Effects of aging on gene expression and mitochondrial DNA in the equine oocyte and follicle cells
Fernando Campos-Chillon A , Todd A. Farmerie B , Gerrit J. Bouma C , Colin M. Clay C and Elaine M. Carnevale C DA California Polytechnic State University, 1 Grand Avenue, San Luis Obispo, CA 93407, USA.
B Washington State University, PO Box 647520, Pullman, WA 99164, USA.
C Colorado State University, 1693 Campus Delivery, Fort Collins, CO 80523, USA.
D Corresponding author. Email: emc@colostate.edu
Reproduction, Fertility and Development 27(6) 925-933 https://doi.org/10.1071/RD14472
Submitted: 26 November 2014 Accepted: 18 February 2015 Published: 19 March 2015
Abstract
We hypothesised that advanced mare age is associated with follicle and oocyte gene alterations. The aims of the study were to examine quantitative and temporal differences in mRNA for LH receptor (LHR), amphiregulin (AREG) and epiregulin (EREG) in granulosa cells, phosphodiesterase (PDE) 4D in cumulus cells and PDE3A, G-protein-coupled receptor 3 (GPR3), growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15) and mitochondrial (mt) DNA in oocytes. Samples were collected from dominant follicles of Young (3–12 years) and Old (≥20 years) mares at 0, 6, 9 and 12 h after administration of equine recombinant LH. LHR mRNA declined after 0 h in Young mares, with no time effect in Old mares. For both ages, gene expression of AREG was elevated at 6 and 9 h and EREG was expression was elevated at 9 h, with higher expression in Old than Young mares. Cumulus cell PDE4D expression increased by 6 h (Old) and 12 h (Young). Oocyte GPR3 expression peaked at 9 and 12 h in Young and Old mares, respectively. Expression of PDE3A increased at 6 h, with the increase greater in oocytes from Old than Young mares at 6 and 9 h. Mean GDF9 and BMP15 transcripts were higher in Young than Old, with a peak at 6 h. Copy numbers of mtDNA did not vary over time in oocytes from Young mares, but a temporal decrease was observed in oocytes from Old mares. The results support an age-associated asynchrony in the expression of genes that are essential for follicular and oocyte maturation before ovulation.
Additional keywords: AREG, BMP15, EREG, follicular aspiration, GDF9, GPR3, PDE3A, PDE4D.
References
Altermatt, J. L., Suh, T. K., Stokes, J. E., and Carnevale, E. M. (2009). Effects of age and equine follicle-stimulating hormone (eFSH) on collection and viability of equine oocytes assessed by morphology and developmental competency after intracytoplasmic sperm injection (ICSI). Reprod. Fertil. Dev. 21, 615–623.| Effects of age and equine follicle-stimulating hormone (eFSH) on collection and viability of equine oocytes assessed by morphology and developmental competency after intracytoplasmic sperm injection (ICSI).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksF2rtbc%3D&md5=21ee49d7434170275d715474414153b4CAS | 19383268PubMed |
American College of Obstetricians and Gynecologists Committee on Gynecologic Practice and Practice Committee (2014). Female age-related fertility decline. Committee Opinion No. 589. Fertil. Steril. 101, 633–634.
| Female age-related fertility decline. Committee Opinion No. 589.Crossref | GoogleScholarGoogle Scholar | 24559617PubMed |
Ascoli, M., Fanelli, F., and Segaloff, D. L. (2002). The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23, 141–174.
| The lutropin/choriogonadotropin receptor, a 2002 perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFWjtr4%3D&md5=fa25dba1bd344b17888b6f1e6e59c333CAS | 11943741PubMed |
Ashkenazi, H., Cao, X., Motola, S., Popliker, M., Conti, M., and Tsafriri, A. (2005). Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146, 77–84.
| Epidermal growth factor family members: endogenous mediators of the ovulatory response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFGmt7jP&md5=7d58c338080346e44e34017a665f547aCAS | 15459120PubMed |
Beg, M. A., and Ginther, O. J. (2006). Follicle selection in cattle and horses: role of intrafollicular factors. Reproduction 132, 365–377.
| Follicle selection in cattle and horses: role of intrafollicular factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCgt77F&md5=485347c17ca5bb51263f3ca4e39eae6dCAS | 16940278PubMed |
Bezard, J., Magistrini, M., Duchamp, G., and Palmer, E. (1989). Chronology of equine fertilisation and embryonic development in vivo and in vitro. Equine Vet. J. 8, 105–110.
