Effects of adrenocorticotrophic hormone on the expression of matrix metalloproteinases and their inhibitors in the bovine ovary
E. M. Belotti A B * , A. N. Amweg A B * , V. Matiller A B , M. L. Varela A , A. F. Stassi A B , M. M. L. Velázquez A B , H. H. Ortega A B , F. Rey A B and N. R. Salvetti A B CA Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral, Universidad Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas, R. P. Kreder 2805, CP3080, Esperanza, Santa Fe, Argentina.
B Facultad de Ciencias Veterinarias del Litoral, Universidad Nacional del Litoral, R. P. Kreder 2805, CP3080, Esperanza, Santa Fe, Argentina.
C Corresponding author. Email: salvetti@fcv.unl.edu.ar
Reproduction, Fertility and Development 32(8) 748-762 https://doi.org/10.1071/RD19232
Submitted: 25 June 2019 Accepted: 1 December 2019 Published: 4 May 2020
Abstract
Cattle undergo numerous environmental and management stressors that reduce fertility and affect ovulation. The extracellular matrix of the follicle wall can be altered by matrix metalloproteinases (MMPs), the activities of which are regulated by interleukins and tissue-specific inhibitors of metalloproteinases (TIMPs), especially during ovulation. The aims of the present study were to: (1) evaluate changes in the hormone milieu, the localisation and activity of MMP2 and MMP9 and the localisation of MMP14, TIMP1 and TIMP2 in response to adrenocorticotrophic hormone (ACTH) during the preovulatory period in cows; and (2) determine the direct effects of ACTH on the mRNA expression of MMP2 and MMP9 in the cultured follicle wall of bovine ovaries obtained from an abattoir. 100 IU ACTH was administered during pro-oestrus every 12 h until ovariectomy, which was performed before ovulation. Cortisol concentrations in the plasma and follicular fluid (FF) of preovulatory follicles were higher in ACTH-treated than control cows. Progesterone presented subluteal concentrations in plasma of ACTH-treated cows (P < 0.05). MMP2 immunostaining and activity in ovaries were higher in ACTH-treated than control cows (P < 0.05), whereas MMP9 immunostaining was similar between the two groups. However, unlike in control cows, MMP9 activity was absent in the FF of ACTH-treated cows. These results suggest that the administration of ACTH during the preovulatory period in cows could cause changes that culminate in modifications in the content and activation of MMPs and TIMPs in the ovary, which could interfere with the ovulation process.
Additional keywords: cattle, reproduction, stress.
References
Alam, M. G. S., Dobson, H., and Fitzpatrick, R. J. (1986). Endocrine response to different doses of ACTH in cows. Br. Vet. J. 142, 239–245.| Endocrine response to different doses of ACTH in cows.Crossref | GoogleScholarGoogle Scholar |
Aljada, A., Ghanim, H., Mohanty, P., Hofmeyer, D., Tripathy, D., and Dandona, P. (2001). Hydrocortisone suppresses intranuclear activator-protein-1 (AP-1) binding activity in mononuclear cells and plasma matrix metalloproteinase 2 and 9 (MMP2 and MMP9). J. Clin. Endocrinol. Metab. 86, 5988–5991.
| Hydrocortisone suppresses intranuclear activator-protein-1 (AP-1) binding activity in mononuclear cells and plasma matrix metalloproteinase 2 and 9 (MMP2 and MMP9).Crossref | GoogleScholarGoogle Scholar | 11739475PubMed |
American Dairy Science Association, American Society of Animal Science, Poultry Science Association (2010). ‘Guide for the care and use of agricultural animals in research and teaching (Ag guide).’ 3rd edn. (Federation of Animal Science Societies: Champaign, IL.)
Amweg, A. N., Paredes, A., Salvetti, N. R., Lara, H. E., and Ortega, H. H. (2011). Expression of melanocortin receptors mRNA, and direct effects of ACTH on steroid secretion in the bovine ovary. Theriogenology 75, 628–637.
| Expression of melanocortin receptors mRNA, and direct effects of ACTH on steroid secretion in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 21111470PubMed |
Amweg, A. N., Salvetti, N. R., Stangaferro, M. L., Paredes, A. H., Lara, H. H., Rodríguez, F. M., and Ortega, H. H. (2013). Ovarian localization of 11β-hydroxysteroid dehydrogenase (11βHSD): effects of ACTH stimulation and its relationship with bovine cystic ovarian disease. Domest. Anim. Endocrinol. 45, 126–140.
