Global gene expression in the bovine corpus luteum is altered after stimulatory and superovulatory treatments
Luciana A. Fátima A E , Pietro S. Baruselli B , Lindsay U. Gimenes B , Mario Binelli B , Francisco P. Rennó C , Bruce D. Murphy D and Paula C. Papa AA Sector of Anatomy, Department of Surgery, Faculty of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo – SP, 05508-270 Brazil.
B Department of Animal Reproduction, Faculty of Veterinary Medicine and Animal Science, University of São Paulo, Pirassununga – SP, 13635-900, Brazil.
C Department of Nutrition and Animal Production, Faculty of Veterinary Medicine and Animal Science, University of São Paulo, Pirassununga – SP, 13635-900, Brazil.
D Animal Reproduction Research Centre (CRRA), University of Montreal, St-Hyacinthe, QC J2S 7C6, Canada.
E Corresponding author. Email: lubiologia2000@yahoo.com.br
Reproduction, Fertility and Development 25(7) 998-1011 https://doi.org/10.1071/RD12155
Submitted: 17 May 2012 Accepted: 5 September 2012 Published: 30 October 2012
Abstract
Equine chorionic gonadotrophin (eCG) has been widely used in superovulation and artificial insemination programmes and usually promotes an increase in corpus luteum (CL) volume and stimulates progesterone production. Therefore, to identify eCG-regulated genes in the bovine CL, the transcriptome was evaluated by microarray analysis and the expression of selected genes was validated by qPCR and western blot. Eighteen Nelore crossbred cows were divided into control (n = 5), stimulated (n = 6) and superovulated groups (n = 7). Ovulation was synchronised using a progesterone device-based protocol. Stimulated animals received 400 IU of eCG at device removal and superovulated animals received 2000 IU of eCG 4 days prior. Corpora lutea were collected 7 days after gonadotrophin-releasing hormone administration. Overall, 242 transcripts were upregulated and 111 transcripts were downregulated in stimulated cows (P ≤ 0.05) and 111 were upregulated and 113 downregulated in superovulated cows compared to the control animals (1.5-fold, P ≤ 0.05). Among the differentially expressed genes, many were involved in lipid biosynthesis and progesterone production, such as PPARG, STAR, prolactin receptors and follistatin. In conclusion, eCG modulates gene expression differently depending on the treatment, i.e. stimulatory or superovulatory. Our data contribute to the understanding of the pathways involved in increased progesterone levels observed after eCG treatment.
Additional keywords : eCG, follistatin, lipid metabolism, progesterone, prolactin receptors, PPARG.
References
Ambrose, J. D., Drost, M., Monson, R. L., Rutledge, J. J., Leibfried-Rutledge, M. L., Thatcher, M. J., Kassa, T., Binelli, M., Hansen, P. J., Chenoweth, P. J., and Thatcher, W. W. (1999). Efficacy of timed embryo transfer with fresh and frozen in vitro-produced embryos to increase pregnancy rates in heat-stressed dairy cattle. J. Dairy Sci. 82, 2369–2376.| Efficacy of timed embryo transfer with fresh and frozen in vitro-produced embryos to increase pregnancy rates in heat-stressed dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnsVGnur8%3D&md5=31bbb485b37130ab0e4514533926f1fdCAS | 10575603PubMed |
Baruselli, P. S., Ferreira, R. M., Sales, J. N., Gimenes, L. U., Sá Filho, M. F., Martins, C. M., Rodrigues, C. A., and Bó, G. A. (2011). Timed embryo transfer programs for management of donor and recipient cattle. Theriogenology 76, 1583–1593.
| Timed embryo transfer programs for management of donor and recipient cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbnvVSkug%3D%3D&md5=5397fb89fa396ae40f1092ebfa4c50d4CAS | 21798580PubMed |
Baruselli, P. S., Sá Filho, M. F., Ferreira, R. M., Sales, J., Gimenes, L. U., Vieira, L., Mendanha, M., and Bó, G. A. (2012). Manipulation of follicle development to ensure optimal oocyte quality and conception rates in cattle. Reprod. Domest. Anim. 47, 134–141.
