Follicular size and stage and gonadotropin concentration affect alginate-encapsulated in vitro growth and survival of pre- and early antral dog follicles
Jennifer Nagashima A B , David E. Wildt A , Alexander J. Travis B C and Nucharin Songsasen A D
+ Author Affiliations
- Author Affiliations
A Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA 22630, USA.
B Baker Institute for Animal Health, Cornell University, Ithaca, NY 14583, USA.
C Atkinson Center for a Sustainable Future, Cornell University, Ithaca, NY 14583, USA.
D Corresponding author. Email: songsasenn@si.edu
Reproduction, Fertility and Development 29(2) 262-273 https://doi.org/10.1071/RD15004
Submitted: 5 January 2015 Accepted: 19 June 2015 Published: 3 August 2015
Abstract
Understanding stage-specific requirements of mammalian folliculogenesis is limited in the domestic dog. The present study examined the effects of two potential regulators of dog follicle growth and survival in vitro, namely the original stage of the follicle (i.e. preantral (≤230 µm diameter) vs early antral (diameter from >230 to ≤330 µm) and FSH and/or LH concentrations. After isolation and alginate encapsulation, follicles were cultured in 0, 1, 10 or 100 µg mL–1 FSH and 0, 1 or 10 ng mL–1 LH for 20 days. Regardless of stage, FSH promoted growth, but LH did the same only in the absence of FSH. Production of 17β-oestradiol and progesterone was detectable, indicating theca cell activity. The greatest growth occurred in preantral (mean (± s.d.) 61.4 ± 25.9%) versus antral (42.6 ± 20.3%) follicles, but neither developmental stage nor gonadotropin affected survival. Antrum detection was minimal due, in part, to antral collapse, and oocytes exhibited an increasingly pale appearance and chromatin degeneration over time. The results demonstrate that pre- and early antral stage dog follicles encapsulated in alginate grow significantly in vitro. However, because FSH and LH alone or in combination fail to promote antrum development, the next step is identifying factors that enhance antral expansion.
Additional keywords: folliculogenesis, FSH, LH, in vitro culture, steroidogenesis.
References
Abir, R., Franks, S., Mobberley, M. A., Moore, P. A., Margara, R. A., and Winston, R. M. L. (1997). Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil. Steril. 68, 682–688.| Mechanical isolation and in vitro growth of preantral and small antral human follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FgtVyiug%3D%3D&md5=fe7e837ec5821c554ef88972a867aaa4CAS | 9341611PubMed |
Adriaens, I., Cortvrindt, R., and Smitz, J. (2004). Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence. Hum. Reprod. 19, 398–408.
| Differential FSH exposure in preantral follicle culture has marked effects on folliculogenesis and oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXos1entQ%3D%3D&md5=0461d9ec2b5377c37d1c5afaf956e916CAS | 14747188PubMed |
Amorim, C. A., Van Langendonckt, A., David, A., Dolmans, M.-M., and Donnez, J. (2009). Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation, and in vitro culture in a calcium alginate matrix. Hum. Reprod. 24, 92–99.
| Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation, and in vitro culture in a calcium alginate matrix.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWjtbbI&md5=acde57c9efa527d5155f65978b7f8c86CAS | 18815120PubMed |
Anderson, A. C., and Simpson, M. E. (1973). ‘The Ovary and Reproductive Cycle of the Dog (Beagle).’ (Geron-X Inc.: Los Altos.)
