Dynamic medium containing growth differentiation factor-9 and FSH maintains survival and promotes in vitro growth of caprine preantral follicles after long-term in vitro culture
A. M. C. V. Alves A E , R. N. Chaves A , R. M. P. Rocha A , L. F. Lima A , P. M. Andrade A , C. A. P. Lopes A , C. E. A. Souza B , A. A. A. Moura B , C. C. Campello A , S. N. Báo C , J. Smitz D and J. R. Figueiredo A
+ Author Affiliations
- Author Affiliations
A Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary Medicine, State University of Ceará, Av. Paranjana 1700, Campus Itaperi, 60740-903, Fortaleza, CE, Brazil.
B Department of Animal Science, Federal University of Ceará, Av. Mister Hull S/N, Campus Pici, 60021-970, Fortaleza, CE, Brazil.
C Departament of Cell Biology, University of Brasília, Campus Universitário Darcy Ribeiro (Asa Norte), 70919-970, Brasília, DF, Brazil.
D Follicle Biology Laboratory, Vrije Universiteit Brussel, Laarbeeklaan 101, 1090 Brussels, Belgium.
E Corresponding author. Email: anelise_alves@yahoo.com.br
Reproduction, Fertility and Development 25(6) 955-965 https://doi.org/10.1071/RD12180
Submitted: 8 June 2012 Accepted: 27 August 2012 Published: 11 October 2012
Abstract
The aim of the present study was to evaluate the effects of growth differentiation factor 9 (GDF-9) and FSH on the in vitro development of caprine preantral follicles cultured for 16 days. Ovarian fragments were cultured in αMEM+ (α-minimum essential medium, pH 7.2–7.4, 10 μg mL–1 insulin, 5.5 μg mL–1 transferrin, 5.0 ng mL–1 selenium, 2 mM glutamine, 2 mM hypoxanthine and 1.25 mg mL–1 bovine serum albumin) in the absence or presence of 200 ng mL–1 GDF-9 and/or 50 ng mL–1 FSH added during the first (Days 0–8) and/or second (Days 8–16) half of the culture period. Non-cultured and cultured fragments were processed for histological and ultrastructural analyses. After 16 days, all treatments using GDF-9 or FSH showed higher rates of follicular survival compared with αMEM+ alone. Compared with non-cultured control, sequential culture media containing GDF-9 and/or FSH significantly increased the percentage of developing follicles and follicle diameter. Moreover, a progressive increase in oocyte diameter was observed only with sequential culture medium containing GDF-9 until Day 8 followed by FSH (GDF-9/FSH) in the second half of the culture period. After 16 days of culture, ultrastructural analysis confirmed the integrity of follicles cultured in the presence of GDF-9/FSH. In conclusion, a dynamic medium containing GDF-9 and FSH (GDF-9/FSH) maintained follicular integrity and promoted activation of primordial follicles and growth during long-term in vitro culture of goat preantral follicles.
Additional keywords : folliculogenesis, goat, hormone, ovary.
References
Amsterdam, A., Hanoch, T., Dantes, A., Tajima, K., Strauss, J. F., and Seger, R. (2002). Mechanisms of gonadotropin desensitization. Mol. Cell. Endocrinol. 187, 69–74.| Mechanisms of gonadotropin desensitization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Sqsb8%3D&md5=e7b89d51b921c37945bdfeeae5a93dd9CAS | 11988313PubMed |
Arunakumari, G., Shanmugasundaram, N., and Rao, V. H. (2010). Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–894.
| Development of morulae from the oocytes of cultured sheep preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjosVSktA%3D%3D&md5=8add359fe5f008fdac31b5deee4aba6cCAS | 20615540PubMed |
Bodensteiner, K. J., Clay, C. M., Moeller, C. L., and Sawyer, H. R. (1999). Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod. 60, 381–386.
| Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotlygsQ%3D%3D&md5=b6ae150384695781ca94dd78b9aadabeCAS | 9916005PubMed |
Chaves, R. N., Martins, F. S., Saraiva, M. V. A., Celestino, J. J. H., Lopes, C. A. P., Correia, J. C., Lima-Verde, I. B., Matos, M. H. T., Báo, S. N., Name, K. P. O., Campello, C. C., Silva, J. R. V., and Figueiredo, J. R. (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro. Reprod. Fertil. Dev. 20, 640–647.
| Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvgvVelsg%3D%3D&md5=80448c9626d40161d6dfc5367d6ce466CAS | 18577361PubMed |
Colonna, R., and Mangia, F. (1983). Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes. Biol. Reprod. 28, 797–803.
| Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXitFegtr0%3D&md5=f60c39a79a452fe2b4629d3715815f1bCAS | 6860738PubMed |
Cortvrindt, R., Smitz, J., and Van Steirteghem, A. C. (1997). Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Hum. Reprod. 12, 759–768.
| Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsF2ntLk%3D&md5=26e68b57fe77f6d010bac08f8c7ea1e2CAS | 9159439PubMed |
Crouch, M. F., Frew, I. J., Simson, L., and Davy, D. A. (1997). Competition by second messenger systems for receptor interaction and activation, implications for tissue-specific responses and disease therapy. Clin. Exp. Pharmacol. Physiol. 24, 632–638.
| Competition by second messenger systems for receptor interaction and activation, implications for tissue-specific responses and disease therapy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtVOrtro%3D&md5=14322694cf3beccc02ec82086ce97191CAS | 9269540PubMed |
Dong, J., Albertini, D. F., Nishimori, K., Kumar, T. R., Lu, N., and Matzuk, M. M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531–535.
| Growth differentiation factor-9 is required during early ovarian folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1GrsL0%3D&md5=fadb112b6c30b8f27931348d2fcd7812CAS | 8849725PubMed |
Eckery, D. C., Whale, L. J., Lawrence, S. B., Wylde, K. A., Mcnatty, K. P., and Juengel, J. L. (2002). Expression of mRNA encoding growth differentiation factor 9 and bone morphogenetic protein 15 during follicular formation and growth in a marsupial, the brushtail possum (Trichosurus vulpecula). Mol. Cell. Endocrinol. 192, 115–126.
| Expression of mRNA encoding growth differentiation factor 9 and bone morphogenetic protein 15 during follicular formation and growth in a marsupial, the brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslGrtLY%3D&md5=296759fcdee78dd49c15291b033e0c57CAS | 12088873PubMed |
Figueiredo, J. R., Rodrigues, A. P. R., Amorim, C. A., and Silva, J. R. V. (2008). Manipulação de oócitos inclusos em folículos ovarianos pré-antrais: MOIFOPA. In ‘Biotécnicas aplicadas à reprodução animal’. (Eds P. B. D. Gonçalves, J. R. Figueiredo and V. J. F. Freitas.) pp. 303–327. (Livraria Roca: São Paulo.)
Gutierrez, C. G., Campbell, B. K., and 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, 608–616.
| Development of a long-term bovine granulosa cell culture system: induction and maintenance of estradiol production, response to follicle-stimulating hormone, and morphological characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1Cqtb4%3D&md5=18107afa6ff8bf4136c5a0791619efa5CAS | 9047004PubMed |
Hillier, S. G. (2001). Gonadotropic control of ovarian follicular growth and development. Mol. Cell. Endocrinol. 179, 39–46.
| Gonadotropic control of ovarian follicular growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVylsLY%3D&md5=4a6ed68fa2d0e331dbc435551f2a6240CAS | 11420129PubMed |
Hosoe, M., Kaneyama, K., Ushizawa, K., Hayashi, K., and Takahashi, T. (2011). Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod. Biol. Endocrinol. 9, 33.
| Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvFCjtLo%3D&md5=d4745d8d9d1f7656e497e19051512520CAS | 21401961PubMed |
Hreinsson, J. G., Scott, J. E., Rasmussen, C., Swahn, M. L., Hsueh, A. J., and Hovatta, O. (2002). Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J. Clin. Endocrinol. Metab. 87, 316–321.
| Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVyksg%3D%3D&md5=09b5177958813ac8adf0a7db81111cb8CAS | 11788667PubMed |
Jayawardana, B. C., Shimizu, T., Nishimoto, H., Kaneko, E., Tetsuka, M., and Miyamoto, A. (2006). Hormonal regulation of expression of growth differentiation factor-9 receptor type I and II genes in the bovine ovarian follicle. Reproduction 131, 545–553.
| Hormonal regulation of expression of growth differentiation factor-9 receptor type I and II genes in the bovine ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs12jsLg%3D&md5=14e0bb26aeaea9214cda4611c267996cCAS | 16514197PubMed |
Joyce, I. M., Pendola, F. L., Wigglesworth, K., and Eppig, J. J. (1999). Oocyte regulation of kit ligand expression in mouse ovarian follicles. Dev. Biol. 214, 342–353.
| Oocyte regulation of kit ligand expression in mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXms1CrtLk%3D&md5=13f512aa2320324b1dd77078fb385cd6CAS | 10525339PubMed |
Kandiel, M. M., Watanabe, G., and Taya, K. (2010). Ovarian expression of inhibin-subunits, 3β-hydroxysteroid dehydrogenase, and cytochrome P450 aromatase during the estrous cycle and pregnancy of shiba goats (Capra hircus). Exp. Anim. 59, 605–614.
| Ovarian expression of inhibin-subunits, 3β-hydroxysteroid dehydrogenase, and cytochrome P450 aromatase during the estrous cycle and pregnancy of shiba goats (Capra hircus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCntr3N&md5=10595b152c6e1f404d2ac1b827b00f83CAS | 21030788PubMed |
Kayampilly, P. P., and Menon, K. M. (2009). Follicle-stimulating hormone inhibits adenosine 5′-monophosphate-activated protein kinase activation and promotes cell proliferation of primary granulosa cells in culture through an Akt-dependent pathway. Endocrinology 150, 929–935.
| Follicle-stimulating hormone inhibits adenosine 5′-monophosphate-activated protein kinase activation and promotes cell proliferation of primary granulosa cells in culture through an Akt-dependent pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Sgtrw%3D&md5=fbcda869fa0997756650ce37ba9b02beCAS | 18927218PubMed |
Kobayashi, N., Orisaka, M., Cao, M., Kotsuji, F., Leader, A., Sakuragi, N., and Tsang, B. K. (2009). Growth differentiation factor-9 mediates follicle-stimulating hormone-thyroid hormone interaction in the regulation of rat preantral follicular development. Endocrinology 150, 5566–5574.
| Growth differentiation factor-9 mediates follicle-stimulating hormone-thyroid hormone interaction in the regulation of rat preantral follicular development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGqtbrL&md5=519b657566c9f341f60e8d70daf6844bCAS | 19833718PubMed |
Magalhães, D. M., Araújo, V. R., Lima-Verde, I. B., Matos, M. H. T., Silva, R. C., Lucci, C. M., Báo, S. N., Campello, C. C., and Figueiredo, J. R. (2009). Different follicle-stimulating hormone (FSH) sources influence caprine preantral follicle viability and development in vitro. Braz. J. Vet. Res. Anim. Sci. 46, 378–386.
Magalhães, D. M., Duarte, A. B. G., Araújo, V. R., Brito, I. R., Soares, T. G., Lima, I. M. T., Lopes, C. A. P., Campello, C. C., Rodrigues, A. P. R., and Figueiredo, J. R. (2011). In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–188.
| In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone.Crossref | GoogleScholarGoogle Scholar | 20875671PubMed |
Martins, F. S., Celestino, J. J. H., Saraiva, M. V. A., Matos, M. H. T., Bruno, J. B., Rocha- Junior, C. M. C., Lima-Verde, I. B., Lucci, C. M., Báo, S. N., and Figueiredo, J. R (2008). Growth and differentiation factor-9 stimulates activation of goat primordial follicles in vitro and their progression to secondary follicles. Reprod. Fertil. Dev. 20, 916–924.
