Reversible meiotic arrest in feline oocytes
Jason R. Herrick
+ Author Affiliations
- Author Affiliations
Department of Comparative Biosciences, University of Illinois at Urbana-Champaign, 2001 South Lincoln Avenue, Urbana, IL 61802, USA.Present address: National Foundation for Fertility Research, 10290 RidgeGate Cr, Lone Tree, CO 80124, USA. Email: jherrick@fertilityresearch.org
Reproduction, Fertility and Development 26(2) 258-267 https://doi.org/10.1071/RD12341
Submitted: 17 October 2012 Accepted: 24 November 2012 Published: 18 January 2013
Abstract
Increasing intracellular concentrations of cyclic adenosine monophosphate (cAMP) within the cumulus–oocyte complex (COC) inhibits or delays spontaneous oocyte maturation and improves the developmental competence of the oocyte in many species, but information for carnivores is limited. The objectives of the present study were to describe the effects of isobutyl methylxanthine (IBMX), which decreases cAMP degradation, and forskolin, which increases cAMP production, on spontaneous and induced maturation (by equine chorionic gonadotrophin (eCG) and epidermal growth factor (EGF)) of feline oocytes and to evaluate the reversibility of IBMX-induced arrest by measuring the resumption of meiosis and embryonic development following IVF. IBMX decreased (P < 0.05) the incidence of spontaneous (6.7% vs 42.0%, metaphase II (MII)) and induced (5.6% vs 66.1% MII) maturation after 24 h of culture. In contrast, forskolin stimulated meiosis (81.7% MII; P < 0.05). Following 12 h of culture with IBMX and an additional 24 h with eCG and EGF in the absence of IBMX, the proportions of oocytes reaching MII (66.1%), cleaving (79.9%) and developing to the blastocyst stage (15.3%) were similar (P > 0.05) to oocytes cultured continuously with eCG and EGF (70.2%, 83.0% and 18.1%, respectively). These results demonstrate that IBMX reversibly inhibits both spontaneous and eCG+EGF-induced meiosis in feline oocytes without compromising the oocyte’s developmental competence.
Additional keywords: assisted reproductive technologies, carnivore, cat.
References
Albuz, F. K., Sasseville, M., Lane, M., Armstrong, D. T., Thompson, J. G., and Gilchrist, R. B. (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro-maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 25, 2999–3011.| Simulated physiological oocyte maturation (SPOM): a novel in vitro-maturation system that substantially improves embryo yield and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbotlKnsg%3D%3D&md5=a2cc604de8f19b7813f9370422a4da50CAS | 20870682PubMed |
Ali, A., and Sirard, M. A. (2002). Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation. Biol. Reprod. 66, 901–905.
| Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCltLs%3D&md5=848015272994ee146cee1c902bd9e4c9CAS | 11906907PubMed |
Bagg, M. A., Nottle, M. B., Armstrong, D. T., and Grupen, C. G. (2009). Effect of follicle size and dibutyryl cAMP on the cAMP content and gap-junctional communication of porcine prepubertal cumulus–oocyte complexes during IVM. Reprod. Fertil. Dev. 21, 796–804.
| Effect of follicle size and dibutyryl cAMP on the cAMP content and gap-junctional communication of porcine prepubertal cumulus–oocyte complexes during IVM.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnvVOhu7g%3D&md5=0d954241fe23732b645e3d9b0fd3b7deCAS | 19567222PubMed |
Banwell, K. M., Lane, M., Russell, D. L., Kind, K. L., and Thompson, J. G. (2007). Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum. Reprod. 22, 2768–2775.
| Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2srlsFKhsA%3D%3D&md5=3b979b9331ea9d2ee03f1e950dc6d311CAS | 17725990PubMed |
Bateman, H. L., Bond, J. B., Campbell, M., Barrie, M., Riggs, G., Snyder, B., and Swanson, W. F. (2009). Characterization of basal seminal traits and reproductive endocrine profiles in North American river otters and Asian small-clawed otters. Zoo Biol. 28, 107–126.
| Characterization of basal seminal traits and reproductive endocrine profiles in North American river otters and Asian small-clawed otters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1yks7o%3D&md5=376181cae8159e01b61e1b72ab55a9c5CAS | 19367624PubMed |
Bilodeau, S., Fortier, M. A., and Sirard, M. A. (1993). Effect of adenylate cyclase stimulation on meiotic resumption and cyclic AMP content of zona-free and cumulus-enclosed bovine oocytes in vitro. J. Reprod. Fertil. 97, 5–11.
