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Defective Histone H3K27 Trimethylation Modification in Embryos Derived from Heated Mouse Sperm

Published online by Cambridge University Press:  09 May 2012

Shi-Bin Chao ,
Lei Chen ,
Jian-Chun Li ,
Xiang-Hong Ou ,
Xiao-Jin Huang ,
Shu Wen ,
Qing-Yuan Sun  and
Guo-Lan Gao
Shi-Bin Chao
Affiliation:
Center of Reproductive Medicine, The First Affiliated Hospital of NanChang University, NanChang, China State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Lei Chen
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Jian-Chun Li
Affiliation:
Center of Reproductive Medicine, The First Affiliated Hospital of NanChang University, NanChang, China
Xiang-Hong Ou
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Xiao-Jin Huang
Affiliation:
Center of Reproductive Medicine, The First Affiliated Hospital of NanChang University, NanChang, China
Shu Wen
Affiliation:
Department of Obstetrics and Gynecology, One Baylor Plaza, Baylor College of Medicine, Houston, TX, USA
Qing-Yuan Sun
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Guo-Lan Gao*
Affiliation:
Center of Reproductive Medicine, The First Affiliated Hospital of NanChang University, NanChang, China Department of Obstetrics and Gynecology, Aviation General Hospital of China, Beijing, China
*
Corresponding author. E-mail: [email protected]
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Abstract

The mouse sperm genome is resistant to in vitro heat treatment, and embryos derived from heated sperm can support full-term embryonic development, but the blastocyst rate and implantation rate are lower compared to embryos derived from fresh sperm. In the present study, the patterns of DNA methylation, histone H4K12 (ACH4K12) acetylation, H3K9 trimethylation (H3K9-TriM), and H3K27 trimethylation (H3K27-TriM) in preimplantation embryos derived from 65°C-heated sperm were investigated. Although no evident changes in global DNA methyaltion, histone H4K12 (ACH4K12) acetylation, and H3K9 trimethylation (H3K9-TriM) were found, significantly lower levels of H3K27-TriM, which was thought to be one of the reasons for low efficiency of mouse cloning, were found in the inner cell mass of heated-sperm derived blastocysts. Thus, defective modification of H3K27-TriM might contribute to compromised development of embryos derived from heated sperm.

Keywords

intracytoplasmic sperm injection (ICSI)epigenetic reprogrammingDNA methylationhistone modificationinner cell mass (ICM)
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 18 , Issue 3 , June 2012 , pp. 476 - 482
Copyright
Copyright © Microscopy Society of America 2012

