Insulin promotes preantral follicle growth and antrum formation through temporal expression of genes regulating steroidogenesis and water transport in the cat
Chommanart Thongkittidilok A C E , Ram Pratap Singh A D , Pierre Comizzoli B , David Wildt A and Nucharin Songsasen A
+ Author Affiliations
- Author Affiliations
A Center for Species Survival, Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA 22630, USA.
B Center for Species Survival, Smithsonian Conservation Biology Institute, National Zoological Park, 3001 Connecticut Avenue, NW, Washington, DC 20008, USA.
C Division of Infectious Diseases, University of Colorado, Anschutz Medical Campus, 12700 East 19th Avenue, Mail Stop B-168, Aurora, CO 80045, USA.
D Salim Ali Centre for Ornithology and Natural History, Anaikatty, Coimbatore, 641108, India.
E Corresponding author. Email: chommanart.thongkittidilok@ucdenver.edu
Reproduction, Fertility and Development 30(10) 1369-1379 https://doi.org/10.1071/RD17454
Submitted: 28 October 2017 Accepted: 27 March 2018 Published: 3 May 2018
Abstract
The aims of the present study were to determine the effects of insulin, in vitro, on: (1) the viability and growth of domestic cat ovarian follicles; (2) mRNA expression of genes regulating steroidogenesis (cytochrome P450 family 17 subfamily, A polypeptide 1 (Cyp17a1), cytochrome P450 family 19 subfamily, A polypeptide 1 (Cyp19a1) and steroidogenic acute regulatory protein (Star)) and water transport (aquaporins (AQPs) Aqp1, Aqp3, Aqp7, Aqp9); and (3) steroid production (17β-oestradiol (E2), progesterone (P4), androstenedione (A4)). Cat secondary follicles were isolated from ovarian cortices and cultured in 0 (Control), 1 or 10 µg mL−1 insulin for 14 days (Day 0 = culture onset). Follicle and oocyte viability (based on neutral red staining), diameter and antrum formation were assessed every 72 h and at the end of incubation (Day 14). Expression of steroidogenic and water transport genes was evaluated on Days 0, 6 and 12, and E2, P4 and A4 concentrations in the culture medium were determined on Day 12. By Day 14, 1 and 10 µg mL−1 insulin had significantly promoted (P < 0.05) both antrum formation in a mean (± s.e.m.) 26.9 ± 9.0% and 78.0 ± 10.0% of follicles respectively, and follicle growth (diameter 151.4 ± 4.5 and 169.9 ± 10.5 µm respectively) compared with Control (antrum formation in 3.3 ± 3.3% of follicles and follicle diameter 129.1 ± 6.6 µm). High insulin (10 µg mL−1) treatment increased follicle viability compared with Control (86.0 ± 9.8% vs 38.1 ± 10.9% respectively; P < 0.05). However, insulin had no beneficial effect (P > 0.05) on oocyte diameter. Cyp17a1 expression on Days 6 and 12 was higher (P < 0.05) in follicles cultured in the low (1 µg mL−1) compared with high (10 µg mL−1) insulin treatment, with no significant difference between low or high insulin vs Control groups. Star expression was higher (P < 0.01) in the low insulin compared with Control group on Day 6, but Star was undetectable in the high insulin group by Day 12. Compared with high insulin, low insulin increased (P < 0.05) Aqp1 expression on Day 6, but there were no significant differences between these two groups on Day 12. In contrast, high insulin decreased (P < 0.05) Aqp9 transcript levels compared with Control. Only P4 production was affected by insulin, with P4 concentrations in the medium being higher (P < 0.05) in the low compared with high insulin and Control groups. In summary, the findings indicate that insulin promotes cat ovarian follicle growth and survival in vitro, including enhanced antrum formation, with the likely mechanism involving temporal expression of Cyp17a1, Star and Aqp9 genes.
Additional keywords: cat, follicle, gene expression, insulin, in vitro culture.
