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Publication Date: 2010-06-18
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Uribe Velásquez, L. F., Restrepo Cadavid, R., & Osorio, J. H. (2010). changes in the secretion of ovarian steroids and luteinizing hormone during the estrous cycle in the ewe - a review. Biosalud, 9(1), 64–78. Retrieved from https://revistasojs.ucaldas.edu.co/index.php/biosalud/article/view/5513
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Abstract
Ewes and rams from temperate latitudes show seasonal variations in reproductive activity. Sheep sexual activity is stimulated by alterations in the photoperiod, so that animals displaying reproductive seasonality can reduce their response to seasonality as latitude decreases. A functional hypothalamic pituitary axis is essential for mammalian reproduction, since the hypothalamus secretes the decapeptide, gonadotropin-releasing hormone (GnRH) that is responsible for initiating the cascade of events that regulate gonadal function. During the estrous cycle of the ewe, circulating LH and P4 levels are inversely related, thus providing circumstantial evidence that progesterone may inhibit tonic LH secretion. Progesterone (P4), in terms of the cumulative duration of its effects, is the most important ovarian steroid secreted during the lifetime of the female mammal and it’s central to the complex regulation of normal reproductive function. During the luteal phase of the estrous cycle, the P4 produced by the corpus luteum inhibits hypothalamic GnRH secretion, and consequently, peripheral gonadotrophin concentrations are low. The follicular phase, which is initiated by the decline in circulating P4 concentrations after luteolysis, is characterized by increased gonadotrophin and Estradiol (E2) secretion. This rise in circulating E2 induces the preovulatory LH surge, which is caused by a robust, abrupt, and continuous increase in GnRH secretion. Serial measurements of E2, P4 and LH during ovulation time in the ewe have shown that maximum secretion of estrogen from pre-ovulatory follicles precedes the LH surge. Recent data show that other steroids secreted by the pre-ovulatory follicle may act synergistically with oestradiol in inducing ovulation. The present review was undertaken to observe discuss the temporal relationship between circulating LH and the secretion of the ovarian steroids, estradiol 17-β and progesterone, during the oestrous cycle in the ewe.
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References
Goodman RL, Karsch FJ. Pulsatile secretion of luteinizing hormone: Differential suppression by ovarian steroids. Endocrinol 1980; 107:1286-1290.
Tsukamura H. Neuroendocrine mechanism regulating luteinizing hormone secretion during periovulatory period: Negative and positive feedback actions of estrogen in the brain. J Reprod Dev 1998; 44:j81-j90.
Joseph IBJK, Rawlings NC. Infusion of estradiol during the luteal phase of the estrous cycle in the ewe completely eliminates LH pulses. Can J Anim Sci 1990; 70:1147-1150.
Thiéry JC, Martin GB. Neurophysiological control of the secretion of gonadotrophin-releasing hormone and luteinizing hormone in sheep -A review. Reprod Fertil Dev 1991; 3:137-173.
Goodman RL, Bittman EL, Foster DL, Karsch FJ. Alterations in the control of luteinizing hormone pulse frequency underline the seasonal variation in estradiol negative feedback in the ewe. Biol Reprod 1982; 27:580-589.
Goodman RL, Bittman EL, Foster DL, Karsch FJ. The endocrine basis of the synergistic suppression of luteinizing hormone by estradiol and progesterone. Endocrinol 1981; 109:1414-1417.
Clarke IJ, Cummins JT. GnRH pulse frequency determines LH pulse amplitude by altering the amount of releasable LH in the pituitary glands of ewes. J Reprod Fertil 1985; 73:425-431.
Whisnant CS, Goodman RL. Effect of anterior hypothalamic deafferentation on the negative feedback of gonadal steroids on luteinizing hormone pulse frequency in the ewe. Domest Anim Endocrinol 1994; 11:151-159.
Legan SJ, Karsch FJ. Neuroendocrine regulation of the estrous cycle and seasonal breeding in the ewe. Biol Reprod 1979; 20:74-85.
