Importance of preovulatory estradiol on uterine receptivity and luteal function
George Allen Perry; Jaclyn Nicole Ketchum; Lacey Kay Quail
Abstract
Keywords
References
Adashi EY, Hsueh AJ. Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa cells. J Biol Chem. 1982;257(11):6077-83.
Albrecht U. Orchestration of gene expression and physiology by the circadian clock. J Physiol Paris. 2006;100(5-6):243-51.
Allrich RD. Endocrine and neural control of estrus in dairy cows. J Dairy Sci. 1994;77(9):2738-44.
Atkins JA, Smith MF, MacNeil MD, Jinks EM, Abreu FM, Alexander LJ, Geary TW. Pregnancy establishment and maintenance in cattle. J Anim Sci. 2013;91(2):722-33.
Bartol FF, Thatcher WW, Lewis GS, Bliss EL, Drost M, Bazer FW. Effect of estradiol-17beta on PGF and total protein content in bovine uterine flushings and peripheral plasma concentration of 13, 14-dihydro-15-keto-PGF(2alpha). Theriogenology. 1981;15(4):345-58.
Baruselli PS, Marques MO, Carvalho NA, Berber RA, Valentim R, Carvalho AFD Fo, Costa WP No. Follicular dynamics and pregnancy rate in embryo recipient (Bos taurus indicus x Bos taurus taurus) treated with” Ovsynch” protocol for fixed-time embryo transfer. Braz J Vet Res Anim Sci. 2003;40:96-106.
Bauersachs S, Blum H, Mallok S, Wenigerkind H, Rief S, Prelle K, Wolf E. Regulation of ipsilateral and contralateral bovine oviduct epithelial cell function in the postovulation period: a transcriptomics approach. Biol Reprod. 2003;68(4):1170-7.
Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, Einspanier R, Wenigerkind H, Vermehren M, Blum H, Sinowatz F, Wolf E. Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes. J Mol Endocrinol. 2005;34(3):889-908.
Bazer FW, Terqui M, Martinat-Butte F. Physiological limits to reproduction. In: Proceedings of the 4th World Congress on Genetics Applied to Livestock Production; 1990 Jul 23-27, Edinburgh, Scotland. Edinburgh: The University of Edinburgh; 1990. p. 292-8.
Bó GA, Cedeño A. Expression of estrus as a relevant factor in fixed-time embryo transfer programs using estradiol/progesterone-based protocols in cattle. Anim Reprod. 2018;15(3):224-30.
Boice ML, Geisert RD, Blair RM, Verhage HG. Identification and characterization of bovine oviductal glycoproteins synthesized at estrus. Biol Reprod. 1990;43(3):457-65.
Bollwein H, Meyer HH, Maierl J, Weber F, Baumgartner U, Stolla R. Transrectal doppler sonography of uterine blood flow in cows during the estrous cycle. Theriogenology. 2000;53(8):1541-52.
Bolzenius JK, Cushman RA, Perry GA. Expression of Na(+)/H(+) exchanger isoforms 1, 2, 3, and 4 in bovine endometrium and the influence of uterine pH at time of fixed-time AI of pregnancy success. Anim Reprod Sci. 2016;171:98-107.
Bridges GA, Mussard ML, Pate JL, Ott TL, Hansen TR, Day ML. Impact of preovulatory estradiol concentrations on conceptus development and uterine gene expression. Anim Reprod Sci. 2012;133(1-2):16-26.
Burghardt RC, Anderson E. Hormonal modulation of gap junctions in rat ovarian follicles. Cell Tissue Res. 1981;214(1):181-93.
Butler WR, Calaman JJ, Beam SW. Plasma and milk urea nitrogen in relation to pregnancy rate in lactating dairy cattle. J Anim Sci. 1996;74(4):858-65.
Chappell PE, White RS, Mellon PL. Circadian gene expression regulates pulsatile gonadotropin-releasing hormone (GnRH) secretory patterns in the hypothalamic GnRH-secreting GT1-7 cell line. J Neurosci. 2003;23(35):11202-13.
Chenault JR, Thatcher WW, Kalra PS, Abrams RM, Wilcox CJ. Transitory changes in plasma progestins, estradiol, and luteinizing hormone approaching ovulation in the bovine. J Dairy Sci. 1975;58(5):709-17.