References
Asai, M., Higuchi, S., Kubota, M., Iguchi, K., Usui, S., and Hirano, K. (2006). Regulators for blood glucose level affect gene expression of aquaporin 3. Biol. Pharm. Bull. 29, 991–996.| Regulators for blood glucose level affect gene expression of aquaporin 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1ehtLg%3D&md5=a65e83f29289725a1844474bb3dafaa9CAS |
Avruch, J. (1998). Insulin signal transduction through protein kinase cascades. Mol. Cell. Biochem. 182, 31–48.
| Insulin signal transduction through protein kinase cascades.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtlOnsrk%3D&md5=f22806ccd840cbb3782122fb90aedd36CAS |
Barrett, S. L., and Woodruff, T. K. (2010). Gamete preservation. Cancer Treat. Res. 156, 25–39.
| Gamete preservation.Crossref | GoogleScholarGoogle Scholar |
Bouvier, D., Rouzaire, M., Marceau, G., Prat, C., Pereira, B., Lemarié, R., Deruelle, P., Fajardy, I., Gallot, D., Blanchon, L., Vambergue, A., and Sapin, V. (2015). Aquaporins and fetal membranes from diabetic parturient women: expression abnormalities and regulation by insulin. J. Clin. Endocrinol. Metab. 100, E1270–E1279.
| Aquaporins and fetal membranes from diabetic parturient women: expression abnormalities and regulation by insulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xjt1Ggt70%3D&md5=58fc81981c2bbcd0f49f25954caada8dCAS |
Camacho, P., Fan, H., Liu, Z., and He, J. (2016). Small mammalian animal model of heart disease. Am. J. Cardiovasc. Dis. 6, 70–80.
| 1:CAS:528:DC%2BC1cXotlyqsLc%3D&md5=7675b35248eb2373ecfc8412296a2aeaCAS |
Castro Parodi, M., Farina, M., Dietrich, V., Abán, C., Szpilbarg, N., Zotta, E., and Damiano, A. E. (2011). Evidence for insulin-mediated control of AQP9 expression in human placenta. Placenta 32, 1050–1056.
| Evidence for insulin-mediated control of AQP9 expression in human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFGjt7nO&md5=a34684f9c4ae3241bc9ffc1913e50646CAS |
Chaves, R. N., Alves, A., Faustino, L., Oliveira, K., Campello, C., Lopes, C., Báo, S., and Figueiredo, J. (2011). How the concentration of insulin affects the development of preantral follicles in goats. Cell Tissue Res. 346, 451–456.
| How the concentration of insulin affects the development of preantral follicles in goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1OqsL3P&md5=37c361cd5b0e5b028db2b34fbaba167aCAS |
Chaves, R. N., Duarte, A. B., Rodrigues, G. Q., Celestino, J. J., Silva, G. M., Lopes, C. A., Almeida, A. P., Donato, M. A., Peixoto, C. A., Moura, A. A., Lobo, C. H., Locatelli, Y., Mermillod, P., Campello, C. C., and Figueiredo, J. R. (2012). The effects of insulin and follicle-simulating hormone (FSH) during in vitro development of ovarian goat preantral follicles and the relative mRNA expression for insulin and FSH receptors and cytochrome P450 aromatase in cultured follicles. Biol. Reprod. 87, 1–11.
| The effects of insulin and follicle-simulating hormone (FSH) during in vitro development of ovarian goat preantral follicles and the relative mRNA expression for insulin and FSH receptors and cytochrome P450 aromatase in cultured follicles.Crossref | GoogleScholarGoogle Scholar |
Comizzoli, P., Crosier, A. E., Songsasen, N., Gunther, M. S., Howard, J. G., and Wildt, D. E. (2009). Advances in reproductive science for wild carnivore conservation. Reprod. Domest. Anim. 44, 47–52.