Martin GB, Thomas GB, Terqui M, Warner P. Pulsatile LH secretion during the preovulatory surge in the ewe: experimental observations and theoretical considerations. Reprod Nutr Dév 1987; 27:1023-1040.
Karsch FJ, Legan SJ, Hauger RL, Foster DL. Negative feedback action of progesterone on tonic luteinizing hormone secretion in the ewe: Dependence on the ovaries. Endocrinol 1977; 101:800-806.
Geschwind II, Dewey R. Dynamics of luteinizing hormone (LH) secretion in the cycling ewe: a radioimmunoassay study. Proc Soc Exp Biol Med 1968; 129:451-459.
Goding JR, Catt KJ, Brown JM, Kaltenbach CC, Cumming IA, Mole BJ. Radioimmunoassay for ovine luteinizing hormone secretion of luteinizing hormone during estrus and following estrogen administration in the sheep. Endocrinol 1969; 85:133-142.
Roche JF, Foster DL, Karsch FJ, Cook B, Dziuk PJ. Levels of luteinizing hormone in sera and pituitaries of ewes during the estrous cycle and anestrus. Endocrinol 1970; 86:568-572.
Abkar AM, Nett TM, Niswender GD. Metabolic clearance and secretion rates of gonadotropins at differents stages of the estrous cycle in ewes. Endocrinol 1974; 94:1310-1024.
Martin GB, Oldham CM, Lindsay DR. Increased plasma LH in seasonally anovular Merino ewes following the introduction of rams. Anim Reprod Sci 1980; 3:125-132.
Karsch FJ, Foster DL, Bittman EL, Goodman RL. A role for estradiol in enhancing luteinizing hormone pulse frequency during the follicular phase of the estrous cycle of sheep. Endocrinol 1983; 113:1333-1339.
Leyva V, Buckrell BC, Walton JS. Regulation of follicular and ovulation in ewes by exogenous progestagen. Theriogenol 1998; 50:395-416.
Martin GB. Factors affecting the secretion of luteinizing hormone in the ewe. Biol Rev 1984; 59:1-87.
Cunningham NF, Symons AM, Saba N. Levels of progesterone, LH and FSH in the plasma of sheep during the oestrus cycle. J Reprod Fertil, 1975; 45:177-180.
Pant HC, Hopkinson CRN, Fitzpatrick RJ. Concentration of oestradiol, progesterone, luteinizing hormone and follicle-stimulating hormone in the jugular venous plasma of ewes during the oestrus cycle. J Endocrinol 1977; 73:247-255.
Chandra RS, Rao PN, Sadhani R. Radioimmunoassay of plasma levels of luteinizing hormone during estrous cycle and early pregnancy in Deccani ewes. Indian Vet J 1990; 67:827-830.
González-Reyna A, Valencia MJ, Foote WC, Murphy BD. Hair sheep in México: reproduction in the Pelibuey sheep. Anim Breed Abstr 1991; 59:509-524.
Smith JF, Briggs RM, Parr J, Johnson DL, Duganzich DM. Seasonal changes in LH profiles of ewes selected for and against an early lambing date. In: Conference of New Zealand Society of Animal Production, 55, 1995, Otago. Proceedings... Otago: New Zealand Society of Animal Production, 1995;224-227.
Campbell BK, Mann GE, McNeilly AS, Baird DT. Pulsatile secretion of inhibin, oestradiol and androstenedione by the ovary of the sheep during the oestrus cycle. J Endocrinol 1990a; 126:385-393.
Yuthasastrakosol P, Palmer WM, Howland BE. Release of LH in anoestrus and cyclic ewes. J Reprod Fertil 1977; 50:319-321.
Foster DL, Lemons JA, Jaffe RB, Niswender GD. Sequencial patterns of circulating luteinizing hormone and follicle-stimulating hormone in female sheep from early postnatal life throught the first estrous cycles. Endocrinol 1975; 97:985-994.
Baird DT, Scaramuzzi RJ. Changes in the secretion of ovarian steroids and pituitary luteinizing hormone in the peri-ovulatory period in the ewe: The effect of progesterone. J Endocrinol 1976; 70:237-245.