| Chronology of equine fertilisation and embryonic development in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |
Bunel, A., Nivet, A. L., Blondin, P., Vigneault, C., Richard, F. J., and Sirard, M. A. (2014). Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes. Reprod. Fertil. Dev. 26, 855–865.
| Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFynsbjO&md5=51d2fefda6a5ae393dab719e637c7072CAS | 23827322PubMed |
Carabatsos, M. J., Sellitto, C., Goodenough, D. A., and Albertini, D. F. (2000). Oocyte–granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev. Biol. 226, 167–179.
| Oocyte–granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFSjtrY%3D&md5=6ce5f614a887dcb63266f5b4a9fd8f21CAS | 11023678PubMed |
Carnevale, E. M. (2008). The mare model for follicular maturation and reproductive aging in the woman. Theriogenology 69, 23–30.
| The mare model for follicular maturation and reproductive aging in the woman.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nN&md5=b1d730b243c0636c9f9498a2aecbc1f0CAS | 17976712PubMed |
Carnevale, E. M., and Ginther, O. J. (1995). Defective oocytes as a cause of subfertility in old mares. In: ‘Equine Reproduction VI’. (Eds D. C. Sharp and F. W. Bazer.) pp. 209–214. (Society for the Study of Reproduction: Madison, WI.)
Carnevale, E. M., Bergfelt, D. R., and Ginther, O. J. (1993a). Aging effects on follicular activity and concentrations of FSH, LH, and progesterone in mares. Anim. Reprod. Sci. 31, 287–299.
| Aging effects on follicular activity and concentrations of FSH, LH, and progesterone in mares.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltV2nsb0%3D&md5=447aae172b61b197d75fb8805cae2dfaCAS |
Carnevale, E. M., Griffin, P. G., and Ginther, O. J. (1993b). Age-associated subfertility before entry of embryos into the uterus in mares. Equine Vet. J. Suppl. 25, 31–35.
| Age-associated subfertility before entry of embryos into the uterus in mares.Crossref | GoogleScholarGoogle Scholar |
Carnevale, E. M., Maclellan, L. J., Coutinho da Silva, M. A., Scott, T. J., and Squires, E. L. (2000). Comparison of culture and insemination techniques for equine oocyte transfer. Theriogenology 54, 981–987.
| Comparison of culture and insemination techniques for equine oocyte transfer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2Fot1Cisw%3D%3D&md5=88d00f25912447b6f17486cab9450e8cCAS | 11097049PubMed |
Conti, M., Andersen, C. B., Richard, F., Mehats, C., Chun, S. Y., Horner, K., Jin, C., and Tsafriri, A. (2002). Role of cyclic nucleotide signaling in oocyte maturation. Mol. Cell. Endocrinol. 187, 153–159.
| Role of cyclic nucleotide signaling in oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Sqtro%3D&md5=11ddb99ed749ba5d29b0d1aa8823ce9fCAS | 11988323PubMed |
Conti, M., Hsieh, M., Park, J. Y., and Su, Y. Q. (2006). Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20, 715–723.
| Role of the epidermal growth factor network in ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1Oqu78%3D&md5=06e54b48b788fbdb26f0c72936d36585CAS | 16051667PubMed |
Cushman, R. A., Allan, M. F., Kuehn, L. A., Snelling, W. M., Cupp, A. S., and Freetly, H. C. (2009). Evaluation of antral follicle count and ovarian morphology in crossbred beef cows: investigation of influence of stage of the estrous cycle, age, and birth weight. J. Anim. Sci. 87, 1971–1980.
| Evaluation of antral follicle count and ovarian morphology in crossbred beef cows: investigation of influence of stage of the estrous cycle, age, and birth weight.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1eju7w%3D&md5=2c69738c716c7123ea25c1fe00937e0eCAS | 19286826PubMed |
DiLuigi, A., Weitzman, V. N., Pace, M. C., Siano, L. J., Maier, D., and Mehlmann, L. M. (2008). Meiotic arrest in human oocytes is maintained by a G(s) signaling pathway. Biol. Reprod. 78, 667–672.