| Advances in reproductive science for wild carnivore conservation.Crossref | GoogleScholarGoogle Scholar |
Das, D., and Arur, S. (2017). Conserved insulin signaling in the regulation of oocyte growth, development, and maturation. Mol. Reprod. Dev. 84, 444–459.
| Conserved insulin signaling in the regulation of oocyte growth, development, and maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXmsVWgtL4%3D&md5=7f136515e271105ff43929e7319d2682CAS |
Dipaz-Berrocal, D. J., Nar, S., Guerreiro, D. D., Celestino, J. J. H., Leiva-Revilla, J., Alves, B. G., Alves, K. A., Santos, R. R., Rodrigues, A. P. R., and Figueiredo, J. R. (2017). Refining insulin concentration in culture medium containing growth factors BMP15 and GDF9: an in vitro study of the effects on follicle development in goats. Anim. Reprod. Sci. 185, 118–127.
| Refining insulin concentration in culture medium containing growth factors BMP15 and GDF9: an in vitro study of the effects on follicle development in goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhsVeis7fM&md5=33f9586c6878ccffd64143e94ea32386CAS |
Duleba, A. J., Spaczynski, R. Z., Olive, D. L., and Behrman, H. R. (1997). Effects of insulin and insulin-like growth factors on proliferation of rat ovarian theca-interstitial cells. Biol. Reprod. 56, 891–897.
| Effects of insulin and insulin-like growth factors on proliferation of rat ovarian theca-interstitial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitFGrtLs%3D&md5=90c2fd9cd6e2183856cbe2b2edc508f3CAS |
Edashige, K., Sakamoto, M., and Kasai, M. (2000). Expression of mRNAs of the aquaporin family in mouse oocytes and embryos. Cryobiology 40, 171–175.
| Expression of mRNAs of the aquaporin family in mouse oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVSks7s%3D&md5=eb124ed24cc5d31f3e5a5974d84df55fCAS |
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=93ec4ea78281b33bb27f0b4c2ee38b88CAS |
Ferreira, A.C.A., Maside, C., Sá, N., Guerreiro, D., Correia, H., Leiva-Revilla, J., Lobo, C., Araújo, V., Apgar, G., and Brandão, F. (2016). Balance of insulin and FSH concentrations improves the in vitro development of isolated goat preantral follicles in medium containing GH. Anim. Reprod. Sci. 165, 1–10.
| Balance of insulin and FSH concentrations improves the in vitro development of isolated goat preantral follicles in medium containing GH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitFSnt7bK&md5=b0a55c99a634fbfa96e5e3e1efb3b0b0CAS |
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 |
Fujihara, M., Comizzoli, P., Wildt, D. E., and Songsasen, N. (2012). Cat and dog primordial follicles enclosed in ovarian cortex sustain viability after in vitro culture on agarose gel in a protein-free medium. Reprod. Domest. Anim. 47, 102–108.
| Cat and dog primordial follicles enclosed in ovarian cortex sustain viability after in vitro culture on agarose gel in a protein-free medium.Crossref | GoogleScholarGoogle Scholar |
Fujihara, M., Comizzoli, P., Keefer, C. L., Wildt, D. E., and Songsasen, N. (2014). Epidermal growth factor (EGF) sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary. Biol. Reprod. 90, 86.
| Epidermal growth factor (EGF) sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary.Crossref | GoogleScholarGoogle Scholar |
Gupta, P. S. P., Ramesh, H. S., Manjunatha, B. M., Nandi, S., and Ravindra, J. P. (2008). Production of buffalo embryos using oocytes from in vitro grown preantral follicles. Zygote 16, 57–63.
| Production of buffalo embryos using oocytes from in vitro grown preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGmt74%3D&md5=dd0b345a126436118c9bcfa6b7d4ce71CAS |
Higuchi, S., Kubota, M., Iguchi, K., Usui, S., Kiho, T., and Hirano, K. (2007). Transcriptional regulation of aquaporin 3 by insulin. J. Cell. Biochem. 102, 1051–1058.