McNeilly AS, Picton HM, Campbell BK, Baird DT. Gonadotrofic control of follicle growth in the ewe. J Reprod Fertil Suppl 1991; 43:177-186.
Scaramuzzi RJ, Adams NR, Baird DT, Campbell BK, Downing JA, Findlay JK, et al. A model for follicle selection and the determination of ovulation rate in the ewe. Reprod Fertil Dev 1993; 5:459-478.
McNatty KP, Hudson NL, Henderson KM, Lun S, Heath DA, Gibb M, et al. Changes in gonadotrophin secretion and ovarian antral follicular activity in seasonally breeding sheep throught the year. J Reprod Fertil 1984; 70:309-321.
Montgomery GW, Martin GB, Pelletier J. Changes in pulsatile LH secretion after ovariectomy in Ilede-France in two seasons. J Reprod Fertil 1993; 73:173-183.
Brooks AN, Lamming GE, Lees PD, Haynes NB. Opiod modulation of LH secretion in the ewe. J Reprod Fertil 1986; 76:693-708.
Haresign W, Cooper AC, Khalid M, Hanrahan JP. Patterns of gonadotropin secretion in cyclic Finn ewes selected for low and again high ovulation rate. Anim Sci 1995; 61:251-257.
Thomas GB, Martin GB, Ford JR, Moore PM, Campbell BK, Lindsay DR. Secretion of LH, FSH and oestradiol-17β during the follicular phase of the oestrus cycle in the ewe. Aust J Biol Sci 1988; 41:303-308.
Norris TA, Weesner GD, Shelton JM, Harms PG, Forrest DW. Biological activity of LH during the peripartum period and the estrous cycle of the ewe. Domest Anim Endocrinol 1989; 61:25-33.
Alecozay A, Selcer KW, Clark JR, Burns JM, Norman RL, Niswender GD, et al. Pattern of ovarian progesterone secretion during the luteal phase of the ovine estrous cycle. Biol Reprod 1988; 39:287-294.
Downing JA, Joss J, Scaramuzzi RJ. Ovulation rate and the concentrations of LH, FSH, GH, prolactin and insulin in ewes infused with tryptophan, tyrosine or tyrosine plus phenyalanine during the luteal phase of the oestrus cycle. Anim Reprod Sci 1997; 45:283-297.
Baird DT, Swanston IA, McNeilly AS. Relationship between LH, FSH, and prolactin concentration and the secretion of androgens and estrogens by the preovulatory follicle in the ewe. Biol Reprod 1981; 24:1013-1025.
Rhind SM, McNeilly AS. Follicle populations, ovulation rates and plasma profiles of LH, FSH and prolactin in Scottish Blackface ewes in high and low levels of body condition. Anim Reprod Sci 1986; 10:105-115.
Cahill LP, Mauleón P. A study of the population of primordial and small follicles in the sheep. J Reprod Fertil 1981; 62:201-206.
Currie WD, Medhamurthy RJ, Cook SJ, Rawlings NC. Seasonal fluctuation in diurnal rhythms of luteinizing hormone secretion in ewes during the mid-luteal phase of the oestrus cycle. J Reprod Fertil 1993; 97:71-74.
Lucy MC, Savio JD, Badinga L, De La Sota RL, Thatcher WW. Factors that affect ovarian follicular dynamics in cattle. J Anim Sci 1992; 70:3615-3626.
Uribe-Velásquez LF, Oba E, Souza MIL. Efeitos da progesterona exógena sobre o desenvolvimento folicular em ovelhas. Arq Bras Med Vet Zoo 2008; 60:58-65.
Driancourt MA, Gougeon A, Royère D, Thibault C. Ovarian function. In: Thibault C, Levasseur MC. Reprod mam man. RHF. Hunter, 1993; 15:283-305.
Baird DT, Land RB, Scaramuzzi RJ, Wheeler AG. Endocrine changes associated with luteal regression in the ewe: the secretion of ovarian oestradiol, progesterone and androstenedione and uterine prostaglandin F2α throught the oestrus cycle. J Endocrinol 1976; 69:275-286.
