Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 8/2014

01-08-2014 | Gamete Biology

Age-associated changes in bovine oocytes and granulosa cell complexes collected from early antral follicles

Authors: N. Itami, R. Kawahara-Miki, H. Kawana, M. Endo, T. Kuwayama, H. Iwata

Published in: Journal of Assisted Reproduction and Genetics | Issue 8/2014

Login to get access

Abstract

Purpose

To assess the age-associated changes in oocytes and granulosa cells derived from early antral follicles (EAFs).

Method

Gene expression analysis of granulosa cells of the EAFs using a genome analyzer (Illumina) and in vitro culture of oocyte-granulosa cell complexes (OGCs) of EAFs (400–700 μm in diameter) collected from ovaries of aged (>120 months) and young (<50 months) cows.

Results

Gene expression profiles in granulosa cells of EAFs of aged cows, which included changes in genes that encode chaperone proteins and antioxidants. In vivo development of EAFs, as determined by oocyte diameter of EAFs and AFs (3–6 mm in diameter), appeared to be impaired in aged cows and the OGCs of aged cows contained low GSH compared to younger counterparts. When the OGCs were cultured in a medium containing low estradiol (E2, 0.1 μg/mL), the ratio of antrum formation was higher for OGCs from aged animals than that from young animals, while higher abnormal fertilization rate and lower total cell number of the blastocysts were observed in the OGCs of aged cows compared with those of young cows. On the contrary, when the OGCs were cultured in a medium containing 10 μg/mL E2, the ratio of antrum formation and fertilization outcome was comparable between the two age groups, whereas the total cell number of the blastocysts was still low in the aged group.

