Hormonal control of the estrous cycle in cattle and sheep
Universidad Cooperativa de Colombia. Sede Bucaramanga.
Docente área de reproducción animal de la Facultad Medicina Veterinaria y Zootecnia de la Universidad Cooperativa de Colombia, sede Bucaramanga.
email: orge.atuesta@campusucc.edu.co
Universidad Cooperativa de Colombia. Sede Bucaramanga.
Docente biotecnología y clínica de reproducción animal de la Facultad Medicina Veterinaria y Zootecnia de la Universidad Cooperativa de Colombia, sede Bucaramanga.
email: angela.gonella@campusucc.edu.co
The goal of this review is conducting a detailed and updated literature description of hormonal mechanisms that regulate the estrous cycle. Indeed, we know that estrous cycle is the time period from one heat to the beginning of the next one. The endocrine events during the estrous cycle are regulated by hypothalamus (through GnRH secretion), the pituitary (lh and fsh secretion), the follicles (estrogens and inhibin secretion), the corpus luteum (progesterone and oxytocin), and uterus (responsible for production of prostaglandin F2α). Within proestrus, a quick decrease in plasma progesterone levels precedes the estrus caused by releasing prostaglandin F2 α from endometrium. Such reduction of progesterone concentrations allows the ovulatory follicle to grow and secrete estradiol; so plasma estradiol binding to specific receptors in the hypothalamus can set off the neural mechanism that triggers behavioral changes associated with the estrus onset. During estrus, or heat, the female is receptive to the male and allows mating. A peak in estradiol levels occurs shortly after the estrus onset and induces the lh pre-ovulatory discharge, which in turn induces the ovulation and the beginning of luteinization process of theca and granulose cells. A new corpus luteum is developed during metestrus with a subsequent increase in progesterone serum concentration. This corpus completes its maturation during diestrus. If a viable embryo in the uterus, it sends a signal for maternal recognition of pregnancy whose recognition prevents luteolisis process and, subsequently, the beginning of a new estrus cycle during pregnancy.
Senger PL. Pathways to pregnancy and parturition. 2nd ed. Pullman (WA): Current Conceptions Inc, 2003
Goodman RL, Inskeep EK. Neuroendocrine control of the ovarian cycle of the sheep. In: Neill J, editor. Knobil and Neill’s Physiology of Reproduction. 3rd ed. San Die-go: Elsevier Incorporated, 2006; p. 2389-447
Duggavathi R. Dynamics and regulation of ovarian antral follicular waves in sheep. Thesis of Doctor of Philosophy. University of Saskatchewan, 2004.
Davies K. Ovarian antral follicular dynamics and regula-tion in sheep. Thesis of Master of Science. University of Saskatchewan, 2005.
Peter AT, Levine H, Drost M, Bergfelt DR. Compilation of classical and contemporary terminology used to des-cribe morphological aspects of ovarian dynamics in cattle. Theriogenology. 2009; 71: 1343-57.
Viñoles C. Effect of nutrition on follicle development and ovulation rate in the ewe. Thesis of Doctor of Philosophy. Swedish University of Agricultural Sciences, 2003.
Driancourt MA. Follicular dynamics in sheep and cattle. Theriogenology. 1991; 35: 55-79.
Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIn-tush EW. Mechanisms controlling the function and life span of the corpus luteum. Phys. Rev. 2000; 80: 1-29.
Weems CW, Weems YS, Randel RD. Prostaglandins and reproduction in female farm animals. Vet. J. 2006; 171: 206-228.
Shirasuna K. Nitric oxide and luteal blood flow in the lu-teolytic cascade in the cow. J. Reprod. Dev. 2010; 56: 9-14.
Spencer TE, Burghardt RC, Johnson GA, Bazer FW. Conceptus signals for establishment and maintenance of pregnancy. Anim. Reprod. Sci. 2004; 82-83: 537-550.
Campling G. Uterine physiology. Anaesth. Intensive Care Med. 2008; 9: 122-123.
Dewitt D, Smith WL. Yes, but they still get headaches? Cell. 1995; 83: 345-348.
Miyamoto A, Shirasuna K, Wijayagunawardane MP, Watanabe S, Hayashi M, et al. Blood flow: a key regu-latory component of corpus luteum function in the cow. Domest. Anim. Endocrinol. 2005; 29: 329-339.
Hansel W, Convey EM. Physiology of the estrous cycle. J. Anim. Sci. 1983; 57: 404-424.