| Transcriptional regulation of aquaporin 3 by insulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSisLrF&md5=79ad74db61958525a2bc6b3b20b71f1bCAS |
Hovatta, O. (2004). Cryopreservation and culture of human ovarian cortical tissue containing early follicles. Eur. J. Obstet. Gynecol. Reprod. Biol. 113, S50–S54.
| Cryopreservation and culture of human ovarian cortical tissue containing early follicles.Crossref | GoogleScholarGoogle Scholar |
Hua, Y., Jiang, W., Zhang, W., Shen, Q., Chen, M., and Zhu, X. (2013). Expression and significance of aquaporins during pregnancy. Front. Biosci. 18, 1373–1383.
| Expression and significance of aquaporins during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFWqtr7I&md5=d88d89f8ba7b987d563887c466c9e56dCAS |
Huang, H. F., He, R. H., Sun, C. C., Zhang, Y., Meng, Q. X., and Ma, Y. Y. (2006). Function of aquaporins in female and male reproductive systems. Hum. Reprod. Update 12, 785–795.
| Function of aquaporins in female and male reproductive systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeisbzL&md5=0ccbc7cd178e0c24c3a2fb06ad92925eCAS |
Hunter, M. G., Robinson, R., Mann, G., and Webb, R. (2004). Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim. Reprod. Sci. 82–83, 461–477.
| Endocrine and paracrine control of follicular development and ovulation rate in farm species.Crossref | GoogleScholarGoogle Scholar |
Jewgenow, K., and Göritz, F. (1995). The recovery of preantral follicles from ovaries of domestic cats and their characterisation before and after culture. Anim. Reprod. Sci. 39, 285–297.
| The recovery of preantral follicles from ovaries of domestic cats and their characterisation before and after culture.Crossref | GoogleScholarGoogle Scholar |
Kezele, P. R., Nilsson, E. E., and Skinner, M. K. (2002). Insulin but not insulin-like growth factor- 1 promotes the primordial to primary follicle transition. Mol. Cell. Endocrinol. 192, 37–43.
| Insulin but not insulin-like growth factor- 1 promotes the primordial to primary follicle transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslGrtL4%3D&md5=dbab7a25d3ae2bdfa9c1ac99a9a53966CAS |
Knight, P. G., and Glister, C. (2003). Local roles of TGF-β superfamily members in the control of ovarian follicle development. Anim. Reprod. Sci. 78, 165–183.
| Local roles of TGF-β superfamily members in the control of ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gtr4%3D&md5=b3a1f9167b45463331f0ebd01865d432CAS |
Lee, H. J., Jee, B. C., Kim, S. K., Kim, H., Lee, J. R., Suh, C. S., and Kim, S. H. (2016). Expressions of aquaporin family in human luteinized granulosa cells and their correlations with IVF outcomes. Hum. Reprod. 31, 822–831.
| Expressions of aquaporin family in human luteinized granulosa cells and their correlations with IVF outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC1cXis1Cltr4%3D&md5=b8e1032906300ab22a61df59baf0a2fcCAS |
Li, X., Ben-Dov, I. Z., Mauro, M., and Williams, Z. (2015). Lowering the quantification limit of the Qubit TM RNA HS Assay using RNA spike-in. BMC Mol. Biol. 16, 9.
| Lowering the quantification limit of the Qubit TM RNA HS Assay using RNA spike-in.Crossref | GoogleScholarGoogle Scholar |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=a80b5e0841c49e736a3564bfe77a7aa6CAS |
Louchami, K., Best, L., Brown, P., Virreira, M., Hupkens, E., Perret, J., Devuyst, O., Uchida, S., Delporte, C., and Malaisse, W. J. (2012). A new role for aquaporin 7 in insulin secretion. Cell. Physiol. Biochem. 29, 65–74.
