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Addition of granulosa cell mass to the culture medium of oocytes derived from early antral follicles increases oocyte growth, ATP content, and acetylation of H4K12

Published online by Cambridge University Press:  03 October 2016

Miyako Sugiyama ,
Mei Sumiya ,
Koumei Shirasuna ,
Takehito Kuwayama  and
Hisataka Iwata
Miyako Sugiyama
Affiliation:
Tokyo University of Agriculture, Funako 1737 Atugi City, Kanagawa 243–0034, Japan
Mei Sumiya
Affiliation:
Tokyo University of Agriculture, Funako 1737 Atugi City, Kanagawa 243–0034, Japan
Koumei Shirasuna
Affiliation:
Tokyo University of Agriculture, Funako 1737 Atugi City, Kanagawa 243–0034, Japan
Takehito Kuwayama
Affiliation:
Tokyo University of Agriculture, Funako 1737 Atugi City, Kanagawa 243–0034, Japan
Hisataka Iwata*
Affiliation:
Tokyo University of Agriculture, Funako 1737 Atugi City, Kanagawa 243-0034, Japan
*
All correspondence to: Hisataka Iwata. Tokyo University of Agriculture, Funako 1737 Atugi City, Kanagawa 243-0034, Japan. Tel:/Fax: +81 46 270 6587. E-mail: hliwata@nodai.ac.jp
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Summary

The main aim of the present study was to examine the hypothesis that an increase in the number of granulosa cells surrounding developing bovine oocytes results in both high ATP levels and an increase in the acetylation level of H4K12 in oocytes grown in vitro. Oocyte–granulosa cell complexes (OGCs) were collected from early antral follicles (EAFs, 0.4–0.7 mm in diameter), and individually cultured on 96-well plates with or without additional granulosa cell mass that had been prepared from other OGCs. After 16 days of culture, we examined: (i) the rate of antrum formation of the OGCs; (ii) the diameter, maturation, and fertilization rate of the oocytes; and (iii) the ATP content and acetylation level of H4K12 in the oocytes grown in vitro. Granulosa cell mass added to the culture medium contributed to the development of OGCs with a higher rate of antrum formation and oocyte growth. Furthermore, the addition of granulosa cells increased the ATP content and acetylation level of H4K12 in oocytes grown in vitro compared with those developed without addition of granulosa cells. In addition, there was a positive correlation between the ATP content in oocytes grown in vitro and the number of granulosa cells in the corresponding OGCs. The results suggest that granulosa cells play a role not only in the development of OGCs and the growth of oocytes, but also in the determination of ATP content and the acetylation of H4K12 in the oocytes developed in vitro.

Keywords

AcetylationATPEarly antral folliclesGranulosa cellsOocytes
Type
Research Article
Information
Zygote , Volume 24 , Issue 6 , December 2016 , pp. 848 - 856
Copyright
Copyright © Cambridge University Press 2016 

