa, J.P. (2000). CpG-island methylation in aging and cancer. Curr. Top Microbiol. Immunol. 249, 101–18.Google Scholar
Iwatani, M., Ikegami, K., Kremenska, Y., Hattori, N., Tanaka, S., Yagi, S. & Shiota, K. (2006). Dimethyl sulfoxide has an impact on epigenetic profile in mouse embryoid body. Stem Cell 24, 2549–56.CrossRefGoogle ScholarPubMed
Jaenisch, R. & Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33, 245–54.Google Scholar
Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., Mccarrey, J., Cedar, H. & Razin, A. (1992). Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Gene Dev. 6, 705–14.Google Scholar
Larman, M.G., Sheehan, C.B. & Gardner, D.K. (2006). Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reproduction 131, 53–61.Google Scholar
Li, E. (2002). Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3, 662–73.Google Scholar
Li, J.J., Pei, Y., Zhou, G.B., Suo, L., Wang, Y.P., Wu, G.Q., Fu, X.W., Hou, Y.P. & Zhu, S.E. (2011). Histone deacetyltransferase1 expression in mouse oocyte and their in vitro-fertilized embryo: effect of oocyte vitrification. Cryo Lett. 32, 1–12.Google Scholar
Mayer, W., Niveleau, A., Walter, J., Fundele, R. & Haaf, T. (2000). Embryogenesis—demethylation of the zygotic paternal genome. Nature 403, 501–2.Google Scholar
Meng, Q.G., Li, X.W., Wu, T.Y., Dinnyes, A. & Zhu, S. (2007). Piezo-actuated zona-drilling improves the fertilisation of ops vitrified mouse oocytes. Acta Vet. Hung. 55, 369–78.Google Scholar
Monk, M., Boubelik, M. & Lehnert, S. (1987). Temporal and regional changes in dna methylation in the embryonic, extraembryonic and germ-cell lineages during mouse embryo development. Development 99, 371–82.Google Scholar
Monk, M., Adams, R.L. P. & Rinaldi, A. (1991). Decrease in DNA methylase activity during preimplantation development in the mouse. Development 112, 189–92.Google Scholar
Morato, R., Izquierdo, D., Albarracin, J.L., Anguita, B., Palomo, M.J., Jimenez-Macedo, A.R., Paramio, M.T. & Mogas, T. (2008). Effects of pre-treating in vitro-matured bovine oocytes with the cytoskeleton stabilizing agent taxol prior to vitrification. Mol. Reprod. Dev. 75, 191–201.Google Scholar
Morgan, H.D., Santos, F., Green, K., Dean, W. & Reik, W. (2005). Epigenetic reprogramming in mammals. Hum. Mol. Genet. 14, R47–58.Google Scholar
Okano, M., Bell, D.W., Haber, D.A. & Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–57.Google Scholar
Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., Dean, W., Reik, W. & Walter, J. (2000). Active demethylation of the paternal genome in the mouse zygote. Cur. Biol. 10, 475–8.CrossRefGoogle ScholarPubMed
Peng, L., Wang, S.Y., Yin, S.W., Li, C.P., Li, Z., Wang, S.L. & Liu, Q.Z. (2008). Autophosphorylation of H2AX in a cell-specific frozen dependent way. Cryobiology 57, 175–7.CrossRefGoogle Scholar
Pukazhenthi, B.S. & Wildt, D.E. (2004). Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reprod. Fertil. Dev. 16, 33–46.Google Scholar
Reynauld, C., Bruno, C., Boullanger, P., Grange, S., Barbesti, S. & Niveleau, A. (1991). Monitoring of urinary excretion of modified nucleosides in cancer patients using a set of six monoclonal antibodies. Cancer Lett. 61, 255–61.Google Scholar
Riggs, A.D. (1975). X-inactivation, differentiation, and DNA methylation. Cytogenet. Cell Genet. 14, 9–25.Google Scholar
Robertson, K.D. & Wolffe, A.P. (2000). DNA methylation in health and disease. Nat. Rev. Genet. 1, 11–9.Google Scholar