Conclusion

Aging affects the gene expression profiles of the granulosa cells, and impairs in vitro developmental ability of OGCs collected from EAFs.
Appendix
Available only for authorised users
Literature
1.
go back to reference Baerwald AR, Adams GP, Pierson RA. Characterization of ovarian follicular wave dynamics in women. Biol Reprod. 2003;69:1023–31.PubMedCrossRef Baerwald AR, Adams GP, Pierson RA. Characterization of ovarian follicular wave dynamics in women. Biol Reprod. 2003;69:1023–31.PubMedCrossRef
2.
go back to reference Malhi PS, Adams GP, Singh J. Bovine model for the study of reproductive aging in women: follicular, luteal, and endocrine characteristics. Biol Reprod. 2005;73:45–53.PubMedCrossRef Malhi PS, Adams GP, Singh J. Bovine model for the study of reproductive aging in women: follicular, luteal, and endocrine characteristics. Biol Reprod. 2005;73:45–53.PubMedCrossRef
3.
go back to reference Malhi PS, Adams GP, Pierson RA, Singh J. Bovine model of reproductive aging: response to ovarian synchronization and superstimulation. Theriogenology. 2006;66:1257–66.PubMedCrossRef Malhi PS, Adams GP, Pierson RA, Singh J. Bovine model of reproductive aging: response to ovarian synchronization and superstimulation. Theriogenology. 2006;66:1257–66.PubMedCrossRef
4.
go back to reference Janny L, Menezo YJ. Maternal age effect on early human embryonic development and blastocyst formation. Mol Reprod Dev. 1996;45:31–7.PubMedCrossRef Janny L, Menezo YJ. Maternal age effect on early human embryonic development and blastocyst formation. Mol Reprod Dev. 1996;45:31–7.PubMedCrossRef
5.
go back to reference Scholtes MC, Zeilmaker GH. Blastocyst transfer in day-5 embryo transfer depends primarily on the number of oocytes retrieved and not on age. Fertil Steril. 1998;69:78–83.PubMedCrossRef Scholtes MC, Zeilmaker GH. Blastocyst transfer in day-5 embryo transfer depends primarily on the number of oocytes retrieved and not on age. Fertil Steril. 1998;69:78–83.PubMedCrossRef
6.
go back to reference Pantos K, Athanasiou V, Stefanidis K, Stavrou D, Vaxevanoglou T, Chronopoulou M. Influence of advanced age on the blastocyst development rate and pregnancy rate in assisted reproductive technology. Fertil Steril. 1999;71:1144–6.PubMedCrossRef Pantos K, Athanasiou V, Stefanidis K, Stavrou D, Vaxevanoglou T, Chronopoulou M. Influence of advanced age on the blastocyst development rate and pregnancy rate in assisted reproductive technology. Fertil Steril. 1999;71:1144–6.PubMedCrossRef
7.
go back to reference Shapiro BS, Richter KS, Harris DC, Daneshmand ST. Influence of patient age on the growth and transfer of blastocyst-stage embryos. Fertil Steril. 2002;77:700–5.PubMedCrossRef Shapiro BS, Richter KS, Harris DC, Daneshmand ST. Influence of patient age on the growth and transfer of blastocyst-stage embryos. Fertil Steril. 2002;77:700–5.PubMedCrossRef
8.
go back to reference Malhi PS, Adams GP, Mapletoft RJ, Singh J. Oocyte developmental competence in a bovine model of reproductive aging. Reproduction. 2007;134:233–9.PubMedCrossRef Malhi PS, Adams GP, Mapletoft RJ, Singh J. Oocyte developmental competence in a bovine model of reproductive aging. Reproduction. 2007;134:233–9.PubMedCrossRef
9.
go back to reference Yamamoto T, Iwata H, Goto H, Shiratuki S, Tanaka H, Monji Y, et al. Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes. Mol Reprod Dev. 2010;77:595–604.PubMedCrossRef Yamamoto T, Iwata H, Goto H, Shiratuki S, Tanaka H, Monji Y, et al. Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes. Mol Reprod Dev. 2010;77:595–604.PubMedCrossRef
10.
go back to reference Iwata H, Goto H, Tanaka H, Sakaguchi Y, Kimura K, Kuwayama T, et al. Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod Fertil Dev. 2011;23:424–32.PubMedCrossRef Iwata H, Goto H, Tanaka H, Sakaguchi Y, Kimura K, Kuwayama T, et al. Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod Fertil Dev. 2011;23:424–32.PubMedCrossRef
11.