| Manipulation of follicle development to ensure optimal oocyte quality and conception rates in cattle.Crossref | GoogleScholarGoogle Scholar | 22827362PubMed |
Belfiore, C. J., Hawkins, D. E., Wiltbank, M. C., and Niswender, G. D. (1994). Regulation of cytochrome P450scc synthesis and activity in the ovine corpus luteum. J. Steroid Biochem. Mol. Biol. 51, 283–290.
| Regulation of cytochrome P450scc synthesis and activity in the ovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsV2itro%3D&md5=5ee5e3ff2d380b0eb310b65af2651b61CAS | 7826890PubMed |
Binelli, M., Thatcher, W. W., Mattos, R., and Baruselli, P. S. (2001). Antiluteolytic strategies to improve fertility in cattle. Theriogenology 56, 1451–1463.
| Antiluteolytic strategies to improve fertility in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjslyqtg%3D%3D&md5=4916d789bb2545c9bb852c011c2e9819CAS | 11768810PubMed |
Bó, G. A., Baruselli, P. S., Moreno, D., Cutaia, L., Caccia, M., Tríbulo, R., Tríbulo, H., and Mapletoft, R. J. (2002). The control of follicular wave development for self-appointed embryo transfer programs in cattle. Theriogenology 57, 53–72.
| The control of follicular wave development for self-appointed embryo transfer programs in cattle.Crossref | GoogleScholarGoogle Scholar | 11775981PubMed |
Bole-Feysot, C., Goffin, V., Edery, M., Binart, N., and Kelly, P. A. (1998). Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr. Rev. 19, 225–268.
| Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVWhs7k%3D&md5=1718da2407efbb290f5df4aaa9c5c13eCAS | 9626554PubMed |
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=a7b3d941b2d4571e1bf03cdd05e3fd69CAS | 942051PubMed |
Brannian, J. D., and Stouffer, R. L. (1993). Native and modified (acetylated) low-density lipoprotein-supported steroidogenesis by macaque granulosa cells collected before and after the ovulatory stimulus: correlation with fluorescent lipoprotein uptake. Endocrinology 132, 591–597.
| Native and modified (acetylated) low-density lipoprotein-supported steroidogenesis by macaque granulosa cells collected before and after the ovulatory stimulus: correlation with fluorescent lipoprotein uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhsVSisL8%3D&md5=f92be22515d32a081486a0a81f4dab35CAS | 8425479PubMed |
Chmurzyńska, A. (2006). The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J. Appl. Genet. 47, 39–48.
| The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism.Crossref | GoogleScholarGoogle Scholar | 16424607PubMed |
Christenson, L. K., and Devoto, L. (2003). Cholesterol transport and steroidogenesis by the corpus luteum. Reprod. Biol. Endocrinol. 1, 90.
| Cholesterol transport and steroidogenesis by the corpus luteum.Crossref | GoogleScholarGoogle Scholar | 14613534PubMed |
Chung, S., Wang, S. P., Pan, L., Mitchell, G., Trasler, J., and Hermo, L. (2001). Infertility and testicular defects in hormone-sensitive lipase-deficient mice. Endocrinology 142, 4272–4281.
| Infertility and testicular defects in hormone-sensitive lipase-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1ert74%3D&md5=9c6defe2db77b20d2dc30fc762f86771CAS | 11564684PubMed |
Clemente, M., de La Fuente, J., Fair, T., Al Naib, A., Gutierrez-Adan, A., Roche, J. F., Rizos, D., and Lonergan, P. (2009). Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction 138, 507–517.
| Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOgtrvL&md5=2ff4b3a7df99df984f790c7a6990d1f5CAS | 19556439PubMed |
Coleman, R. A., Lewin, T. M., Van Horn, C. G., and Gonzalez-Baró, M. R. (2002). Do long-chain acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? J. Nutr. 132, 2123–2126.
