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H1foo is essential for in vitro meiotic maturation of bovine oocytes

Published online by Cambridge University Press:  11 March 2014

Yan Yun
Affiliation:
College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Center, Northwest A&F University, Yangling 712100, China. School of Biomedical Sciences, University of Newcastle, Callaghan, New South Wales 2308, Australia.
Peng An
Affiliation:
College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Center, Northwest A&F University, Yangling 712100, China.
Jing Ning
Affiliation:
College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Center, Northwest A&F University, Yangling 712100, China.
Gui-Ming Zhao
Affiliation:
College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Center, Northwest A&F University, Yangling 712100, China.
Wen-Lin Yang
Affiliation:
College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Center, Northwest A&F University, Yangling 712100, China.
An-Min Lei*
Affiliation:
College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Center, Northwest A&F University, Yangling 712100, China.
*
All correspondence to: An-Min Lei. College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Center, Northwest A&F University, Yangling 712100, China. Tel.: +86 29 87080068. Fax: +86 29 87080068. e-mail: anminleiryan@nwsuaf.edu.cn

Summary

Oocyte-specific linker histone, H1foo, is localized on the oocyte chromosomes during the process of meiotic maturation, and is essential for mouse oocyte maturation. Bovine H1foo has been identified, and its expression profile throughout oocyte maturation and early embryo development has been established. However, it has not been confirmed if H1foo is indispensable during bovine oocyte maturation. Effective siRNAs against H1foo were screened in HeLa cells, and then siRNA was microinjected into bovine oocytes to down-regulate H1foo expression. H1foo overexpression was achieved via mRNA injection. Reverse transcription polymerase chain reaction (RT-PCR) results indicated that H1foo was up-regulated by 200% and down-regulated by 70%. Based on the first polar body extrusion (PB1E) rate, H1foo overexpression apparently promoted meiotic progression. The knockdown of H1foo significantly impaired bovine oocyte maturation compared with H1foo overexpression and control groups (H1foo overexpression = 88.7%, H1foo siRNA = 41.2%, control = 71.2%; P < 0.05). This decrease can be rescued by co-injection of a modified H1foo mRNA that has escaped from the siRNA target. However, the H1e (somatic linker histone) overexpression had no effect on PB1E rate when compared with the control group. Therefore we concluded that H1foo is essential for bovine oocyte maturation and its overexpression stimulates the process.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