go back to reference Takeo S, Goto H, Kuwayama T, Monji Y, Iwata H. Effect of maternal age on the ratio of cleavage and mitochondrial DNA copy number in early developmental stage bovine embryos. J Reprod Dev. 2012;59:174–9.PubMedCentralPubMedCrossRef Takeo S, Goto H, Kuwayama T, Monji Y, Iwata H. Effect of maternal age on the ratio of cleavage and mitochondrial DNA copy number in early developmental stage bovine embryos. J Reprod Dev. 2012;59:174–9.PubMedCentralPubMedCrossRef
12.
13.
go back to reference Bancsi LF, Broekmans FJ, Eijkemans MJ, de Jong FH, Habbema JD, te Velde ER. Predictors of poor ovarian response in in vitro fertilization: a prospective study comparing basal markers of ovarian reserve. Fertil Steril. 2002;77:328–36.PubMedCrossRef Bancsi LF, Broekmans FJ, Eijkemans MJ, de Jong FH, Habbema JD, te Velde ER. Predictors of poor ovarian response in in vitro fertilization: a prospective study comparing basal markers of ovarian reserve. Fertil Steril. 2002;77:328–36.PubMedCrossRef
14.
go back to reference Malhi PS, Adams GP, Mapletoft RJ, Singh J. Superovulatory response in a bovine model of reproductive aging. Anim Reprod Sci. 2008;109:100–9.PubMedCrossRef Malhi PS, Adams GP, Mapletoft RJ, Singh J. Superovulatory response in a bovine model of reproductive aging. Anim Reprod Sci. 2008;109:100–9.PubMedCrossRef
15.
go back to reference Xu J, Bernuci MP, Lawson MS, Yeoman RR, Fisher TE, Zelinski MB, et al. Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction. 2010;140:685–97.PubMedCentralPubMedCrossRef Xu J, Bernuci MP, Lawson MS, Yeoman RR, Fisher TE, Zelinski MB, et al. Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction. 2010;140:685–97.PubMedCentralPubMedCrossRef
16.
go back to reference Choi JK, Ahn JI, Park JH, Lim JM. Derivation of developmentally competent oocytes by in vitro culture of preantral follicles retrieved from aged mice. Fertil Steril. 2011;95:1487–9.PubMedCrossRef Choi JK, Ahn JI, Park JH, Lim JM. Derivation of developmentally competent oocytes by in vitro culture of preantral follicles retrieved from aged mice. Fertil Steril. 2011;95:1487–9.PubMedCrossRef
17.
go back to reference Orisaka M, Tajima K, Tsang BK, Kotsuji F. 2009. Oocyte-granulosa-theca cell interactions during preantral follicular development. J Ovarian Res. 2009;2:9. Orisaka M, Tajima K, Tsang BK, Kotsuji F. 2009. Oocyte-granulosa-theca cell interactions during preantral follicular development. J Ovarian Res. 2009;2:9.
18.
go back to reference Tatone C, Carbone MC, Falone S, Aimola P, Giardinelli A, Caserta D, et al. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod. 2006;12:655–60.PubMedCrossRef Tatone C, Carbone MC, Falone S, Aimola P, Giardinelli A, Caserta D, et al. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod. 2006;12:655–60.PubMedCrossRef
19.
go back to reference Hurwitz JM, Jindal S, Greenseid K, Berger D, Brooks A, Santoro N, et al. Reproductive aging is associated with altered gene expression in human uteinizedgranulosa cells. Reprod Sci. 2010;17:56–67.PubMedCrossRef Hurwitz JM, Jindal S, Greenseid K, Berger D, Brooks A, Santoro N, et al. Reproductive aging is associated with altered gene expression in human uteinizedgranulosa cells. Reprod Sci. 2010;17:56–67.PubMedCrossRef
20.
go back to reference Ito M, Miyado K, Nakagawa K, Muraki M, Imai M, Yamakawa N, et al. Age-associated changes in the subcellular localization of phosphorylated p38 MAPK in human granulosa cells. Mol Hum Reprod. 2010;16:928–37.PubMedCrossRef Ito M, Miyado K, Nakagawa K, Muraki M, Imai M, Yamakawa N, et al. Age-associated changes in the subcellular localization of phosphorylated p38 MAPK in human granulosa cells. Mol Hum Reprod. 2010;16:928–37.PubMedCrossRef
21.
go back to reference Goto H, Iwata H, Takeo S, Nisinosono K, Murakami S, Monji Y, et al. Effect of bovine age on the proliferative activity, global DNA methylation, relative telomere length and telomerase activity of granulosa cells. Zygote. 2013;21:256–64.PubMedCrossRef Goto H, Iwata H, Takeo S, Nisinosono K, Murakami S, Monji Y, et al. Effect of bovine age on the proliferative activity, global DNA methylation, relative telomere length and telomerase activity of granulosa cells. Zygote. 2013;21:256–64.PubMedCrossRef
22.
23.