| 1:CAS:528:DC%2BD38XmtF2qsL0%3D&md5=a018836c689f66a2335b178deb4a9e9dCAS | 12163649PubMed |
Devoto, L., Vega, M., Kohen, P., Castro, A., Castro, O., Christenson, L. K., Carvallo, P., and Strauss, J. F. (2000). Endocrine and paracrine–autocrine regulation of the human corpus luteum during the mid-luteal phase. J. Reprod. Fertil. Suppl. 55, 13–20.
| 1:CAS:528:DC%2BD3cXjsFaktrs%3D&md5=0500342e54acb7b08bfe46634693fb6bCAS | 10889830PubMed |
Doody, K. J., Lorence, M. C., Mason, J. I., and Simpson, E. R. (1990). Expression of messenger ribonucleic acid species encoding steroidogenic enzymes in human follicles and corpora lutea throughout the menstrual cycle. J. Clin. Endocrinol. Metab. 70, 1041–1045.
| Expression of messenger ribonucleic acid species encoding steroidogenic enzymes in human follicles and corpora lutea throughout the menstrual cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXit12rt78%3D&md5=43c4207dff86f0d4c6353f1dd72a6073CAS | 2180973PubMed |
Fields, S. D., Gebhart, K. L., Perry, B. L., Gonda, M. G., Wright, C. L., Bott, R. C., and Perry, G. A. (2012). Influence of standing oestrus before an injection of GnRH during a beef cattle fixed-time AI protocol on LH release, subsequent concentrations of progesterone and steroidogenic enzyme expression. Domest. Anim. Endocrinol. 42, 11–19.
| Influence of standing oestrus before an injection of GnRH during a beef cattle fixed-time AI protocol on LH release, subsequent concentrations of progesterone and steroidogenic enzyme expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1SlurrJ&md5=ecb0e7b28a66f596bde898bc44074a1bCAS | 22019093PubMed |
Findlay, J. K. (1993). An update on the roles of inhibin, activin and follistatin as local regulators of folliculogenesis. Biol. Reprod. 48, 15–23.
| An update on the roles of inhibin, activin and follistatin as local regulators of folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlt1GntQ%3D%3D&md5=7af1891e66e34942f34876887b6fa7f9CAS | 8418903PubMed |
Furuhashi, M., and Hotamisligil, G. S. (2008). Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat. Rev. Drug Discov. 7, 489–503.
| Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVOjsbk%3D&md5=82b9db95a332677cb70363b97e417d45CAS | 18511927PubMed |
Garcia-Bojalil, C. M., Staples, C. R., Risco, C. A., Savio, J. D., and Thatcher, W. W. (1998). Protein degradability and calcium salts of long-chain fatty acids in the diets of lactating dairy cows: reproductive responses. J. Dairy Sci. 81, 1385–1395.
| Protein degradability and calcium salts of long-chain fatty acids in the diets of lactating dairy cows: reproductive responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsVyjsr0%3D&md5=f5cc4bb12dd8cff8a4d4d03277eb743dCAS | 9621242PubMed |
Golos, T. G., and Strauss, J. F. (1988). 8-bromoadenosine cyclic 3′,5′-phosphate rapidly increases 3-hydroxy-3-methylglutaryl coenzyme A reductase mRNA in human granulosa cells: role of cellular sterol balance in controlling the response to tropic stimulation. Biochemistry 27, 3503–3506.
| 8-bromoadenosine cyclic 3′,5′-phosphate rapidly increases 3-hydroxy-3-methylglutaryl coenzyme A reductase mRNA in human granulosa cells: role of cellular sterol balance in controlling the response to tropic stimulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvVChtr8%3D&md5=7ccd24d9d721b59c764f8c597b309b20CAS | 3390448PubMed |
Grosdemouge, I., Bachelot, A., Lucas, A., Baran, N., Kelly, P. A., and Binart, N. (2003). Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod. Biol. Endocrinol. 1, 12.
| Effects of deletion of the prolactin receptor on ovarian gene expression.Crossref | GoogleScholarGoogle Scholar | 12646063PubMed |
Gwynne, J. T., and Strauss, J. F. (1982). The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands. Endocr. Rev. 3, 299–329.