| Effect of adenylate cyclase stimulation on meiotic resumption and cyclic AMP content of zona-free and cumulus-enclosed bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXht1Wkt7g%3D&md5=e28b6cdf865b5e781acef036a76ca00bCAS | 7681878PubMed |
Bilodeau-Goeseels, S. (2006). Effects of culture media and energy sources on the inhibition of nuclear maturation in bovine oocytes. Theriogenology 66, 297–306.
| Effects of culture media and energy sources on the inhibition of nuclear maturation in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 16384597PubMed |
Bornslaeger, E. A., and Schultz, R. M. (1985). Regulation of mouse oocyte maturation: effect of elevating cumulus cell cAMP on oocyte cAMP levels. Biol. Reprod. 33, 698–704.
| Regulation of mouse oocyte maturation: effect of elevating cumulus cell cAMP on oocyte cAMP levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlsFOqtL4%3D&md5=55259c3e47c4802d5dba8f986b80748dCAS | 2996645PubMed |
Chen, J., Chi, M. M., Moley, K. H., and Downs, S. M. (2009). cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 138, 759–770.
| cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsValt7rP&md5=267c047cb0d95ce836667bcb7dbd50f4CAS | 19700529PubMed |
Conti, M., Andersen, C. B., Richard, F. J., Shitsukawa, K., and Tsafriri, A. (1998). Role of cyclic nucleotide phosphodiesterases in resumption of meiosis. Mol. Cell. Endocrinol. 145, 9–14.
| Role of cyclic nucleotide phosphodiesterases in resumption of meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1eitr8%3D&md5=d84598faf00963e75b893d1407c5acfeCAS | 9922093PubMed |
Dekel, N., Aberdam, E., and Sherizly, I. (1984). Spontaneous maturation in vitro of cumulus-enclosed rat oocytes is inhibited by forskolin. Biol. Reprod. 31, 244–250.
| Spontaneous maturation in vitro of cumulus-enclosed rat oocytes is inhibited by forskolin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXls1OqsLw%3D&md5=33baeded1c2bf0b57381396affd90830CAS | 6089921PubMed |
Desmarais, J. A., Bordignon, V., Lopes, F. L., Smith, L. C., and Murphy, B. D. (2004). The escape of the mink embryo from obligate diapause. Biol. Reprod. 70, 662–670.
| The escape of the mink embryo from obligate diapause.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1ChsL4%3D&md5=5e7c0f3a1af6983e82ddf8dd7ea10177CAS | 14585805PubMed |
Downs, S. M. (2011). Mouse versus rat: profound differences in meiotic regulation at the level of the isolated oocyte. Mol. Reprod. Dev. 78, 778–794.
| Mouse versus rat: profound differences in meiotic regulation at the level of the isolated oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagu7vN&md5=4a9f30f766efd3380714e62f083c0bf9CAS | 21953615PubMed |
Downs, S. M., and Hunzicker-Dunn, M. (1995). Differential regulation of oocyte maturation and cumulus expansion in the mouse oocyte–cumulus cell complex by site-selective analogues of cyclic adenosine monophosphate. Dev. Biol. 172, 72–85.
| Differential regulation of oocyte maturation and cumulus expansion in the mouse oocyte–cumulus cell complex by site-selective analogues of cyclic adenosine monophosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptFGru7o%3D&md5=1309224bede3ae8c1ac93e27316b3e97CAS | 7589815PubMed |
Downs, S. M., Daniel, S. A. J., and Eppig, J. J. (1988). Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J. Exp. Zool. 245, 86–96.
| Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXht1Ghsr0%3D&md5=c38bee9d01f350765d05baf29253bc18CAS | 2832512PubMed |
Downs, S. M., Daniel, S. A. J., Bornslaeger, E. A., Hoppe, P. C., and Eppig, J. J. (1989). Maintenance of meiotic arrest in mouse oocytes by purines: modulation of cAMP levels and cAMP phosphodiesterase activity. Gamete Res. 23, 323–334.