Angelova, B., and Schmauder, H. P. (1999). Lipophilic compounds in biotechnology: interactions with cells and technological problems. J. Biotechnol. 67, 13–32.
| Lipophilic compounds in biotechnology: interactions with cells and technological problems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotFWitb0%3D&md5=b27b2e6b6bb3cb074b652e48344289a1CAS | 9987845PubMed |
Bolamba, D., Borden-Russ, K. D., and Durrant, B. S. (1998). In vitro maturation of domestic dog oocytes cultured in advanced preantral and early antral follicles. Theriogenology 49, 933–942.
| In vitro maturation of domestic dog oocytes cultured in advanced preantral and early antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1Kmsg%3D%3D&md5=d9a77930d4c06bdb8e8df982518580f1CAS | 10732101PubMed |
Bolamba, D., Russ, K. D., Olson, M. A., Sandler, J. L., and Durrant, B. S. (2002). In vitro maturation of bitch oocytes from advanced preantral follicles in synthetic oviduct fluid medium: serum is not essential. Theriogenology 58, 1689–1703.
| In vitro maturation of bitch oocytes from advanced preantral follicles in synthetic oviduct fluid medium: serum is not essential.Crossref | GoogleScholarGoogle Scholar | 12472139PubMed |
Bona Gallo, A., and Licht, P. (1979). Differences in the properties of FSH and LH binding sites in the avian gonad revealed by homologous radioligands. Gen. Comp. Endocrinol. 37, 521–532.
| Differences in the properties of FSH and LH binding sites in the avian gonad revealed by homologous radioligands.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M3hsVCgtg%3D%3D&md5=a05803b9591915b3d8a554b24eb93d2bCAS | 222647PubMed |
Campbell, B. K., Baird, D. T., and Webb, R. (1998). Effects of dose of LH on androgen production and luteinization of ovine theca cells cultured in a serum-free system. J. Reprod. Fertil. 112, 69–77.
| Effects of dose of LH on androgen production and luteinization of ovine theca cells cultured in a serum-free system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVKqtrc%3D&md5=59d662ab2b9f31afa8a65cf3f7777dccCAS | 9538331PubMed |
Concannon, P. W. (2009). Endocrinologic control of normal canine ovarian function. Reprod. Domest. Anim. 44, 3–15.
| Endocrinologic control of normal canine ovarian function.Crossref | GoogleScholarGoogle Scholar | 19754529PubMed |
Concannon, P. W. (2011). Reproductive cycles of the domestic bitch. Anim. Reprod. Sci. 124, 200–210.
| Reproductive cycles of the domestic bitch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvFWhtbs%3D&md5=fabaa1bd8146d25ce80ce247d1df8163CAS | 21055888PubMed |
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=623e970233a5154dbe4c4ce2224251cbCAS | 9647562PubMed |
De Liberto, T. J., Gese, E. M., Knowlton, F. F., Mason, J. R., Conover, M. R., Miller, L., Schmidt, R. H., and Holland, M. K. (1998). Fertility control in coyotes: is it a potential management tool? In ‘Proceedings of the 18th Vertebrate Pest Conference’, 2–5 March 1998, Costa Mesa. (Eds R. O. Baker and A. C. Crabb.) pp. 144–149. (Vertebrate Pest Council: Costa Mesa.)
Diez, D. (2013). Survival analysis in R. Available at: http://www.openintro.org/stat/down/Survival-Analysis-in-R.pdf [verified 1 June 2014].
Dolmans, M.-M., Michaux, N., Camboni, A., Martinez-Madrid, B., Van Langendonckt, A., Annarita Nottola, S., and Donnez, J. (2006). Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles. Hum. Reprod. 21, 413–420.
| Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmslymtg%3D%3D&md5=81661e1bbfbcce1efa22584269b59709CAS | 16199426PubMed |
Dufau, M. L., and Catt, K. J. (1979). Gonadotropin receptors and regulation of steroidogenesis in the testis and ovary. Vitam. Horm. 36, 462–592.
Eppig, J. J., and O’Brien, M. J. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54, 197–207.
| Development in vitro of mouse oocytes from primordial follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSisLjO&md5=f9f45ebc57f714300a2f7181e4eab4acCAS | 8838017PubMed |
Eppig, J. J., and Schroeder, A. C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol. Reprod. 41, 268–276.
| Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FivVGhsA%3D%3D&md5=82dae8737d983297c7553178dd9fe134CAS | 2508774PubMed |
Evans, H. M., and Cole, H. H. (1931). ‘An Introduction to the Study of the Oestrous Cycle in the Dog.’ (University of California Press: Berkeley, CA.)