| The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xlt1Smu7o%3D&md5=76cd73dea7cad74ce4f6838a9237e0dbCAS | 6288367PubMed |
Hansen, P. J., Drost, M., Rivera, R. M., Paula-Lopes, F. F., al-Katanani, Y. M., Krininger, C. E., and Chase, C. C. (2001). Adverse impact of heat stress on embryo production: causes and strategies for mitigation. Theriogenology 55, 91–103.
| Adverse impact of heat stress on embryo production: causes and strategies for mitigation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7nslaqtw%3D%3D&md5=37832f9752e4d6b73c8a448123cd2ca0CAS | 11198091PubMed |
Haunerland, N. H., and Spener, F. (2004). Fatty acid-binding proteins – insights from genetic manipulations. Prog. Lipid Res. 43, 328–349.
| Fatty acid-binding proteins – insights from genetic manipulations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVSgsrY%3D&md5=12bd292d8764eff6c4295da429033304CAS | 15234551PubMed |
Hennebold, J. D. (2004). Characterization of the ovarian transcriptome through the use of differential analysis of gene expression methodologies. Hum. Reprod. Update 10, 227–239.
| Characterization of the ovarian transcriptome through the use of differential analysis of gene expression methodologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktFCqsLc%3D&md5=cf7d1b61fcc925552c3c406bc125e6fdCAS | 15140870PubMed |
Hillier, S. G., and Miró, F. (1993). Inhibin, activin and follistatin. Potential roles in ovarian physiology. Ann. N. Y. Acad. Sci. 687, 29–38.
| Inhibin, activin and follistatin. Potential roles in ovarian physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltV2is7g%3D&md5=492ff52701a2af2915569f0f6ce00ca4CAS | 8323185PubMed |
Juengel, J. L., Nett, T. M., Anthony, R. V., and Niswender, G. D. (1997). Effects of luteotrophic and luteolytic hormones on expression of mRNA encoding insulin-like growth factor I and growth hormone receptor in the ovine corpus luteum. J. Reprod. Fertil. 110, 291–298.
| Effects of luteotrophic and luteolytic hormones on expression of mRNA encoding insulin-like growth factor I and growth hormone receptor in the ovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFKrs7g%3D&md5=19fcba4a170d230b6c94568179be6750CAS | 9306983PubMed |
Kaipainen, A., Korhonen, J., Mustonen, T., van Hinsbergh, V. W., Fang, G. H., Dumont, D., Breitman, M., and Alitalo, K. (1995). Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc. Natl. Acad. Sci. USA 92, 3566–3570.
| Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXltFSmsLg%3D&md5=fd04a2e2bece117c330e3697988c4090CAS | 7724599PubMed |
Kliewer, S. A., Sundseth, S. S., Jones, S. A., Brown, P. J., Wisely, G. B., Koble, C. S., Devchand, P., Wahli, W., Willson, T. M., Lenhard, J. M., and Lehmann, J. M. (1997). Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proc. Natl. Acad. Sci. USA 94, 4318–4323.
| 1:CAS:528:DyaK2sXjtVyht7w%3D&md5=d6670b370ccca21ee45971b852c1a0b6CAS | 9113987PubMed |
Komar, C. M. (2005). Peroxisome proliferator-activated receptors (PPARs) and ovarian function – implications for regulating steroidogenesis, differentiation and tissue remodelling. Reprod. Biol. Endocrinol. 3, 41.
| Peroxisome proliferator-activated receptors (PPARs) and ovarian function – implications for regulating steroidogenesis, differentiation and tissue remodelling.Crossref | GoogleScholarGoogle Scholar | 16131403PubMed |
Kraemer, F. B., Patel, S., Singh-Bist, A., Gholami, S. S., Saedi, M. S., and Sztalryd, C. (1993). Detection of hormone-sensitive lipase in various tissues. II. Regulation in the rat testis by human chorionic gonadotrophin. J. Lipid Res. 34, 609–616.