| Maintenance of meiotic arrest in mouse oocytes by purines: modulation of cAMP levels and cAMP phosphodiesterase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltlWmtL0%3D&md5=b5c0d0258444eaec3fa4e0b95401c0acCAS | 2476369PubMed |
Downs, S. M., Humpherson, P. G., and Leese, H. J. (2002). Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorous. Mol. Reprod. Dev. 62, 113–123.
| Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorous.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVChu7s%3D&md5=db8b28bdd5293529ce1dc9bb610fb884CAS | 11933168PubMed |
Edwards, R. G. (1965). Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349–351.
| Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF287lsVagsg%3D%3D&md5=05a4dcf9967df0fb87147e975f2cfcdeCAS | 4957259PubMed |
Fan, H. Y., Li, M. Y., Tong, C., Chen, D. Y., Xia, G. L., Song, X. F., Schatten, H., and Sun, Q. Y. (2002). Inhibitory effects of cAMP and protein kinase C on meiotic maturation and MAP kinase phosphorylation in porcine oocytes. Mol. Reprod. Dev. 63, 480–487.
| Inhibitory effects of cAMP and protein kinase C on meiotic maturation and MAP kinase phosphorylation in porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotlCgtrk%3D&md5=713612e43bc3eee40f0b535852c707c5CAS | 12412051PubMed |
Funahashi, H., and Day, B. N. (1993). Effects of duration of exposure to hormone supplements on cytoplasmic maturation of pig oocytes in vitro. J. Reprod. Fertil. 98, 179–185.
| Effects of duration of exposure to hormone supplements on cytoplasmic maturation of pig oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltV2htr8%3D&md5=321fec6a00a1a30b4303e3f382f47e4fCAS | 8345463PubMed |
Funahashi, H., Cantley, T. C., and Day, B. N. (1997). Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol. Reprod. 57, 49–53.
| Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktFCntb0%3D&md5=47d8032577a493be5bdbfd87fda7a9a2CAS | 9209079PubMed |
Gilchrist, R. B. (2011). Recent insights into oocyte–follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod. Fertil. Dev. 23, 23–31.
| Recent insights into oocyte–follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 21366977PubMed |
Gilchrist, R. B., and Thompson, J. G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6–15.
| Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro.Crossref | GoogleScholarGoogle Scholar | 17092551PubMed |
Godard, N. M., Pukazhenthi, B. S., Wildt, D. E., and Comizzoli, P. (2009). Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro of denuded oocytes in the cat model. Fertil. Steril. 91, 2051–2060.
| Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro of denuded oocytes in the cat model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsVeisrY%3D&md5=51abdf6de235acc474ca685224396cfdCAS | 18692794PubMed |
Herrick, J. R., Brad, A. M., and Krisher, R. L. (2006a). Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131, 289–298.
| Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsLs%3D&md5=6981341af2536fa40fff96f12e5677afCAS | 16452722PubMed |
Herrick, J. R., Lane, M., Gardner, D. K., Behboodi, E., Memili, E., Blash, S., Echelard, Y., and Krisher, R. L. (2006b). Metabolism, protein content and in vitro embryonic development of goat cumulus–oocyte complexes matured with physiological concentrations of glucose and l-lactate. Mol. Reprod. Dev. 73, 256–266.
| Metabolism, protein content and in vitro embryonic development of goat cumulus–oocyte complexes matured with physiological concentrations of glucose and l-lactate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjslyntw%3D%3D&md5=3f7e5d20cb182f489bd7d2eafea70083CAS | 16250005PubMed |
Herrick, J. R., Bond, J. B., Magarey, G. M., Bateman, H. L., Krisher, R. L., Dunford, S. A., and Swanson, W. F. (2007). Toward a feline optimised culture medium: impact of ions, carbohydrates, essential amino acids, vitamins and serum on development and metabolism of IVF-derived feline embryos relative to embryos grown in vivo. Biol. Reprod. 76, 858–870.
| Toward a feline optimised culture medium: impact of ions, carbohydrates, essential amino acids, vitamins and serum on development and metabolism of IVF-derived feline embryos relative to embryos grown in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1OhsLo%3D&md5=6d00a10e7de4b6fc0846f2172b1f1d2cCAS | 17267698PubMed |
Herrick, J. R., Campbell, M., Levens, G., Moore, T., Benson, K., D’Agostino, J., West, G., Okeson, D. M., Coke, R., Portacio, S. C., Leiske, K., Kreider, C., Polumbo, P. J., and Swanson, W. F. (2010). In vitro fertilization and sperm cryopreservation in the black-footed cat (Felis nigripes) and sand cat (Felis margarita). Biol. Reprod. 82, 552–562.