Gordon, I. (1994). ‘Laboratory Production of Cattle Embryos.’ (CAB International: Wallingford, UK.)
Guraya, S. S. (1965). A histochemical analysis of lipid yolk deposition in the oocytes of cat and dog. J. Exp. Zool. 160, 123–135.
| A histochemical analysis of lipid yolk deposition in the oocytes of cat and dog.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF287jvFeitA%3D%3D&md5=2eb3bb48c52e3eebd6afdcecacc1960dCAS | 5894324PubMed |
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=0d28f8d287605e10fd36a48e314c8498CAS | 10775183PubMed |
Heise, M., Koepsel, R., Russel, A. J., and McGee, E. A. (2005). Calcium alginate microencapsulation of ovarian follicle impacts FSH delivery and follicle morphology. Reprod. Biol. Endocrinol. 3, 47.
| Calcium alginate microencapsulation of ovarian follicle impacts FSH delivery and follicle morphology.Crossref | GoogleScholarGoogle Scholar | 16162282PubMed |
Honda, A., Hirose, M., Hara, K., Matoba, S., Inoue, K., Miki, H., Hiura, H., Kanatsu-Shinohara, M., Kanai, Y., and Kono, T. (2007). Isolation, characterization, and in vitro and in vivo differentiation of putative thecal stem cells. Proc. Natl Acad. Sci. USA 104, 12 389–12 394.
| Isolation, characterization, and in vitro and in vivo differentiation of putative thecal stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1ehtrc%3D&md5=65adfdb2060789c7c3273ab689f4fa38CAS |
Hovatta, O., Wright, C., Krausz, T., Hardy, K., and Winston, R. M. L. (1999). Human primordial, primary, and secondary ovarian follicles in long-term culture: effect of partial isolation. Hum. Reprod. 14, 2519–2524.
| Human primordial, primary, and secondary ovarian follicles in long-term culture: effect of partial isolation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MvlvFentg%3D%3D&md5=dfa73b85a575c8aa04c5a0064086ae40CAS | 10527981PubMed |
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=e6a69478502e8a99f15b5e1d602a43b1CAS | 12297524PubMed |
Jin, S. Y., Lei, L., Shikanov, A., Shea, L. D., and Woodruff, T. K. (2010). A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil. Steril. 93, 2633–2639.
| A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse.Crossref | GoogleScholarGoogle Scholar | 20004373PubMed |
Kinis, A., Vergos, E., Gordon, I., Gordon, A., and Gallagher, M. (1990). Studies in the production of chimaeric cattle embryos by aggregation of blastomeres from embryos derived from oocytes matured and fertilized in vitro. Theriogenology 33, 268.
| Studies in the production of chimaeric cattle embryos by aggregation of blastomeres from embryos derived from oocytes matured and fertilized in vitro.Crossref | GoogleScholarGoogle Scholar |
Kooistra, H. S., Okkens, A. C., Bevers, M. M., Popp-Snijders, C., van Haaften, B., Dieleman, S. J., and Schoemaker, J. (1999). Concurrent pulsatile secretion of luteinizing hormone and follicle-stimulating hormone during different phases of the estrous cycle and anestrus in beagle bitches. Biol. Reprod. 60, 65–71.
| Concurrent pulsatile secretion of luteinizing hormone and follicle-stimulating hormone during different phases of the estrous cycle and anestrus in beagle bitches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFylsg%3D%3D&md5=38f082bee093f13e6a2cc2f6c5af41cbCAS | 9858487PubMed |
Kreeger, P. K., Fernandes, N. N., Woodruff, T. K., and Shea, L. D. (2005). Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol. Reprod. 73, 942–950.
| Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGktb%2FM&md5=81e925998ca9077f2c0baa57650aead0CAS | 15987824PubMed |
Kutzler, M. A. (2005). Induction and synchronization of estrus in dogs. Theriogenology 64, 766–775.