| Ovarian localization of 11β-hydroxysteroid dehydrogenase (11βHSD): effects of ACTH stimulation and its relationship with bovine cystic ovarian disease.Crossref | GoogleScholarGoogle Scholar | 23972491PubMed |
Amweg, A. N., Rodríguez, F. M., Huber, E., Marelli, B. E., Gareis, N. C., Belotti, E. M., Rey, F., Salvetti, N. R., and Ortega, H. H. (2017). Detection and activity of 11 beta hydroxylase (CYP11B1) in the bovine ovary. Reproduction 153, 433–441.
| Detection and activity of 11 beta hydroxylase (CYP11B1) in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 28069904PubMed |
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 | 15459120PubMed |
Bello, N. M., Steibel, J. P., and Pursley, J. R. (2006). Optimizing ovulation to first GnRH improved outcomes to each hormonal injection of ovsynch in lactating dairy cows. J. Dairy Sci. 89, 3413–3424.
| Optimizing ovulation to first GnRH improved outcomes to each hormonal injection of ovsynch in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 16899674PubMed |
Biran, D., Braw-Tal, R., Gendelman, M., Lavon, Y., and Roth, Z. (2015). ACTH administration during formation of preovulatory follicles impairs steroidogenesis and angiogenesis in association with ovulation failure in lactating cows. Domest. Anim. Endocrinol. 53, 52–59.
| ACTH administration during formation of preovulatory follicles impairs steroidogenesis and angiogenesis in association with ovulation failure in lactating cows.Crossref | GoogleScholarGoogle Scholar | 26099839PubMed |
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 | 942051PubMed |
Brandt, Y., Einarsson, S., Ljung, A., Lundeheim, N., Rodríguez-Martínez, H., and Madej, A. (2009). Effects of continuous elevated cortisol concentrations during oestrus on concentrations and patterns of progesterone, oestradiol and LH in the sow. Anim. Reprod. Sci. 110, 172–185.
| Effects of continuous elevated cortisol concentrations during oestrus on concentrations and patterns of progesterone, oestradiol and LH in the sow.Crossref | GoogleScholarGoogle Scholar | 18308488PubMed |
Brännström, M. (2004). Potential role of cytokines in ovarian physiology: the case for interleukin-1. In ‘The Ovary’. 2nd edn. (Eds P. C. K. Leung and E. Y. Adashi.) pp. 261–271. (Elsevier Academic Press: Vancouver.)
Braw-Tal, R., and Yossefi, S. (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil. 109, 165–171.
| Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary.Crossref | GoogleScholarGoogle Scholar | 9068428PubMed |
Carroll, J. A., and Forsberg, N. E. (2007). Influence of stress and nutrition on cattle immunity. Vet. Clin. North Am. Food Anim. Pract. 23, 105–149.
| Influence of stress and nutrition on cattle immunity.Crossref | GoogleScholarGoogle Scholar | 17382844PubMed |
Chaffin, C. L., and Stouffer, R. L. (1999). Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: time course and steroid regulation. Biol. Reprod. 61, 14–21.
| Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: time course and steroid regulation.Crossref | GoogleScholarGoogle Scholar | 10377026PubMed |
Curry, T. E., and Osteen, K. G. (2003). The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr. Rev. 24, 428–465.
| The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle.Crossref | GoogleScholarGoogle Scholar | 12920150PubMed |
Curry, T. E., and Smith, M. F. (2006). Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition. Semin. Reprod. Med. 24, 228–241.
| Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition.Crossref | GoogleScholarGoogle Scholar | 16944420PubMed |
Cury, P. R., Araújo, V. C., Canavez, F., Furuse, C., and Araújo, N. S. (2007). Hydrocortisone affects the expression of matrix metalloproteinases (MMP1, -2, -3, -7, and -11) and tissue inhibitor of matrix metalloproteinases (TIMP1) in human gingival fibroblasts. J. Periodontol. 78, 1309–1315.
| Hydrocortisone affects the expression of matrix metalloproteinases (MMP1, -2, -3, -7, and -11) and tissue inhibitor of matrix metalloproteinases (TIMP1) in human gingival fibroblasts.Crossref | GoogleScholarGoogle Scholar | 17608586PubMed |
Dejager, L., Vandevyver, S., Petta, I., and Libert, C. (2014). Dominance of the strongest: inflammatory cytokines versus glucocorticoids. Cytokine Growth Factor Rev. 25, 21–33.