go back to reference Beg MA, Bergfelt DR, Kot K, Wiltbank MC, Ginther OJ. Follicular-fluid factors and granulosa-cell gene expression associated with follicle deviation in cattle. Biol Reprod. 2001;64:432–41.PubMedCrossRef Beg MA, Bergfelt DR, Kot K, Wiltbank MC, Ginther OJ. Follicular-fluid factors and granulosa-cell gene expression associated with follicle deviation in cattle. Biol Reprod. 2001;64:432–41.PubMedCrossRef
24.
go back to reference Endo M, Kawahara-Miki R, Cao F, Kimura K, Kuwayama T, Monji Y, et al. Estradiol supports in vitro development of bovine early antral follicles. Reproduction. 2013;145:85–96.PubMedCrossRef Endo M, Kawahara-Miki R, Cao F, Kimura K, Kuwayama T, Monji Y, et al. Estradiol supports in vitro development of bovine early antral follicles. Reproduction. 2013;145:85–96.PubMedCrossRef
25.
go back to reference Hirao Y, Itoh T, Shimizu M, Iga K, Aoyagi K, Kobayashi M, et al. 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. 2004;70:83–91.PubMedCrossRef Hirao Y, Itoh T, Shimizu M, Iga K, Aoyagi K, Kobayashi M, et al. 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. 2004;70:83–91.PubMedCrossRef
26.
go back to reference Hirao Y. Conditions affecting growth and developmental competence of mammalian oocytes in vitro. Anim Sci J. 2011;82:187–97.PubMedCrossRef Hirao Y. Conditions affecting growth and developmental competence of mammalian oocytes in vitro. Anim Sci J. 2011;82:187–97.PubMedCrossRef
27.
go back to reference Takahashi Y, First NL. In vitro development of bovine one-cell embryos: Influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology. 1992;37:963–78.PubMedCrossRef Takahashi Y, First NL. In vitro development of bovine one-cell embryos: Influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology. 1992;37:963–78.PubMedCrossRef
28.
go back to reference Takeo S, Kawahara-Miki R, Goto H, Cao F, Kimura K, Monji Y, et al. Age-associated changes in gene expression and developmental competence of bovine oocytes, and a possible countermeasure against age-associated events. Mol Reprod Dev. 2013;80:508–21.PubMedCrossRef Takeo S, Kawahara-Miki R, Goto H, Cao F, Kimura K, Monji Y, et al. Age-associated changes in gene expression and developmental competence of bovine oocytes, and a possible countermeasure against age-associated events. Mol Reprod Dev. 2013;80:508–21.PubMedCrossRef
29.
go back to reference Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5:621–8.PubMedCrossRef Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5:621–8.PubMedCrossRef
30.
go back to reference Tasaki H, Iwata H, Sato D, Monji Y, Kuwayama T. Estradiol has a major role in antrum formation of porcine preantral follicles cultured in vitro. Theriogenology. 2013;5:809–14.CrossRef Tasaki H, Iwata H, Sato D, Monji Y, Kuwayama T. Estradiol has a major role in antrum formation of porcine preantral follicles cultured in vitro. Theriogenology. 2013;5:809–14.CrossRef
31.
go back to reference Greenaway J, Gentry PA, Feige JJ, LaMarre J, Petrik JJ. Thrombospondin and vascular endothelial growth factor are cyclically expressed in an inverse pattern during bovine ovarian follicle development. Biol Reprod. 2005;72:1071–8.PubMedCrossRef Greenaway J, Gentry PA, Feige JJ, LaMarre J, Petrik JJ. Thrombospondin and vascular endothelial growth factor are cyclically expressed in an inverse pattern during bovine ovarian follicle development. Biol Reprod. 2005;72:1071–8.PubMedCrossRef
32.
go back to reference Harlow CR, Bradshaw AC, Rae MT, Shearer KD, Hillier SG. Oestrogen formation and connective tissue growth factor expression in rat granulosa cells. J Endocrinol. 2007;192:41–52.PubMedCrossRef Harlow CR, Bradshaw AC, Rae MT, Shearer KD, Hillier SG. Oestrogen formation and connective tissue growth factor expression in rat granulosa cells. J Endocrinol. 2007;192:41–52.PubMedCrossRef
33.
go back to reference Assidi M, Dufort I, Ali A, Hamel M, Algriany O, Dielemann S, et al. Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol Reprod. 2008;79:209–22.PubMedCrossRef Assidi M, Dufort I, Ali A, Hamel M, Algriany O, Dielemann S, et al. Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol Reprod. 2008;79:209–22.PubMedCrossRef