| In vitro fertilization and sperm cryopreservation in the black-footed cat (Felis nigripes) and sand cat (Felis margarita).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXisVeku7w%3D&md5=74b386e5df1ca74f11fdc23e631bb1c9CAS | 19906688PubMed |
Horner, K., Livera, G., Hinckley, M., Trinh, K., Storm, D., and Conti, M. (2003). Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Dev. Biol. 258, 385–396.
| Rodent oocytes express an active adenylyl cyclase required for meiotic arrest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVyrs7c%3D&md5=2dba46b04d96b4abfee1dfbb78ec6c93CAS | 12798295PubMed |
Jensen, J. T., Schwinof, K. M., Zelinski-Wooten, M. B., Conti, M., DePaolo, L. V., and Stouffer, R. L. (2002). Phosphodiesterase 3 inhibitors selectively block the spontaneous resumption of meiosis by macaque oocytes in vitro. Hum. Reprod. 17, 2079–2084.
| Phosphodiesterase 3 inhibitors selectively block the spontaneous resumption of meiosis by macaque oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xms1Kmt7Y%3D&md5=046bfe7d585773eb21071abe2c859b37CAS | 12151440PubMed |
Kawashima, I., Okazaki, T., Noma, N., Nishibori, M., Yamashita, Y., and Shimada, M. (2008). Sequential exposure of porcine cumulus cells to FSH and/or LH is critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vitro. Reproduction 136, 9–21.
| Sequential exposure of porcine cumulus cells to FSH and/or LH is critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVSgu7o%3D&md5=4ad27f2f244abba5e10af88f48e10c6aCAS | 18456902PubMed |
Laforest, M. F., Pouliot, E., Guéguen, L., and Richard, F. J. (2005). Fundamental significance of specific phosphodiesterases in the control of spontaneous meiotic resumption in porcine oocytes. Mol. Reprod. Dev. 70, 361–372.
| Fundamental significance of specific phosphodiesterases in the control of spontaneous meiotic resumption in porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVShu7Y%3D&md5=a476430361c1e0709a18e40ad468adedCAS | 15625697PubMed |
Lane, M., Gardner, D. K., Hasler, M. J., and Hasler, J. F. (2003). Use of G1.2/G2.2 media for commercial bovine embryo culture: equivalent development and pregnancy rates compared to co-culture. Theriogenology 60, 407–419.
| Use of G1.2/G2.2 media for commercial bovine embryo culture: equivalent development and pregnancy rates compared to co-culture.Crossref | GoogleScholarGoogle Scholar | 12763155PubMed |
Lastro, M., Collins, S., and Currie, W. B. (2006). Adenylyl cyclases in oocyte maturation: a characterization of AC isoforms in bovine cumulus cells. Mol. Reprod. Dev. 73, 1202–1210.
| Adenylyl cyclases in oocyte maturation: a characterization of AC isoforms in bovine cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvFahtro%3D&md5=91f026c1b3aceece0d97029443839b1aCAS | 16804883PubMed |
Liang, C. G., Huo, L. J., Zhong, Z. S., Chen, D. Y., Schatten, H., and Sun, Q. Y. (2005). Cyclic adenosine 3′,5′-monophosphate-dependent activation of mitogen-activated protein kinase in cumulus cells is essential for germinal vesicle breakdown of porcine cumulus-enclosed oocytes. Endocrinology 146, 4437–4444.
| Cyclic adenosine 3′,5′-monophosphate-dependent activation of mitogen-activated protein kinase in cumulus cells is essential for germinal vesicle breakdown of porcine cumulus-enclosed oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGmurfL&md5=1919cdb5cab2e3efc199604b19c67d4cCAS | 16002524PubMed |
Littell, R. C., Milliken, G. A., Stroup, W. W., and Wolfinger, R. D. (1996). ‘SAS System for Mixed Models’. (SAS Institute Inc.: Cary, USA.)
