Effects of growth differentiation factor-9 and FSH on in vitro development, viability and mRNA expression in bovine preantral follicles
G. L. Vasconcelos A , M. V. A. Saraiva A , J. J. N. Costa A , M. J. Passos A , A. W. B. Silva A , R. O. D. S. Rossi A , A. M. L. R. Portela A , A. B. G. Duarte C , D. M. Magalhães-Padilha C , C. C. Campelo C , J. R. Figueiredo C , R. van den Hurk B and J. R. V. Silva A D
+ Author Affiliations
- Author Affiliations
A Biotechnology Nucleus of Sobral (NUBIS), Federal University of Ceara, CEP 62042-280, Sobral, CE, Brazil.
B Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, PO Box 80.163, Utrecht, The Netherlands.
C LAMOFOPA, Faculty of Veterinary Medicine, State University of Ceara, CEP 60740-000, Fortaleza, CE, Brazil.
D Corresponding author. Email: jrvsilva@ufc.br
Reproduction, Fertility and Development 25(8) 1194-1203 https://doi.org/10.1071/RD12173
Submitted: 30 May 2012 Accepted: 16 November 2012 Published: 17 December 2012
Abstract
The present study investigated the role of growth differentiation factor (GDF)-9 and FSH, alone or in combination, on the growth, viability and mRNA expression of FSH receptor, proliferating cell nuclear antigen (PCNA) and proteoglycan-related factors (i.e. hyaluronan synthase (HAS) 1, HAS2, versican, perlecan) in bovine secondary follicles before and after in vitro culture. After 12 days culture, sequential FSH (100 ng mL–1 from Days 0 to 6 and 500 ng mL–1 from Days 7 to 12) increased follicular diameter and resulted in increased antrum formation (P < 0.05). Alone, 200 ng mL–1 GDF-9 significantly reduced HAS1 mRNA levels, but increased versican and perlecan mRNA levels in whole follicles, which included the oocyte, theca and granulosa cells. Together, FSH and GDF-9 increased HAS2 and versican (VCAN) mRNA levels, but decreased PCNA mRNA expression, compared with levels in follicles cultured in α-minimum essential medium supplemented with 3.0 mg mL–1 bovine serum albumin, 10 µg mL–1 insulin, 5.5 µg mL–1 transferrin, 5 ng mL–1 selenium, 2 mM glutamine, 2 mM hypoxanthine and 50 μg mL–1 ascorbic acid (α-MEM+). Comparisons of uncultured (0.2 mm) and α-MEM+ cultured follicles revealed that HAS1 mRNA expression was higher, whereas VCAN expression was lower, in cultured follicles (P < 0.05). Expression of HAS1, VCAN and perlecan (HSPG2) was higher in cultured than in vivo-grown (0.3 mm) follicles. In conclusion, FSH and/or GDF-9 promote follicular growth and antrum formation. Moreover, GDF-9 stimulates expression of versican and perlecan and interacts positively with FSH to increase HAS2 expression.
Additional keyword: culture.
References
Aaltonen, J., Laitinen, M. P., Vuojolainen, K., Jaatinen, R., Horelli-Kuitunen, N., Seppa, L., Louhio, H., Tuuri, T., Sjoberg, J., Butzow, R., Hovata, O., Dale, L., and Ritvos, O. (1999). Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab. 84, 2744–2750.| Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltFCltro%3D&md5=196be2fd8f39c32150d8b3c879c07624CAS | 10443672PubMed |
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 |
Bellin, M. E., Lenz, R. W., Steadman, L. E., and Ax, R. L. (1983). Proteoglycan production by bovine granulosa cells in vitro occurs in response to FSH. Mol. Cell. Endocrinol. 29, 51–65.
