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Effect of bovine age on the proliferative activity, global DNA methylation, relative telomere length and telomerase activity of granulosa cells

Published online by Cambridge University Press:  27 July 2011

Hiroya Goto ,
Hisataka Iwata ,
Shun Takeo ,
Keiko Nisinosono ,
Sayoko Murakami ,
Yasunori Monji  and
Takehito Kuwayama
Hiroya Goto
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.
Shun Takeo
Affiliation:
Tokyo University of Agriculture, Funako 1737, Atugi City, Kanagawa 243–0034, Japan.
Keiko Nisinosono
Affiliation:
Tokyo University of Agriculture, Funako 1737, Atugi City, Kanagawa 243–0034, Japan.
Sayoko Murakami
Affiliation:
Tokyo University of Agriculture, Funako 1737, Atugi City, Kanagawa 243–0034, Japan.
Yasunori Monji
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.
*
All correspondence to: Hisataka Iwata. Tokyo University of Agriculture, Funako 1737, Atugi City, Kanagawa 243–0034, Japan. Tel:/Fax: +81 462706587. E-mail [email protected]
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Summary

Granulosa cells influence the growth and acquisition of the developmental competence of oocytes. We investigated the effects of ageing on the proliferative activity, global genomic DNA methylation, relative telomere length and telomerase activity of bovine granulosa cells. The proliferative activity of cells was examined by bromodeoxyuridine (BrdU) assay, genomic DNA methylation was examined by enzyme-linked immunosorbent assay (ELISA), and relative telomere length and telomerase activity were examined by real-time polymerase chain reaction. We first compared the proliferative activity of the granulosa cells of the medium follicles between in dominant phase ovaries and growth phase ovaries. We observed that the proliferative activity of the granulosa cells of dominant phase ovaries was significantly lower than those of growth phase ovaries. In addition, the proliferative activity of granulosa cells was inversely associated with follicular size. Based on the results, we used granulosa cells harvested from the medium follicles (3–5 mm in diameter) on the surfaces of the dominant phase ovaries collected from cows at a slaughterhouse. The proliferative activity of the granulosa cells harvested from the ovaries of old cows (N = 8; average age 165.1 months) was lower than that of the cells from young cows (N = 8; average age 30.9 months). Global loss of cytosine methylation was detected in the granulosa cells of old cows (N = 12; average age 141.0 months) compared with young cows (N = 15; average age 27.4 months). Although the relative telomere lengths of cumulus cells were similar in the two age groups, the relative telomere lengths and telomerase activity of the granulosa cells from old cows (N = 17 and 9; average age, 164.6 and 151.3 months, respectively) tended to be shorter than those of the cells from young cows (N = 17 and 10; average age 30.6 and 28.1 months, respectively); however, this difference was not significant p = 0.09 and 0.053, respectively). In conclusion, the proliferative activity and genomic global DNA methylation significantly decreased, and the relative telomere lengths and telomerase activity of granulosa cells tended to be shorter with the age of donor cows.

Keywords

AgeingDNA methylationGranulosa cellsProliferative activityTelomere length
Type
Research Article
Information
Zygote , Volume 21 , Issue 3 , August 2013 , pp. 256 - 264
Copyright
Copyright © Cambridge University Press 2011 