Luciano, A. M., Modina, S., Vassena, R., Milanesi, E., Lauria, A., and Gandolfi, F. (2004). Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol. Reprod. 70, 465–472.
| Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsl2juw%3D%3D&md5=3b049151694f2f9ab4f514668438865bCAS | 14568913PubMed |
Luvoni, G. C., Chigioni, S., Perego, L., Lodde, V., Modina, S., and Luciano, A. M. (2006). Effect of gonadotrophins during in vitro maturation of feline oocytes on oocyte–cumulus cells functional coupling and intracellular glutathione. Anim. Reprod. Sci. 96, 66–78.
| Effect of gonadotrophins during in vitro maturation of feline oocytes on oocyte–cumulus cells functional coupling and intracellular glutathione.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1Ciu7Y%3D&md5=2e64beb402653bf78095eee75e365cfcCAS | 16386859PubMed |
Mehlmann, L. M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–799.
| Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt12nsg%3D%3D&md5=0c13aeac32f532c420598e1b846ee56fCAS | 16322539PubMed |
Nogueira, D., Ron-El, R., Friedler, S., Schachter, M., Raziel, A., Cortvrindt, R., and Smitz, J. (2006). Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol. Reprod. 74, 177–184.
| Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCjsrfO&md5=adb3ce0934fe38acedbab611f966e1feCAS | 16207840PubMed |
Norris, R. P., Ratzan, W. J., Freudzon, M., Mehlmann, L. M., Krall, J., Movsesian, M. A., Wang, H., Ke, H., Nikolaev, V. O., and Jaffe, L. A. (2009). Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136, 1869–1878.
| Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot1aktbw%3D&md5=44d08d073bae0e2d7f41dc23d2f49815CAS | 19429786PubMed |
Ozawa, M., Nagai, T., Somfai, T., Nakai, M., Maedomari, N., Fahrudin, M., Karja, N. W. K., Kaneko, H., Noguchi, J., Ohnuma, K., Yoshimi, N., Miyazaki, H., and Kikuchi, K. (2008). Comparison between effects of 3-isobutyl-1-methylxanthine and FSH on gap-junctional communication, LH-receptor expression and meiotic maturation of cumulus–oocyte complexes in pigs. Mol. Reprod. Dev. 75, 857–866.
| Comparison between effects of 3-isobutyl-1-methylxanthine and FSH on gap-junctional communication, LH-receptor expression and meiotic maturation of cumulus–oocyte complexes in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktFGhtr0%3D&md5=0e62e5ab9953cbd3008bdcb7d7010465CAS | 18022826PubMed |
Papadopoulos, S., Rizos, D., Duffy, P., Wade, M., Quinn, K., Boland, M. P., and Lonergan, P. (2002). Embryo survival and recipient pregnancy rates after transfer of fresh or vitrified, in vivo- or in vitro-produced ovine blastocysts. Anim. Reprod. Sci. 74, 35–44.
| Embryo survival and recipient pregnancy rates after transfer of fresh or vitrified, in vivo- or in vitro-produced ovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nitFKqtw%3D%3D&md5=b8e3b8247051daec6dd24ce448dd7b7bCAS | 12379373PubMed |
Pursel, V. G., Wall, R. J., Rexroad, C. E., Hammer, R. E., and Brinster, R. L. (1985). A rapid whole-mount staining procedure for nuclei of mammalian embryos. Theriogenology 24, 687–691.
| A rapid whole-mount staining procedure for nuclei of mammalian embryos.Crossref | GoogleScholarGoogle Scholar |
Racowsky, C. (1984). Effect of forskolin on the spontaneous maturation and cyclic AMP content of rat oocyte–cumulus complexes. J. Reprod. Fertil. 72, 107–116.
| Effect of forskolin on the spontaneous maturation and cyclic AMP content of rat oocyte–cumulus complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmt1emsr4%3D&md5=250c54cbf13298911b352a361a91e41fCAS | 6088768PubMed |
Racowsky, C. (1985a). Effect of forskolin on the spontaneous maturation and cyclic AMP content of hamster oocyte–cumulus complexes. J. Exp. Zool. 234, 87–96.
| Effect of forskolin on the spontaneous maturation and cyclic AMP content of hamster oocyte–cumulus complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhvVeiurg%3D&md5=4d2f4a468cb1540a92f31fb5ce4ae868CAS | 2985733PubMed |
Racowsky, C. (1985b). Effect of forskolin on maintenance of meiotic arrest and stimulation of cumulus expansion, progesterone and cyclic AMP production by pig oocyte–cumulus complexes. J. Reprod. Fertil. 74, 9–21.