| Proteoglycan production by bovine granulosa cells in vitro occurs in response to FSH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXotlyksg%3D%3D&md5=5e9c30beba8dcf102e3cffd7fbc374a1CAS | 6298031PubMed |
Cain, L. S., Chatterjee, A., and Collins, T. J. (1995). In vitro folliculogenesis of rat preantral follicles. Endocrinology 136, 3369–3377.
| In vitro folliculogenesis of rat preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntFKntrw%3D&md5=bc331d9ba6b6d74857aef69d1b746966CAS |
Cecconi, S., Barboni, B., Coccia, M., and Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594–601.
| In vitro development of sheep preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFekt7g%3D&md5=39074501a412181e6c07022b15ed8632CAS | 10026104PubMed |
Chaves, R. N., Martins, F. S., Saraiva, M. V., Celestino, J. J., Lopes, C. A., Correia, J. C., Verde, I. B., Matos, M. H., Báo, S. N., Name, K. P., Campello, C. C., Silva, J. R., 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 |
Chen, A. Q., Yu, S. D., Wang, Z. G., Xu, Z. R., and Yang, Z. G. (2009). Stage-specific expression of bone morphogenetic protein type I and type II receptor genes: effects of follicle-stimulating hormone on ovine antral follicles. Anim. Reprod. Sci. 111, 391–399.
| Stage-specific expression of bone morphogenetic protein type I and type II receptor genes: effects of follicle-stimulating hormone on ovine antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFKmtL8%3D&md5=f754ca7d869adabbf489bca8e88e8a56CAS | 18462895PubMed |
Clarke, H. G., Hope, S. A., Byers, S., and Rodgers, R. J. (2006). Formation of ovarian follicular fluid may be due to the osmotic potential of large glycosaminoglycans and proteoglycans. Reproduction 132, 119–131.
| Formation of ovarian follicular fluid may be due to the osmotic potential of large glycosaminoglycans and proteoglycans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1OgtrY%3D&md5=f5ec1f2c4ba7d2e5626e5c97f2d6fc67CAS | 16816338PubMed |
Cortvrindt, R., Hu, Y., and Smitz, J. (1998). Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone-supplemented mouse preantral follicle culture. Hum. Reprod. 13, 1292–1302.
| Recombinant luteinizing hormone as a survival and differentiation factor increases oocyte maturation in recombinant follicle stimulating hormone-supplemented mouse preantral follicle culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktF2htbs%3D&md5=2eaa5fabf3f9520877bd6e5f03dcdec1CAS | 9647562PubMed |
Demeestere, I., Simon, P., Englert, Y., and Delbaere, A. (2003). Preliminary experience of varian tissue cryopreservation procedure: alternatives, perspectives and feasibility. Reprod. Biomed. Online 7, 572–579.
| Preliminary experience of varian tissue cryopreservation procedure: alternatives, perspectives and feasibility.Crossref | GoogleScholarGoogle Scholar | 14680552PubMed |
Driancourt, M., Reynaud, K., Cortvrindt, R., and Smitz, J. (2000). Roles of kit and kit ligand in ovarian function. Rev. Reprod. 5, 143–152.
| Roles of kit and kit ligand in ovarian function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnt1altLc%3D&md5=26a756087f2b69c7b32575f26cd8c59aCAS | 11006164PubMed |
Eagle, H. (1955). Nutrition needs of mammalian cells in tissue culture. Science 122, 501–504.
| Nutrition needs of mammalian cells in tissue culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG28Xptlen&md5=f393ea00aeabb279b5e33e89b51e41bfCAS | 13255879PubMed |
El-Hefnawy, T., and Zeleznik, A. J. (2001). Synergism between FSH and activin in the regulation of proliferating cell nuclear antigen (PCNA) and cyclin D2 expression in rat granulosa cells. Endocrinology 142, 4357–4362.