| 1:CAS:528:DyaK3sXisVOqt7w%3D&md5=7bc7b46c5d96f10aaef0cfae7ec77407CAS | 8496666PubMed |
Labrie, F., Simard, J., Luu-The, V., Pelletier, G., Belanger, A., Lachance, Y., Zhao, H.F., Labrie, C., Breton, N., de Launoit, Y., et al. (1992). Structure and tissue-specific expression of 3 beta-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase genes in human and rat classical and peripheral steroidogenic tissues. J. Steroid Biochem. Mol. Biol. 41, 421–435.
| Structure and tissue-specific expression of 3 beta-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase genes in human and rat classical and peripheral steroidogenic tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsVGksLc%3D&md5=1bb8a45572a3e7c6c9d1a587a407b3fbCAS | 1562516PubMed |
Lawrence, D. A. (1996). Transforming growth factor-beta: a general review. Eur. Cytokine Netw. 7, 363–374.
| 1:CAS:528:DyaK28Xmt1yqt7c%3D&md5=4f81f93d3cecf57a84190d5acebbf464CAS | 8954178PubMed |
Li, Q., Jimenez-Krassel, F., Ireland, J. J., and Smith, G. W. (2009). Gene expression profiling of bovine preovulatory follicles: gonadotrophin surge and prostanoid-dependent up-regulation of genes potentially linked to the ovulatory process. Reproduction 137, 297–307.
| Gene expression profiling of bovine preovulatory follicles: gonadotrophin surge and prostanoid-dependent up-regulation of genes potentially linked to the ovulatory process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ksLs%3D&md5=ee93bbfe7442202a017ad0b643dcf915CAS | 18996975PubMed |
Lin, D., Sugawara, T., Strauss, J. F., Clark, B. J., Stocco, D. M., Saenger, P., Rogol, A., and Miller, W. L. (1995). Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 267, 1828–1831.
| Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkslWgtb0%3D&md5=8876a5a6b89bdf1a6c5c2a5bf282112bCAS | 7892608PubMed |
Liu, Z., Rudd, M. D., Hernandez-Gonzalez, I., Gonzalez-Robayna, I., Fan, H. Y., Zeleznik, A. J., and Richards, J. S. (2009). FSH and FOXO1 regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells. Mol. Endocrinol. 23, 649–661.
| FSH and FOXO1 regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFCgtrw%3D&md5=8a58bb6bd1cc64b1b82c506704ec3843CAS | 19196834PubMed |
Madureira, E. H. (2004). Sincronização com progestágenos. Biotecnologia da reprodução em bovinos 1, 117–128.
Matsuyama, S., and Takahashi, M. (1995). Immunoreactive (ir)-transforming growth factor (TGF)-beta in rat corpus luteum: ir-TGF beta is expressed by luteal macrophages. Endocr. J. 42, 203–217.
| Immunoreactive (ir)-transforming growth factor (TGF)-beta in rat corpus luteum: ir-TGF beta is expressed by luteal macrophages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntlSmsLg%3D&md5=f4137c4aee7064ad3b366ec74297a357CAS | 7627265PubMed |
Miller, W. L. (1988). Molecular biology of steroid hormone synthesis. Endocr. Rev. 9, 295–318.
| Molecular biology of steroid hormone synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlvVemtbw%3D&md5=f9ed1eb64e0109c6626a69e56201a656CAS | 3061784PubMed |
Miller, W. L. (2007). Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. Biochim. Biophys. Acta 1771, 663–676.
| Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlWgtr4%3D&md5=59bb5ac8816da4ccb583f1d5cbad5d64CAS | 17433772PubMed |
Murphy, B. D., and Martinuk, S. D. (1991). Equine chorionic gonadotrophin. Endocr. Rev. 12, 27–44.
| Equine chorionic gonadotrophin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlt1Oiu7k%3D&md5=456531f3ba1168c8362f7817afe8ff9eCAS | 2026120PubMed |
Niswender, G. D. (2002). Molecular control of luteal secretion of progesterone. Reproduction 123, 333–339.
| Molecular control of luteal secretion of progesterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Clsr8%3D&md5=0bdb043c857dc7f746163c279eb2cee6CAS | 11882010PubMed |
Niswender, G. D., and Nett, T. M. (1994). The corpus luteum and its control in infraprimate species. In ‘The Physiology of Reproduction’. (Eds E. Knobil and J. D. Neill.) pp. 781–816. (Roven Press 1: New York.)