| Growth and differentiation factor-9 stimulates activation of goat primordial follicles in vitro and their progression to secondary follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Oks77L&md5=574bd9850b2ac20a271d4e5d99eb1615CAS | 19007556PubMed |
Matos, M. H. T., Lima-Verde, I. B., Luque, M. C. A., Maia, J. E., Silva, J. R. V., Celestino, J. J. H., Martins, F. S., Báo, S. N., Lucci, C. M., and Figueiredo, J. R. (2007). Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote 15, 173–182.
| Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVWqtb0%3D&md5=5a912f30f7b021cf5581064b6a1d6bb9CAS |
Méduri, G., Charnaux, N., Driancourt, M. A., Combettes, L., Granet, P., Vannier, B., Loosfelt, H., and Milgrom, E. (2002). Follicle-stimulating hormone receptors in oocytes? J. Clin. Endocrinol. Metab. 87, 2266–2276.
| Follicle-stimulating hormone receptors in oocytes?Crossref | GoogleScholarGoogle Scholar | 11994374PubMed |
Nonowaki, S., Takahashi, K., and Horiuchi, T. (2010). Culture media affect follicle survival and oocyte maturation in preantral mouse follicle cultures. J. Mammal. Ova Res. 27, 35–41.
| Culture media affect follicle survival and oocyte maturation in preantral mouse follicle cultures.Crossref | GoogleScholarGoogle Scholar |
Nottola, S. A., Cecconi, S., Bianchi, S., Motta, C., Rossi, G., Continenza, M. A., and Macchiarelli, G. (2011). Ultrastructure of isolated mouse ovarian follicles cultured in vitro. Reprod. Biol. Endocrinol. 9, 1–13.
| Ultrastructure of isolated mouse ovarian follicles cultured in vitro.Crossref | GoogleScholarGoogle Scholar |
Orisaka, M., Orisaka, S., Jiang, J. Y., Craig, J., Wang, Y., Kotsuji, F., and Tsang, B. K. (2006). Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage. Mol. Endocrinol. 20, 2456–2468.
| Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOht7jK&md5=b366f58de31aa8aae982e17360f034a4CAS | 16740654PubMed |
Ota, T., Choi, K., Gilks, C. B., Leung, P. C. K., and Auersperg, N. (2006). Cell type- and stage-specific changes in HOXA7 protein expression in human ovarian folliculogenesis, possible role of GDF-9. Differentiation 74, 1–10.
| Cell type- and stage-specific changes in HOXA7 protein expression in human ovarian folliculogenesis, possible role of GDF-9.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVeks74%3D&md5=4ad17ea97a22ff4b3a0356f93edb1ff1CAS | 16466395PubMed |
Peng, X., Yang, M., Wang, L., Tong, C., and Guo, Z. (2010). In vitro culture of sheep lamb ovarian cortical tissue in a sequential culture medium. J. Assist. Reprod. Genet. 27, 247–257.
| In vitro culture of sheep lamb ovarian cortical tissue in a sequential culture medium.Crossref | GoogleScholarGoogle Scholar | 20393796PubMed |
Rossetto, R., Lima-Verde, I. B., Matos, M. H. T., Saraiva, M. V. A., Martins, F. S., Faustino, L. R., Araújo, V. R., Silva, C. M. G., Name, K. P. O., Báo, S. N., Campello, C. C., Figueiredo, J. R., and Blume, H. (2009). Interaction between ascorbic acid and follicle-stimulating hormone maintains follicular viability after long-term in vitro culture of caprine preantral follicles. Domest. Anim. Endocrinol. 37, 112–123.