| Synergism between FSH and activin in the regulation of proliferating cell nuclear antigen (PCNA) and cyclin D2 expression in rat granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1ertLo%3D&md5=7c5b68c6c9ab773a8eca990719101b50CAS | 11564698PubMed |
Eriksen, G. V., Carlstedt, I., Morgelin, M., Uldbjerg, N., and Malmstrom, A. (1999). Isolation and characterization of proteoglycans from human follicular fluid. Biochem. J. 340, 613–620.
| Isolation and characterization of proteoglycans from human follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVeisrc%3D&md5=39fb35c36ff76891212d59e447f02fa9CAS | 10359644PubMed |
Familiari, G., Nottola, S. A., and Motta, P. M. (1987). Focal cell contacts detected by ruthenium red, Triton X100 and saponin in the granulosa cells of mouse ovary. Tissue Cell 19, 207–215.
| Focal cell contacts detected by ruthenium red, Triton X100 and saponin in the granulosa cells of mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXkt1Whtbc%3D&md5=1e7e98f4561777d9637a17937f1c140fCAS | 2438807PubMed |
Fortune, J. E., Yang, M. Y., and Muruvi, W. (2011). In vitro and in vivo regulation of follicular formation and activation in cattle. Reprod. Fertil. Dev. 23, 15–22.
| In vitro and in vivo regulation of follicular formation and activation in cattle.Crossref | GoogleScholarGoogle Scholar | 21366976PubMed |
Grimek, H. J., and Ax, R. L. (1982). Chromatographic comparison of chondroitin-containing proteoglycan from small and large bovine ovarian follicles. Biochem. Biophys. Res. Commun. 104, 1401–1406.
| Chromatographic comparison of chondroitin-containing proteoglycan from small and large bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhsFOrsrw%3D&md5=c2e96724846e9e39f89a35ebb57b8365CAS | 6803803PubMed |
Grimek, H. J., Bellin, M. E., and Ax, R. L. (1984). Characteristics of proteoglycans isolated from small and large bovine ovarian follicles. Biol. Reprod. 30, 397–409.
| Characteristics of proteoglycans isolated from small and large bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhtlCls7o%3D&md5=325559a4f525c15bdc4d7db39422f61cCAS | 6423006PubMed |
Gulyas, B. J., Hodgen, G. D., Tullner, W. W., and Ross, G. T. (1977). Effects of fetal or maternal hypophysectomy on endocrine organs and body weight in infant rhesus monkeys (Macaca mulatta): with particular emphasis on oogenesis. Biol. Reprod. 16, 216–227.
| Effects of fetal or maternal hypophysectomy on endocrine organs and body weight in infant rhesus monkeys (Macaca mulatta): with particular emphasis on oogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s%2FovVWgtA%3D%3D&md5=f71f637aa71967bbd60e9aea18a07730CAS | 401655PubMed |
Gutierrez, C. G., Ralph, J. H., Telfer, E. E., Wilmut, I., and Webb, R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62, 1322–1328.
| Growth and antrum formation of bovine preantral follicles in long-term culture in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisl2htLc%3D&md5=be48e8f72566049622a9e135a94b16b4CAS | 10775183PubMed |
Haidari, K., Salehnia, M., and Valojerdi, M. R. (2008). The effect of leukemia inhibitory factor and co-culture on the in vitro maturation and ultrastructure of vitrified isolated mouse preantral follicles. Fertil. Steril. 90, 2389–2397.
| The effect of leukemia inhibitory factor and co-culture on the in vitro maturation and ultrastructure of vitrified isolated mouse preantral follicles.Crossref | GoogleScholarGoogle Scholar | 18462725PubMed |
Halpin, D. M., Jones, A., Fink, G., and Charlton, H. M. (1986). Postnatal ovarian follicle development in hypogonadal (HPG) and normal mice and associated changes in the hypothalamic–pituitary ovarian axis. J. Reprod. Fertil. 77, 287–296.