| Dominance of the strongest: inflammatory cytokines versus glucocorticoids.Crossref | GoogleScholarGoogle Scholar | 24412262PubMed |
Díaz, P. U., Stangaferro, M. L., Gareis, N. C., Silvia, W. J., Matiller, V., Salvetti, N. R., Rey, F., Barberis, F., Cattaneo, L., and Ortega, H. H. (2015). Characterization of persistent follicles induced by prolonged treatment with progesterone in dairy cows: an experimental model for the study of ovarian follicular cysts. Theriogenology 84, 1149–1160.
| Characterization of persistent follicles induced by prolonged treatment with progesterone in dairy cows: an experimental model for the study of ovarian follicular cysts.Crossref | GoogleScholarGoogle Scholar | 26187329PubMed |
Díaz, P. U., Hein, G. J., Belotti, E. M., Rodríguez, F. M., Rey, F., Amweg, A. N., Matiller, V., Baravalle, M. E., Ortega, H. H., and Salvetti, N. R. (2016). BMP2, 4 and 6 and BMPR1B are altered from early stages of bovine cystic ovarian disease development. Reproduction 152, 333–350.
| BMP2, 4 and 6 and BMPR1B are altered from early stages of bovine cystic ovarian disease development.Crossref | GoogleScholarGoogle Scholar | 27486268PubMed |
Duffy, D. M., Ko, C., Jo, M., Brannstrom, M., and Curry, T. E. (2019). Ovulation: parallels with inflammatory processes. Endocr. Rev. 40, 369–416.
| Ovulation: parallels with inflammatory processes.Crossref | GoogleScholarGoogle Scholar | 30496379PubMed |
Espey, L. L., Belilinger, A. S., and Healy, J. A. (2004). Ovulation: an inflamatory cascade of gene expression. In ‘The Ovary’. 2nd edn. (Eds P. C. K. Leung and E. Y. Adashi.) pp. 145–165. (Elsevier Academic Press: Vancouver.)
Goldman, S., and Shalev, E. (2004). MMPs and TIMPs in ovarian physiology and pathophysiology. Front. Biosci. 9, 2474–2483.
| MMPs and TIMPs in ovarian physiology and pathophysiology.Crossref | GoogleScholarGoogle Scholar | 15353300PubMed |
Gwazdauskas, F. C., Thatcher, W., and Wilcox, J. (1972). Adrenocorticotropin alteration of bovine peripheral plasma concentrations of cortisol, corticosterone, and progesterone. J. Dairy Sci. 55, 1165–1169.
| Adrenocorticotropin alteration of bovine peripheral plasma concentrations of cortisol, corticosterone, and progesterone.Crossref | GoogleScholarGoogle Scholar | 4340432PubMed |
Hashii, K., Fujiwara, H., Yoshioka, S., Kataoka, N., Yamada, S., Hirano, T., Mori, T., Fujii, S., and Maeda, M. (1998). Peripheral blood mononuclear cells stimulate progesterone production by luteal cells derived from pregnant and non-pregnant women: possible involvement of interleukin-4 and interleukin-10 in corpus luteum function and differentiation. Hum. Reprod. 13, 2738–2744.
| Peripheral blood mononuclear cells stimulate progesterone production by luteal cells derived from pregnant and non-pregnant women: possible involvement of interleukin-4 and interleukin-10 in corpus luteum function and differentiation.Crossref | GoogleScholarGoogle Scholar | 9804222PubMed |
Hatler, T. B., Hayes, S. H., Ray, D. L., Reames, P. S., and Silvia, W. J. (2008). Effect of subluteal concentrations of progesterone on luteinizing hormone and ovulation in lactating dairy cows. Vet. J. 177, 360–368.
| Effect of subluteal concentrations of progesterone on luteinizing hormone and ovulation in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 17692545PubMed |
Hein, K. G., and Allrich, R. D. (1992). Influence of exogenous adrenocorticotropic hormone on estrous behavior in cattle. J. Anim. Sci. 70, 243–247.
| Influence of exogenous adrenocorticotropic hormone on estrous behavior in cattle.Crossref | GoogleScholarGoogle Scholar | 1316341PubMed |
Huet, C., Monget, P., Pisselet, C., Hennequet, C., Locatelli, A., and Monniaux, D. (1998). Chronology of events accompanying follicular atresia in hypophysectomized ewes. Changes in levels of steroidogenic enzymes, connexin 43, insulin-like growth factor II/mannose 6 phosphate receptor, extracellular matrix components, and matrix metalloproteinases. Biol. Reprod. 58, 175–185.