| A new role for aquaporin 7 in insulin secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xltl2murg%3D&md5=f7ca6743eb102829a229e9f5bf0a9fc5CAS |
Louhio, H., Hovatta, O., Sjöberg, J., and Tuuri, T. (2000). The effects of insulin, and insulin-like growth factors I and II on human ovarian follicles in long-term culture. Mol. Hum. Reprod. 6, 694–698.
| The effects of insulin, and insulin-like growth factors I and II on human ovarian follicles in long-term culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVCitL4%3D&md5=70834175a9a9a1d789a3432a7abc0c89CAS |
Luz, V. B., Araujo, V. R., Duarte, A. B., Celestino, J. J., Silva, T. F., Magalhaes-Padilha, D. M., Chaves, R. N., Brito, I. R., Almeida, A. P., Campello, C. C., Feltrin, C., Bertolini, M., Santos, R. R., and Figueiredo, J. R. (2012). Eight-cell parthenotes originated from in vitro grown sheep preantral follicles. Reprod. Sci. 19, 1219–1225.
| Eight-cell parthenotes originated from in vitro grown sheep preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslWju7bP&md5=9f8fe7c6a43df417c12e313ff3043685CAS |
Magalhães, D. M., Duarte, A. B., Araujo, V. R., Brito, I. R., Soares, T. G., Lima, I. M., Lopes, C. A., Campello, C. C., Rodrigues, A. P., 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 |
May, J. V., McCarty, K., Reichert, L. E., and Schomberg, D. W. (1980). Follicle-stimulating hormone-mediated induction of functional luteinizing hormone/human chorionic gonadotropin receptors during monolayer culture of porcine granulosa cells. Endocrinology 107, 1041–1049.
| Follicle-stimulating hormone-mediated induction of functional luteinizing hormone/human chorionic gonadotropin receptors during monolayer culture of porcine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlvFyitbk%3D&md5=ce0caf1843b42b89d57a0c9e9aa0669aCAS |
McConnell, N. A., Yunus, R. S., Gross, S. A., Bost, K. L., Clemens, M. G., Francis, M., and Hughes, J. (2002). Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology 143, 2905–2912.
| Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Sgtrs%3D&md5=fbae1c46621937102d77eb8f6a90a20aCAS |
McLaughlin, E. A., and McIver, S. C. (2009). Awakening the oocyte: controlling primordial follicle development. Reproduction 137, 1–11.
| Awakening the oocyte: controlling primordial follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKgsL4%3D&md5=045e08a48f894ff3b2552ebe4bc2628fCAS |
Miller, W. L., Geller, D. H., and Rosen, M. (2006). Ovarian and adrenal androgen biosynthesis and metabolism. In ‘Androgen Excess Disorders in Women’. (Eds R. Azziz, J. E. Nestler and D. Dewailly.) pp. 19–33. (Springer: Totowa, NJ.)
Moulavi, F., Hosseini, S. M., Tanhaie-Vash, N., Ostadhosseini, S., Hosseini, S. H., Hajinasrollah, M., Asghari, M. H., Gourabi, H., Shahverdi, A., Vosough, A. D., and Nasr-Esfahani, M. H. (2017). Interspecies somatic cell nuclear transfer in Asiatic cheetah using nuclei derived from post-mortem frozen tissue in absence of cryo-protectant and in vitro matured domestic cat oocytes. Theriogenology 1, 197–203.
| Interspecies somatic cell nuclear transfer in Asiatic cheetah using nuclei derived from post-mortem frozen tissue in absence of cryo-protectant and in vitro matured domestic cat oocytes.Crossref | GoogleScholarGoogle Scholar |
Narfström, K., Deckman, K. H., and Menotti-Raymond, M. (2013). Cats: a gold mine for opthalmology. Annu. Rev. Anim. Biosci. 1, 157–177.