| Postnatal ovarian follicle development in hypogonadal (HPG) and normal mice and associated changes in the hypothalamic–pituitary ovarian axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltVyru7c%3D&md5=b786e078a7279b08f930d28fabfd795bCAS | 3088270PubMed |
Hartshorne, G. M. (1997). In vitro culture of ovarian follicles. Rev. Reprod. 2, 94–104.
| In vitro culture of ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktV2nur0%3D&md5=ea70eab9920f62fb8d16b95bcde1f710CAS | 9414471PubMed |
Hayashi, M., McGee, E. A., Min, G., Klein, C., Rose, U. M., Van Duin, M., and Hsueh, A. J. (1999). Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236–1244.
| Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFCjtb0%3D&md5=621b0b4a937a547ccf875c48d49d9b74CAS | 10067849PubMed |
Hillier, S. G. (1994). Current concepts the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Hum. Reprod. 9, 188–191.
| 1:CAS:528:DyaK2cXjtFGqsro%3D&md5=4362d99c7d210d7aef9d4c3a37e8c488CAS | 8027271PubMed |
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 |
Irving-Rodgers, H. F., Harland, M. L., and Rodgers, R. J. (2004). A novel basal lamina matrix of the stratified epithelium of the ovarian follicle. Matrix Biol. 23, 207–217.
| A novel basal lamina matrix of the stratified epithelium of the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVGntrk%3D&md5=2a861b194ef4ca41eb3403412acd6aeaCAS | 15296935PubMed |
Itoh, T., Kacchi, M., Abe, H., Sendai, Y., and Hoshi, H. (2002). Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol. Reprod. 67, 1099–1105.
| Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2rtr4%3D&md5=ed238d36a4d7605639e77a0616bbc1b4CAS | 12297524PubMed |
Juengel, J. L., Hudson, N. L., Heath, D. A., Smith, P., Reader, K. L., Lawrence, S. B., O’Connell, A. R., Laitinen, M. P. E., Cranfield, M., Groome, N. P., Ritvos, O., and McNatty, K. P. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 67, 1777–1789.
| Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptVelsLo%3D&md5=d9696cf5f298ac9fd577e903b601f93dCAS | 12444053PubMed |
Kedem, A., Fisch, B., Garor, R., Ben-Zaken, A., Gizunterman, T., Felz, C., Ben-Haroush, A., Kravarusic, D., and Abir, R. (2011). Growth differentiating factor 9 (GDF9) and bone morphogenetic protein 15 both activate development of human primordial follicles in vitro, with seemingly more beneficial effects of GDF9. J. Clin. Endocrinol. Metab. 96, E1246.
| Growth differentiating factor 9 (GDF9) and bone morphogenetic protein 15 both activate development of human primordial follicles in vitro, with seemingly more beneficial effects of GDF9.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKhsbzJ&md5=db02507bea0ffd86c9f363999fa30ff5CAS | 21632818PubMed |
Kishore, S., Luber, S., and Zavolan, M. (2010). Deciphering the role of RNA-binding proteins in the post-transcriptional control of gene expression. Brief. Funct. Genomics 9, 391–404.
| Deciphering the role of RNA-binding proteins in the post-transcriptional control of gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlemu70%3D&md5=4984c4f6913d8a575d187e6b727ae038CAS | 21127008PubMed |
Kresse, H., and Schonherr, E. (2001). Proteoglycans of the extracellular matrix and growth control. J. Cell. Physiol. 189, 266–274.
| Proteoglycans of the extracellular matrix and growth control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFGqsbk%3D&md5=71c0d3d329a26fd3a96674dca519cd33CAS | 11748584PubMed |
Krishna, T. S. R., Kong, X.-P., Gary, S., Burgers, P. M., and Kuriyan, J. (1994). Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79, 1233–1243.
| Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXivVajsr8%3D&md5=68787dc3d266a3a66672fdb768c5dbe9CAS |
LeBaron, R. G., Zimmermann, D. R., and Ruoslahti, E. (1992). Hyaluronate binding properties of versican. J. Biol. Chem. 267, 10 003–10 010.