34.
35.
go back to reference Chen AQ, Wang ZG, Xu ZR, Yu SD, Yang ZG. Analysis of gene expression in granulosa cells of ovine antral growing follicles using suppressive subtractive hybridization. Anim Reprod Sci. 2009;115:39–48.PubMedCrossRef Chen AQ, Wang ZG, Xu ZR, Yu SD, Yang ZG. Analysis of gene expression in granulosa cells of ovine antral growing follicles using suppressive subtractive hybridization. Anim Reprod Sci. 2009;115:39–48.PubMedCrossRef
36.
go back to reference Hayashi KG, Ushizawa K, Hosoe M, Takahashi T. Differential genome-wide gene expression profiling of bovine largest and second-largest follicles: identification of genes associated with growth of dominant follicles. Reprod Biol Endocrinol. 2010;5:8–11. Hayashi KG, Ushizawa K, Hosoe M, Takahashi T. Differential genome-wide gene expression profiling of bovine largest and second-largest follicles: identification of genes associated with growth of dominant follicles. Reprod Biol Endocrinol. 2010;5:8–11.
37.
go back to reference Mora JM, Fenwick MA, Castle L, Baithun M, Ryder TA, Mobberley M, et al. Characterization and significance of adhesion and junction-related proteins in mouse ovarian follicles. Biol Reprod. 2012;153:1–14. Mora JM, Fenwick MA, Castle L, Baithun M, Ryder TA, Mobberley M, et al. Characterization and significance of adhesion and junction-related proteins in mouse ovarian follicles. Biol Reprod. 2012;153:1–14.
38.
go back to reference Fargnoli J, Kunisada T, Fornace Jr AJ, Schneider EL, Holbrook NJ. Decreased expたさきssion of heat shock protein 70 mRNA and protein after heat treatment in cells of aged rats. Proc Natl Acad Sci U S A. 1990;87:846–50.PubMedCentralPubMedCrossRef Fargnoli J, Kunisada T, Fornace Jr AJ, Schneider EL, Holbrook NJ. Decreased expたさきssion of heat shock protein 70 mRNA and protein after heat treatment in cells of aged rats. Proc Natl Acad Sci U S A. 1990;87:846–50.PubMedCentralPubMedCrossRef
39.
go back to reference Pratsinis H, Tsagarakis S, Zervolea I, Giannakopoulos F, Stathakos D, Thalassinos N, Kletsas D. Chronic in vivo exposure to glucocorticoids prolongs cellular lifespan: the case of Cushing’s syndrome-patients’ fibroblasts. 2002;37:1237–45. Pratsinis H, Tsagarakis S, Zervolea I, Giannakopoulos F, Stathakos D, Thalassinos N, Kletsas D. Chronic in vivo exposure to glucocorticoids prolongs cellular lifespan: the case of Cushing’s syndrome-patients’ fibroblasts. 2002;37:1237–45.
40.
go back to reference Gagliano N, Grizzi F, Annoni G. Mechanisms of aging and liver functions. Dig Dis. 2007;25:118–23.PubMedCrossRef Gagliano N, Grizzi F, Annoni G. Mechanisms of aging and liver functions. Dig Dis. 2007;25:118–23.PubMedCrossRef
41.
go back to reference Velazquez MM, Alfaro NS, Dupuy CR, Salvetti NR, Rey F, Ortega HH. Heat shock protein patterns in the bovine ovary and relation with cystic ovarian disease. Anim Reprod Sci. 2010;118:201–9.PubMedCrossRef Velazquez MM, Alfaro NS, Dupuy CR, Salvetti NR, Rey F, Ortega HH. Heat shock protein patterns in the bovine ovary and relation with cystic ovarian disease. Anim Reprod Sci. 2010;118:201–9.PubMedCrossRef
42.
go back to reference Gola G, Reggiani L, Romanzi F, Beraudo ML. Principle data in the functional treatment of the antero-posterior and vertical dimensions of the arch. Parodontol Stomatol (Nuova). 1985;24:223–32. Gola G, Reggiani L, Romanzi F, Beraudo ML. Principle data in the functional treatment of the antero-posterior and vertical dimensions of the arch. Parodontol Stomatol (Nuova). 1985;24:223–32.
43.
go back to reference Liu Z, Youngquist RS, Garverick HA, Antoniou E. Molecular mechanisms regulating bovine ovarian follicular selection. Mol Reprod Dev. 2009;76:351–66.PubMedCrossRef Liu Z, Youngquist RS, Garverick HA, Antoniou E. Molecular mechanisms regulating bovine ovarian follicular selection. Mol Reprod Dev. 2009;76:351–66.PubMedCrossRef
44.