| Interaction between ascorbic acid and follicle-stimulating hormone maintains follicular viability after long-term in vitro culture of caprine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnvValu7c%3D&md5=1ef8aa756255f1c7aa99a1c24d01c79eCAS | 19493642PubMed |
Saraiva, M. V. A., Rossetto, R., Brito, I. R., Celestino, J. J. H., Silva, C. M. G., Faustino, L. R., Almeida, A. P., Bruno, J. B., Magalhães, D. M., Matos, M. H. T., Campello, C. C., and Figueiredo, J. R. (2010). Dynamic medium produces caprine embryo from preantral follicles grown in vitro. Reprod. Sci. 17, 1135–1143.
| Dynamic medium produces caprine embryo from preantral follicles grown in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1akt77F&md5=363db319fd4e968a0bf9600ffd4b2a15CAS |
Sasseville, M., Ritter, L. J., Nguyen, T. M., Liu, F., Mottershead, D. G., Russell, D. L., and Gilchrist, R. B. (2010). Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulosa and cumulus cells. J. Cell Sci. 123, 3166–3176.
| Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulosa and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGls73I&md5=16baa54662b5574d0dab1c83048f3970CAS | 20736313PubMed |
Silva, J. R. V., Van Den Hurk, R., Van Tol, H. T., Roelen, B. A., and Figueiredo, J. R. (2005). Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP-15), and BMP receptors in the ovaries of goats. Mol. Reprod. Dev. 70, 11–19.
| Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP-15), and BMP receptors in the ovaries of goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOitrzO&md5=d764250099938b73a9d0897344c49c7aCAS |
Spicer, L. J., Aad, P. Y., Allen, D., Mazerbourg, S., and Hsueh, A. J. (2006). Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells. J. Endocrinol. 189, 329–339.
| Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVyqtbs%3D&md5=134f179fbda29543d734836f8f75cc3fCAS | 16648300PubMed |
Telfer, E. E., McLaughlin, M., Ding, C., and Thong, K. J. (2008). A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum. Reprod. 23, 1151–1158.
| A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1ags7o%3D&md5=2fab09c7ce9553497845e389be7ac4bdCAS | 18326514PubMed |
Thomas, F. H., Ethier, J. F., Shimasaki, S., and Vanderhyden, B. C. (2005). Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. Endocrinology 146, 941–949.
| Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXotlWnuw%3D%3D&md5=4d9094ab6dc16fd5664bc7df2c86eb97CAS | 15539559PubMed |
Ting, A. Y., Yeoman, R. R., Lawson, M. S., and Zelinski, M. B. (2011). In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum. Reprod. 26, 2461–2472.
| In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification.Crossref | GoogleScholarGoogle Scholar | 21705370PubMed |
Vitt, U. A., Mcgee, E. A., Hayashi, M., and Hsueh, A. J. W. (2000). In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141, 3814–3820.
| In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvVGmtr8%3D&md5=f3fff9788d1cc7a91a4127a84b9da6e6CAS | 11014238PubMed |
Wang, J., and Roy, S. K. (2004). Growth differentiation factor-9 and stem cell factor promote primordial follicle formation in the hamster, modulation by follicle-stimulating hormone. Biol. Reprod. 70, 577–585.
| Growth differentiation factor-9 and stem cell factor promote primordial follicle formation in the hamster, modulation by follicle-stimulating hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Chsrc%3D&md5=5f72c862b0ee42a1e30a9ac29999bbbcCAS | 14585807PubMed |
Wang, X. L., Wu, Y., Tan, L. B., Tian, Z., Liu, J. H., Zhu, D. S., and Zeng, S. M. (2012). Follicle-stimulating hormone regulates pro-apoptotic protein bcl-2-interacting mediator of cell death-extra long (BimEL) induced porcine granulosa cell apoptosis. J. Biol. Chem. 287, 10 166–10 177.
| Follicle-stimulating hormone regulates pro-apoptotic protein bcl-2-interacting mediator of cell death-extra long (BimEL) induced porcine granulosa cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktlKrsr4%3D&md5=ea31c258a39b73515381e704e0a7f178CAS |