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References

Aerts, J.M. & Bols, P.E. (2010). Ovarian follicular dynamics. A review with emphasis on the bovine species. Part II: Antral development, exogenous influence and future prospects. Reprod. Domest. Anim. 45, 180–7.CrossRefGoogle ScholarPubMed
Baird, D.T., Collins, J., Egozcue, J., Evers, L.H., Gianaroli, L., Leridon, H., Sunde, A., Templeton, A., Van, Steirteghem, A., Cohen, J., Crosignani, P.G., Devroey, P., Diedrich, K., Fauser, B.C., Fraser, L., Glasier, A., Liebaers, I., Mautone, G., Penney, G. & Tarlatzis, B; ESHRE, Capri Workshop Group. (2005). Fertility and ageing. Hum. Reprod. Update 11, 261–76.Google ScholarPubMed
Broekmans, F.J., Knauff, E.A., Te, Velde, E.R., Macklon, N.S. & Fauser, B.C. (2007). Female reproductive ageing: current knowledge and future trends. Trends Endocrinol. Metab. 18, 58–65.CrossRefGoogle ScholarPubMed
Downs, S.M.Regulation of the G2/M transition in rodent oocytes. Mol. Reprod. Dev. (2010). 77, 566–85.CrossRefGoogle ScholarPubMed
Fortune, J.E., Rivera, G.M. & Yang, M.Y. (2004). Follicular development: the role of the follicular microenvironment in selection of the dominant follicle. Anim. Reprod. Sci. 82–83:109–26.Google ScholarPubMed
Fuke, C., Shimabukuro, M., Petronis, A., Sugimoto, J., Oda, T., Miura, K., Miyazaki, T., Ogura, C., Okazaki, Y. & Jinno, Y. (2004). Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann. Hum. Genet. 68, 196–204.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ritter, L.J. & Armstrong, D.T. (2004). Oocyte-somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–46.CrossRefGoogle ScholarPubMed
Gutiérrez, C.G., Campbell, B.K. & Webb, R. (1997). Development of a long-term bovine granulosa cell culture system: induction and maintenance of estradiol production, response to follicle-stimulating hormone, and morphological characteristics. Biol. Reprod. 56, 608–16.CrossRefGoogle ScholarPubMed
Hagemann, L.J. (1999). Influence of the dominant follicle on oocytes from subordinate follicles. Theriogenology 51, 449–59.CrossRefGoogle ScholarPubMed
Hagemann, L.J., Beaumont, S.E., Berg, M., Donnison, M.J., Ledgard, A., Peterson, A.J., Schurmann, A. & Tervit, H.R. (1999). Development during single IVP of bovine oocytes from dissected follicles: interactive effects of estrous cycle stage, follicle size and atresia. Mol. Reprod. Dev. 53, 451–8.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Hamel, M., Dufort, I., Robert, C., Gravel, C., Leveille, M.C., Leader, A. & Sirard, M.A. (2008). Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum. Reprod. 23, 1118–27.CrossRefGoogle ScholarPubMed
Huang, Z. & Wells, D. (2010). The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Mol. Hum. Reprod. 16, 715–25.CrossRefGoogle ScholarPubMed
Hunter, M.G. (2000). Oocyte maturation and ovum quality in pigs. Rev. Reprod. 5, 122–30.CrossRefGoogle ScholarPubMed
Ito, M., Muraki, M., Takahashi, Y., Imai, M., Tsukui, T., Yamakawa, N., Nakagawa, K., Ohgi, S., Horikawa, T., Iwasaki, W., Iida, A., Nishi, Y., Yanase, T., Nawata, H., Miyado, K., Kono, T., Hosoi, Y. & Saito, H. (2008). Glutathione S-transferase theta 1 expressed in granulosa cells as a biomarker for oocyte quality in age-related infertility. Fertil. Steril. 90, 1026–35.CrossRefGoogle ScholarPubMed
Ito, M., Miyado, K., Nakagawa, K., Muraki, M., Imai, M., Yamakawa, N., Qin, J., Hosoi, Y., Saito, H. & Takahashi, Y. (2010). Age-associated changes in the subcellular localization of phosphorylated p38 MAPK in human granulosa cells. Mol. Hum. Reprod. 16, 928–37.CrossRefGoogle ScholarPubMed
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
Kim, K.C., Friso, S. & Choi, S.W. (2009). DNA methylation, an epigenetic mechanism connecting folate to healthy embryonic development and aging. J. Nutr Biochem. 20, 917–26.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Liu, J.P. & Li, H. (2010). Telomerase in the ovary. Reproduction 140, 215–22.CrossRefGoogle ScholarPubMed
Lucidi, P., Bernabò, N., Turriani, M., Barboni, B. & Mattioli, M. (2003). Cumulus cells steroidogenesis is influenced by the degree of oocyte maturation. Reprod. Biol. Endocrinol. 28, 45.CrossRefGoogle Scholar