| Meiotic arrest in human oocytes is maintained by a G(s) signaling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjvVaiur8%3D&md5=ea51e1d2c466fc3dcf234997026c8d1dCAS | 18184921PubMed |
Donnison, M., and Pfeffer, P. L. (2004). Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development. Biol. Reprod. 71, 1813–1821.
| Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsr%2FL&md5=bc65b49d5abe93e684bd4c99dcf53565CAS | 15286031PubMed |
El Shourbagy, S. H., Spikings, E. C., Freitas, M., and St John, J. C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–245.
| Mitochondria directly influence fertilisation outcome in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsL4%3D&md5=81e347d8550baa8858c909052e562a0dCAS | 16452717PubMed |
Han, S. J., Vaccari, S., Nedachi, T., Andersen, C. B., Kovacina, K. S., Roth, R. A., and Conti, M. (2006). Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. EMBO J. 25, 5716–5725.
| Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlShsbzO&md5=98d991b44d424e5371aad6e886612c0aCAS | 17124499PubMed |
Hsieh, R. H., Au, H. K., Yeh, T. S., Chang, S. J., Cheng, Y. F., and Tzeng, C. R. (2004). Decreased expression of mitochondrial genes in human unfertilized oocytes and arrested embryos. Fertil. Steril. 81, 912–918.
| Decreased expression of mitochondrial genes in human unfertilized oocytes and arrested embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitFGhsb8%3D&md5=5245c70bfce2d07fb11db6e1a614551dCAS | 15019829PubMed |
Hsieh, M., Lee, D., Panigone, S., Homer, K., Chen, R., Theologis, A., Lee, D. C., Threadgill, D. W., and Conti, M. (2007). Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol. Cell. Biol. 27, 1914–1924.
| Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1Wgu74%3D&md5=be93cc934352fca4b72bf486bd6342ddCAS | 17194751PubMed |
Hussein, T. S., Thompson, J. G., and Gilchrist, R. B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–521.
| Oocyte-secreted factors enhance oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2gsb4%3D&md5=00c769153fa81c05146e56febba70e9dCAS | 16854407PubMed |
Jablonka-Shariff, A., Roser, J. F., Bousfield, G. R., Michael, W. W., Sibley, L. E., Colgin, M., and Boime, I. (2007). Expression and bioactivity of a single chain recombinant equine luteinizing hormone (reLH). Theriogenology 67, 311–320.
| Expression and bioactivity of a single chain recombinant equine luteinizing hormone (reLH).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhtlars7rF&md5=891b48c636f24cfc5e35d0d992dbb470CAS | 17049590PubMed |
Jansen, R. P. S., and Burton, G. J. (2004). Mitochondrial dysfunction in reproduction. Mitochondrion 4, 577–600.
| Mitochondrial dysfunction in reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCgs7nL&md5=6c0d80df249e567234fa46943a6eb5e7CAS |
Jin, S. L. C., Richard, F. J., Kuo, W. P., D’Ercole, A. J., and Conti, M. (1999). Impaired growth and fertility of cAMP-specific phosphodiesterase PDE4D-deficient mice. Proc. Natl Acad. Sci. USA 96, 11 998–12 003.
| Impaired growth and fertility of cAMP-specific phosphodiesterase PDE4D-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvVGjsLY%3D&md5=e0f45a6459ada27c0c0a482a91fdad49CAS |
Juengel, J. L., and McNatty, K. P. (2005). The role of proteins of the transforming growth factor-β superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 11, 144–161.
| The role of proteins of the transforming growth factor-β superfamily in the intraovarian regulation of follicular development.Crossref | GoogleScholarGoogle Scholar |
Ledent, C., Demeestere, I., Blum, D., Petermans, J., Hamalainen, T., Smits, G., and Vassart, G. (2005). Premature ovarian aging in mice deficient for Gpr3. Proc. Natl Acad. Sci. USA 102, 8922–8926.
| Premature ovarian aging in mice deficient for Gpr3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvF2qu78%3D&md5=967766b379cd5c6b4b241f760608f4b1CAS | 15956199PubMed |
Li, X., Qin, Y., Wilsher, S., and Allen, W. R. (2006). Centrosome changes during meiosis in horse oocytes and first embryonic cell cycle organization following parthenogenesis, fertilization and nuclear transfer. Reproduction 131, 661–667.