Stabenfeldt GH, Holt JA, Ewing LL. Peripheral plasma progesterone levels during the ovine estrous cycle. Endocrinol 1969; 85:11-15.
Chamley WA, Buckmaster JM, Cain MD, Cerini J, Cerini ME, et al. The effect of prostaglandin F2α on progesterone, oestradiol and luteinizing hormone secretion in sheep with ovarian transplants. J Endocrinol 1972; 55:253-263.
Quirke JF, Hanrahan JP, Gosling JP. Plasma progesterone levels throughout the oestrus cycle and release of LH at oestrus in sheep with different ovulation rates. J Reprod Fertil 1979; 55:37-44.
Hauger RL, Karsch FD, Foster DL. A new concept for control of the estrous cycle of the ewe based on the temporal relationship between luteinizing hormone, estradiol and progesterone in peripheral serum and evidence that progesterone inhibits tonic LH secretion. Endocrinol 1977; 101:807-817.
Baird DT, Swanston I, Scaramuzzi RJ. Pulsatile release of LH and secretion of ovarian steroids in sheep during the luteal phase of the estrous cycle. Endocrinol 1976; 98:1490-1496.
Karsch FJ, Foster DL, Legan SJ, Ryan KD, Peter GK. Control of the preovulatory endocrine events in the ewe: Interrelationship of estradiol, progesterone, and luteinizing hormone. Endocrinol 1979; 105:421-426.
Uribe-Velásquez LF, Oba E, Souza MIL. Población folicular y concentraciones plasmáticas de progesterona (P4) en ovejas sometidas a diferentes protocolos de sincronización. Arch Med Vet 2008; 40:83-88.
Evans G, Robinson TJ. The control of fertility in sheep: endocrine and ovarian response to progestagen-PMSG treatment in the breeding season and in anoestrous. J Agric Sci 1980; 94:69-88.
Uribe-Velásquez LF, Souza MIL, Osorio JH. Resposta ovariana de cabras submetidas a implantes de progesterona seguidos de aplicações de gonadotrofina coriônica equina. R Bras Zootec 2010; 39:1214-1222.
Tsonis CG, Carson RS, Findlay J.K. Relationships between aromatase activity, follicular fluid oestradiol-17β and testosterone concentrations, and diameter and atresia of individual ovine follicles. J Reprod Fertil 1984; 72:153-163.
Rhind SM, McNeilly AS. Effect of level of food intake on ovarian follicle number, size and steroidogenic capacity in the ewe. Anim Reprod Sci 1998; 52:131-138.
Campbell BK, Mann GE, McNeilly AS, Baird DT. The pattern of ovarian inhibin, estradiol, and androstenedione secretion during the estrous cycle of the ewe. Endocrinol 1990; 127:227-235.
Holst PJ, Braden AWH, Mattner PE. Oestradiol-17β secretion from the ewe ovary and related ovarian morphology days 2 and 3 of the cycle. J Reprod Fertil 1972; 28:136.
Holst PJ, Braden AWH, Mattner PE. Association between ovarian follicular development and oestradiol-17β secretion 3 to 4 days after oestrus in ewes. J Endocrinol 1972; 53:171-172.
Dott HM, Hay MF, Cran DG, Moor RM. Effect of exogenous gonadotrophin (PMSG) on the antral follicle population in the sheep. J Reprod Fertil 1979; 56:683-689.
Webb R, England BG. Identification of the ovulatory follicle in the ewe: Associated changes in follicular size, thecal and granulosa cell luteinizing hormone receptors, antral fluid steorids, and circulating hormones during the preovulatory period. Endocrinol 1982; 110:873-881.
Hay MF, Moor RM. Functional and structural relationship in the graafian follicle population of the sheep ovary. J Reprod Fertil 1975; 45:583-593.
Johnson SK, Dailey RA, Inskeep EK, Lewis PE. Effect of peripheral concentrations of progesterone on follicular growth and fertility in ewes. Domest Anim Endocrinol 1996; 13:69-79.