| Cats: a gold mine for opthalmology.Crossref | GoogleScholarGoogle Scholar |
Pelican, K. M., Wildt, D. E., and Howard, J. G. (2006). GnRH agonist Lupron (R) (leuprolide acetate) pre-treatments prevent ovulation in response to gonadotropin stimulation in the clouded leopard (Neofelis nebulosa). Theriogenology 66, 1768–1777.
| GnRH agonist Lupron (R) (leuprolide acetate) pre-treatments prevent ovulation in response to gonadotropin stimulation in the clouded leopard (Neofelis nebulosa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1Oiu74%3D&md5=82f6cf0c62377d1769c96a068170978bCAS |
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=31ad340e46d632244f9aaadfc81bdee1CAS |
Quesnel, H. (1999). Localization of binding sites for IGF-I, insulin and GH in the sow ovary. J. Endocrinol. 163, 363–372.
| Localization of binding sites for IGF-I, insulin and GH in the sow ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12it70%3D&md5=0cdb259a4e6e7ff7590918e2f7394309CAS |
Repetto, G., del Peso, A., and Zurita, J. L. (2008). Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat. Protoc. 3, 1125–1131.
| Neutral red uptake assay for the estimation of cell viability/cytotoxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotFakurk%3D&md5=19a95e230b9a2ec7d590e610c90c2295CAS |
Reynaud, K., Gicquel, C., Thoumire, S., Chebrout, M., Ficheux, C., Bestandji, M., and Chastant‐Maillard, S. (2009). Folliculogenesis and morphometry of oocyte and follicle growth in the feline ovary. Reprod. Domest. Anim. 44, 174–179.
| Folliculogenesis and morphometry of oocyte and follicle growth in the feline ovary.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3jsVOquw%3D%3D&md5=f1b6d404b818164edc1fa183ea9d90e5CAS |
Rossetto, R., Saraiva, M., Bernuci, M., Silva, G., Brito, I., Alves, A., Magalhães-Padilha, D., Báo, S., Campello, C., and Rodrigues, A. (2016). Impact of insulin concentration and mode of FSH addition on the in vitro survival and development of isolated bovine preantral follicles. Theriogenology 86, 1137–1145.
| Impact of insulin concentration and mode of FSH addition on the in vitro survival and development of isolated bovine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnsVWltbs%3D&md5=743e3377c2c2cc89ce07ef76c4662743CAS |
Sales, A. D., Duarte, A., Rodrigues, G., Lima, L., Silva, G., Carvalho, A., Brito, I., da Maranguape, R., Lobo, C., and Aragão, J. (2015). Steady-state level of messenger RNA and immunolocalization of aquaporins 3, 7, and 9 during in vitro growth of ovine preantral follicles. Theriogenology 84, 1–10.
| Steady-state level of messenger RNA and immunolocalization of aquaporins 3, 7, and 9 during in vitro growth of ovine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXmsFSmsLg%3D&md5=5e96899e96d29edf69b6020a360b25e0CAS |
Selvaraju, S., Agarwal, S., Karche, S., and Majumdar, A. (2003). Ovarian response, embryo production and hormonal profile in superovulated goats treated with insulin. Theriogenology 59, 1459–1468.
| Ovarian response, embryo production and hormonal profile in superovulated goats treated with insulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1Wksg%3D%3D&md5=3f11485a6a5206b79518ba913388f65bCAS |
Serafim, M. K., Silva, G. M., Duarte, A. B., Araújo, V., Silva, T., Lima, A., Chaves, R., Campello, C., Silva, L., and Figueiredo, J. (2013). High insulin concentrations promote the in vitro growth and viability of canine preantral follicles. Reprod. Fertil. Dev. 25, 927–934.
| High insulin concentrations promote the in vitro growth and viability of canine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSrtr3E&md5=0d39de709e863cb0d3b259ea511959d1CAS |
Shimizu, T., Murayama, C., Sudo, N., Kawashima, C., Tetsuka, M., and Miyamoto, A. (2008). Involvement of insulin and growth hormone (GH) during follicular development in the bovine ovary. Anim. Reprod. Sci. 106, 143–152.