Niswender, G. D., Juengel, J. L., McGuire, W. J., Belfiore, C. J., and Wiltbank, M. C. (1994). Luteal function: the oestrous cycle and early pregnancy. Biol. Reprod. 50, 239–247.
| Luteal function: the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVeju7w%3D&md5=15b140bfa64842f9fd3e0c749de5f3d8CAS | 8142542PubMed |
Nogueira, M. F., Melo, D. S., Carvalho, L. M., Fuck, E. J., Trinca, L. A., and Barros, C. M. (2004). Do high progesterone concentrations decrease pregnancy rates in embryo recipients synchronized with PGF2alpha and eCG? Theriogenology 61, 1283–1290.
| Do high progesterone concentrations decrease pregnancy rates in embryo recipients synchronized with PGF2alpha and eCG?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVOmtbg%3D&md5=a0b2f2d6c048bf2d0e847ee56577ca1fCAS | 15036962PubMed |
Papa, P. C., Moura, C. E., Artoni, L. P., Fátima, L. A., Campos, D. B., Marques, J. E., Baruselli, P. S., Binelli, M., Pfarrer, C., and Leiser, R. (2007). VEGF system expression in different stages of oestrous cycle in the corpus luteum of non-treated and superovulated water buffalo. Domest. Anim. Endocrinol. 33, 379–389.
| VEGF system expression in different stages of oestrous cycle in the corpus luteum of non-treated and superovulated water buffalo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFenu77F&md5=2cbeffcddb14c80a45f86627ea32a76fCAS | 17014980PubMed |
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
| A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=54b36b3c1054987092ad32dfe1b8f6acCAS | 11328886PubMed |
Picazo, R. A., García Ruiz, J. P., Santiago Moreno, J., González de Bulnes, A., Muñoz, J., Silván, G., Lorenzo, P. L., and Illera, J. C. (2004). Cellular localization and changes in expression of prolactin receptor isoforms in sheep ovary throughout the oestrous cycle. Reproduction 128, 545–553.
| Cellular localization and changes in expression of prolactin receptor isoforms in sheep ovary throughout the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSis7jL&md5=44ffe513ea9b62bebbfe0d55ce11b418CAS | 15509700PubMed |
Ramakers, C., Ruijter, J. M., Deprez, R. H., and Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–66.
| Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1Kks70%3D&md5=e52aa9c386e7ff8008cfd9fb23cf2240CAS | 12618301PubMed |
Rennert, H., Fischer, R. T., Alvarez, J. G., Trzaskos, J. M., and Strauss, J. F. (1990). Generation of regulatory oxysterols: 26-hydroxylation of cholesterol by ovarian mitochondria. Endocrinology 127, 738–746.
| Generation of regulatory oxysterols: 26-hydroxylation of cholesterol by ovarian mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlt1KksLg%3D&md5=b59fc1b15184ca6893030bf2a00d5477CAS | 2373053PubMed |
Richards, R. G., and Almond, G. W. (1994). Tumour necrosis factor-alpha differentially alters progesterone and prostaglandin F2 alpha production by porcine luteal cells. J. Endocrinol. 143, 75–83.
| Tumour necrosis factor-alpha differentially alters progesterone and prostaglandin F2 alpha production by porcine luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1yms7s%3D&md5=ff30fab43178c92c06b595e28f36ce13CAS | 7964324PubMed |
Roberts, A. J., and Skinner, M. K. (1991). Transforming growth factor-alpha and -beta differentially regulate growth and steroidogenesis of bovine thecal cells during antral follicle development. Endocrinology 129, 2041–2048.