| 1:CAS:528:DyaK38XktVejsL0%3D&md5=8afdb5c550f56bda380139bdbc37af00CAS |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the –2ΔΔCt method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the –2ΔΔCt method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c02316d2aa02af4c464251269a77c9c9CAS | 11846609PubMed |
Maga, G., and Hübscher, U. (2003). Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell Sci. 116, 3051–3060.
| Proliferating cell nuclear antigen (PCNA): a dancer with many partners.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmslKlsbY%3D&md5=0dc2b048581a5f10eb282379fc254615CAS | 12829735PubMed |
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 |
Mao, J., Wu, G., Smith, M. F., McCauley, T. C., Cantley, T. C., Prather, R. S., Didion, B. A., and Day, B. N. (2002). Effects of culture medium, serum type, and various concentrations of follicle-stimulating hormone on porcine preantral follicular development and antrum formation in vitro. Biol. Reprod. 67, 1197–1203.
| Effects of culture medium, serum type, and various concentrations of follicle-stimulating hormone on porcine preantral follicular development and antrum formation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2rt7w%3D&md5=139a2e801614587af155fa108f5e380dCAS | 12297536PubMed |
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., Maia, J. E., Silva, J. R. V., Celestino, J. J., 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 |
Mazerbourg, S., Klein, C., Roh, J., Kaivo-Oja, N., Mottershead, D. G., Korchynskyi, O., Ritvos, O., and Hsueh, A. J. (2004). Growth differentiation factor-9 (GDF-9) signalling is mediated by the type 1 receptor ALK5. Mol. Endocrinol. 18, 653–665.
| Growth differentiation factor-9 (GDF-9) signalling is mediated by the type 1 receptor ALK5.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivFCqtrs%3D&md5=a6bf9340177ca8c018ab2978276fff3eCAS | 14684852PubMed |
McArthur, M. E., Irving-Rodgers, H. F., Byers, S., and Rodgers, R. J. (2000). Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles. Biol. Reprod. 63, 913–924.
| Identification and immunolocalization of decorin, versican, perlecan, nidogen, and chondroitin sulfate proteoglycans in bovine small-antral ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFChsrk%3D&md5=30fd1f5a20997c1456799214c0e4c985CAS | 10952939PubMed |
McGee, E., Spears, N., Minami, S., Hsu, S. Y., Chun, S. Y., Billig, H., and Hsueh, A. J. W. (1997). Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3′-5′-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinology 138, 2417–2424.
| Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3′-5′-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsVeitLc%3D&md5=e738bc0e9375b5f5419e2d23e119770aCAS | 9165031PubMed |
Minj, A., Mondal, S., Tiwari, A. K., Sharma, B., and Varshney, V. P. (2008). Molecular characterization of follicle stimulating hormone receptor (FSHR) gene in the Indian river buffalo (Bubalus bubalis). Gen. Comp. Endocrinol. 158, 147–153.
| Molecular characterization of follicle stimulating hormone receptor (FSHR) gene in the Indian river buffalo (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVykur%2FK&md5=a0dee2f6c0e3ddbf5bb3879b6012cae2CAS | 18675816PubMed |
Miyake, Y., Sakurai, M., Tanaka, S., Tunjung, W. A. S., Yokoo, M., Matsumoto, H., Aso, H., Yamaguchi, T., and Sato, E. (2009). Expression of hyaluronan synthase 1 and distribution of hyaluronan during follicular atresia in pig ovaries. Biol. Reprod. 80, 249–257.
| Expression of hyaluronan synthase 1 and distribution of hyaluronan during follicular atresia in pig ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOitLo%3D&md5=697645cedd4c37a0c9871baa4c145a77CAS | 18923162PubMed |
Muskhelishvili, L., Wingard, S. K., and Latendresse, J. R. (2005). Proliferating cell nuclear antigen: a marker for ovarian follicle counts. Toxicol. Pathol. 33, 365–368.