| Induction and synchronization of estrus in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1artLw%3D&md5=8987b0a5415542717016ee7c9a4f2774CAS | 15993937PubMed |
Licht, P., Muller, C. H., and Tsui, H. W. (1976). Effects of mammalian and nonmammalian gonadotropins on androgen production by minced rabbit testis. Biol. Reprod. 14, 194–201.
| Effects of mammalian and nonmammalian gonadotropins on androgen production by minced rabbit testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XkvVOksrg%3D&md5=477f20c112fea0fe07957a05c4df01dcCAS |
Licht, P., Gallo, A. B., Aggarwal, B. B., Farmer, S. W., Castelino, J. B., and Parkoff, H. (1979). Biological and binding activities of equine pituitary gonadotrophins and pregnant mare serum gonadotrophin. J. Endocrinol. 83, 311–322.
| Biological and binding activities of equine pituitary gonadotrophins and pregnant mare serum gonadotrophin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXht1aitrg%3D&md5=0c479d82050b918b368d8ef1d5aaf3f5CAS | 536667PubMed |
Maltaris, T., Kaya, H., Hoffmann, I., Mueller, A., Beckmann, M. W., and Dittrich, R. (2006). Comparison of xenografting in SCID mice and LIVE/DEAD assay as a predictor of the developmental potential of cryopreserved ovarian tissue. In Vivo 20, 11–16.
| 1:STN:280:DC%2BD28%2FksVeqsQ%3D%3D&md5=37395a28dd749b7989e6afc7f6598edfCAS | 16433022PubMed |
McLaughlin, M., and Telfer, E. E. (2010). Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two-step serum-free culture system. Reproduction 139, 971–978.
| Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two-step serum-free culture system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXns12qsLk%3D&md5=94e201b65c1989309d1b47fc1f83e7bcCAS | 20207724PubMed |
Monfort, S., Wasser, S., Mashburn, K., Burke, M., Brewer, B., and Creel, S. (1997). Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus). Zoo Biol. 16, 533–548.
| Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvFGhurw%3D&md5=cf371572317d7f8686fd2841573bd85eCAS |
Morley, P., Calaresu, F., Barbe, G., and Armstrong, D. (1989). Insulin enhances luteinizing hormone-stimulated steroidogenesis by porcine theca cells. Biol. Reprod. 40, 735–743.
| Insulin enhances luteinizing hormone-stimulated steroidogenesis by porcine theca cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXksFSrt7o%3D&md5=670f9d0b56ef783a6b90a7c1bf29b71cCAS | 2473786PubMed |
Mousset-Siméon, N., Jouannet, P., Le Cointre, L., Coussieu, C., and Poirot, C. (2005). Comparison of three in vitro culture systems for maturation of early preantral mouse ovarian follicles. Zygote 13, 167–175.
| Comparison of three in vitro culture systems for maturation of early preantral mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 16128412PubMed |
Moyle, W. R., Campbell, R. K., Myers, R. V., Bernard, M. P., Han, Y., and Wang, X. (1994). Co-evolution of ligand-receptor pairs. Nature 368, 251–255.
| Co-evolution of ligand-receptor pairs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVSjur8%3D&md5=623230b98cf3d3e85a7316de697b070cCAS | 8145825PubMed |
Olson, P. N., Bowen, R. A., Behrendt, M. D., Olson, J. D., and Nett, T. M. (1982). Concentration of reproductive hormones in canine serum throughout late anestrus, proestrus, and estrus. Biol. Reprod. 27, 1196–1206.
| Concentration of reproductive hormones in canine serum throughout late anestrus, proestrus, and estrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXivVahtw%3D%3D&md5=390a83e0b882c83bd46dbe34a29e3fdcCAS | 6819009PubMed |
Orisaka, M., Hattori, K., Fukuda, S., Mizutani, T., Miyamoto, K., Sato, T., Tsang, B. K., Kotsuji, F., and Yoshida, Y. (2013). Dysregulation of ovarian follicular development in female rat: LH decreases FSH sensitivity during preantral–early antral transition. Endocrinology 154, 2870–2880.