Hunzicker-Dunn M, Mayo K. Gonadotropin Signaling in the Ovary. In: Neill J, editor. Knobil and Neill’s Physiology of Reproduction. 3rd ed. San Diego: Elsevier Incorpora-ted, 2006; p. 547-92.
Spencer TE, Bazer FW. Biology of progesterone action during pregnancy recognition and maintenance of preg-nancy. Front. Biosci. 2002; 7: d1879-d1898.
Bishop CV, Stormshak F. Non-genomic actions of pro-gesterone and estrogens in regulating reproductive events in domestic animals. Vet. J. 2008; 176: 270-280.
Mann GE. Hormone control of prostaglandin F (2 alpha) production and oxytocin receptor concentrations in bovi-ne endometrium in explant culture. Domest. Anim. Endo-crinol. 2001; 20: 217-226.
Bogacki M, Silvia WJ, Rekawiecki R, Kotwica J. Direct inhibitory effect of progesterone on oxytocin-induced se-cretion of prostaglandin F(2alpha) from bovine endome-trial tissue. Biol. Reprod. 2002; 67: 184-188.
Couse JF, Hewitt SC, Korach KS. Steroid Receptors in the Ovary and Uterus. In: Neill J, editor. Knobil and Neill’s Physiology of Reproduction. 3rd ed. San Diego: Elsevier Incorporated, 2006; p. 593-678
Spencer T, Johnson GA, Burghardt RC, Bazer FW. Pro-gesterone and Placental Hormone Actions on the Uterus: Insights from Domestic Animals. Biol. Reprod. 2004; 71: 2-10.
Hernández J, Zarco A. 1998. Función del cuerpo lúteo y muerte embrionaria en rumiantes. Ciencia Vet. Mex. 1998; 8: 1-28.
McCracken JA, Schramm W, Okulicz WC. Hormone re-ceptor control of pulsatile secretion of pgf-2alpha from the ovine uterus during luteolysis and its abrogation in early pregnancy. Anim. Reprod. Sci. 1984; 7: 31-55.
Vallet JL, Lamming GE, Batten M. Control of endome-trial oxytocin receptor and uterine response to oxytocin by progesterone and oestradiol in the ewe. J. Reprod. Fertil. 1990; 90: 625-634.
McCracken JA, Custer EE, Lamsa JC. 1999. Luteolysis: a neuroendocrine-mediated event. Phys. Rev. 1999; 79: 263-323.
McGuire WJ, Juengel JL, Niswender GD. 1994. Protein kinase C second messenger system mediates the antiste-roidogenic effects of prostaglandin F2α in the ovine cor-pus luteum in vivo. Biol. Reprod. 1994; 51: 800-806.
Miyamoto A, Shirasuna K, Sasahara K. Local regula-tion of corpus luteum development and regression in the cow: Impact of angiogenic and vasoactive factors. Domest. Anim. Endocrinol. 2009; 37: 159-169.
Mamluk R, Chen D, Greber Y, Davis JS, Meidan R. Cha-racterization of messenger ribonucleic acid expression for prostaglandin F2α and luteinizing hormone receptors in various bovine luteal cell types. Biol. Reprod. 1998; 58: 849-856.
Girsh E, Wang W, Mamluk R, Arditi F, Friedman A, et al. Regulation of endothelin-1 in the bovine corpus luteum: elevation by prostaglandin F2 alpha. Endocrinology. 1996; 137: 5191-5196.
Huggins JP, Pelton JT, Miller RC. The structure and spe-cificity of endothelin receptors: their importance in phy-siology and medicine. Pharmacol. Ther. 1993; 59: 55-123.
Niswender GD, Juengel JL, McGuire WJ, Belfiore CJ, Wiltbank MC. Luteal function: the estrous cycle and early pregnancy. Biol. Reprod.1994; 50: 239-247.
Ohtani M, Kobayshi S, Miyamoto A, Hayashi K, Fukul Y. Real-time relationships between intraluteal and plasma concentrations of endothelin, oxytocin, and progesterone during prostaglandin F2α-induced luteolysis in the cow. Biol. Reprod. 1998; 58: 103-108.
Papadopoulos V, Brown AS. Role of the peripheral type benzodiazepine receptor and the polypeptide diazepam binding inhibitor in steroidogenesis. The J. Steroid Bio-chem. Mol. Biol. 1995; 53: 103-110.
Stocco DM, Clark BJ. Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem. Pharmacol. 1996; 51: 197-205.