| Effect of forskolin on maintenance of meiotic arrest and stimulation of cumulus expansion, progesterone and cyclic AMP production by pig oocyte–cumulus complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlsFyitrs%3D&md5=63ee7f4b22d733549065676863aeca20CAS | 2991512PubMed |
Richard, F. J., Tsafriri, A., and Conti, M. (2001). Role of phosphodiesterase type 3A in rat oocyte maturation. Biol. Reprod. 65, 1444–1451.
| Role of phosphodiesterase type 3A in rat oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVers7w%3D&md5=13af8f44f308cbc3f02c95b1e92dc109CAS | 11673261PubMed |
Sanbuissho, A., Coskun, S., and Lin, Y. C. (1992). Role of cyclic adenosine monophosphate (cAMP) in vitro on bovine oocyte maturation. Theriogenology 38, 153–163.
| Role of cyclic adenosine monophosphate (cAMP) in vitro on bovine oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVyjsLg%3D&md5=90542941f29d619ec09df4b35c16c1d8CAS | 16727127PubMed |
Sasseville, M., Albuz, F. K., Côté, N., Guillemette, C., Gilchrist, R. B., and Richard, F. J. (2009). Characterization of novel phosphodiesterases in the bovine ovarian follicle. Biol. Reprod. 81, 415–425.
| Characterization of novel phosphodiesterases in the bovine ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVaiurg%3D&md5=177020d7c3dc17f3d69e74b9acf0e4ecCAS | 19357367PubMed |
Sato, E., and Koide, S. S. (1984). Forskolin and mouse oocyte maturation in vitro. J. Exp. Zool. 230, 125–129.
| Forskolin and mouse oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXktVWmtL4%3D&md5=20eda3c19267cf5a345f553128462f89CAS | 6427389PubMed |
Schroeder, A. C., and Eppig, J. J. (1984). The developmental capacity of mouse oocytes that matured spontaneously in vitro is normal. Dev. Biol. 102, 493–497.
| The developmental capacity of mouse oocytes that matured spontaneously in vitro is normal.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7lvFaitQ%3D%3D&md5=abc6d4e1c97495e9e59954ff66f06047CAS | 6706011PubMed |
Schultz, R. M., Montgomery, R. R., and Belanoff, J. R. (1983). Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev. Biol. 97, 264–273.
| Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktVentLs%3D&md5=63d9b8bd107f06ae147751db7a387939CAS | 6189752PubMed |
Shimada, M., and Terada, T. (2002). Roles of cAMP in regulation of both MAP kinase and p34cdc2 kinase activity during meiotic progression, especially beyond the MI stage. Mol. Reprod. Dev. 62, 124–131.
| Roles of cAMP in regulation of both MAP kinase and p34cdc2 kinase activity during meiotic progression, especially beyond the MI stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVChu7g%3D&md5=16c8db08284ac82307e655bc7100d9aaCAS | 11933169PubMed |
Shu, Y. M., Zeng, H. T., Ren, Z., Zhuang, G. L., Liang, X. Y., Shen, H. W., Yao, S. Z., Ke, P. Q., and Wang, N. N. (2008). Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum. Reprod. 23, 504–513.
| Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVOhtr0%3D&md5=9d2118860ea7cd60d2048fb7e2175882CAS | 18216034PubMed |
Sirard, M. A., and First, N. L. (1988). In vitro inhibition of oocyte nuclear maturation in the bovine. Biol. Reprod. 39, 229–234.
| In vitro inhibition of oocyte nuclear maturation in the bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXls1Cgsr0%3D&md5=63de0538449590148924c2b1c9c15f45CAS | 2460146PubMed |
Somfai, T., Kikuchi, K., Onishi, A., Iwamoto, M., Fuchimoto, D. I., Papp, A. B., Sato, E., and Nagai, T. (2003). Meiotic arrest maintained by cAMP during initiation of maturation enhances meiotic potential and developmental competence and reduces polyspermy of IVM/IVF porcine oocytes. Zygote 11, 199–206.
| Meiotic arrest maintained by cAMP during initiation of maturation enhances meiotic potential and developmental competence and reduces polyspermy of IVM/IVF porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot12gsL0%3D&md5=4d2329d1a1f3630acbd87dc84a987726CAS | 14640184PubMed |
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=07144c8ba48a235ab5335ed114c694fbCAS | 17097840PubMed |
Stokes, Y. M., Clark, A. R., and Thompson, J. G. (2008). Mathematical modelling of glucose supply toward successful in vitro maturation of mammalian oocytes. Tissue Eng. 14, 1539–1547.