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References

Ball, M.J. (1987). Effect of two disinfectant treatments on laboratory analyses. J R Soc Med 80(8), 482–484.CrossRefGoogle ScholarPubMed
Banks, S., King, S.A., Irvine, D.S. & Saunders, P.T. (2005). Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction 129(4), 505–514.CrossRefGoogle ScholarPubMed
Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., Jaenisch, R., Wagschal, A., Feil, R., Schreiber, S.L. & Lander, E.S. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2), 315–326.CrossRefGoogle ScholarPubMed
Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S. & Zhang, Y. (2002). Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298(5595), 1039–1043.CrossRefGoogle ScholarPubMed
Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. & Smith, A. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113(5), 643–655.CrossRefGoogle ScholarPubMed
Chao, S.B., Guo, L., Ou, X.H., Luo, S.M., Wang, Z.B., Schatten, H., Gao, G.L. & Sun, Q.Y. (2012). Heated spermatozoa: Effects on embryonic development and epigenetics. Hum Reprod 27(4), 1016–1024.CrossRefGoogle ScholarPubMed
Cozzi, J., Monier-Gavelle, F., Lievre, N., Bomsel, M. & Wolf, J.P. (2001). Mouse offspring after microinjection of heated spermatozoa. Biol Reprod 65(5), 1518–1521.CrossRefGoogle ScholarPubMed
Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., Wolf, E. & Reik, W. (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA 98(24), 13734–13738.CrossRefGoogle ScholarPubMed
Erhardt, S., Su, I.H., Schneider, R., Barton, S., Bannister, A.J., Perez-Burgos, L., Jenuwein, T., Kouzarides, T., Tarakhovsky, A. & Surani, M.A. (2003). Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 130(18), 4235–4248.CrossRefGoogle ScholarPubMed
Feil, R. (2009). Epigenetic asymmetry in the zygote and mammalian development. Int J Dev Biol 53(2-3), 191–201.CrossRefGoogle ScholarPubMed
Feng, S., Jacobsen, S.E. & Reik, W. (2010). Epigenetic reprogramming in plant and animal development. Science 330(6004), 622–627.CrossRefGoogle ScholarPubMed
Fleming, T.P., Kwong, W.Y., Porter, R., Ursell, E., Fesenko, I., Wilkins, A., Miller, D.J., Watkins, A.J. & Eckert, J.J. (2004). The embryo and its future. Biol Reprod 71(4), 1046–1054.CrossRefGoogle ScholarPubMed
Jiang, M.X., Zhu, Y., Zhu, Z.Y., Sun, Q.Y. & Chen, D.Y. (2005). Effects of cooling, cryopreservation and heating on sperm proteins, nuclear DNA, and fertilization capability in mouse. Mol Reprod Dev 72(1), 129–134.CrossRefGoogle Scholar
Jones, P.A. & Takai, D. (2001). The role of DNA methylation in mammalian epigenetics. Science 293(5532), 1068–1070.CrossRefGoogle ScholarPubMed
Kaneko, T., Whittingham, D.G. & Yanagimachi, R. (2003). Effect of pH value of freeze-drying solution on the chromosome integrity and developmental ability of mouse spermatozoa. Biol Reprod 68(1), 136–139.CrossRefGoogle ScholarPubMed
Khosla, S., Dean, W., Brown, D., Reik, W. & Feil, R. (2001). Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 64(3), 918–926.CrossRefGoogle ScholarPubMed
Kim, J.M., Ogura, A., Nagata, M. & Aoki, F. (2002). Analysis of the mechanism for chromatin remodeling in embryos reconstructed by somatic nuclear transfer. Biol Reprod 67(3), 760–766.CrossRefGoogle ScholarPubMed
Kimura, Y. & Yanagimachi, R. (1995). Intracytoplasmic sperm injection in the mouse. Biol Reprod 52(4), 709–720.CrossRefGoogle ScholarPubMed
Klose, R.J. & Zhang, Y. (2007). Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8(4), 307–318.CrossRefGoogle ScholarPubMed
Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128(4), 693–705.CrossRefGoogle ScholarPubMed
Kwon, I.K., Park, K.E. & Niwa, K. (2004). Activation, pronuclear formation, and development in vitro of pig oocytes following intracytoplasmic injection of freeze-dried spermatozoa. Biol Reprod 71(5), 1430–1436.CrossRefGoogle ScholarPubMed
Lachner, M. & Jenuwein, T. (2002). The many faces of histone lysine methylation. Curr Opin Cell Biol 14(3), 286–298.CrossRefGoogle ScholarPubMed
Lepikhov, K. & Walter, J. (2004). Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev Biol 4, 12.CrossRefGoogle ScholarPubMed
Li, C., Mizutani, E., Ono, T. & Wakayama, T. (2009). Production of normal mice from spermatozoa denatured with high alkali treatment before ICSI. Reproduction 137(5), 779–792.CrossRefGoogle ScholarPubMed
Li, E. (2002). Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 3(9), 662–673.CrossRefGoogle ScholarPubMed
Mayer, W., Niveleau, A., Walter, J., Fundele, R. & Haaf, T. (2000). Demethylation of the zygotic paternal genome. Nature 403(6769), 501–502.CrossRefGoogle ScholarPubMed
Metivier, R., Gallais, R., Tiffoche, C., Le Peron, C., Jurkowska, R.Z., Carmouche, R.P., Ibberson, D., Barath, P., Demay, F., Reid, G., Benes, V., Jeltsch, A., Gannon, F. & Salbert, G. (2008). Cyclical DNA methylation of a transcriptionally active promoter. Nature 452(7183), 45–50.CrossRefGoogle ScholarPubMed
Miller, D., Brinkworth, M. & Iles, D. (2009). Paternal DNA packaging in spermatozoa: More than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139(2), 287–301.CrossRefGoogle Scholar
Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M. & Yamanaka, S. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113(5), 631–642.CrossRefGoogle ScholarPubMed
Morgan, H.D., Santos, F., Green, K., Dean, W. & Reik, W. (2005). Epigenetic reprogramming in mammals. Hum Mol Genet 14(1), R47–R58.CrossRefGoogle ScholarPubMed
Paul, C., Murray, A.A., Spears, N. & Saunders, P.T. (2008). A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136(1), 73–84.CrossRefGoogle ScholarPubMed
Santos, F., Hendrich, B., Reik, W. & Dean, W. (2002). Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241(1), 172–182.CrossRefGoogle ScholarPubMed
Surani, M.A., Hayashi, K. & Hajkova, P. (2007). Genetic and epigenetic regulators of pluripotency. Cell 128(4), 747–762.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (1998). Development of normal mice from oocytes injected with freeze-dried spermatozoa. Nat Biotechnol 16(7), 639–641.CrossRefGoogle ScholarPubMed
Ward, W.S., Kimura, Y. & Yanagimachi, R. (1999). An intact sperm nuclear matrix may be necessary for the mouse paternal genome to participate in embryonic development. Biol Reprod 60(3), 702–706.CrossRefGoogle ScholarPubMed
Yan, W., Morozumi, K., Zhang, J., Ro, S., Park, C. & Yanagimachi, R. (2008). Birth of mice after intracytoplasmic injection of single purified sperm nuclei and detection of messenger RNAs and MicroRNAs in the sperm nuclei. Biol Reprod 78(5), 896–902.CrossRefGoogle ScholarPubMed
Yanagida, K., Yanagimachi, R., Perreault, S.D. & Kleinfeld, R.G. (1991). Thermostability of sperm nuclei assessed by microinjection into hamster oocytes. Biol Reprod 44(3), 440–447.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (2011). Mammalian sperm acrosome reaction: Where does it begin before fertilization? Biol Reprod 85(1), 4–5.CrossRefGoogle ScholarPubMed
Yazawa, H., Yanagida, K., Hayashi, S. & Sato, A. (2009). The oocyte activation and Ca2+ oscillation-inducing abilities of mouse and human dead (sonicated) spermatozoa. Zygote 17(2), 175–184.CrossRefGoogle ScholarPubMed
Yeo, S., Lee, K.K., Han, Y.M. & Kang, Y.K. (2005). Methylation changes of lysine 9 of histone H3 during preimplantation mouse development. Mol Cells 20(3), 423–428.CrossRefGoogle ScholarPubMed
Yoshida, N. & Perry, A.C.F. (2007). Piezo-actuated mouse intracytoplasmic sperm injection (ICSI). Nat Protoc 2(2), 296–304.CrossRefGoogle ScholarPubMed
Zhang, M., Wang, F., Kou, Z., Zhang, Y. & Gao, S. (2009). Defective chromatin structure in somatic cell cloned mouse embryos. J Biol Chem 284(37), 24981–24987.CrossRefGoogle ScholarPubMed