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References

Albertini, D.F., Combelles, C.M., Benecchi, E. & Carabatsos, M.J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121, 647–53.Google Scholar
Arunakumari, G., Shanmugasundaram, N. & Rao, V.H. (2010). Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–94.Google Scholar
Binelli, M. & Murphy, B.D. (2010). Coordinated regulation of follicle development by germ and somatic cells. Reprod. Fertil. Dev. 22, 1–12.Google Scholar
Dalton, C.M., Szabadkai, G., & Carroll, J. (2014). Measurement of ATP in single oocytes: impact of maturation and cumulus cells on levels and consumption. J. Cell Physiol. 229, 353–61.Google Scholar
Downs, S.M. & Utecht, A.M. (1999). Metabolism of radiolabeled glucose by mouse oocytes and oocyte-cumulus cell complexes. Biol. Reprod. 60, 1446–52.CrossRefGoogle ScholarPubMed
Endo, M., Kimura, K., Kuwayama, T., Monji, Y. & Iwata, H. (2012). Effect of estradiol during culture of bovine oocyte–granulosa cell complexes on the mitochondrial DNA copies of oocytes and telomere length of granulosa cells. Zygote 22, 431–9.Google Scholar
Gu, L., Liu, H., Gu, X., C, Boots, Moley, K.H. & Wang, Q. (2014). Metabolic control of oocyte development: linking maternal nutrition and reproductive outcomes. Cell Mol. Life Sci. 72, 251–71.CrossRefGoogle ScholarPubMed
Gutierrez, C.G., Ralph, J.H., Telfer, E.E., Wilmut, I. & Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro . Biol. Reprod. 62, 1322–8.Google Scholar
Itami, N., Shiratsuki, S., Shirasuna, K., Kuwayama, T. & Iwata, H. (2015). Mitochondrial biogenesis and degradation are induced by CCCP treatment of porcine oocytes. Reproduction 150, 97–104.Google Scholar
Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T. & Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424–32.CrossRefGoogle ScholarPubMed
Kageyama, S., Liu, H., Kaneko, N., Ooga, M., Nagata, M. & Aoki, F. (2007). Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 133, 85–94.Google Scholar
Luz, V.B., Araújo, V.R., Duarte, A.B., Celestino, J.J., Silva, T.F., Magalhães-Padilha, D.M., Chaves, R.N., Brito, I.R., Almeida, A.P., Campello, C.C., Feltrin, C., Bertolini, M., Santos, R.R. & Figueiredo, J.R. (2012). Eight-cell parthenotes originated from in vitro grown sheep preantral follicles. Reprod. Sci. 19, 1219–25.Google Scholar
Maalouf, W.E., Alberio, R. & Campbell, K.H. (2008). Differential acetylation of histone H4 lysine during development of in vitro fertilized, cloned and parthenogenetically activated bovine embryos. Epigenetics 3, 199–209.Google Scholar
Magalhães, D.M., Duarte, A.B., Araújo, V.R., Brito, I.R., Soares, T.G., Lima, I.M., Lopes, C.A., Campello, C.C., Rodrigues, A.P. & Figueiredo, J.R. (2011). In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–8.Google Scholar
Manosalva, I. & González, A. (2009). Aging alters histone H4 acetylation and CDC2A in mouse germinal vesicle stage oocytes. Biol. Reprod. 81, 1164–71.Google Scholar
Matzuk, M.M., Burns, K.H., Viveiros, M.M. & Eppig, J.J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178–80.Google Scholar
Morrish, F., Noonan, J., Perez-Olsen, C., Gafken, P.R., Fitzgibbon, M., Kelleher, J., Van Gilst, M. & Hockenbery, D. (2010). Myc-dependent mitochondrial generation of acetyl-CoA contributes to fatty acid biosynthesis and histone acetylation during cell cycle entry. J. Biol. Chem. 285, 36267–74.CrossRefGoogle ScholarPubMed
Moussaieff, A., Rouleau, M., Kitsberg, D., Cohen, M., Levy, G., Barasch, D., Nemirovski, A., Shen-Orr, S, Laevsky, I., Amit, M., Bomze, D., Elena-Herrmann, B., Scherf, T., Nissim-Rafinia, M., Kempa, S., Itskovitz-Eldor, J., Meshorer, E., Aberdam, D. & Nahmias, Y. (2015). Glycolysis-mediated changes in acetyl-CoA and histone acetylation control the early differentiation of embryonic stem cells. Cell Metab. 21, 392–402.CrossRefGoogle ScholarPubMed
Oi, A., Tasaki, H., Munakata, Y., Shirasuna, K., Kuwayama, T. & Iwata, H. (2015). Effects of reaggregated granulosa cells and oocytes derived from early antral follicles on the properties of oocytes grown in vitro . J. Reprod. Dev. 61, 191–7.Google Scholar
Orisaka, M., Tajima, K., Tsang, B.K. & Kotsuji, F. (2009). Oocyte–granulosa-theca cell interactions during preantral follicular development. J. Ovarian Res. 2, 9.Google Scholar
Racedo, S.E., Wrenzycki, C., Lepikhov, K., Salamone, D., Walter, J. & Niemann, H. (2009). Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation. Reprod. Fertil. Dev. 21, 738–48.Google Scholar
Sato, D., Itami, N., Tasaki, H., Takeo, S., Kuwayama, T. & Iwata, H. (2014). Relationship between mitochondrial DNA copy number and SIRT1 expression in porcine oocytes. PLoS One 9, e94488.Google Scholar
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