Ciernia LA, Perry GA, Smith MF, Rich JJ, Northrop EJ, Perkins SD, Green JA, Zezeski AL, Geary TW. Effect of estradiol preceding and progesterone subsequent to ovulation on proportion of postpartum beef cows pregnant. Anim Reprod Sci. 2021;227:106723.
Coe BL, Allrich RD. Relationship between endogenous estradiol-17 beta and estrous behavior in heifers. J Anim Sci. 1989;67(6):1546-51.
Dalton JC, Nadir S, Noftsinger M, Bame J, Saacke RG. Management factors associated with male fertility. In: Applied Reproductive Strategies in Beef Cattle; 2006; Rapid City, United States. 2006. p. 279-290.
Davoodi S, Cooke RF, Fernandes AC, Cappellozza BI, Vasconcelos JL, Cerri RL. Expression of estrus modifies the gene expression profile in reproductive tissues on day 19 of gestation in beef cows. Theriogenology. 2016;85(4):645-55.
DeJarnette JM, Saacke RG, Bame J, Vogler CJ. Accessory sperm: their importance to fertility and embryo quality, and attempts to alter their numbers in artificially inseminated cattle. J Anim Sci. 1992;70(2):484-91.
Demetrio DG, Santos RM, Demetrio CG, Vasconcelos JL. Factors affecting conception rates following artificial insemination or embryo transfer in lactating Holstein cows. J Dairy Sci. 2007;90(11):5073-82.
Diskin MG, Niswender GD. Effect of progesterone supplementation on pregnancy and embryo survival in ewes. J Anim Sci. 1989;67(6):1559-63.
Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development. 2000;127(19):4277-91.
Erb RE, Garverick HA, Randel RD, Brown BL, Callahan CJ. Profiles of reproductive hormones associated with fertile and nonfertile inseminations of dairy cows. Theriogenology. 1976;5(5):227-42.
Fanjul LF, Ruiz de Galarreta CM, Hsueh AJ. Estrogen regulation of progestin biosynthetic enzymes in cultured rat granulosa cells. Biol Reprod. 1984;30(4):903-12.
Farookhi R, Desjardins J. Luteinizing hormone receptor induction in dispersed granulosa cells requires estrogen. Mol Cell Endocrinol. 1986;47(1-2):13-24.
Fields SD, Gebhart KL, Perry BL, Gonda MG, Wright CL, Bott RC, Perry GA. Influence of standing estrus before an injection of GnRH during a beef cattle fixed-time AI protocol on LH release, subsequent concentrations of progesterone, and steriodogenic enzyme expression. Domest Anim Endocrinol. 2012;42(1):11-9.
Ford SP, Chenault JR. Blood flow to the corpus luteum-bearing ovary and ipsilateral uterine horn of cows during the oestrous cycle and early pregnancy. J Reprod Fertil. 1981;62(2):555-62.
Forde N, Carter F, Fair T, Crowe MA, Evans AC, Spencer TE, Bazer FW, McBride R, Boland MP, O’Gaora P, Lonergan P, Roche JF. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod. 2009;81(4):784-94.
Forde N, Spencer TE, Bazer FW, Song G, Roche JF, Lonergan P. Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol Genomics. 2010;41(1):53-62.
Fortune JE, Quirk SM. Regulation of steroidogensis in bovine preovulatory follicles. J Anim Sci. 1988;66(Suppl 2):1-8.
Gauvreau D, Moisan V, Roy M, Fortier MA, Bilodeau JF. Expression of prostaglandin E synthases in the bovine oviduct. Theriogenology. 2010;73(1):103-11.
Geisert RD, Morgan GL, Short EC Jr, Zavy MT. Endocrine events associated with endometrial function and conceptus development in cattle. Reprod Fertil Dev. 1992;4(3):301-5.
Goldenberg RL, Bridson WE, Kohler PO. Estrogen stimulation of progesterone synthesis by porcine granulosa cells in culture. Biochem Biophys Res Commun. 1972;48(1):101-7.
Goltz JS, Gardner TK, Kanous KS, Lindemann CB. The interaction of pH and cyclic adenosine 3′,5′-monophosphate on activation of motility in Triton X-100 extracted bull sperm. Biol Reprod. 1988;39(5):1129-36.
Gray CA, Taylor KM, Ramsey WS, Hill JR, Bazer FW, Bartol FF, Spencer TE. Endometrial glands are required for preimplantation conceptus elongation and survival. Biol Reprod. 2001;64(6):1608-13.
