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Effect of estradiol during culture of bovine oocyte–granulosa cell complexes on the mitochondrial DNA copies of oocytes and telomere length of granulosa cells

Published online by Cambridge University Press:  12 December 2012

M. Endo ,
K. Kimura ,
T. Kuwayama ,
Y. Monji  and
H. Iwata
M. Endo
Affiliation:
Tokyo University of Agriculture, Department of Animal Science, Funako 1737, Atsugi City, Kanagawa Prefecture 243–0034, Japan.
K. Kimura
Affiliation:
National Institute of Livestock and Grassland Science, Tochigi 329–2793, Japan.
T. Kuwayama
Affiliation:
Tokyo University of Agriculture, Department of Animal Science, Funako 1737, Atsugi City, Kanagawa Prefecture 243–0034, Japan.
Y. Monji
Affiliation:
Tokyo University of Agriculture, Department of Animal Science, Funako 1737, Atsugi City, Kanagawa Prefecture 243–0034, Japan.
H. Iwata*
Affiliation:
Tokyo University of Agriculture, Department of Animal Science, Funako 1737, Atsugi City, Kanagawa Prefecture 243–0034, Japan.
*
All correspondence to H. Iwata. Tokyo University of Agriculture, Department of Animal Science, Funako 1737, Atsugi City, Kanagawa Prefecture 243–0034, Japan. Tel: +81 46 270 6587. Fax: +81 46 270 6587. E-mail: h1iwata@nodai.ac.jp
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Summary

During the development of oocytes from early antral follicles (EAFs) to antral follicles (AFs), the mitochondrial DNA copy number (Mt DNA number) increases, and granulosa cells markedly proliferate. This study examined the effect of supplementation of culture medium with estradiol-17β (E2) on the in vitro growth of oocytes, and increases in the Mt DNA number, and telomere length during the in vitro culture of oocytes derived from EAFs (0.4–0.7 mm in diameter). The E2 supplementation improved antrum formation and the ratio of oocytes reaching the metaphase II (MII) stage, and there was a significant difference in these values between addition E2 concentrations of 10 μg/ml and 0.1 μg/ml. When the oocytes were cultured in the medium containing 10 μg/ml E2, the Mt DNA number determined by real-time polymerase chain reaction (PCR) significantly increased, and the ratio of the Mt DNA number at the end of culture to the Mt DNA number at the beginning of the culture was greatly different among cows, and could be predicted by the degree of the difference between the Mt DNA number of oocytes derived from EAFs and that of oocytes derived from AFs (3–6 mm in diameter). When oocytes were cultured for 16 days in a medium containing 10 μg/ml E2 or 0.1 μg/ml E2, the Mt DNA number of oocytes grown in vitro did not differ, but the telomere length of the granulosa cells was significantly greater in the 10 μg/ml E2 group than in the 0.1 μg/ml group. In conclusion, E2 supplementation in culture medium improved the growth of oocytes derived from EAFs, and a high E2 concentration increased the telomere length of the granulosa cells.

Keywords

Early antral follicleEstradiolMitochondrial numberTelomere length
Type
Research Article
Information
Zygote , Volume 22 , Issue 4 , November 2014 , pp. 431 - 439
Copyright
Copyright © Cambridge University Press 2012 