| Dysregulation of ovarian follicular development in female rat: LH decreases FSH sensitivity during preantral–early antral transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtF2nurfE&md5=6856951a2ba5922da9497e210619043dCAS | 23709086PubMed |
Parrott, J. A., and Skinner, M. K. (1998). Developmental and hormonal regulation of keratinocyte growth factor expression and action in the ovarian follicle 1. Endocrinology 139, 228–235.
| 1:CAS:528:DyaK1cXhtFKntA%3D%3D&md5=bb2070aad4d5f5c3aa847fed9765818eCAS | 9421419PubMed |
Picton, H. M., Harris, S. E., Muruvi, W., and Chambers, E. L. (2008). The in vitro growth and maturation of follicles. Reproduction 136, 703–715.
| The in vitro growth and maturation of follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1CktA%3D%3D&md5=3169c95f5e75bc1097a0ba5494e96129CAS | 19074213PubMed |
Rajkovic, A., Pangas, S. A., and Matzuk, M. M. (2006). Follicular development: mouse, sheep, and human models. In ‘Knobil and Neill’s Physiology of Reproduction’, Vol. 1, 3rd edn. (Ed. J. D. Neill.) pp. 383–424. (Academic Press: London.)
Rasmussen, L. E., Buss, I. O., Hess, D. L., and Schmidt, M. J. (1984). Testosterone and dihydrotestosterone concentrations in elephant serum and temporal gland secretions. Biol. Reprod. 30, 352–362.
| Testosterone and dihydrotestosterone concentrations in elephant serum and temporal gland secretions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhsFWhs70%3D&md5=6e6d06889d49a1449e5eaff6e0695cd3CAS | 6704470PubMed |
Reynaud, K., Fontbonne, A., Marseloo, N., Thoumire, S., Chebrout, M., de Lesegno, C. V., and Chastant-Maillard, S. (2005). In vivo meiotic resumption, fertilization, and early embryonic development in the bitch. Reproduction 130, 193–201.
| In vivo meiotic resumption, fertilization, and early embryonic development in the bitch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVSksbvI&md5=c53d5ab8bdcf0306a747b1c1b3a21f58CAS | 16049157PubMed |
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=26e0db2b267e371d92b707656299f124CAS |
Seal, U. S., Plotka, E. D., Packard, J. M., and Mech, L. D. (1979). Endocrine correlates of reproduction in the wolf. I. Serum progesterone, estradiol, and LH during the estrous cycle. Biol. Reprod. 21, 1057–1066.
| Endocrine correlates of reproduction in the wolf. I. Serum progesterone, estradiol, and LH during the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXntlKgsQ%3D%3D&md5=7133025e62dee0a1de72881a3172c6b0CAS | 574776PubMed |
Shikanov, A., Xu, M., Woodruff, T. K., and Shea, L. D. (2009). Interpenetrating fibrin–alginate matrices for in vitro ovarian follicle development. Biomaterials 30, 5476–5485.
| Interpenetrating fibrin–alginate matrices for in vitro ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvFCgtbk%3D&md5=a5733564469d46341335c01e392d36afCAS | 19616843PubMed |
Shikanov, A., Smith, R. M., Xu, M., Woodruff, T. K., and Shea, L. D. (2011). Hydrogel network design using multifunctional macromers to coordinate tissue maturation in ovarian follicle culture. Biomaterials 32, 2524–2531.
| Hydrogel network design using multifunctional macromers to coordinate tissue maturation in ovarian follicle culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Sqs7o%3D&md5=2ca5d2d1e72509d6a1031555483438d2CAS | 21247629PubMed |
Silva, C. M. G., Castro, S. V., Faustino, L. R., Rodrigues, G. Q., Brito, I. R., Saraiva, M. V. A., Rossetto, R., Silva, T. F. P., Campello, C. C., and Figueiredo, J. R. (2011). Moment of addition of LH to the culture medium improves in vitro survival and development of secondary goat pre-antral follicles. Reprod. Domest. Anim. 46, 579–584.