Hasler JF. Factors affecting frozen and fresh embryo transfer pregnancy rates in cattle. Theriogenology. 2001;56(9):1401-15.
Hasler JF. Forty years of embryo transfer in cattle: a review focusing on the journal Theriogenology, the growth of the industry in North America, and personal reminisces. Theriogenology. 2014;81(1):152-69.
Hawk HW, Cooper BS. Improvement of sperm transport by the administration of estradiol to estrous ewes. J Anim Sci. 1975;41(5):1400-6.
Hawk HW, Tanabe TY. Effect of unilateral cornual insemination upon fertilization rate in superovulating and single-ovulating cattle. J Anim Sci. 1986;63(2):551-60.
Hawk HW. Sperm survival and transport in the female reproductive tract. J Dairy Sci. 1983;66(12):2645-60.
He PJ, Hirata M, Yamauchi N, Hattori MA. Up-regulation of Per1 expression by estradiol and progesterone in the rat uterus. J Endocrinol. 2007;194(3):511-9.
Henricks DM, Lamond DR, Hill JR, Dickey JF. Plasma progesterone concentrations before mating and in early pregnancy in the beef heifer. J Anim Sci. 1971;33(2):450-4.
Hill JL, Walker SK, Brown GH, Nancarrow CD. The effects of an estrus-associated oviductal glycoprotein on the in vitro fertilization and development of ovine oocytes matured in vitro. Theriogenology. 1996;46(8):1379-88.
Hunter RH, Wilmut I. Sperm transport in the cow: peri-ovulatory redistribution of viable cells within the oviduct. Reprod Nutr Dev. 1984;24(5A):597-608.
Ing NH, Roberts RM. The major progesterone-modulated proteins secreted into the sheep uterus are members of the serpin superfamily of serine protease inhibitors. J Biol Chem. 1989;264(6):3372-9.
Ishiwata H, Katsuma S, Kizaki K, Patel OV, Nakano H, Takahashi T, Imai K, Hirasawa A, Shiojima S, Ikawa H, Suzuki Y, Tsujimoto G, Izaike Y, Todoroki J, Hashizume K. Characterization of gene expression profiles in early bovine pregnancy using a custom cDNA microarray. Mol Reprod Dev. 2003;65(1):9-18.
Jinks EM, Smith MF, Atkins JA, Pohler KG, Perry GA, Macneil MD, Roberts AJ, Waterman RC, Alexander LJ, Geary TW. Preovulatory estradiol and the establishment and maintenance of pregnancy in suckled beef cows. J Anim Sci. 2013;91(3):1176-85.
Jones JM, Bavister BD. Acidification of intracellular pH in bovine spermatozoa suppresses motility and extends viable life. J Androl. 2000;21(5):616-24. PMid:10975407.
Jones RL, Stoikos C, Findlay JK, Salamonsen LA. TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction. 2006;132(2):217-32.
Kennaway DJ. The role of circadian rhythmicity in reproduction. Hum Reprod Update. 2005;11(1):91-101.
Kerbler TL, Buhr MM, Jordan LT, Leslie KE, Walton JS. Relationship between maternal plasma progesterone concentration and interferon-tau synthesis by the conceptus in cattle. Theriogenology. 1997;47(3):703-14.
Kessel B, Liu YX, Jia XC, Hsueh AJ. Autocrine role of estrogens in the augmentation of luteinizing hormone receptor formation in cultured rat granulosa cells. Biol Reprod. 1985;32(5):1038-50.
King RS, Killian GJ. Purification of bovine estrus-associated protein and localization of binding on sperm. Biol Reprod. 1994;51(3):34-42.
Koligian KB, Stormshak F. Progesterone inhibition of estrogen receptor replenishment in ovine endometrium. Biol Reprod. 1977;17(3):412-6.
Larimore EL, Amundson OL, Bird SL, Funnell BJ, Kruse SG, Bridges GA, Perry GA. Influence of estrus at fixed-time artificial insemination on early embryonic development in beef cattle. J Anim Sci. 2015;93(6):2806-12.
Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell. 1997;91(2):197-208.
Lohuis M. Potential benefits of bovine embryo-manipulation technologies to genetic improvement programs. Theriogenology. 1995;43(1):51-60.
Lopes AS, Butler ST, Gilbert RO, Butler WR. Relationship of pre-ovulatory follicle size, estradiol concentrations and season to pregnancy outcome in dairy cows. Anim Reprod Sci. 2007;99(1-2):34-43.