| Chronology of events accompanying follicular atresia in hypophysectomized ewes. Changes in levels of steroidogenic enzymes, connexin 43, insulin-like growth factor II/mannose 6 phosphate receptor, extracellular matrix components, and matrix metalloproteinases.Crossref | GoogleScholarGoogle Scholar | 9472939PubMed |
Imai, K., Khandoker, M. A. M. Y., Yonai, M., Takahashi, T., Sato, T., Ito, A., Hasegawa, Y., and Hashizume, K. (2003). Matrix metalloproteinases-2 and -9 activities in bovine follicular fluid of different-sized follicles: relationship to intra-follicular inhibin and steroid concentrations. Domest. Anim. Endocrinol. 24, 171–183.
| Matrix metalloproteinases-2 and -9 activities in bovine follicular fluid of different-sized follicles: relationship to intra-follicular inhibin and steroid concentrations.Crossref | GoogleScholarGoogle Scholar | 12586316PubMed |
Inderdeo, D. S., Edwards, D. R., Han, V. K., and Khokha, R. (1996). Temporal and spatial expression of tissue inhibitors of metalloproteinases during the natural ovulatory cycle of the mouse. Biol. Reprod. 55, 498–508.
| Temporal and spatial expression of tissue inhibitors of metalloproteinases during the natural ovulatory cycle of the mouse.Crossref | GoogleScholarGoogle Scholar | 8862765PubMed |
Kliem, H., Welter, H., Kraetzl, W. D., Steffl, M., Meyer, H. H. D., Schams, D., and Berisha, B. (2007). Expression and localisation of extracellular matrix degrading proteases and their inhibitors during the oestrous cycle and after induced luteolysis in the bovine corpus luteum. Reproduction 134, 535–547.
| Expression and localisation of extracellular matrix degrading proteases and their inhibitors during the oestrous cycle and after induced luteolysis in the bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 17709571PubMed |
LeMaire, W. J. (1989). Mechanism of mammalian ovulation. Steroids 54, 455–469.
| Mechanism of mammalian ovulation.Crossref | GoogleScholarGoogle Scholar | 2559497PubMed |
Magomedova, L., and Cummins, C. L. (2016). Glucocorticoids and metabolic control. Handb. Exp. Pharmacol. 233, 73–93.
| Glucocorticoids and metabolic control.Crossref | GoogleScholarGoogle Scholar | 25917083PubMed |
McNeilly, A. S., Picton, H. M., Campbell, B. K., and Baird, D. T. (1991). Gonadotrophic control of follicle growth in the ewe. J. Reprod. Fertil. Suppl. 43, 177–186.
| 1843339PubMed |
Moenter, S. M., Caraty, A., and Karsch, F. J. (1990). The estradiol-induced surge of gonadotropin-releasing hormone in the ewe. Endocrinology 127, 1375–1384.
| The estradiol-induced surge of gonadotropin-releasing hormone in the ewe.Crossref | GoogleScholarGoogle Scholar | 2201536PubMed |
Oksjoki, S., Rahkonen, O., Haarala, M., Vuorio, E., and Anttila, L. (2004). Differences in connective tissue gene expression between normally functioning, polycystic and post-menopausal ovaries. Mol. Hum. Reprod. 10, 7–14.
| Differences in connective tissue gene expression between normally functioning, polycystic and post-menopausal ovaries.Crossref | GoogleScholarGoogle Scholar | 14665701PubMed |
Ortega, H. H., Salvetti, N. R., and Padmanabhan, V. (2009). Developmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance. Reproduction 137, 865–877.
| Developmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance.Crossref | GoogleScholarGoogle Scholar | 19261835PubMed |
Papacleovoulou, G., Critchley, H. O., Hillier, S. G., and Mason, J. I. (2011). IL1α and IL4 signalling in human ovarian surface epithelial cells. J. Endocrinol. 211, 273–283.
| IL1α and IL4 signalling in human ovarian surface epithelial cells.Crossref | GoogleScholarGoogle Scholar | 21903865PubMed |
Peng, J. Y., Han, P., Xin, H. Y., Ji, S. Y., Gao, K. X., An, X. P., and Cao, B. Y. (2015). Molecular characterization and hormonal regulation of tissue inhibitor of metalloproteinase 1 in goat ovarian granulosa cells. Domest. Anim. Endocrinol. 52, 1–10.