| Moment of addition of LH to the culture medium improves in vitro survival and development of secondary goat pre-antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2hsL7P&md5=c9689061b4b0686af95b24249ac9a4aaCAS |
Smitz, J., and Cortvrindt, R. (1999). Oocyte in vitro maturation and follicle culture: current clinical achievements and future directions. Hum. Reprod. 14, 145–161.
| Oocyte in vitro maturation and follicle culture: current clinical achievements and future directions.Crossref | GoogleScholarGoogle Scholar | 10573031PubMed |
Smitz, J., Dolmans, M. M., Donnez, J., Fortune, J. E., Hovatta, O., Jewgenow, K., Picton, H. M., Plancha, C., Shea, L. D., and Stouffer, R. L. (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=d950ad8c4759d349d3520a7b81b89668CAS | 20124287PubMed |
Songsasen, N., and Wildt, D. E. (2005). Size of the donor follicle, but not stage of reproductive cycle or seasonality, influences meiotic competency of selected domestic dog oocytes. Mol. Reprod. Dev. 72, 113–119.
| Size of the donor follicle, but not stage of reproductive cycle or seasonality, influences meiotic competency of selected domestic dog oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntlClsLo%3D&md5=44f4abc58b8e9d3e6de649076aea0fb9CAS | 15915515PubMed |
Songsasen, N., and Wildt, D. E. (2007). Oocyte biology and challenges in developing in vitro maturation systems in the domestic dog. Anim. Reprod. Sci. 98, 2–22.
| Oocyte biology and challenges in developing in vitro maturation systems in the domestic dog.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Slu7Y%3D&md5=ef12ddfab8ebea3c8942d886e77cedeaCAS | 17097840PubMed |
Songsasen, N., Fickes, A., Pukazhenthi, B. S., and Wildt, D. E. (2009). Follicular morphology, oocyte diameter, and localisation of fibroblast growth factors in the domestic dog ovary. Reprod. Domest. Anim. 44, 65–70.
| Follicular morphology, oocyte diameter, and localisation of fibroblast growth factors in the domestic dog ovary.Crossref | GoogleScholarGoogle Scholar | 19754538PubMed |
Songsasen, N., Woodruff, T. K., and Wildt, D. E. (2011). In vitro growth and steroidogenesis of dog follicles as influenced by the physical and hormonal microenvironment. Reproduction 142, 113–122.
| In vitro growth and steroidogenesis of dog follicles as influenced by the physical and hormonal microenvironment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFSqu7zI&md5=bbe86c9e4f44fc11e59d33aa37ab19c6CAS | 21502334PubMed |
Tani, H., Inaba, T., Tamada, H., Sawada, T., Mori, J., and Torii, R. (1996). Increasing gonadotropin-releasing hormone release by perifused hypothalamus from early to late anestrus in the beagle bitch. Neurosci. Lett. 207, 1–4.
| Increasing gonadotropin-releasing hormone release by perifused hypothalamus from early to late anestrus in the beagle bitch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVWntLo%3D&md5=eacff21b75dfe405d63ffea23b90536aCAS | 8710197PubMed |
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=9bf84c253156fe836d703ef8231cc87aCAS | 18326514PubMed |
Turathum, B., Saikhun, K., Sangsuwan, P., and Kitiyanant, Y. (2010). Effects of vitrification on nuclear maturation, ultrastructural changes, and gene expression of canine oocytes. Reprod. Biol. Endocrinol. 8, 70–78.
| Effects of vitrification on nuclear maturation, ultrastructural changes, and gene expression of canine oocytes.Crossref | GoogleScholarGoogle Scholar | 20565987PubMed |
Valdespino, C., Asa, C. S., and Bauman, J. E. (2002). Estrous cycles, copulation, and pregnancy in the fennec fox (Vulpes zerda). J. Mammal. 83, 99–109.