Macmillan KL, Peterson AJ. A new intervagional progesterone releasing device for cattle (CIDR-B) for oestrous synchronisation, increasing pregnancy rates and the treatment of post-partum anestrus. Anim Reprod Sci. 1993;33(1-4):1-25.
Madsen CA, Perry GA, Mogck CL, Daly RF, MacNeil MD, Geary TW. Effects of preovulatory estradiol on embryo survival and pregnancy establishment in beef cows. Anim Reprod Sci. 2015;158:96-103.
Malayer JR, Hansen PJ, Buhi WC. Secretion of proteins by cultured bovine oviducts collected from estrus through early diestrus. J Exp Zool. 1988;248(3):345-53.
Mann GE, Lamming GE, Fisher PA. Progesterone control of embryonic interferon tau production during early pregnancy in the cow. J Reprod Fertil. 1998;21:37.
Mann GE, Lamming GE. Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction. 2001;121(1):175-80.
Martus NS, Verhage HG, Mavrogianis PA, Thibodeaux JK. Enhancement of bovine oocyte fertilization in vitro with a bovine oviductal specific glycoprotein. J Reprod Fertil. 1998;113(2):323-9.
McDonald LE, Nichols RE, McNutt SH. Study of corpus luteum ablation and progesterone replacement therapy during pregnancy in the cow. Am J Vet Res. 1952;13:446-51. PMid:12996761.
McNatty KP, Hunter WM, McNeilly AS, Sawers RS. Changes in the concentration of pituitary and steroid hormones in the follicular fluid of human graafian follicles throughout the menstrual cycle. J Endocrinol. 1975;64(3):555-71.
McNatty KP, Smith DM, Makris A, Osathanondh R, Ryan KJ. The microenvironment of the human antral follicle: interrelationships among the steroid levels in antral fluid, the population of granulosa cells, and the status of the oocyte in vivo and in vitro. J Clin Endocrinol Metab. 1979;49(6):851-60.
Merk FB, Botticelli CR, Albright JT. An intercellular response to estrogen by granulosa cells in the rat ovary; an electron microscope study. Endocrinology. 1972;90(4):992-1007.
Miller BG, Moore NW, Murphy L, Stone GM. Early pregnancy in the ewe: effects of oestradiol and progesterone on uterine metabolism and on embryo survival. Aust J Biol Sci. 1977;30(4):279-88.
Miller BG, Moore NW. Effect of progesterone and oestradiol on endometrial metabolism and embryo survival in the ovariectomized ewe. Theriogenology. 1976;6(6):636.
Monteiro PL Jr, Nascimento AB, Pontes GC, Fernandes GO, Melo LF, Wiltbank MC, Sartori R. Progesterone supplementation after ovulation: effects on corpus luteum function and on fertility of dairy cows subjected to AI or ET. Theriogenology. 2015;84(7):1215-24.
Nadir S, Saacke RG, Bame J, Mullins J, Degelos S. Effect of freezing semen and dosage of sperm on number of accessory sperm, fertility, and embryo quality in artificially inseminated cattle. J Anim Sci. 1993;71(1):199-204.
Nakamura TJ, Moriya T, Inoue S, Shimazoe T, Watanabe S, Ebihara S, Shinohara K. Estrogen differentially regulates expression of Per1 and Per2 genes between central and peripheral clocks and between reproductive and nonreproductive tissues in female rats. J Neurosci Res. 2005;82(5):622-30.
Nancarrow CD, Hill JL. Co-culture, oviduct secretion and the function of oviduct-specific glycoproteins. Cell Biol Int. 1994;18(12):1105-14.
Nephew KP, Cardenas H, McClure KE, Ott TL, Bazer FW, Pope WF. Effects of administration of human chorionic gonadotropin or progesterone before maternal recognition of pregnancy on blastocyst development and pregnancy in sheep. J Anim Sci. 1994;72(2):453-8.
Northrop EJ, Rich JJJ, Cushman RA, McNeel AK, Soares EM, Brooks K, Spencer TE, Perry GA. Effects of preovulatory estradiol on uterine environment and conceptus survival from fertilization to maternal recognition of pregnancy. Biol Reprod. 2018;99(3):629-38.
Ozturk S, Demir R. Particular functions of estrogen and progesterone in establishment of uterine receptivity and embryo implantation. Histol Histopathol. 2010;25(9):1215-28. PMid:20607663.