Baird DT, Scaramuzzi RJ. The source of ovarian oestradiol and androstenedione in the sheep during the luteal phase. Acta Endocrinol 1976; 83:402-409.
Scaramuzzi RJ, Land RB. Oestradiol levels in sheep plasma during the oestrus cycle. J Reprod Fertil 1983; 53:167-171.
Scaramuzzi RJ, Radford HM. Factors regulating ovulation rate in the ewe. J Reprod Fertil 1983; 69:353-367.
Kruip AM, Brand A. Follicular growth during the normal cycle and after treatment with progestagens in the ewe. Ann Biol Anim Biochem Biophys 1975; 15:191-204.
Mattner PE, Braden AWH. Secretion of oestradiol-17β by the ovine ovary during the luteal phase of the oestrus cycle in relation to ovulation. J Reprod Fertil 1972; 28:136-137.
Uribe-Velásquez LF, Souza MIL, Loaiza AM. Efecto de la sincronización del estro con prostaglandina-F2α vs CIDR + 500 UI de eCG en ovejas Bergamacia durante el inicio de la fase luteal. Rev Científica 2008; XVIII: 4:368-373.
Uribe-Velásquez LF, Oba E, Lara-Herrera LC. Respostas endócrinas e ovarianas associadas com o folículo dominante da primeira onda folicular em ovelhas sincronizadas com CIDR ou PGF2α. Rev Bras Zoo 2002; 31: 2: 944-953.
Tsukamura H. Neuroendocrine mechanism regulating luteinizing hormone secretion during periovulatory period: Negative and positive feedback actions of estrogen in the brain. J Reprod Dev 1998; 44:j81-j90.
Joseph IBJK, Rawlings NC. Infusion of estradiol during the luteal phase of the estrous cycle in the ewe completely eliminates LH pulses. Can J Anim Sci 1990; 70:1147-1150.
Thiéry JC, Martin GB. Neurophysiological control of the secretion of gonadotrophin-releasing hormone and luteinizing hormone in sheep -A review. Reprod Fertil Dev 1991; 3:137-173.
Goodman RL, Bittman EL, Foster DL, Karsch FJ. Alterations in the control of luteinizing hormone pulse frequency underline the seasonal variation in estradiol negative feedback in the ewe. Biol Reprod 1982; 27:580-589.
Goodman RL, Bittman EL, Foster DL, Karsch FJ. The endocrine basis of the synergistic suppression of luteinizing hormone by estradiol and progesterone. Endocrinol 1981; 109:1414-1417.
Clarke IJ, Cummins JT. GnRH pulse frequency determines LH pulse amplitude by altering the amount of releasable LH in the pituitary glands of ewes. J Reprod Fertil 1985; 73:425-431.
Whisnant CS, Goodman RL. Effect of anterior hypothalamic deafferentation on the negative feedback of gonadal steroids on luteinizing hormone pulse frequency in the ewe. Domest Anim Endocrinol 1994; 11:151-159.
Legan SJ, Karsch FJ. Neuroendocrine regulation of the estrous cycle and seasonal breeding in the ewe. Biol Reprod 1979; 20:74-85.
Martin GB, Thomas GB, Terqui M, Warner P. Pulsatile LH secretion during the preovulatory surge in the ewe: experimental observations and theoretical considerations. Reprod Nutr Dév 1987; 27:1023-1040.
Karsch FJ, Legan SJ, Hauger RL, Foster DL. Negative feedback action of progesterone on tonic luteinizing hormone secretion in the ewe: Dependence on the ovaries. Endocrinol 1977; 101:800-806.
Geschwind II, Dewey R. Dynamics of luteinizing hormone (LH) secretion in the cycling ewe: a radioimmunoassay study. Proc Soc Exp Biol Med 1968; 129:451-459.
Goding JR, Catt KJ, Brown JM, Kaltenbach CC, Cumming IA, Mole BJ. Radioimmunoassay for ovine luteinizing hormone secretion of luteinizing hormone during estrus and following estrogen administration in the sheep. Endocrinol 1969; 85:133-142.