| Molecular characterization and hormonal regulation of tissue inhibitor of metalloproteinase 1 in goat ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar | 25700266PubMed |
Peralta, M. B., Baravalle, M. E., Belotti, E. M., Stassi, A., Salvetti, N. R., Ortega, H. H., Rey, F., and Velázquez, M. M. L. (2017). Involvement of matrix metalloproteinases and their inhibitors in bovine cystic ovarian disease. J. Comp. Pathol. 156, 191–201.
| Involvement of matrix metalloproteinases and their inhibitors in bovine cystic ovarian disease.Crossref | GoogleScholarGoogle Scholar | 27993358PubMed |
Portela, V. M., Veiga, A., and Price, C. A. (2009). Regulation of MMP2 and MMP9 metalloproteinases by FSH and growth factors in bovine granulosa cells. Genet. Mol. Biol. 32, 516–520.
| Regulation of MMP2 and MMP9 metalloproteinases by FSH and growth factors in bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 21637514PubMed |
Puttabyatappa, M., Jacot, T. A., Al-Alem, F. L., Rosewell, K. L., Duffy, D. M., Brännström, M., and Curry, T. E. (2014). Ovarian membrane-type matrix metalloproteinases: induction of MMP14 and MMP16 during the periovulatory period in the rat, macaque, and human. Biol. Reprod. 91, 34.
| Ovarian membrane-type matrix metalloproteinases: induction of MMP14 and MMP16 during the periovulatory period in the rat, macaque, and human.Crossref | GoogleScholarGoogle Scholar | 24920038PubMed |
Ranefall, P., Wester, K., and Bengtsson, E. (1998). Automatic quantification of immunohistochemically stained cell nuclei using unsupervised image analysis. Anal. Cell. Pathol. 16, 29–43.
| Automatic quantification of immunohistochemically stained cell nuclei using unsupervised image analysis.Crossref | GoogleScholarGoogle Scholar | 9584898PubMed |
Ribadu, A. Y., Nakada, K., Moriyoshi, M., Zhang, W. C., Tanaka, Y., and Nakao, T. (2000). The role of LH pulse frequency in ACTH induced ovarian follicular cysts in heifers. Anim. Reprod. Sci. 64, 21–31.
| The role of LH pulse frequency in ACTH induced ovarian follicular cysts in heifers.Crossref | GoogleScholarGoogle Scholar | 11078964PubMed |
Ribeiro, L. A., Turba, M. E., Zannoni, A., Bacci, M. L., and Forni, M. (2006). Gelatinases, endonuclease and vascular endothelial growth factor during development and regression of swine luteal tissue. BMC Dev. Biol. 6, 58.
| Gelatinases, endonuclease and vascular endothelial growth factor during development and regression of swine luteal tissue.Crossref | GoogleScholarGoogle Scholar | 17137503PubMed |
Riley, S. C., Gibson, A. H., Leask, R., Mauchline, D. J., Pedersen, H. G., and Watson, E. D. (2001). Secretion of matrix metalloproteinases 2 and 9 and tissue inhibitor of metalloproteinases into follicular fluid during follicle development in equine ovaries. Reproduction 121, 553–560.
| Secretion of matrix metalloproteinases 2 and 9 and tissue inhibitor of metalloproteinases into follicular fluid during follicle development in equine ovaries.Crossref | GoogleScholarGoogle Scholar | 11277874PubMed |
Riollet, C., Rainard, P., and Poutrel, B. (2001). Cell subpopulations and cytokine expression in cow milk in response to chronic staphylococcus aureus infection. J. Dairy Sci. 84, 1077–1084.
| 11384034PubMed |
Robinson, T. L., Sutherland, I. A., and Sutherland, J. (2007). Validation of candidate bovine reference genes for use with real-time PCR. Vet. Immunol. Immunopathol. 115, 160–165.
| Validation of candidate bovine reference genes for use with real-time PCR.Crossref | GoogleScholarGoogle Scholar | 17074403PubMed |
Smith, M. F., Ricke, W. A., Bakke, L. J., Dow, M. P., and Smith, G. W. (2002). Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors. Mol. Cell. Endocrinol. 191, 45–56.
| Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors.Crossref | GoogleScholarGoogle Scholar | 12044918PubMed |
Stassi, A. F., Baravalle, M. E., Belotti, E. M., Rey, F., Gareis, N. C., Díaz, P. U., Rodríguez, F. M., Leiva, C. J., Ortega, H. H., and Salvetti, N. R. (2017). Altered expression of cytokines IL-1α, IL-6, IL-8 and TNF-α in bovine follicular persistence. Theriogenology 97, 104–112.
| Altered expression of cytokines IL-1α, IL-6, IL-8 and TNF-α in bovine follicular persistence.Crossref | GoogleScholarGoogle Scholar | 28583593PubMed |
Strongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A., and Goldberg, G. I. (1995). Mechanism of cell surface activation of 72-kDa type IV collagenase: isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270, 5331–5338.
| Mechanism of cell surface activation of 72-kDa type IV collagenase: isolation of the activated form of the membrane metalloprotease.Crossref | GoogleScholarGoogle Scholar | 7890645PubMed |
Thatcher, W. W., Moreira, F., Pancarci, S. M., Bartolome, J. A., and Santos, J. E. P. (2002). Strategies to optimize reproductive efficiency by regulation of ovarian function. Domest. Anim. Endocrinol. 23, 243–254.
| Strategies to optimize reproductive efficiency by regulation of ovarian function.Crossref | GoogleScholarGoogle Scholar | 12142241PubMed |
Thurston, L. M., Jonas, K. C., Abayasekara, D. R. E., and Michael, A. E. (2003). Ovarian modulators of 11β-hydroxysteroid dehydrogenase (11βHSD) activity in follicular fluid from bovine and porcine large antral follicles and spontaneous ovarian cysts. Biol. Reprod. 68, 2157–2163.
| Ovarian modulators of 11β-hydroxysteroid dehydrogenase (11βHSD) activity in follicular fluid from bovine and porcine large antral follicles and spontaneous ovarian cysts.Crossref | GoogleScholarGoogle Scholar | 12606327PubMed |
Tsafriri, A., and Reich, R. (1999). Molecular aspects of mammalian ovulation. Exp. Clin. Endocrinol. Diabetes 107, 1–11.
| Molecular aspects of mammalian ovulation.Crossref | GoogleScholarGoogle Scholar | 10077349PubMed |
Wang, C. J., Zhou, Z. G., Holmqvist, A., Zhang, H., Li, Y., Adell, G., and Sun, X. F. (2009). Survivin expression quantified by Image Pro-Plus compared with visual assessment. Appl. Immunohistochem. Mol. Morphol. 17, 530–535.
| Survivin expression quantified by Image Pro-Plus compared with visual assessment.Crossref | GoogleScholarGoogle Scholar | 19407655PubMed |
Woessner, J. F. (1991). Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 5, 2145–2154.
| Matrix metalloproteinases and their inhibitors in connective tissue remodeling.Crossref | GoogleScholarGoogle Scholar | 1850705PubMed |
Woods, A. M., and Judd, A. M. (2008). Interleukin-4 increases cortisol release and decreases adrenal androgen release from bovine adrenal cells. Domest. Anim. Endocrinol. 34, 372–382.
| Interleukin-4 increases cortisol release and decreases adrenal androgen release from bovine adrenal cells.Crossref | GoogleScholarGoogle Scholar | 18055157PubMed |
Yahia Khandoker, M. A. M., Imai, K., Takahashi, T., and Hashizume, K. (2001). Role of gelatinase on follicular atresia in the bovine ovary. Biol. Reprod. 65, 726–732.
| Role of gelatinase on follicular atresia in the bovine ovary.Crossref | GoogleScholarGoogle Scholar |
Yang, E. V., Bane, C. M., MacCallum, R. C., Kiecolt-Glaser, J. K., Malarkey, W. B., and Glaser, R. J. (2002). Stress-related modulation of matrix metalloproteinase expression. J. Neuroimmunol. 133, 144–150.
| Stress-related modulation of matrix metalloproteinase expression.Crossref | GoogleScholarGoogle Scholar | 12446017PubMed |
Zhang, B., Moses, M. A., and Tsang, P. C. W. (2003). Temporal and spatial expression of tissue inhibitors of metalloproteinases 1 and 2 (TIMP1 and -2) in the bovine corpus luteum. Reprod. Biol. Endocrinol. 1, 85.
| Temporal and spatial expression of tissue inhibitors of metalloproteinases 1 and 2 (TIMP1 and -2) in the bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 14613539PubMed |