Parrish JJ, Susko-Parrish JL, First NL. Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biol Reprod. 1989;41(4):683-99.
Parrott JA, Skinner MK. Developmental and hormonal regulation of keratinocyte growth factor expression and action in the ovarian follicle. Endocrinology. 1998;139(1):228-35.
Pereira MH, Rodrigues AD, Carvalho RJ, Wiltbank MC, Vasconcelos JL. Increasing length of an estradiol and progesterone timed artificial insemination protocol decreases pregnancy losses in lactating dairy cows. J Dairy Sci. 2014;97(3):1454-64.
Perry GA, Perry BL. Effect of preovulatory concentrations of estradiol and initiation of standing estrus on uterine pH in beef cows. Domest Anim Endocrinol. 2008a;34(3):333-8.
Perry GA, Perry BL. Effects of standing estrus and supplemental estradiol on changes in uterine pH during a fixed-time artificial insemination protocol. J Anim Sci. 2008b;86(11):2928-35.
Perry GA, Smith MF, Lucy MC, Green JA, Parks TE, MacNeil MD, Roberts AJ, Geary TW. Relationship between follicle size at insemination and pregnancy success. Proc Natl Acad Sci USA. 2005;102(14):5268-73.
Perry GA, Smith MF, Roberts AJ, MacNeil MD, Geary TW. Relationship between size of ovulatory follicle and pregnancy success in beef heifers. J Anim Sci. 2007;85(3):684-9.
Pursley JR, Mee MO, Wiltbank MC. Synchronization of ovulation in dairy cows using PGF2α and GnRH. Theriogenology. 1995;44(7):915-23.
Quail LK, Cushman RA, Keel BN, Gonda MG, Perry GA. Preovulatory estradiol concentrations influence oviductal gene expression. In: Society for the Study of Reproduction Annual Meeting; 2021 Dec 15-18; St. Louis, United States. Reston: Society for the Study of Reproduction; 2021. p. MO2021.
Rawy M, Mido S, Ali HE-S, Derar D, Megahed G, Kitahara G, Osawa T. Effect of exogenous estradiol Benzoate on uterine blood flow in postpartum dairy cows. Anim Reprod Sci. 2018;192:136-45.
Reilly CM, Cannady WE, Mahesh VB, Stopper VS, De Sevilla LM, Mills TM. Duration of estrogen exposure prior to follicle-stimulating hormone stimulation is critical to granulosa cell growth and differentiation in rats. Biol Reprod. 1996;54(6):1336-42.
Richardson BN, Hill SL, Stevenson JS, Djira GD, Perry GA. Expression of estrus before fixed-time AI affects conception rates and factors that impact expression of estrus and the repeatability of expression of estrus in sequential breeding seasons. Anim Reprod Sci. 2016;166:133-40.
Robinson NA, Leslie KE, Walton JS. Effect of treatment with progesterone on pregnancy rate and plasma concentrations of progesterone in Holstein cows. J Dairy Sci. 1989;72(1):202-7.
Ryan M, Mihm M, Roche JF. Effect of GnRH given before or after dominance on gonadotrophin response and fate of that follicle wave in postpartum dairy cows. J Reprod Fertil. 1998;21:61.
Santos JE, Thatcher WW, Chebel RC, Cerri RL, Galvao KN. The effect of embryonic death rates in cattle on the efficacy of estrus synchronization programs. Anim Reprod Sci. 2004;82-83:513-35.
Sartori R, Gumen A, Guenther JN, Souza AH, Caraviello DZ, Wiltbank MC. Comparison of artificial insemination versus embryo transfer in lactating dairy cows. Theriogenology. 2006;65(7):1311-21.
Seidel GE. Reproductive biotechnologies for profitable beef production. In: Beef Improvement Federation 27th Research Symposium and Annual Meeting; 1995 May-Jun 31-3; Sheridan, WY, United States. Beef Improvement Federation; 1995. p. 28.
Souza AH, Silva EP, Cunha AP, Gumen A, Ayres H, Brusveen DJ, Guenther JN, Wiltbank MC. Ultrasonographic evaluation of endometrial thickness near timed AI as a predictor of fertility in high-producing dairy cows. Theriogenology. 2011;75(4):722-33.
Spencer TE, Bazer FW. Uterine and placental factors regulating conceptus growth in domestic animals. J Anim Sci. 2004;82(E-Suppl):E4-13. PMid:15471813.