| Proliferating cell nuclear antigen: a marker for ovarian follicle counts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvVyhu74%3D&md5=918d538524f1ccb2a7d655fc5f92da38CAS | 15805074PubMed |
Oktay, K., Schenken, R. S., and Nelson, J. F. (1995). Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biol. Reprod. 53, 295–301.
| Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntVSmur8%3D&md5=f59cf6b48c50f18190064dfebe58106dCAS | 7492681PubMed |
Orisaka, M., Orisaka, S. J., Jiang, J.-Y., Craig, J., Wang, Y., Kotsuji, F., and Tsang, B. K. (2006). Growth differentiation factor-9 is anti-apoptotic during follicular development from preantral to early antral stage. Mol. Endocrinol. 20, 2456–2468.
| Growth differentiation factor-9 is anti-apoptotic during follicular development from preantral to early antral stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOht7jK&md5=b366f58de31aa8aae982e17360f034a4CAS | 16740654PubMed |
Pennetier, S., Uzbekova, S., Perreau, C., Papillier, P., Mermillod, P., and Dalbies-Tran, R. (2004). Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos. Biol. Reprod. 71, 1359–1366.
| Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGquro%3D&md5=41cbbfeb8404e4c372120cac9d5346c8CAS | 15189828PubMed |
Princivalle, M., Hasan, S., Hosseini, G., and Agostini, A. I. (2001). Anticoagulant heparan sulfate proteoglycans expression in the rat ovary peaks in preovulatory granulosa cells. Glycobiology 11, 183–194.
| Anticoagulant heparan sulfate proteoglycans expression in the rat ovary peaks in preovulatory granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslWhu7s%3D&md5=d8e7fdc8fddaf751a21153a1126d38f2CAS | 11320057PubMed |
Rodgers, R. J., and Irving-Rodgers, H. F. (2010). Formation of the ovarian follicular antrum and follicular fluid. Biol. Reprod. 82, 1021–1029.
| Formation of the ovarian follicular antrum and follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgtrs%3D&md5=2cf7ec0b2dcc4be067cbf037e16e5db9CAS | 20164441PubMed |
Russell, D. L., Ochsner, S. A., Hsieh, M., Mulders, S., and Richards, J. S. (2003). Hormoneregulated expression and localization of versican in the rodent ovary. Endocrinology 144, 1020–1031.
| Hormoneregulated expression and localization of versican in the rodent ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslCqtr0%3D&md5=c38477480de72a279300244e0f3883d5CAS | 12586779PubMed |
Saraiva, M. V. A., Celestino, J. J. H., Chaves, R. N., Martins, F. S., Bruno, J. B., Lima-Verde, I. B., Matos, M. H. T., Silva, G. M., Porfirio, E. P., Báo, S. N., Campello, C. C., Silva, J. R. V., and Figueiredo, J. R. (2008). Influence of different concentrations of LH and FSH on in vitro caprine primordial ovarian follicle development. Small Rumin. Res. 78, 87–95.
| Influence of different concentrations of LH and FSH on in vitro caprine primordial ovarian follicle development.Crossref | GoogleScholarGoogle Scholar |
Saraiva, M. V. A., Celestino, J. J. H., Araújo, V. R., Chaves, R. N., Almeida, A. P., Lima-Verde, I. B., Duarte, A. B. G., Silva, G. M., Martins, F. S., Bruno, J. B., Matos, M. H. T., Campello, C. C., Silva, J. R. V., and Figueiredo, J. R. (2011). Expression of follicle-stimulating hormone receptor (FSHR) in goat ovarian follicles and the impact of sequential culture medium on in vitro development of caprine preantral follicles. Zygote 19, 205–214.