Roche JF, Foster DL, Karsch FJ, Cook B, Dziuk PJ. Levels of luteinizing hormone in sera and pituitaries of ewes during the estrous cycle and anestrus. Endocrinol 1970; 86:568-572.
Abkar AM, Nett TM, Niswender GD. Metabolic clearance and secretion rates of gonadotropins at differents stages of the estrous cycle in ewes. Endocrinol 1974; 94:1310-1024.
Martin GB, Oldham CM, Lindsay DR. Increased plasma LH in seasonally anovular Merino ewes following the introduction of rams. Anim Reprod Sci 1980; 3:125-132.
Karsch FJ, Foster DL, Bittman EL, Goodman RL. A role for estradiol in enhancing luteinizing hormone pulse frequency during the follicular phase of the estrous cycle of sheep. Endocrinol 1983; 113:1333-1339.
Leyva V, Buckrell BC, Walton JS. Regulation of follicular and ovulation in ewes by exogenous progestagen. Theriogenol 1998; 50:395-416.
Martin GB. Factors affecting the secretion of luteinizing hormone in the ewe. Biol Rev 1984; 59:1-87.
Cunningham NF, Symons AM, Saba N. Levels of progesterone, LH and FSH in the plasma of sheep during the oestrus cycle. J Reprod Fertil, 1975; 45:177-180.
Pant HC, Hopkinson CRN, Fitzpatrick RJ. Concentration of oestradiol, progesterone, luteinizing hormone and follicle-stimulating hormone in the jugular venous plasma of ewes during the oestrus cycle. J Endocrinol 1977; 73:247-255.
Chandra RS, Rao PN, Sadhani R. Radioimmunoassay of plasma levels of luteinizing hormone during estrous cycle and early pregnancy in Deccani ewes. Indian Vet J 1990; 67:827-830.
González-Reyna A, Valencia MJ, Foote WC, Murphy BD. Hair sheep in México: reproduction in the Pelibuey sheep. Anim Breed Abstr 1991; 59:509-524.
Smith JF, Briggs RM, Parr J, Johnson DL, Duganzich DM. Seasonal changes in LH profiles of ewes selected for and against an early lambing date. In: Conference of New Zealand Society of Animal Production, 55, 1995, Otago. Proceedings... Otago: New Zealand Society of Animal Production, 1995;224-227.
Campbell BK, Mann GE, McNeilly AS, Baird DT. Pulsatile secretion of inhibin, oestradiol and androstenedione by the ovary of the sheep during the oestrus cycle. J Endocrinol 1990a; 126:385-393.
Yuthasastrakosol P, Palmer WM, Howland BE. Release of LH in anoestrus and cyclic ewes. J Reprod Fertil 1977; 50:319-321.
Foster DL, Lemons JA, Jaffe RB, Niswender GD. Sequencial patterns of circulating luteinizing hormone and follicle-stimulating hormone in female sheep from early postnatal life throught the first estrous cycles. Endocrinol 1975; 97:985-994.
Baird DT, Scaramuzzi RJ. Changes in the secretion of ovarian steroids and pituitary luteinizing hormone in the peri-ovulatory period in the ewe: The effect of progesterone. J Endocrinol 1976; 70:237-245.
McNeilly AS, Picton HM, Campbell BK, Baird DT. Gonadotrofic control of follicle growth in the ewe. J Reprod Fertil Suppl 1991; 43:177-186.
Scaramuzzi RJ, Adams NR, Baird DT, Campbell BK, Downing JA, Findlay JK, et al. A model for follicle selection and the determination of ovulation rate in the ewe. Reprod Fertil Dev 1993; 5:459-478.
McNatty KP, Hudson NL, Henderson KM, Lun S, Heath DA, Gibb M, et al. Changes in gonadotrophin secretion and ovarian antral follicular activity in seasonally breeding sheep throught the year. J Reprod Fertil 1984; 70:309-321.