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References

Bayne, S., Li, H., Jones, M.E., Pinto, A.R., van Sinderen, M., Drummond, A., Simpson, E.R. & Liu, J.P. (2011). Estrogen deficiency reversibly induces telomere shortening in mouse granulosa cells and ovarian aging in vivo. Protein Cell 2, 333–46.Google Scholar
Beker-van Woudenberg, A.R., van Tol, H.T., Roelen, B.A., Colenbrander, B. & Bevers, M.M. (2004). Estradiol and its membrane-impermeable conjugate (estradiol-bovine serum albumin) during in vitro maturation of bovine oocytes: effects on nuclear and cytoplasmic maturation, cytoskeleton, and embryo quality. Biol. Reprod. 70, 1465–74.Google Scholar
Chen, J.Q., Cammarata, P.R., Baines, C.P. & Yager, J.D. (2009). Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim. Biophys. Acta. 1793, 1540–70.Google Scholar
Chiaratti, M.R., Bressan, F.F., Ferreira, C.R., Caetano, A.R., Smith, L.C., Vercesi, A.E. & Meirelles, F.V. (2010). Embryo mitochondrial DNA depletion is reversed during early embryogenesis in cattle. Biol. Reprod. 82, 76–85.Google Scholar
Couse, J.F., Yates, M.M., Deroo, B.J. & Korach, K.S. (2005). Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 146, 3247–62.CrossRefGoogle ScholarPubMed
El Shourbagy, S.H., Spikings, E.C., Freitas, M. & St John, J.C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–45.CrossRefGoogle ScholarPubMed
Emmen, J.M., Couse, J.F., Elmore, S.A., Yates, M.M., Kissling, G.E. & Korach, K.S. (2005). In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER)α and ERβ null mice indicate a role for ERβ in follicular maturation. Endocrinology 146, 2817–26.Google Scholar
Evans, A.C., Ireland, J.L., Winn, M.E., Lonergan, P., Smith, G.W., Coussens, P.M. & Ireland, J.J. (2004). Identification of genes involved in apoptosis and dominant follicle development during follicular waves in cattle. Biol. Reprod. 70, 1475–84.Google Scholar
Hattori, M.A., Arai, M., Saruwatari, K. & Kato, Y. (2004). Estrogen regulation of nitric oxide synthesis in the porcine oocyte. Mol. Cell. Biochem. 260, 13–9.Google Scholar
Hirao, Y., Itoh, T., Shimizu, M., Iga, K., Aoyagi, K., Kobayashi, M., Kacchi, M., Hoshi, H. & Takenouchi, N. (2004). In vitro growth and development of bovine oocyte-granulosa cell complexes on the flat substratum: effects of high polyvinylpyrrolidone concentration in culture medium. Biol. Reprod. 70, 83–91.Google Scholar
Huynh, K., Jones, G., Thouas, G., Britt, K.L., Simpson, E.R. & Jones, M.E. (2004). Estrogen is not directly required for oocyte developmental competence. Biol. Reprod. 70, 1263–9.CrossRefGoogle Scholar
Iwata, H., Hayashi, T., Sato, H., Kimura, K., Kuwayama, T., & Monji, Y. (2006). Modification of ovary stock solution with magnesium and raffinose improves the developmental competence of oocytes after long preservation. Zygote 13, 303–8.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.Google Scholar
Kondoh, K., Tsuji, N., Asanuma, K., Kobayashi, D. & Watanabe, N. (2007). Inhibition of estrogen receptor beta-mediated human telomerase reverse transcriptase gene transcription via the suppression of mitogen-activated protein kinase signaling plays an important role in 15-deoxy-delta(12,14)-prostaglandin J(2)-induced apoptosis in cancer cells. Exp. Cell. Res. 313, 3486–96.Google Scholar
Lavranos, T.C., Mathis, J.M., Latham, S.E., Kalionis, B., Shay, J.W. & Rodgers, R.J. (1999). Evidence for ovarian granulosa stem cells: telomerase activity and localization of the telomerase ribonucleic acid component in bovine ovarian follicles. Biol. Reprod. 61, 358–66.Google Scholar
Ling, S., Zhou, L., Li, H., Dai, A., Liu, J.P., Komesaroff, P.A. & Sudhir, K. (2006). Effects of 17beta-estradiol on growth and apoptosis in human vascular endothelial cells: influence of mechanical strain and tumor necrosis factor-alpha. Steroids 71, 799–808.CrossRefGoogle ScholarPubMed
Liu, J.P. & Li, H. (2010). Telomerase in the ovary. Reproduction 140, 215–22.Google Scholar
Mastromonaco, G.F., Perrault, S.D., Betts, D.H. & King, W.A. (2006). Role of chromosome stability and telomere length in the production of viable cell lines for somatic cell nuclear transfer. BMC Dev. Biol. 9, 6–41.Google Scholar
Mattingly, K.A., Ivanova, M.M., Riggs, K.A., Wickramasinghe, N.S., Barch, M.J. & Klinge, C.M. (2008). Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol. Endocrinol. 22, 609–22.Google Scholar
Misiti, S., Nanni, S., Fontemaggi, G., Cong, Y.S., Wen, J., Hirte, H.W., Piaggio, G., Sacchi, A., Pontecorvi, A., Bacchetti, S. & Farsetti, A. (2000). Induction of hTERT expression and telomerase activity by estrogens in human ovary epithelium cells. Mol. Cell. Biol. 20, 3764–71.Google Scholar
Reynier, P., May-Panloup, P., Chrétien, M.F., Morgan, C.J., Jean, M., Savagner, F., Barrière, P. & Malthièry, Y. (2001). Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 7, 425–9.Google Scholar
Russo, V., Berardinelli, P., Martelli, A., Di Giacinto, O., Nardinocchi, D., Fantasia, D. & Barboni, B. (2006). Expression of telomerase reverse transcriptase subunit (TERT) and telomere sizing in pig ovarian follicles. J. Histochem. Cytochem. 54, 443–55.Google Scholar
Sakamoto, A., Iwata, H., Sato, H., Hayashi, T., Kuwayama, , , T., & Monji, Y. (2006). Effect of modification of ovary preservation solution by adding glucose on the maturation and development of pig oocytes after prolonged storage. J. Reprod. Dev. 52, 669–74.CrossRefGoogle ScholarPubMed
Santos, T.A., Shourbagy, S. & John, J.C. (2006). Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584–91.Google Scholar
Sastre-Serra, J., Nadal-Serrano, M., Pons, D.G., Valle, A., Oliver, J. & Roca, P. (2012). The effects of 17β-estradiol on mitochondrial biogenesis and function in breast cancer cell lines are dependent on the ERα/ERβ ratio. Cell. Physiol. Biochem. 29, 261–8.Google Scholar
Wai, T., Ao, A., Zhang, X., Cyr, D., Dufort, D. & Shoubridge, E.A. (2010). The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod. 83, 52–62.Google Scholar
Wang, L.Y., Wang, D.H., Zou, X.Y. & Xu, C.M. (2009). Mitochondrial functions on oocytes and preimplantation embryos. J. Zhejiang Univ. Sci. B. 10, 483–92.CrossRefGoogle ScholarPubMed
Weber, T.A. & Reichert, A.S. (2010). Impaired quality control of mitochondria: aging from a new perspective. Exp. Gerontol. 45, 503–11.Google Scholar
West-Farrell, E.R., Xu, M., Gomberg, M.A., Chow, Y.H., Woodruff, T.K. & Shea, L.D. (2008). The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles. Biol. Reprod. 80, 432–9.Google Scholar
Xu, M., West, E., Shea, L.D. & Woodruff, T.K. (2006). Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol. Reprod. 75, 916–23.Google Scholar
Yamagata, Y., Nakamura, Y., Umayahara, K., Harada, A., Takayama, H., Sugino, N. & Kato, H. (2002). Changes in telomerase activity in experimentally induced atretic follicles of immature rats. Endocr. J. 49, 589–95.Google Scholar