Luck, M.R., Rodgers, R.J. & Findlay, J.K. (1990). Secretion and gene expression of inhibin, oxytocin and steroid hormones during the in vitro differentiation of bovine granulosa cells. Reprod. Fertil. Dev. 2, 11–25.CrossRefGoogle ScholarPubMed
Maillet, G., Bréard, E., Benhaïm, A., Leymarie, P. & Féral, C. (2002). Hormonal regulation of apoptosis in rabbit granulosa cells in vitro: evaluation by flow cytometric detection of plasma membrane phosphatidylserine externalization. Reproduction 123, 243–51.CrossRefGoogle ScholarPubMed
Malhi, P.S., Adams, G.P. & Singh, J. (2005). Bovine model for the study of reproductive aging in women: follicular, luteal, and endocrine characteristics. Biol. Reprod. 73, 45–53.CrossRefGoogle Scholar
Malhi, P.S., Adams, G.P., Pierson, R.A. & Singh, J. (2006). Bovine model of reproductive aging: response to ovarian synchronization and superstimulation. Theriogenology 66, 1257–66.CrossRefGoogle ScholarPubMed
Malhi, P.S., Adams, G.P., Mapletoft, R.J. & Singh, J. (2007). Reproduction 134, 233–9.CrossRefGoogle Scholar
Malhi, P.S., Adams, G.P., Mapletoft, R.J. & Singh, J. (2008). Superovulatory response in a bovine model of reproductive aging. Anim. Reprod. Sci. 109, 100–9.CrossRefGoogle 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. 6, 41.CrossRefGoogle ScholarPubMed
Murgatroyd, C., Wu, Y., Bockmühl, Y. & Spengler, D. (2010). The Janus face of DNA methylation in aging. Aging 20, 107–10.CrossRefGoogle Scholar
Olovnikov, A.M. (1996). Telomeres, telomerase, and aging: origin of the theory. Exp. Gerontol. 31, 443–8.CrossRefGoogle ScholarPubMed
Orisaka, M., Tajima, K., Tsang, BK. & Kotsuji, F. (2009). Oocyte-granulosa-theca cell interactions during preantral follicular development. J. Ovarian Res. 2, 9.CrossRefGoogle ScholarPubMed
Ottolenghi, C., Uda, M., Hamatani, T., Crisponi, L., Garcia, J.E., Ko, M., Pilia, G., Sforza, C., Schlessinger, D. & Forabosco, A. (2004). Aging of oocyte, ovary, and human reproduction. Ann. NY Acad. Sci. 1034, 117–31.CrossRefGoogle ScholarPubMed
Pandey, A.N., Tripathi, A., Premkumar, K.V., Shrivastav, T.G. & Chaube, S.K. (2010). Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes. J. Cell Biochem. 111, 521–8.CrossRefGoogle ScholarPubMed
Parborell, F., Irusta, G., Vitale, A., Gonzalez, O., Pecci, A. & Tesone, M. (2005). Gonadotropin-releasing hormone antagonist antide inhibits apoptosis of preovulatory follicle cells in rat ovary. Biol. Reprod. 72, 659–66.CrossRefGoogle ScholarPubMed
Rodgers, R.J. & Irving-Rodgers, H.F. (2010). Morphological classification of bovine ovarian follicles. Reproduction 139, 309–18.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Schams, D. & Berisha, B. (2002). Steroids as local regulators of ovarian activity in domestic animals. Domest. Anim. Endocrinol. 23, 53–65.CrossRefGoogle ScholarPubMed
Su, Y.Q., Sugiura, K. & Eppig, J.J. (2009). Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin. Reprod. Med. 27, 32–42.CrossRefGoogle ScholarPubMed
Tatone, C., Carbone, M.C., Falone, S., Aimola, P., Giardinelli, A., Caserta, D., Marci, R., Pandolfi, A., Ragnelli, A.M. & Amicarelli, F. (2006). Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol. Hum. Reprod. 12, 655–60.CrossRefGoogle ScholarPubMed
Wezel, I.L. & Rodgers, R.J. (1996). Morphological characterization of bovine primordial follicles and their environment in vivo. Biol. Reprod. 55, 1003–11.CrossRefGoogle ScholarPubMed
Wathes, D.C., Perks, C.M., Davis, A.J. & Denning-Kendall, P.A. (1995). Regulation of insulin-like growth factor-I and progesterone synthesis by insulin and growth hormone in the ovine ovary. Biol. Reprod. 53, 882–9.CrossRefGoogle ScholarPubMed
Yamamoto, T., Iwata, H., Goto, H., Shiratuki, S., Tanaka, H., Monji, Y. & Kuwayama, T. (2010). Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes. Mol. Reprod. Dev. 77, 595–604.CrossRefGoogle ScholarPubMed
Zheng, X., Price, C.A., Tremblay, Y., Lussier, J.G. & Carrière, P.D. (2008). Role of transforming growth factor-beta1 in gene expression and activity of estradiol and progesterone-generating enzymes in FSH-stimulated bovine granulosa cells. Reproduction 136, 447–57.CrossRefGoogle ScholarPubMed