| Transforming growth factor-alpha and -beta differentially regulate growth and steroidogenesis of bovine thecal cells during antral follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmt1Cktb4%3D&md5=5946ff1f05f10ca163c42809518c9c31CAS | 1915085PubMed |
Sá Filho, M. F., Torres-Júnior, J. R., Penteado, L., Gimenes, L. U., Ferreira, R. M., Ayres, H., Castro, E. P. L. A., Sales, J. N., and Baruselli, P. S. (2010). Equine chorionic gonadotrophin improves the efficacy of a progestin-based fixed-time artificial insemination protocol in Nelore (Bos indicus) heifers. Anim. Reprod. Sci. 118, 182–187.
| Equine chorionic gonadotrophin improves the efficacy of a progestin-based fixed-time artificial insemination protocol in Nelore (Bos indicus) heifers.Crossref | GoogleScholarGoogle Scholar | 19939592PubMed |
Sales, J. N., Crepaldi, G. A., Girotto, R. W., Souza, A. H., and Baruselli, P. S. (2011). Fixed-time AI protocols replacing eCG with a single dose of FSH were less effective in stimulating follicular growth, ovulation and fertility in suckled–anoestrus Nelore beef cows. Anim. Reprod. Sci. 124, 12–18.
| Fixed-time AI protocols replacing eCG with a single dose of FSH were less effective in stimulating follicular growth, ovulation and fertility in suckled–anoestrus Nelore beef cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVyjsr8%3D&md5=98d321bcda7005a8890619d0495e5dbbCAS | 21376482PubMed |
Seto-Young, D., Avtanski, D., Strizhevsky, M., Parikh, G., Patel, P., Kaplun, J., Holcomb, K., Rosenwaks, Z., and Poretsky, L. (2007). Interactions among peroxisome proliferator-activated receptor-gamma, insulin signalling pathways and steroidogenic acute regulatory protein in human ovarian cells. J. Clin. Endocrinol. Metab. 92, 2232–2239.
| Interactions among peroxisome proliferator-activated receptor-gamma, insulin signalling pathways and steroidogenic acute regulatory protein in human ovarian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslOgs74%3D&md5=44190bcecd85654343917e722501e715CAS | 17374711PubMed |
Singh, J., and Adams, G. P. (1998). Immunohistochemical distribution of follistatin in dominant and subordinate follicles and the corpus luteum of cattle. Biol. Reprod. 59, 561–570.
| Immunohistochemical distribution of follistatin in dominant and subordinate follicles and the corpus luteum of cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVSkurc%3D&md5=cc8aae5348505eb74b4e9c2e6e3a7d0fCAS | 9716554PubMed |
Souza, A. H., Viechnieski, S., Lima, F. A., Silva, F. F., Araujo, R., Bo, G. A., Wiltbank, M. C., and Baruselli, P. S. (2009). Effects of equine chorionic gonadotrophin and type of ovulatory stimulus in a timed AI protocol on reproductive responses in dairy cows. Theriogenology 72, 10–21.
| Effects of equine chorionic gonadotrophin and type of ovulatory stimulus in a timed AI protocol on reproductive responses in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1Smsbc%3D&md5=8eaf8396bfd386a946262e03ad77c44aCAS | 19269685PubMed |
Sriperumbudur, R., Zorrilla, L., and Gadsby, J. E. (2010). Transforming growth factor-beta (TGFbeta) and its signalling components in peri-ovulatory pig follicles. Anim. Reprod. Sci. 120, 84–94.
| Transforming growth factor-beta (TGFbeta) and its signalling components in peri-ovulatory pig follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFWrt7w%3D&md5=ec2a15fb569506f1c6d43214fc47940dCAS | 20378284PubMed |
Stocco, C. (2012). The long and short of the prolactin receptor: the corpus luteum needs them both! Biol. Reprod. 86, 1–2.
| The long and short of the prolactin receptor: the corpus luteum needs them both!Crossref | GoogleScholarGoogle Scholar |
Stocco, D. M., and Clark, B. J. (1996). Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem. Pharmacol. 51, 197–205.
| Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtV2lsLY%3D&md5=2ef2bd5478b43ced18caec266a5f9d90CAS | 8573184PubMed |
Stocco, C. O., Chedrese, J., and Deis, R. P. (2001). Luteal expression of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, 3beta-hydroxysteroid dehydrogenase and 20alpha-hydroxysteroid dehydrogenase genes in late pregnant rats: effect of luteinizing hormone and RU486. Biol. Reprod. 65, 1114–1119.