Montgomery GW, Martin GB, Pelletier J. Changes in pulsatile LH secretion after ovariectomy in Ilede-France in two seasons. J Reprod Fertil 1993; 73:173-183.
Brooks AN, Lamming GE, Lees PD, Haynes NB. Opiod modulation of LH secretion in the ewe. J Reprod Fertil 1986; 76:693-708.
Haresign W, Cooper AC, Khalid M, Hanrahan JP. Patterns of gonadotropin secretion in cyclic Finn ewes selected for low and again high ovulation rate. Anim Sci 1995; 61:251-257.
Thomas GB, Martin GB, Ford JR, Moore PM, Campbell BK, Lindsay DR. Secretion of LH, FSH and oestradiol-17β during the follicular phase of the oestrus cycle in the ewe. Aust J Biol Sci 1988; 41:303-308.
Norris TA, Weesner GD, Shelton JM, Harms PG, Forrest DW. Biological activity of LH during the peripartum period and the estrous cycle of the ewe. Domest Anim Endocrinol 1989; 61:25-33.
Alecozay A, Selcer KW, Clark JR, Burns JM, Norman RL, Niswender GD, et al. Pattern of ovarian progesterone secretion during the luteal phase of the ovine estrous cycle. Biol Reprod 1988; 39:287-294.
Downing JA, Joss J, Scaramuzzi RJ. Ovulation rate and the concentrations of LH, FSH, GH, prolactin and insulin in ewes infused with tryptophan, tyrosine or tyrosine plus phenyalanine during the luteal phase of the oestrus cycle. Anim Reprod Sci 1997; 45:283-297.
Baird DT, Swanston IA, McNeilly AS. Relationship between LH, FSH, and prolactin concentration and the secretion of androgens and estrogens by the preovulatory follicle in the ewe. Biol Reprod 1981; 24:1013-1025.
Rhind SM, McNeilly AS. Follicle populations, ovulation rates and plasma profiles of LH, FSH and prolactin in Scottish Blackface ewes in high and low levels of body condition. Anim Reprod Sci 1986; 10:105-115.
Cahill LP, Mauleón P. A study of the population of primordial and small follicles in the sheep. J Reprod Fertil 1981; 62:201-206.
Currie WD, Medhamurthy RJ, Cook SJ, Rawlings NC. Seasonal fluctuation in diurnal rhythms of luteinizing hormone secretion in ewes during the mid-luteal phase of the oestrus cycle. J Reprod Fertil 1993; 97:71-74.
Lucy MC, Savio JD, Badinga L, De La Sota RL, Thatcher WW. Factors that affect ovarian follicular dynamics in cattle. J Anim Sci 1992; 70:3615-3626.
Uribe-Velásquez LF, Oba E, Souza MIL. Efeitos da progesterona exógena sobre o desenvolvimento folicular em ovelhas. Arq Bras Med Vet Zoo 2008; 60:58-65.
Driancourt MA, Gougeon A, Royère D, Thibault C. Ovarian function. In: Thibault C, Levasseur MC. Reprod mam man. RHF. Hunter, 1993; 15:283-305.
Baird DT, Land RB, Scaramuzzi RJ, Wheeler AG. Endocrine changes associated with luteal regression in the ewe: the secretion of ovarian oestradiol, progesterone and androstenedione and uterine prostaglandin F2α throught the oestrus cycle. J Endocrinol 1976; 69:275-286.
Stabenfeldt GH, Holt JA, Ewing LL. Peripheral plasma progesterone levels during the ovine estrous cycle. Endocrinol 1969; 85:11-15.
Chamley WA, Buckmaster JM, Cain MD, Cerini J, Cerini ME, et al. The effect of prostaglandin F2α on progesterone, oestradiol and luteinizing hormone secretion in sheep with ovarian transplants. J Endocrinol 1972; 55:253-263.
Quirke JF, Hanrahan JP, Gosling JP. Plasma progesterone levels throughout the oestrus cycle and release of LH at oestrus in sheep with different ovulation rates. J Reprod Fertil 1979; 55:37-44.