| Mathematical modelling of glucose supply toward successful in vitro maturation of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWlt7jM&md5=150c1eeb877cb84a6e6f61b8541119eaCAS |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2004). Cumulus expansion and glucose utilization by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone. Reproduction 128, 313–319.
| Cumulus expansion and glucose utilization by bovine cumulus–oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1KitLk%3D&md5=f8e07ce67421d20b258a3fb3e2856904CAS | 15333782PubMed |
Tang-Pedersen, M., Westergaard, L. G., Erb, K., and Mikkelsen, A. L. (2012). Combination of IVF and IVM in naturally cycling women. Reprod. Biomed. Online 24, 47–53.
| Combination of IVF and IVM in naturally cycling women.Crossref | GoogleScholarGoogle Scholar | 22116074PubMed |
Thomas, R. E., Armstrong, D. T., and Gilchrist, R. B. (2002). Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev. Biol. 244, 215–225.
| Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1ygsLs%3D&md5=6ed0e1e3ae8dc3a9d50a0b5e9b6d072eCAS | 11944932PubMed |
Thomas, R. E., Armstrong, D. T., and Gilchrist, R. B. (2004a). Bovine cumulus cell–oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosphate levels. Biol. Reprod. 70, 548–556.
| Bovine cumulus cell–oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosphate levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Chsrs%3D&md5=4ccecd4ebabc0b7b3060a183e66e45e5CAS | 14568915PubMed |
Thomas, R. E., Thompson, J. G., Armstrong, D. T., and Gilchrist, R. B. (2004b). Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol. Reprod. 71, 1142–1149.
| Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqt7Y%3D&md5=6f6d004eb386594a3ea2d7e3ba9741d2CAS | 15189837PubMed |
Vanhoutte, L., Nogueira, D., Gerris, J., Dhont, M., and DeSutter, P. (2008). Effect of temporary nuclear arrest by phosphodiesterase 3-inhibitor on morphological and functional aspects of in vitro-matured mouse oocytes. Mol. Reprod. Dev. 75, 1021–1030.
| Effect of temporary nuclear arrest by phosphodiesterase 3-inhibitor on morphological and functional aspects of in vitro-matured mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsVWjtrY%3D&md5=3b9f49f3bd9a7a84aaf91e2df1f80f97CAS | 18163445PubMed |
Wildt, D. E., Comizzoli, P., Pukazhenthi, B., and Songsasen, N. (2010). Lessons from biodiversity – the value of non-traditional species to advance reproductive science, conservation and human health. Mol. Reprod. Dev. 77, 397–409.
| Lessons from biodiversity – the value of non-traditional species to advance reproductive science, conservation and human health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFKqtr0%3D&md5=abaaf367938523496a27c03201828cf6CAS | 19967718PubMed |
Wood, T. C., Byers, A. P., Jennette, B. E., and Wildt, D. E. (1995). Influence of protein and hormone supplementation on in vitro maturation and fertilization of domestic cat eggs. J. Reprod. Fertil. 104, 315–323.
| Influence of protein and hormone supplementation on in vitro maturation and fertilization of domestic cat eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntlCjs7k%3D&md5=91a08e05368fe159a5f2c15b7274965cCAS | 7473424PubMed |
Yoshioka, K., Suzuki, C., Itoh, S., Kikuchi, K., Iwamura, S., and Rodriguez-Martinez, H. (2003). Production of piglets derived from in vitro-produced blastocysts fertilized and cultured in chemically defined media: effects of theophylline, adenosine and cysteine during in vitro fertilization. Biol. Reprod. 69, 2092–2099.
| Production of piglets derived from in vitro-produced blastocysts fertilized and cultured in chemically defined media: effects of theophylline, adenosine and cysteine during in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCntrw%3D&md5=e704f836f76e7a128f641d4cc92ef53fCAS | 12930720PubMed |
Zhang, M., Su, Y. Q., Sugiura, K., Xia, G., and Eppig, J. J. (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–369.
| Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OisL7P&md5=d6d63abf43a20add7731ef5ab0049846CAS | 20947764PubMed |