| Involvement of insulin and growth hormone (GH) during follicular development in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktlCqsbk%3D&md5=a3f03bb797c14f17e32f9ec9ad70701dCAS |
Silva, J. M., and Price, C. (2002). Insulin and IGF-I are necessary for FSH-induced cytochrome P450 aromatase but not cytochrome P450 side-chain cleavage gene expression in oestrogenic bovine granulosa cells in vitro. J. Endocrinol. 174, 499–507.
| Insulin and IGF-I are necessary for FSH-induced cytochrome P450 aromatase but not cytochrome P450 side-chain cleavage gene expression in oestrogenic bovine granulosa cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnslGjurk%3D&md5=5c495d3f94d654a562d2c455e504c8c4CAS |
Silva, G. M., Brito, I., Sales, A., Aguiar, F., Duarte, A., Araújo, V., Vieira, L., Magalhães-Padilha, D., Lima, L., and Alves, B. (2017). In vitro growth and maturation of isolated caprine preantral follicles: influence of insulin and FSH concentration, culture dish, coculture, and oocyte size on meiotic resumption. Theriogenology 90, 32–41.
| In vitro growth and maturation of isolated caprine preantral follicles: influence of insulin and FSH concentration, culture dish, coculture, and oocyte size on meiotic resumption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvFCjtbjJ&md5=c53782bc0b8c365a87ca640bd21f8aabCAS |
Skowronski, M. T., Kwon, T. H., and Nielsen, S. (2009). Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system. J. Histochem. Cytochem. 57, 61–67.
| Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXis1ahtQ%3D%3D&md5=1a5f90e6a91e8fb593f0fcf87e7dd440CAS |
Songsasen, N., Comizzoli, P., Nagashima, J., Fujihara, M., and Wildt, D. E. (2012). The domestic dog and cat as models for understanding the regulation of ovarian follicle development in vitro. Reprod. Domest. Anim. 47, 13–18.
| The domestic dog and cat as models for understanding the regulation of ovarian follicle development in vitro.Crossref | GoogleScholarGoogle Scholar |
Songsasen, N., Thongkittidilok, C., Yamamizu, K., Wildt, D., and Comizzoli, P. (2017). Short-term hypertonic exposure enhances in vitro follicle growth and meiotic competence of enclosed oocytes while modestly affecting mRNA expression of aquaporin and steroidogenic genes in the domestic cat model. Theriogenology 90, 228–236.
| Short-term hypertonic exposure enhances in vitro follicle growth and meiotic competence of enclosed oocytes while modestly affecting mRNA expression of aquaporin and steroidogenic genes in the domestic cat model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitFOhsr7I&md5=9ff666e6191fe0fc49fee3f73ccdfcc7CAS |
Spicer, L. J., Alpizar, E., and Echternkamp, S. (1993). Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, estradiol production, and (or) insulin-like growth factor I production in vitro. J. Anim. Sci. 71, 1232–1241.
| Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, estradiol production, and (or) insulin-like growth factor I production in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1els7s%3D&md5=5608a4798293c052c329114a989cf5b7CAS |
Thoroddsen, A., Dahm-Kähler, P., Lind, A. K., Weijdegård, B., Lindenthal, B., Müller, J., and Brännström, M. (2011). The water permeability channels aquaporins 1–4 are differentially expressed in granulosa and theca cells of the preovulatory follicle during precise stages of human ovulation. J. Clin. Endocrinol. Metab. 96, 1021–1028.
| The water permeability channels aquaporins 1–4 are differentially expressed in granulosa and theca cells of the preovulatory follicle during precise stages of human ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltF2qtLw%3D&md5=c24bec8d2b0822e654b709668cb3b8a1CAS |
Thuwanut, P., Comizzoli, P., Wildt, D. E., Keefer, C. L., and Songsasen, N. (2016). Stem cell factor (SCF) promotes in vitro ovarian follicle development in the domestic cat by upregulating c-kit mRNA expression and stimulating PI3K–Akt pathway. Reprod. Fertil. Dev. 29, 1356–1368.