| Centrosome changes during meiosis in horse oocytes and first embryonic cell cycle organization following parthenogenesis, fertilization and nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jtrw%3D&md5=89cc53f02cde381c0ca2dd5253877047CAS | 16595717PubMed |
Lindbloom, S. M., Farmerie, T. A., Clay, C. M., Seidel, G. E., and Carnevale, E. M. (2008). Potential involvement of EGF-like growth factors and phosphodiesterases in initiation of equine oocyte maturation. Anim. Reprod. Sci. 103, 187–192.
| Potential involvement of EGF-like growth factors and phosphodiesterases in initiation of equine oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWktb3L&md5=2a3e7d44535d42c669984780373c5e80CAS | 17507186PubMed |
Liu, X., Xie, F., Zamah, A. M., Cao, B., and Conti, M. (2014). Multiple pathways mediate luteinizing hormone regulation of cGMP signaling in the mouse ovarian follicle. Biol. Reprod. 91, 9.
| Multiple pathways mediate luteinizing hormone regulation of cGMP signaling in the mouse ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 24740605PubMed |
Masciarelli, S., Horner, K., Liu, C. Y., Park, S. H., Hinckley, M., Hockman, S., Nedachi, T., Jin, C., Conti, M., and Manganiello, V. (2004). Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J. Clin. Invest. 114, 196–205.
| Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFWmsLk%3D&md5=e274028cca39566a35c1076a82317b9fCAS | 15254586PubMed |
Mayes, M. A., and Sirard, M. A. (2002). Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol. Reprod. 66, 180–184.
| Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1yrsw%3D%3D&md5=11589bdcc85f3d7bd31615f4e41350fbCAS | 11751280PubMed |
McConnell, J. M. L., and Petrie, L. (2004). Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors. Reprod. Biomed. Online 9, 418–424.
| Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlKqsLk%3D&md5=3d95f9b5a7b39dee1924989d0268ac73CAS |
Mehlmann, L. M. (2005a). Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes. Dev. Biol. 288, 397–404.
| Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlaitrvP&md5=6ec143388b36bc17a21cede0c72af253CAS | 16289135PubMed |
Mehlmann, L. M. (2005b). 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=61121f4380f8ed09af6ae5eddb9e4d03CAS | 16322539PubMed |
Mehlmann, L. M., Saeki, Y., Tanaka, S., Brennan, T. J., Evsikov, A. V., Pendola, F. L., Knowles, B. B., Eppig, J. J., and Jaffe, L. A. (2004). The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306, 1947–1950.
| The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCqtbvE&md5=f2286891d51c88ba9db6de62f7872610CAS | 15591206PubMed |
Menon, K. M., Munshi, U. M., Clouser, C. L., and Nair, A. K. (2004). Regulation of luteinizing hormone/human chorionic gonadotropin receptor expression: a perspective. Biol. Reprod. 70, 861–866.
| Regulation of luteinizing hormone/human chorionic gonadotropin receptor expression: a perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1SitLc%3D&md5=f9de641ceae60a2721421c0947940a11CAS | 14668203PubMed |
Nivet, A. L., Vigneault, C., Blondin, P., and Sirard, M. A. (2013). Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine. Reproduction 145, 555–565.
| Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWmsbnJ&md5=8a194321f5685bf0e66c802d68d56cb7CAS | 23564726PubMed |
Panigone, S., Hsieh, M., Fu, M., Persani, L., and Conti, M. (2008). LH signaling in preovulatory follicles involves early activation of the EGFR pathway. Mol. Endocrinol. 22, 924–936.
| LH signaling in preovulatory follicles involves early activation of the EGFR pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkt1Cnsbs%3D&md5=03c7d3fbd1ae4836d5bcc0c8a31cacaeCAS | 18187604PubMed |
Park, J. Y., Richard, F., Chun, S. Y., Park, J. H., Law, E., Horner, K., Jin, S. L. C., and Conti, M. (2003). Phosphodiesterase regulation is critical for the differentiation and pattern of gene expression in granulosa cells of the ovarian follicle. Mol. Endocrinol. 17, 1117–1130.
| Phosphodiesterase regulation is critical for the differentiation and pattern of gene expression in granulosa cells of the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlymtrs%3D&md5=ece8280dae4e31e5b85298885a8f72c3CAS | 12649328PubMed |
Park, J. Y., Su, Y. Q., Ariga, M., Law, E., Jin, S. L. C., and Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.