Becker, M., Becker, A., Miyara, F., Han, Z., Kihara, M., Brown, D.T., Hager, G.L., Latham, K., Adashi, E.Y. & Misteli, T. (2005). Differential in vivo binding dynamics of somatic and oocyte-specific linker histones in oocytes and during ES cell nuclear transfer. Mol. Biol. Cell 16, 3887–95.CrossRefGoogle ScholarPubMed
Dworkin-Rastl, E., Kandolf, H. & Smith, R.C. (1994). The maternal histone H1 variant, H1M (B4 protein), is the predominant H1 histone in Xenopus pregastrula embryos. Dev. Biol. 161, 425–39.Google Scholar
Fan, Y., Sirotkin, A., Russell, R.G., Ayala, J. & Skoultchi, A.I. (2001). Individual somatic H1 subtypes are dispensable for mouse development even in mice lacking the H1(0) replacement subtype. Mol. Cell. Biol. 21, 7933–43.CrossRefGoogle ScholarPubMed
Fan, Y., Nikitina, T., Morin-Kensicki, E.M., Zhao, J., Magnuson, T.R., Woodcock, C.L. & Skoultchi, A.I. (2003). H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo . Mol. Cell. Biol. 23, 4559–72.Google Scholar
Fu, G., Ghadam, P., Sirotkin, A., Khochbin, S., Skoultchi, A.I. & Clarke, H.J. (2003). Mouse oocytes and early embryos express multiple histone H1 subtypes. Biol. Reprod. 68, 1569–76.Google Scholar
Furuya, M., Tanaka, M., Teranishi, T., Matsumoto, K., Hosoi, Y., Saeki, K., Ishimoto, H., Minegishi, K., Iritani, A. & Yoshimura, Y. (2007). H1foo is indispensable for meiotic maturation of the mouse oocyte, J. Reprod. Dev. 53, 895902.Google Scholar
Gao, S., Chung, Y.G., Parseghian, M.H., King, G.J., Adashi, E.Y. & Latham, K.E. (2004). Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: evidence for a uniform developmental program in mice, Dev. Biol. 266, 6275.Google Scholar
Godde, J.S. & Ura, K. (2009). Dynamic alterations of linker histone variants during development. Int. J. Dev. Biol. 53, 215–29.Google Scholar
Happel, N. & Doenecke, D. (2009). Histone H1 and its isoforms: contribution to chromatin structure and function. Gene 431, 112.Google Scholar
Izzo, A., Kamieniarz, K. & Schneider, R. (2008). The histone H1 family: specific members, specific functions? Biol. Chem. 389, 333–43.Google Scholar
Jullien, J., Astrand, C., Halley-Stott, R.P., Garrett, N. & Gurdon, J.B. (2010). Characterization of somatic cell nuclear reprogramming by oocytes in which a linker histone is required for pluripotency gene reactivation. Proc. Natl. Acad. Sci. USA 107, 5483–8.Google Scholar
Khochbin, S. & Wolffe, A.P. (1994). Developmentally regulated expression of linker-histone variants in vertebrates. Eur. J. Biochem. 225, 501–10.Google Scholar
Liu, W.Q., Yin, J.Q., Zhao, G.M., Yun, Y., Wu, S.J., Jones, K.T. & Lei, A.M. (2012). Differential regulation of cyclin B1 degradation between the first and second meiotic divisions of bovine oocytes. Theriogenology 78, 1171–81.Google Scholar
McGraw, S., Vigneault, C., Tremblay, K. & Sirard, M.A. (2006). Characterization of linker histone H1FOO during bovine in vitro embryo development. Mol. Reprod. Dev. 73, 692–9.Google Scholar
Medrzycki, M., Zhang, Y., Cao, K. & Fan, Y. (2012). Expression analysis of mammalian linker-histone subtypes. J. Vis. Exp. DOI: 10.3791/3577.Google Scholar
Mizusawa, Y., Kuji, N., Tanaka, Y., Tanaka, M., Ikeda, E., Komatsu, S., Kato, S. & Yoshimura, Y. (2010). Expression of human oocyte-specific linker histone protein and its incorporation into sperm chromatin during fertilization. Fertil. Steril. 93, 1134–41.CrossRefGoogle ScholarPubMed
Paradis, F., Vigneault, C., Robert, C. & Sirard, M.A. (2005). RNA interference as a tool to study gene function in bovine oocytes. Mol. Reprod. Dev. 70, 111–21.Google Scholar
Tanaka, M., Hennebold, J.D., Macfarlane, J. & Adashi, E.Y. (2001). A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development 128, 655–64.Google Scholar
Tanaka, Y., Kato, S., Tanaka, M., Kuji, N. & Yoshimura, Y. (2003a). Structure and expression of the human oocyte-specific histone H1 gene elucidated by direct RT-nested PCR of a single oocyte. Biochem. Biophys. Res. Commun. 304, 351–7.Google Scholar
Tanaka, M., Kihara, M., Meczekalski, B., King, G.J. & Adashi, E.Y. (2003b). H1oo: a pre-embryonic H1 linker histone in search of a function. Mol. Cell. Endocrinol. 202, 59.Google Scholar
Tanaka, M., Kihara, M., Hennebold, J.D., Eppig, J.J., Viveiros, M.M., Emery, B.R., Carrell, D.T., Kirkman, N.J., Meczekalski, B., Zhou, J., Bondy, C.A., Becker, M., Schultz, R.M., Misteli, T., De La Fuente, R., King, G.J. & Adashi, E.Y. (2005). H1FOO is coupled to the initiation of oocytic growth. Biol. Reprod. 72, 135–42.Google Scholar
Teranishi, T., Tanaka, M., Kimoto, S., Ono, Y., Miyakoshi, K., Kono, T. & Yoshimura, Y. (2004). Rapid replacement of somatic linker histones with the oocyte-specific linker histone H1foo in nuclear transfer. Dev. Biol. 266, 7686.Google Scholar
Terme, J.M., Sese, B., Millan-Arino, L., Mayor, R., Belmonte, J.C., Barrero, M.J. & Jordan, A. (2011). Histone H1 variants are differentially expressed and incorporated into chromatin during differentiation and reprogramming to pluripotency. J. Biol. Chem. 286, 35347–57.Google Scholar
Yun, Y., Zheng, X.B., Liu, W.Q., Dou, Z.Y. & Lei, A.M. (2008). Construction of eukaryotic expression vector of bovine Nanog gene and screening for effective siRNA. Scientia Agricultura Sinica 41, 4180–6. [in Chinese]Google Scholar
Yun, Y., Zhao, G.M., Wu, S.J., Li, W. & Lei, A.M. (2012). Replacement of H1 linker histone during bovine somatic cell nuclear transfer. Theriogenology 78, 1371–80.Google Scholar
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