| Stem cell factor (SCF) promotes in vitro ovarian follicle development in the domestic cat by upregulating c-kit mRNA expression and stimulating PI3K–Akt pathway.Crossref | GoogleScholarGoogle Scholar |
Troyer, J. L., Roelke, M. E., Jespersen, J. M., Baggett, N., Buckley-Beason, V., MacNulty, D., Craft, M., Packer, C., Pecon-Slattery, J., and O’Brien, S. J. (2011). FIV diversity: FIV Ple subtype composition may influence disease outcome in African lions. Vet. Immunol. Immunopathol. 143, 338–346.
| FIV diversity: FIV Ple subtype composition may influence disease outcome in African lions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFaitL7F&md5=4d6d074e197c9721f52935655716d656CAS |
West-Farrell, E. R., Xu, M., Gomberg, M. A., Chow, Y. H., Woodruff, T. K., and Shea, L. D. (2009). The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles. Biol. Reprod. 80, 432–439.
| The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXis1amtL4%3D&md5=192447e36502a36e06d098dce38d9f04CAS |
Willis, D., Mason, H., Gilling-Smith, C., and Franks, S. (1996). Modulation by insulin of follicle-stimulating hormone and luteinizing hormone actions in human granulosa cells of normal and polycystic ovaries. J. Clin. Endocrinol. Metab. 81, 302–309.
| 1:CAS:528:DyaK28XkvVyqug%3D%3D&md5=dabbf589af1fe610dd8775f9dffab907CAS |
Wongbandue, G., Jewgenow, K., and Chatdarong, K. (2013). Effects of thyroxin (T4) and activin A on in vitro growth of preantral follicles in domestic cats. Theriogenology 79, 824–832.
| Effects of thyroxin (T4) and activin A on in vitro growth of preantral follicles in domestic cats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitFKmtb0%3D&md5=ef02c93d1b367e12e6986c1a73d95776CAS |
Wu, J., Emery, B. R., and Carrell, D. T. (2001). In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol. Reprod. 64, 375–381.
| In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFCruw%3D%3D&md5=e35e5bc30fcf9211e21f1fd04e2be91dCAS |
Xie, F., Xiao, P., Chen, D., Xu, L., and Zhang, B. (2012). miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol. Biol. 80, 75–84.
| miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2rs7vK&md5=ec188c5397d3afb14378362a116a7dadCAS |
Xu, M., Kreeger, P. K., Shea, L. D., and Woodruff, T. K. (2006). 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=882c3f370e7ee153752c8ab9eb8cb1f4CAS |
Xu, M., West-Farrell, E. R., Stouffer, R. L., Shea, L. D., Woodruff, T. K., and Zelinski, M. B. (2009). 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=03987a7bf91314cc027a0409a68ef91aCAS |
Xu, M., Fazleabas, A. T., Shikanov, A., Jackson, E., Barrett, S. L., Hirshfeld-Cytron, J., Kiesewetter, S. E., Shea, L. D., and Woodruff, T. K. (2011). In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes. Biol. Reprod. 84, 689–697.
| In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvFanurs%3D&md5=ba81fd16757e0d22a56168d05baca1b0CAS |
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=3cd674380693e5bd6c51ab88d4b69c3aCAS |
Zhang, P., Chao, H., Sun, X., Li, L., Shi, Q., and Shen, W. (2010). Murine folliculogenesis in vitro is stage-specifically regulated by insulin via the Akt signaling pathway. Histochem. Cell Biol. 134, 75–82.
| Murine folliculogenesis in vitro is stage-specifically regulated by insulin via the Akt signaling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVaitr4%3D&md5=ce8513bdc02afd27f5a6dbf00648d4d7CAS |