go back to reference Pan X, Zhao J, Zhang WN, Li HY, Mu R, Zhou T, et al. Induction of SOX4 by DNA damage is critical for p53 stabilization and function. Proc Natl Acad Sci U S A. 2009;106:3788–93.PubMedCentralPubMedCrossRef Pan X, Zhao J, Zhang WN, Li HY, Mu R, Zhou T, et al. Induction of SOX4 by DNA damage is critical for p53 stabilization and function. Proc Natl Acad Sci U S A. 2009;106:3788–93.PubMedCentralPubMedCrossRef
45.
go back to reference Qi M, Zhang J, Zeng W, Chen X. DNAJB1 stabilizes MDM2 and contributes to cancer cell proliferation in a p53-dependent manner. Biochim Biophys Acta. 1839;2014:62–9. Qi M, Zhang J, Zeng W, Chen X. DNAJB1 stabilizes MDM2 and contributes to cancer cell proliferation in a p53-dependent manner. Biochim Biophys Acta. 1839;2014:62–9.
46.
go back to reference Valente P, Fassina G, Melchiori A, Masiello L, Cilli M, Vacca A, et al. TIMP-2 over-expression reduces invasion and angiogenesis and protects B16F10 melanoma cells from apoptosis. Int J Cancer. 1998;19(75):246–53.CrossRef Valente P, Fassina G, Melchiori A, Masiello L, Cilli M, Vacca A, et al. TIMP-2 over-expression reduces invasion and angiogenesis and protects B16F10 melanoma cells from apoptosis. Int J Cancer. 1998;19(75):246–53.CrossRef
47.
go back to reference Stetler-Stevenson WG, Seo DW. TIMP-2: an endogenous inhibitor of angiogenesis. Trends Mol Med. 2005;11:97–103.PubMedCrossRef Stetler-Stevenson WG, Seo DW. TIMP-2: an endogenous inhibitor of angiogenesis. Trends Mol Med. 2005;11:97–103.PubMedCrossRef
48.
go back to reference Valeri C, Pappalardo S, De Felici M, Manna C. Correlation of oocyte morphometry parameters with woman’s age. J Assist Reprod Genet. 2011;28:545–52.PubMedCentralPubMedCrossRef Valeri C, Pappalardo S, De Felici M, Manna C. Correlation of oocyte morphometry parameters with woman’s age. J Assist Reprod Genet. 2011;28:545–52.PubMedCentralPubMedCrossRef
49.
go back to reference Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 1995;270:1491–4.PubMedCrossRef Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 1995;270:1491–4.PubMedCrossRef
50.
go back to reference Tschugguel W, Dietrich W, Zhegu Z, Stonek F, Kolbus A, Huber JC. Differential regulation of proteasome-dependent estrogen receptor alpha and beta turnover in cultured human uterine artery endothelial cells. J Clin Endocrinol Metab. 2003;88:2281–7.PubMedCrossRef Tschugguel W, Dietrich W, Zhegu Z, Stonek F, Kolbus A, Huber JC. Differential regulation of proteasome-dependent estrogen receptor alpha and beta turnover in cultured human uterine artery endothelial cells. J Clin Endocrinol Metab. 2003;88:2281–7.PubMedCrossRef
51.
go back to reference Pinzone JJ, Stevenson H, Strobl JS, Berg PE. Molecular and cellular determinants of estrogen receptor alpha expression. Mol Cell Biol. 2004;24:4605–12.PubMedCentralPubMedCrossRef Pinzone JJ, Stevenson H, Strobl JS, Berg PE. Molecular and cellular determinants of estrogen receptor alpha expression. Mol Cell Biol. 2004;24:4605–12.PubMedCentralPubMedCrossRef
52.
go back to reference Soltysik K, Czekaj P. Membrane estrogen receptors - is it an alternative way of estrogen action? J Physiol Pharmacol. 2013;64:129–42.PubMed Soltysik K, Czekaj P. Membrane estrogen receptors - is it an alternative way of estrogen action? J Physiol Pharmacol. 2013;64:129–42.PubMed
53.
go back to reference Yan J, Suzuki J, Yu X, Kan FW, Qiao J, Chian RC. Cryo-survival, fertilization and early embryonic development of vitrified oocytes derived from mice of different reproductive age. J Assist Reprod Genet. 2010;27:605–11.PubMedCentralPubMedCrossRef Yan J, Suzuki J, Yu X, Kan FW, Qiao J, Chian RC. Cryo-survival, fertilization and early embryonic development of vitrified oocytes derived from mice of different reproductive age. J Assist Reprod Genet. 2010;27:605–11.PubMedCentralPubMedCrossRef
Metadata
Title
Age-associated changes in bovine oocytes and granulosa cell complexes collected from early antral follicles
Authors
N. Itami
R. Kawahara-Miki
H. Kawana
M. Endo
T. Kuwayama
H. Iwata
Publication date
01-08-2014
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 8/2014
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-014-0251-y

Other articles of this Issue 8/2014

Journal of Assisted Reproduction and Genetics 8/2014 Go to the issue