Pescador N, Soumano K, Stocco DM, Price CA, Murphy BD. Steroidogenic acute regulatory protein in bovine cor-pora lutea. Biol. Reprod. 1996; 55: 485-491.
Juengel JL, Meberg BM, Turzillo AM, Nett TM, Niswen-der GD. Hormonal regulation of mRNA encoding steroi-dogenic acute regulatory protein in ovine corpora lutea. Endocrinology. 1995; 136: 5423-5429.
Bell RM, Burns DJ. Lipid activation of protein kinase C. J. Biol. Chem. 1991; 266: 4661-4664.
Sawyer HR, Niswender KD, Braden DT, Niswender GD. Nuclear changes in ovine luteal cells in response to PGF2α. Domest. Anim. Endocrinol. 1990; 7: 229-238.
Rajkovic A, Pangas SP, Matzuk MM. Follicular Develo-pment: Mouse, Sheep, and Human Models. In: Neill J, editor. Knobil and Neill’s Physiology of Reproduction. 3rd ed. San Diego: Elsevier Incorporated, 2006; p. 383-423.
Kinder JE, Kojima FN, Bergfeld EG, Wehrman ME, Fike KE. Progestin and estrogen regulation of pulsatile lh re-lease and development of persistent ovarian follicles in cattle. J. Anim. Sci. 1996; 74: 1424-1440.
Bartlewski PM. The relationships between ovarian antral follicle dynamics, luteal function and endocrine variables in ewes. Thesis of Doctor of Philosophy. University of Sas-katchewan, 2001.
Pedram A, Razandi M, Aitkenhead M, Hughes, CCW, Levin ER. Integration of the non-genomic and genomic actions of estrogen. Membrane-initiated signaling by ste-roid to transcription and cell biology. J. Biol. Chem. 2002; 277: 50768-50775.
Espey LL, Richards JS. Ovulation. In: Neill J, editor. Kno-bil and Neill’s Physiology of Reproduction. 3rd ed. San Diego: Elsevier Incorporated, 2006; p. 425-74.
Stojilkovic SS, Reinhart J, Catt KJ. Gonadotropin-relea-sing hormone receptors: structure and signal transduction pathways. Endocrine Rev. 1994; 15: 462-499.
Clarke IJ, Pomolo S. Synthesis and secretion de GnRH. Anim. Reprod. Sci. 2005; 88: 29-55.
Foradori CD. The role of endogenous opioid peptides in the ovine estrous cycle. Thesis of Doctor of Philosophy. University of Cincinnati, 2003.
Joseph IBJK, Ravindra JP, Rawlings NC. Oestradiol and the preovulatory surges of luteinising hormone and follicle stimulating hormone in ewes during the breeding season and transition into anoestrus. Anim. Reprod. Sci. 1995; 40: 291-298.
Richards JS, Liu Z, Shimada M. Immune-like mecha-nisms in ovulation. Trends Endocrinol. Metab. 2008; 19: 191-196.
Brannstrom M, Zackrisson U, Hagstrom HG, Josefsson B, Hellberg P, et al. Preovulatory changes of blood in di-fferent regions of the human follicle. Fertil. Steril. 1998; 69: 435-442.
Hernández A, Jiménez C. El ciclo estral. En: Reproduc-ción en la vaca: fisiología y aplicaciones. Bogotá: Editorial Universidad Nacional de Colombia, 2008; p. 42-86.
Varga B, Horvath E, Folly G, Stark E. Study of the lutei-nizing hormone-induced increase of ovarian blood flow during the estrous cycle in the rat. Biol. Reprod. 1985; 32: 480-488.
Acosta TJ, Miyamoto A. Vascular control of ovarian function: ovulation, corpus luteum formation and regres-sion. Anim. Reprod. Sci. 2004; 82-83: 127-140.
Berisha B, Schams D. Ovarian function in ruminants. Do-mestic Animal Endocrinology. 2005; 29: 305-317.
Richards JS, Russell DL, Ochsner S, Espey LL. Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu. Rev. Physiol. 2002; 64: 69-92.
Ohnishi J, Ohnishi E, Shibuya H, Takahashi T. Functions for proteinases in the ovulatory process. Biochim. Biophys. Acta. 2005; 1751: 95-109.
Weigel PH, Hascall VC, Tammi M. Hyaluronan syntha-ses. J. Biol. Chem. 1997; 272: 13997-14000.