| Luteal expression of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, 3beta-hydroxysteroid dehydrogenase and 20alpha-hydroxysteroid dehydrogenase genes in late pregnant rats: effect of luteinizing hormone and RU486.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1Cms78%3D&md5=cff11a7b30fe70c9e30a805f8c1b94c5CAS | 11566732PubMed |
Strauss, J. F., Kishida, T., Christenson, L. K., Fujimoto, T., and Hiroi, H. (2003). START domain proteins and the intracellular trafficking of cholesterol in steroidogenic cells. Mol. Cell. Endocrinol. 202, 59–65.
| START domain proteins and the intracellular trafficking of cholesterol in steroidogenic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFSnsLo%3D&md5=f01a1cf5099918571236184b5d5e4c6fCAS | 12770731PubMed |
Trzeciak, W. H., Sonnenborn, U., Balkow, C., and Kunau, W. H. (1984). Regulation of steroidogenesis in rat adrenal gland: identification of the bifunctional, hormone-sensitive cholesterol esterase–triacylglycerol lipase enzyme protein and its discrimination from hormone-insensitive lipases. Mol. Cell. Endocrinol. 35, 131–141.
| Regulation of steroidogenesis in rat adrenal gland: identification of the bifunctional, hormone-sensitive cholesterol esterase–triacylglycerol lipase enzyme protein and its discrimination from hormone-insensitive lipases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXktFOlt7o%3D&md5=e45a7cc4c028079711a04610fe30bb14CAS | 6734927PubMed |
Varga, T., Czimmerer, Z., and Nagy, L. (2011). PPARs are a unique set of fatty acid-regulated transcription factors controlling both lipid metabolism and inflammation. Biochim. Biophys. Acta 1812, 1007–1022.
| PPARs are a unique set of fatty acid-regulated transcription factors controlling both lipid metabolism and inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVOktLw%3D&md5=a7c9c70c76b7dc07f8e689dd05c66080CAS | 21382489PubMed |
Webb, R., Woad, K. J., and Armstrong, D. G. (2002). Corpus luteum (CL) function: local control mechanisms. Domest. Anim. Endocrinol. 23, 277–285.
| Corpus luteum (CL) function: local control mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Wktbg%3D&md5=b6404e890d268f279b68516f6ed2991bCAS | 12142244PubMed |
Wildman, E. E. (1982). Dairy cow body-condition scoring system and its relationship to selected production characteristics. J. Dairy Sci. 65, 495–501.
| Dairy cow body-condition scoring system and its relationship to selected production characteristics.Crossref | GoogleScholarGoogle Scholar |
Wiltbank, M. C., Belfiore, C. J., and Niswender, G. D. (1993). Steroidogenic enzyme activity after acute activation of protein kinase (PK) A and PKC in ovine small and large luteal cells. Mol. Cell. Endocrinol. 97, 1–7.
| Steroidogenic enzyme activity after acute activation of protein kinase (PK) A and PKC in ovine small and large luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtlSku7g%3D&md5=ad566cc06481330f30af77ac4a375cb9CAS | 8143891PubMed |
Wright, G. W., and Simon, R. M. (2003). A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 19, 2448–2455.
| A random variance model for detection of differential gene expression in small microarray experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVSis7k%3D&md5=84048d345ecea8871f21ce16f562a36bCAS | 14668230PubMed |
Wu, T., Tian, J., Cutler, R. G., Telljohann, R. S., Bernlohr, D. A., Mattson, M. P., and Handa, J. T. (2010). Knockdown of FABP5 mRNA decreases cellular cholesterol levels and results in decreased apoB100 secretion and triglyceride accumulation in ARPE-19 cells. Lab. Invest. 90, 963–965.
| Knockdown of FABP5 mRNA decreases cellular cholesterol levels and results in decreased apoB100 secretion and triglyceride accumulation in ARPE-19 cells.Crossref | GoogleScholarGoogle Scholar | 20508649PubMed |