| Estrous cycles, copulation, and pregnancy in the fennec fox (Vulpes zerda).Crossref | GoogleScholarGoogle Scholar |
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=4ab5027607a77a44db0e365b49dbefdcCAS | 15763114PubMed |
West, E. R., Xu, M., Woodruff, T. K., and Shea, L. D. (2007). Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials 28, 4439–4448.
| Physical properties of alginate hydrogels and their effects on in vitro follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFSqtr4%3D&md5=7a7d691e703f203c3e8f5bb5efb65042CAS | 17643486PubMed |
Wildt, D. E., Levinson, C. J., and Seager, S. W. (1977). Laparoscopic exposure and sequential observation of the ovary of the cycling bitch. Anat. Rec. 189, 443–449.
| Laparoscopic exposure and sequential observation of the ovary of the cycling bitch.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c%2FjvVemsw%3D%3D&md5=2e7bf36a21d79921a4553790bfd96da2CAS | 144445PubMed |
Wildt, D. E., Panko, W. B., Chakraborty, P. K., and Seager, S. W. J. (1979). Relationship of serum estrone, estradiol-17β, and progesterone to LH, sexual behavior, and time of ovulation in the bitch. Biol. Reprod. 20, 648–658.
| Relationship of serum estrone, estradiol-17β, and progesterone to LH, sexual behavior, and time of ovulation in the bitch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktFOmtbg%3D&md5=1dcba96aba41344b45b3ef8958052dddCAS | 572240PubMed |
Wu, J., Nayudu, P. L., Kiesel, P. S., and Michelmann, H. W. (2000). Luteinizing hormone has a stage-limited effect on preantral follicle development in vitro. Biol. Reprod. 63, 320–327.
| Luteinizing hormone has a stage-limited effect on preantral follicle development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2rsbg%3D&md5=e92770c3ecb4da2948f09d13318179a3CAS | 10859274PubMed |
Xu, M., Kreeger, P., Shea, L. D., and Woodruff, T. K. (2006a). Tissue engineered follicles produce live fertile offspring. Tissue Eng. 12, 2739–2746.
| Tissue engineered follicles produce live fertile offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSht7fF&md5=9cd68bde5ac7c7a3618a577c10b34d04CAS | 17518643PubMed |
Xu, M., West, E., Shea, L. D., and Woodruff, T. K. (2006b). Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol. Reprod. 75, 916–923.
| Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yjtr7O&md5=afdffbe2f1d612e20af070dd437f1011CAS | 16957022PubMed |
Xu, M., Barrett, S. L., West-Farrell, E., Kondapalli, L. A., Kiesewetter, S. E., Shea, L. D., and Woodruff, T. K. (2009a). In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum. Reprod. 24, 2531–2540.
| In vitro grown human ovarian follicles from cancer patients support oocyte growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOqurnE&md5=bc4f763d864bafd71f008a0c9a93a30dCAS | 19597190PubMed |
Xu, M., West-Farrell, E. R., Stouffer, R. L., Shea, L. D., Woodruff, T. K., and Zelinski, M. B. (2009b). Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol. Reprod. 81, 587–594.
| Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChu7zL&md5=4ec29cddf24c70ab65caddde15eb5a43CAS | 19474063PubMed |
Xu, J., Bernuci, M. P., Lawson, M. S., Yeoman, R. R., Fisher, T. E., Zelinski, M. B., and Stouffer, R. L. (2010). 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 140, 685–697.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsbfK&md5=3484dd02cc429db57c571a9cde891ebdCAS | 20729335PubMed |
Young, J. M., and McNeilly, A. S. (2010). Theca: the forgotten cell of the ovarian follicle. Reproduction 140, 489–504.
| Theca: the forgotten cell of the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCqurrM&md5=cd85de3678adb1659d226efb0a7f7820CAS | 20628033PubMed |