Hauger RL, Karsch FD, Foster DL. A new concept for control of the estrous cycle of the ewe based on the temporal relationship between luteinizing hormone, estradiol and progesterone in peripheral serum and evidence that progesterone inhibits tonic LH secretion. Endocrinol 1977; 101:807-817.
Baird DT, Swanston I, Scaramuzzi RJ. Pulsatile release of LH and secretion of ovarian steroids in sheep during the luteal phase of the estrous cycle. Endocrinol 1976; 98:1490-1496.
Karsch FJ, Foster DL, Legan SJ, Ryan KD, Peter GK. Control of the preovulatory endocrine events in the ewe: Interrelationship of estradiol, progesterone, and luteinizing hormone. Endocrinol 1979; 105:421-426.
Uribe-Velásquez LF, Oba E, Souza MIL. Población folicular y concentraciones plasmáticas de progesterona (P4) en ovejas sometidas a diferentes protocolos de sincronización. Arch Med Vet 2008; 40:83-88.
Evans G, Robinson TJ. The control of fertility in sheep: endocrine and ovarian response to progestagen-PMSG treatment in the breeding season and in anoestrous. J Agric Sci 1980; 94:69-88.
Uribe-Velásquez LF, Souza MIL, Osorio JH. Resposta ovariana de cabras submetidas a implantes de progesterona seguidos de aplicações de gonadotrofina coriônica equina. R Bras Zootec 2010; 39:1214-1222.
Tsonis CG, Carson RS, Findlay J.K. Relationships between aromatase activity, follicular fluid oestradiol-17β and testosterone concentrations, and diameter and atresia of individual ovine follicles. J Reprod Fertil 1984; 72:153-163.
Rhind SM, McNeilly AS. Effect of level of food intake on ovarian follicle number, size and steroidogenic capacity in the ewe. Anim Reprod Sci 1998; 52:131-138.
Campbell BK, Mann GE, McNeilly AS, Baird DT. The pattern of ovarian inhibin, estradiol, and androstenedione secretion during the estrous cycle of the ewe. Endocrinol 1990; 127:227-235.
Holst PJ, Braden AWH, Mattner PE. Oestradiol-17β secretion from the ewe ovary and related ovarian morphology days 2 and 3 of the cycle. J Reprod Fertil 1972; 28:136.
Holst PJ, Braden AWH, Mattner PE. Association between ovarian follicular development and oestradiol-17β secretion 3 to 4 days after oestrus in ewes. J Endocrinol 1972; 53:171-172.
Dott HM, Hay MF, Cran DG, Moor RM. Effect of exogenous gonadotrophin (PMSG) on the antral follicle population in the sheep. J Reprod Fertil 1979; 56:683-689.
Webb R, England BG. Identification of the ovulatory follicle in the ewe: Associated changes in follicular size, thecal and granulosa cell luteinizing hormone receptors, antral fluid steorids, and circulating hormones during the preovulatory period. Endocrinol 1982; 110:873-881.
Hay MF, Moor RM. Functional and structural relationship in the graafian follicle population of the sheep ovary. J Reprod Fertil 1975; 45:583-593.
Johnson SK, Dailey RA, Inskeep EK, Lewis PE. Effect of peripheral concentrations of progesterone on follicular growth and fertility in ewes. Domest Anim Endocrinol 1996; 13:69-79.
Baird DT, Scaramuzzi RJ. The source of ovarian oestradiol and androstenedione in the sheep during the luteal phase. Acta Endocrinol 1976; 83:402-409.
Scaramuzzi RJ, Land RB. Oestradiol levels in sheep plasma during the oestrus cycle. J Reprod Fertil 1983; 53:167-171.
Scaramuzzi RJ, Radford HM. Factors regulating ovulation rate in the ewe. J Reprod Fertil 1983; 69:353-367.
Kruip AM, Brand A. Follicular growth during the normal cycle and after treatment with progestagens in the ewe. Ann Biol Anim Biochem Biophys 1975; 15:191-204.
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