Spencer TE, Sandra O, Wolf E. Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction. 2008;135(2):165-79.
Stanke DF, Sikes JD, DeYoung DW, Tumbleson ME. Proteins and amino acids in bovine oviducal fluid. J Reprod Fertil. 1974;38(2):493-6.
Sugiura T, Akiyoshi S, Inoue F, Yanagawa Y, Moriyoshi M, Tajima M, Katagiri S. Relationship between bovine endometrial thickness and plasma progesterone and estradiol concentrations in natural and induced estrus. J Reprod Dev. 2018;64(2):135-43.
Sutton R, Nancarrow CD, Wallace AL. Oestrogen and seasonal effects on the production of an oestrus-associated glycoprotein in oviducal fluid of sheep. J Reprod Fertil. 1986;77(2):645-53.
Ulbrich SE, Frohlich T, Schulke K, Englberger E, Waldschmitt N, Arnold GJ, Reichenbach HD, Reichenbach M, Wolf E, Meyer HH, Bauersachs S. Evidence for estrogen-dependent uterine serpin (SERPINA14) expression during estrus in the bovine endometrial glandular epithelium and lumen. Biol Reprod. 2009;81(4):795-805.
Van Cleeff J, Drost M, Thatcher WW. Effects of postinsemination progesterone supplementation on fertility and subsequent estrous response on dairy heifers. Theriogenology. 1991;36(5):795-807.
Vasconcelos JL, Sartori R, Oliveira HN, Guenther JG, Wiltbank MC. Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate. Theriogenology. 2001;56(2):307-14.
Vasconcelos JL, Silcox RW, Rosa GJ, Pursley JR, Wiltbank MC. Synchronization rate, size of the ovulatory follicle, and pregnancy rate after synchronization of ovulation beginning on different days of the estrous cycle in lactating dairy cows. Theriogenology. 1999;52(6):1067-78.
Walton JS, Halbert GW, Robinson NA, Leslie KE. Effects of progesterone and human chorionic gonadotrophin administration five days postinsemination on plasma and milk concentrations of progesterone and pregnancy rates of normal and repeat breeder dairy cows. Can J Vet Res. 1990;54(3):305-8. PMid:2379109.
Wang XN, Greenwald GS. Synergistic effects of steroids with FSH on folliculogenesis, steroidogenesis and FSH- and hCG-receptors in hypophysectomized mice. J Reprod Fertil. 1993;99(2):403-13.
Wegner CC, Killian GJ. In vitro and in vivo association of an oviduct estrus-associated protein with bovine zona pellucida. Mol Reprod Dev. 1991;29(1):77-84.
Welsh TH Jr, Zhuang L-Z, Hsueh AJW. Estrogen augmentation of gonadotropin-stimulated progestin biosynthesis in cultured rat granulosa cells. Endocrinology. 1983;112(6):1916-24.
Wijayagunawardane MP, Miyamoto A, Taquahashi Y, Gabler C, Acosta TJ, Nishimura M, Killian G, Sato K. In vitro regulation of local secretion and contraction of the bovine oviduct: stimulation by luteinizing hormone, endothelin-1 and prostaglandins, and inhibition by oxytocin. J Endocrinol. 2001;168(1):117-30.
Winuthayanon W, Bernhardt ML, Padilla-Banks E, Myers PH, Edin ML, Lih FB, Hewitt SC, Korach KS, Williams CJ. Oviductal estrogen receptor alpha signaling prevents protease-mediated embryo death. eLife. 2015;4:e10453.
Witkowska E. Reactivity of the epithelial cells of the bovine oviduct in vitro on the exogenic gonadotrophic and steroid hormones. Folia Histochem Cytochem. 1979;17(3):225-38.
Wong PY, Lee WM, Tsang AY. The effects of extracellular sodium on acid release and motility initiation in rat caudal epididymal spermatozoa in vitro. Exp Cell Res. 1981;131(1):97-104.
Zelinski MB, Noel P, Weber DW, Stormshak F. Characterization of cytoplasmic progesterone receptors in the bovine endometrium during proestrus and diestrus. J Anim Sci. 1982;55(2):376-83.
Zhuang L-Z, Adashi EY, Hsueh AJW. Direct enhancement of gonadotropin-stimulated ovarian estrogen biosynthesis by estrogen and clomiphene citrate. Endocrinology. 1982;110(6):2219-21.
Submitted date:
05/04/2023
Accepted date:
07/18/2023