Rogers, J.M., Francis, B.M., Sulik, K.K., Alles, A.J., Massaro, E.J., Zucker, R.M., Elstein, K.H., Rosen, M.B. & Chernoff, N. (1994) Cell death and cell cycle perturbation in the developmental toxicity of the demethylating agent, 5-AZA-2′-deoxycytidine. Teratology 50, 332–9.Google Scholar
Rojas, C., Palomo, M.J., Albarracin, J.L. & Mogas, T. (2004). Vitrification of immature and in vitro matured pig oocytes: study of distribution of chromosomes, microtubules, and actin microfilaments. Cryobiology 49, 211–20.Google Scholar
Rougier, N., Bourc'his, D., Gomes, D.M., Niveleau, A., Plachot, M., Paldi, A. & Viegas- Pequignot, E. (1998). Chromosome methylation patterns during mammalian preimplantation development. Gene Dev. 12, 2108–13.Google Scholar
Santos, F. & Dean, W. (2004). Epigenetic reprogramming during early development in mammals. Reproduction 127, 643–51.Google Scholar
Santos, F. & Dean, W. (2006). Using immunofluorescence to observe methylation changes in mammalian preimplantation embryos changes in mammalian preimplantation embryos. Methods Mol. Biol. 325, 129–37.Google Scholar
Santos, F., Hendrich, B., Reik, W. & Dean, W. (2002). Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172–82.Google Scholar
Shaw, J.M., Oranratnachai, A. & Trounson, A. O. (2000). Fundamental cryobiology of mammalian oocytes and ovarian tissue. Theriogenology 53, 59–72.Google Scholar
Shi, L.Y., Jin, H.F., Kim, J.G., Kumar, B.M., Balasubramanian, S., Choe, S.Y. & Rho, G.J. (2007). Ultra-structural changes and developmental potential of porcine oocytes following vitrification. Anim. Reprod. Sci. 100, 128–40.Google Scholar
Soares, J., Pinto, A.E., Cunha, C.V., Andre, S., Barao, I., Sousa, J.M. & Cravo, M. (1999). Global DNA hypomethylation in breast carcinoma. Cancer 85, 112–8.Google Scholar
Tian, S.J., Yan, C.L., Yang, H.X., Zhou, G.B., Yang, Z.Q. & Zhu, S.E. (2007). Vitrification solution containing DMSO and EG can induce parthenogenetic activation of in vitro matured ovine oocytes and decrease sperm penetration. Anim. Reprod. Sci. 101, 365–71.Google Scholar
Urnov, F.D. & Wolffe, A.P. (2001). Above and within the genome: epigenetics past and present. J. Mamm. Gland Biol. Neo. 6, 153–67.Google Scholar
Vajta, G. (2000). Vitrification of the oocytes and embryos of domestic animals. Anim. Reprod. Sci. 60, 357–64.Google Scholar
Vajta, G., Booth, P.J., Holm, P., Greve, T. & Callesen, H. (1997). Successful vitrification of early stage bovine in vitro produced embryos with the open pulled straw (OPS) method. Cryo-Letters 18, 191–5.Google Scholar
Vajta, G., Holm, P., Kuwayama, M., Booth, P.J., Jacobsen, H., Greve, T. & Callesen, H. (1998). Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol. Reprod. Dev. 51, 53–8.Google Scholar
Valojerdi, M.R. & Salehnia, M. (2005). Developmental potential and ultrastructural injuries of metaphase II (MII) mouse oocytes after slow freezing or vitrification. J. Assist. Reprod. Genet. 22, 119–27.Google Scholar
Wang, Z.Y., Xu, L. & He, F. F. (2010). Embryo vitrification affects the methylation of the H19/Igf2 differentially methylated domain and the expression of H19 and Igf2. Fertil. Steril. 93, 2729–33.Google Scholar
Whittingham, D.G. (1977). Fertilization in vitro and development to term of unfertilized mouse oocytes previously stored at –196°C. J. Reprod. Fertil. 49, 89–94.Google Scholar
Wolffe, A.P. & Matzke, M. A. (1999). Epigenetics: regulation through repression. Science 286, 481–6.Google Scholar
Yoder, J.A., Walsh, C.P. & Bestor, T.H. (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13, 335–40.Google Scholar