Yoshioka S, Ochsner S, Russell DL, Ujioka T, Fujii S, et al. Expression of tumor necrosis factor stimulated gene- 6 in the rat ovary in response to an ovulatory dose of gonado-tropin. Endocrinology. 2000; 141: 4114-4119. [59] Salustri A, Camaioni A, Giacomo MD, Fulop C, Hascall VC. Hyaluronan and proteoglycans in ovarian follicles. Hum. Reprod. Update. 1999; 5: 293-301.
Webb R, Woad KJ, Armstrong DG. Corpus luteum (cl) function: local control mechanisms. Domest. Anim. En-docrinol. 2002; 23: 277-285.
Stouffer RL. Structure, Function, and Regulation of the Corpus Luteum. In: Neill J, editor. Knobil and Neill’s Physiology of Reproduction. 3rd ed. San Diego: Elsevier Incorporated, 2006; p. 475-526.
Jablonka-Shariff A, Grazul-Bilska AT, Redmer DA, Rey-nolds LP. Growth and cellular proliferation of ovine cor-pora lutea throughout the estrous cycle. Endocrinology. 1993; 133: 1871-1879.
Bao B, Garverick HA. Expression of steroidogenic en-zyme and gonadotropin receptor genes in bovine folli-cles during ovarian follicular waves: a review. J. Anim. Sci. 1998; 76: 1903-1921.
Reynolds L, Grazul-Bilska A, Redmer D. Angiogenesis in the corpus luteum. Endocrine. 2000; 12: 1-9.
Kobayashi S, Berisha B, Amselburger W, Schams D, Mi-yamoto A. Production and localization of angiotensin II in the bovine early corpus luteum: a possible interaction with luteal angiogenic factors and prostaglandin F2a. J. Endocrinol. 2001; 170: 369-380.
Krisans SK. Cell compartmentalization of cholesterol byosynthesis. Ann. N. Y. Acad. Sci. 1996; 804: 142-164.
Scallen TJ, Pastuszyn A, Noland BJ, Chanderbhan R Kharroubi A, Vahouny GV. 1985. Sterol carrier and lipid transfer proteins. Chem. Phys. Lipids. 1985; 38: 239-261.
Stevens VL, Xu T, Lambeth JD. Cholesterol trafficking in steroidogenic cells: reversible cycloheximide-dependent accumulation of cholesterol in a presteroidogenic pool. Eur. J. Biochem. 1993; 216: 557-563.
Hanukoglu I. Steroidogenic enzymes: structure, function, and role in regulation of steroid hormone biosynthesis. J. Steroid Biochem. Mol. Biol. 1992; 43: 779-804.
Koelle S, Sinowatz F, Boie G, Lincoln D. Developmental changes in the expression of the growth hormone recep-tor messenger ribonucleic acid and protein in the bovine ovary. Biol. Reprod. 1998; 59: 836-842.
Tekpetey FR, Armstrong DT. Steroidogenic response of rat and pig luteal cells to estradiol-17β and catecholestro-gens in vitro. Biol. Reprod. 1991; 45: 498-505.
Chegini N, Lei ZM, Rao CV, Hansel W. Cellular distri-bution and cycle phase dependence of gonadotropin and eicosanoid binding sites in bovine corpora lutea. Biol. Re-prod. 1991; 45: 506-513.
Schams D, Berisha B. Regulations of corpus luteum function in cattle –an overview. Reprod. Domest. Anim. 2004; 39: 241-251.
Schams D, Berisha B. Steroids as local regulators of ova-rian activity in domestic animals. Domest. Anim. Endo-crinol. 2002; 23: 53-65.
En calidad de autor del artículo, declaro que este, es un trabajo original, inédito, de mi creación exclusiva, que no se ha postulado a evaluación simultánea en otra publicación y que no cuenta con algún impedimento de cualquier naturaleza para la concesión de los derechos previstos en este contrato.
En ese sentido, me comprometo a esperar un resultado de evaluación de la revista, antes de considerar su presentación a otro medio, en caso de que la respuesta de publicación no sea positiva; adicionalmente, me comprometo a responder por cualquier acción de reivindicación, plagio u otra clase de reclamación que al respecto pudiera sobrevivir por parte de terceros.
Asimismo, declaro que como autor o coautor, estoy de acuerdo por completo con los contenidos presentados en este trabajo y cedo todos los derechos patrimoniales, es decir, la reproducción, comunicación pública, distribución, divulgación, transformación, puesta a disposición y demás formas de explotación de la obra por cualquier medio o procedimiento, a la revista y a la Editorial de la Universidad Cooperativa de Colombia.