| EGF-like growth factors as mediators of LH action in the ovulatory follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVKlsg%3D%3D&md5=5d954a7ad7a1fe0e2878c16ac4ee2563CAS | 14726596PubMed |
Rambags, B. P. B., van Boxtel, D. C. J., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. E. (2006). Maturation in vitro leads to mitochondrial degeneration in oocytes recovered from aged but not young mares. Anim. Reprod. Sci. 94, 359–361.
| Maturation in vitro leads to mitochondrial degeneration in oocytes recovered from aged but not young mares.Crossref | GoogleScholarGoogle Scholar |
Rambags, B. P. B., van Boxtel, D. C. J., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. E. (2014). Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology 81, 959–965.
| Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsF2gurc%3D&md5=ad6e368a68b30907f0750967a230eb4dCAS |
Reader, K. L., Mottershead, D. G., Martin, G. A., Gilchrist, R. B., Heath, D. A., McNatty, K. P., and Juengel, J. L. (2014). Signalling pathways involved in the synergistic effects of human growth differentiation factor 9 and bone morphogenetic protein 15. Reprod. Fertil. Dev. , .
| Signalling pathways involved in the synergistic effects of human growth differentiation factor 9 and bone morphogenetic protein 15.Crossref | GoogleScholarGoogle Scholar | 25155366PubMed |
Reynier, P., May-Panloup, P., Chretien, M. F., Morgan, C. J., Jean, M., Savagner, F., Barriere, P., and Malthiery, Y. (2001). Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 7, 425–429.
| Mitochondrial DNA content affects the fertilizability of human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1CqsLg%3D&md5=0085b23718f670a2255c713cfb0e4dc4CAS | 11331664PubMed |
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=d847447d2275c237c388d327df4b96cbCAS | 11673261PubMed |
Ridge, P. G., Maxwell, T. J., Foutz, S. J., Bailey, M. H., Corcoran, C. D., Tschanz, J. T., Norton, M. C., Munger, R. G., O’Brien, E., Kerber, R. A., Cawthon, R. M., and Kauwe, J. S. (2014). Mitochondrial genomic variation associated with higher mitochondrial copy number: the Cache County Study on Memory Health and Aging. BMC Bioinformatics 15, S6.
| Mitochondrial genomic variation associated with higher mitochondrial copy number: the Cache County Study on Memory Health and Aging.Crossref | GoogleScholarGoogle Scholar | 25077862PubMed |
Santos, T. A., El Shourbagy, S., and St John, J. C. (2006). Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584–591.
| Mitochondrial content reflects oocyte variability and fertilization outcome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVChsr0%3D&md5=44608f7ae2e3ffae80f03b8cd2a33e56CAS | 16500323PubMed |
Sayasith, K., Lussier, J., Dore, M., and Sirois, J. (2013). Human chorionic gonadotropin-dependent up-regulation of epiregulin and amphiregulin in equine and bovien follicles during the ovulatory process. Gen. Comp. Endocrinol. 180, 39–47.
| Human chorionic gonadotropin-dependent up-regulation of epiregulin and amphiregulin in equine and bovien follicles during the ovulatory process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2rsbjM&md5=6b470b921bd1b77c92fe337631aa397aCAS | 23178756PubMed |
Sherman, G. B., Wolfe, M. W., Farmerie, T. A., Clay, C. M., Threadgill, D. S., Sharp, D. C., and Nilson, J. H. (1992). A single gene encodes the beta-subunits of equine luteinizing hormone and chorionic gonadotropin. Mol. Endocrinol. 6, 951–959.
| 1:CAS:528:DyaK3sXkt1Wlt78%3D&md5=e95cb2f0275728e99a6f97baa2605186CAS | 1379674PubMed |
Shimada, M., Hernandez-Gonzalez, I., Gonzalez-Robayna, I., and Richards, J. S. (2006). Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol. Endocrinol. 20, 1352–1365.
| Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlSrsb8%3D&md5=ad79a247f77c76a270922ac73fba667dCAS | 16543407PubMed |
Shoubridge, E. A., and Wai, T. (2007). Mitochondrial DNA and the mammalian oocyte. Curr. Top. Dev. Biol. 77, 87–111.
| Mitochondrial DNA and the mammalian oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltbo%3D&md5=121c7deb6e125bf1e015b31d783cab46CAS | 17222701PubMed |
Siddiqui, M. A., Gastal, E. L., Ju, J. C., Gastal, M. O., Beg, M. A., and Ginther, O. J. (2009). Nuclear configuration, spindle morphology and cytoskeletal organization of in vivo maturing horse oocytes. Reprod. Domest. Anim. 44, 435–440.