| Expression of follicle-stimulating hormone receptor (FSHR) in goat ovarian follicles and the impact of sequential culture medium on in vitro development of caprine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1amsbo%3D&md5=811371d0069c329c02d3fe2731970341CAS |
Sharma, G. T., Dubey, P. K., and Kumar, G. S. (2011). Localization and expression of follicle-stimulating hormone receptor gene in buffalo (Bubalus bubalis) pre-antral follicles. Reprod. Domest. Anim. 46, 114–120.
| Localization and expression of follicle-stimulating hormone receptor gene in buffalo (Bubalus bubalis) pre-antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisF2gtL8%3D&md5=2ce76caea87bea26353f007e95a8813dCAS | 20403128PubMed |
Sher, I., Zisman-Rozen, S., Eliahu, L., Whitelock, J. M., Maas-Szabowski, N., Yamada, Y., Breitkreutz, D., Fusenig, N. E., Arikawa-Hirasawa, E., Iozzo, R. V., Bergman, R., and Ron, D. (2006). Targeting perlecan in human keratinocytes reveals novel roles for perlecan in epidermal formation. J. Biol. Chem. 281, 5178–5187.
| Targeting perlecan in human keratinocytes reveals novel roles for perlecan in epidermal formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhs1ektL8%3D&md5=83fdfcb8e9fa42bf7c89edd15d9a094dCAS | 16269412PubMed |
Silva, J. R. V., van den Hurk, R., Matos, M. H. T., Santos, R. R., Pessoa, C., Moraes, M. O., and Figueiredo, J. R. (2004). Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology 61, 1691–1704.
| Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslWnu7o%3D&md5=67f8846ab6ba93cedc3b25387c715c39CAS |
Silva, J. R. V., Van den Hurk, R., Van Tol, H. T. A., Roelen, B. A. J., and Figueiredo, J. R. (2005). Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), 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 (BMP15), and BMP receptors in the ovaries of goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOitrzO&md5=d764250099938b73a9d0897344c49c7aCAS |
Skinner, M. K. (2005). Regulation of primordial follicle assembly and development. Hum. Reprod. Update 11, 461–471.
| Regulation of primordial follicle assembly and development.Crossref | GoogleScholarGoogle Scholar | 16006439PubMed |
Smitz, J., Dolmans, M. M., Donnez, J., Fortune, J. E., Hovatta, O., Jewgenow, K., Picton, H. M., Plancha, C., Shea, L. D., Stouffer, R. L., Telfer, E. E., Woodruff, T. K., and Zelinski, M. B. (2010). Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum. Reprod. Update 16, 395–414.
| Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvhtlymtQ%3D%3D&md5=779e7126b28e463c6172e7fcb59f2840CAS | 20124287PubMed |
Spears, N., Murray, A. A., Alisson, V., Boland, N. I., and Gosden, R. G. (1998). Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro. J. Reprod. Fertil. 113, 19–26.
| Role of gonadotrophins and ovarian steroids in the development of mouse follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsVSgtLc%3D&md5=75fd36d4f0d16a5162fbd62189988c2cCAS | 9713372PubMed |
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 |
Spicer, L. J., Aad, P. Y., Allen, D. T., Mazerbourg, S., Payne, A. H., and Hsueh, A. J. (2008). Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: Influence of follicle size on responses to GDF9. Biol. Reprod. 78, 243–253.
| Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: Influence of follicle size on responses to GDF9.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Kru7o%3D&md5=ce8dd0b4ea96cbf7625e4bbf5672e6dbCAS | 17959852PubMed |
ten Dijk, P., Miyazono, K., and Heldin, C. H. (2000). Signaling inputs converge on nuclear effectors in TGF-β signaling. Trends Biochem. Sci. 25, 64–70.
| Signaling inputs converge on nuclear effectors in TGF-β signaling.Crossref | GoogleScholarGoogle Scholar |
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 |
van den Hurk, R., and Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–1751.
| Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitF2js70%3D&md5=a97e34d35b6a1c1c9671bba598cb1583CAS | 15763114PubMed |
Vitt, U. A., Hayashi, M., Klein, C., and Hsueh, A. J. (2000). Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol. Reprod. 62, 370–377.
| Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVOqsA%3D%3D&md5=c5ffee1734ceae3d84f77f507a6f58bfCAS | 10642575PubMed |
Vitt, U. A., Mazerbourg, S., Klein, C., and Hsueh, A. J. W. (2002). Bone morphogenetic rotein receptor type II is a receptor for growth differentiation factor-9. Biol. Reprod. 67, 473–480.
| Bone morphogenetic rotein receptor type II is a receptor for growth differentiation factor-9.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsFKqt7o%3D&md5=f7c15a6451795728dff2f64b66245049CAS | 12135884PubMed |
Wandji, S. A., Pelletier, G., and Sirard, M. A. (1992). Ontogeny and cellular localization of 125I-labeled basic fibroblast growth factor and 125I-labeled epidermal growth factor binding sites in ovaries from bovine fetuses and neonatal calves. Biol. Reprod. 47, 807–813.
| Ontogeny and cellular localization of 125I-labeled basic fibroblast growth factor and 125I-labeled epidermal growth factor binding sites in ovaries from bovine fetuses and neonatal calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xmt1Ojtbo%3D&md5=d883155c0d251e1be78c4c5765cfcb55CAS | 1477206PubMed |
Wandji, S. A., Srsen, V., Voss, A. K., Eppig, J. J., and Fortune, J. E. (1996). Initiation in vitro of growth of bovine primordial follicles. Biol. Reprod. 55, 942–948.
| Initiation in vitro of growth of bovine primordial follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmtlamsr4%3D&md5=9e29959bc975967fa606373c1cd84a8fCAS | 8902203PubMed |
Wandji, S. A., Srsen, V., Nathanielsz, P. W., Eppig, J. J., and Fortune, J. E. (1997). Initiation of growth of baboon primordial follicles in vitro. Hum. Reprod. 12, 1993–2001.
| Initiation of growth of baboon primordial follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FivVenuw%3D%3D&md5=8b3560160e3b20c0cff6b7d6d2b664d7CAS | 9363719PubMed |
Wight, T. N. (2002). Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr. Opin. Cell Biol. 14, 617–623.
| Versican: a versatile extracellular matrix proteoglycan in cell biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVCrtbk%3D&md5=830a13abf9a79bbed85ced95a9b31661CAS | 12231358PubMed |
Wu, X., and Brewer, G. (2012). The regulation of mRNA stability in mammalian cells: 2.0. Gene 500, 10–21.
| The regulation of mRNA stability in mammalian cells: 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltF2jsbw%3D&md5=d5f75345f87e261bebd1d233647b376fCAS | 22452843PubMed |
Xu, Z., Garverick, H. A., Smith, G. W., Smith, M. F., Hamilton, S. A., and Youngquist, R. S. (1995). Expression of folliclestimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave. Biol. Reprod. 53, 951–957.
| Expression of folliclestimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFyisrk%3D&md5=2a5c231777cbc4adff6e298e40908b59CAS | 8547492PubMed |
Zhao, J., Taverne, M. A. M., van der Weijden, G. C., Bevers, M. M., and van den Hurk, R. (2001). Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II. Biol. Reprod. 65, 967–977.
| Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFemsbs%3D&md5=353792f8f091e25103dbe06cab49cbd3CAS | 11514365PubMed |
Zhou, H., and Zhang, Y. (2005). Regulation of in vitro growth of preantral follicles by growth factors in goats. Domest. Anim. Endocrinol. 28, 235–242.
| Regulation of in vitro growth of preantral follicles by growth factors in goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitFeqtrk%3D&md5=78f57e81e8ec3318802a4b10fbb24155CAS | 15760665PubMed |