| Nuclear configuration, spindle morphology and cytoskeletal organization of in vivo maturing horse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrisFWgsA%3D%3D&md5=55bed0afa48922001990e8dbb8b8a0f3CAS | 18992126PubMed |
Su, Y. Q., Sugiura, K., Wigglesworth, K., O’Brien, M. J., Affourtit, J. P., Pangas, S. A., Matzuk, M. M., and Eppig, J. J. (2008). Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135, 111–121.
| Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhslGmtLw%3D&md5=65193b8da0288818ca87dc566ac4a04bCAS | 18045843PubMed |
Sugiura, K., Su, Y. Q., Diaz, F. J., Pangas, S. A., Sharma, S., Wigglesworth, K., O’Brien, M. J., Matzuk, M. M., Shimasaki, S., and Eppig, J. J. (2007). Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134, 2593–2603.
| Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsFeju7k%3D&md5=df54766b689a7f23fed934c7886c6656CAS | 17553902PubMed |
Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (2000). Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol. Reprod. 63, 582–590.
| Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltl2gurw%3D&md5=340cbccfa16c7fe9092bf2e5d5abc5e9CAS | 10906068PubMed |
Swinnin, J. V., Jospeh, D. R., and Conti, M. (1989). The mRNA encoding a high-affinity cAMP phophodiesterase is regulated by hormones and cAMP. Proc. Natl. Acad. Sci. USA 86, 8197–8201.
Thundathil, J., Filion, F., and Smith, L. C. (2005). Molecular control of mitochondrial function in preimplantation mouse embryos. Mol. Reprod. Dev. 71, 405–413.
| Molecular control of mitochondrial function in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFSltLk%3D&md5=9a7b046ebc00c7c939ee51773ec88e58CAS | 15895466PubMed |
Tsafriri, A., Chun, S. Y., Zhang, R., Hsueh, A. J. W., and Conti, M. (1996). Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178, 393–402.
| Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvVCksr0%3D&md5=a290a08816c0869dda377fcd1255875fCAS | 8812137PubMed |
Wai, T., Asangla, A., Zhang, Z., Cyr, D., Dufort, D., and Shoubridge, E. A. (2010). The role of mitochondrial DNA copy nuber in mammalian fertility. Biol. Reprod. 83, 52–62.
| The role of mitochondrial DNA copy nuber in mammalian fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqtLo%3D&md5=46ce3598089e81edd1f349205c92f95eCAS | 20130269PubMed |
Wang, L. Y., Wang, D. H., Zou, X. Y., and Xu, C. M. (2009). Mitochondrial functions on oocytes and preimplantation embryos. J. Zhejiang Univ. Sci. B 10, 483–492.
| Mitochondrial functions on oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotV2qtbo%3D&md5=25f23923fe2676d4a98906ce43e41c31CAS | 19585665PubMed |
Yan, C., Wang, P., DeMayo, J., DeMayo, F. J., Elvin, J. A., Carino, C., Prasad, S. V., Skinner, S. S., Dunbar, B. S., Dube, J. L., Celeste, A. J., and Matzuk, M. M. (2001). Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 15, 854–866.
| Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFKjs7o%3D&md5=79174391908d5b54202aa63d2bf763dfCAS | 11376106PubMed |
Yeo, C. X., Gilchrist, R. B., Thompson, J. G., and Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 67–73.
| Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWgsbzF&md5=fee97cfb36229062f98153978300e40aCAS | 17933754PubMed |
Yoon, M. J., Bolme, I., Colgin, M., Niswender, K. D., King, S. S., Alvarenga, M., Jablonka-Shariff, A., Pearl, C. A., and Roser, J. F. (2007). The efficacy of a single chain recombinant equine luteinizing hormone (reLH) in mares: Induction of ovulation, hormone profiles, and inter-ovulatory intervals. Domest. Anim. Endocrinol. 33, 470–479.
| The efficacy of a single chain recombinant equine luteinizing hormone (reLH) in mares: Induction of ovulation, hormone profiles, and inter-ovulatory intervals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFenu7rO&md5=ec42c7c343221fc30977cbd773a4b72aCAS | 17658237PubMed |