Animal Reproduction (AR)
http://www.animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0045
Animal Reproduction (AR)
Conference Paper

Physiological mechanisms involved in maintaining the corpus luteum during the first two months of pregnancy

Milo C. Wiltbank, Megan A. Mezera, Mateus Z. Toledo, Jessica N. Drum, Giovanni M. Baez, Alvaro García-Guerra, Roberto Sartori

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Abstract

Maintenance of the corpus luteum (CL) during pregnancy is essential for continuing the elevated circulating progesterone (P4) that is required to maintain pregnancy. The mechanisms that protect the CL during early pregnancy when the non-pregnant animal would typically undergo CL regression have been extensively investigated. It is clear uterine prostaglandin F2α (PGF) causes regression of the CL in non-pregnant ruminants and that maintenance of the CL during early pregnancy is dependent upon secretion of interferon-tau (IFNT) from the elongating embryo. A number of specific mechanisms appear to be activated by IFNT. Most studies indicate that there is an inhibition of oxytocin-induced secretion of uterine PGF. There is also evidence for increased resistance to PGF action, perhaps due to secretion of PGE2 and PGE1 or direct endocrine actions of circulating IFNT. These mechanisms occur concurrently and each may help to maintain the CL during the first month of pregnancy. However, during the second month of pregnancy, IFNT is no longer secreted by the embryo. Attachment of the embryo to the uterus and subsequent placentome development have been linked to silencing of expression from the IFNT gene. In addition, there is some evidence that oxytocin responsiveness of the uterus returns during the second month of pregnancy leading to substantial basal secretion of PGF and perhaps PGF pulses. There is also no evidence that the CL during the second month of pregnancy is resistant to the actions of PGF as observed during the first month. Thus, this manuscript attempts to compare the mechanisms that maintain the CL during the first and second months of pregnancy in ruminants and provides a new, speculative, physiological model for maintenance of the CL during month two of pregnancy that is distinct from the previously-described mechanisms that maintain the CL during the first month of pregnancy.

Keywords

corpus luteum, interferon-tau, pregnancy.

References

Antoniazzi AQ, Webb BT, Romero JJ, Ashley RL, Smirnova NP, Henkes LE, Bott RC, Oliveira JF, Niswender GD, Bazer FW, Hansen TR. 2013. Endocrine delivery of interferon tau protects the corpus luteum from prostaglandin F2 Alpha-induced luteolysis in ewes. Biol Reprod, 88. doi: 10.1095/biolreprod.112.105684.

Araujo RR, Ginther OJ, Ferreira JC, Palhao MM, Beg MA, Wiltbank MC. 2009. Role of follicular estradiol-17beta in timing of luteolysis in heifers. Biol Reprod, 81:426-437.

Arnold DR, Binelli M, Vonk J, Alexenko AP, Drost M, Wilcox CJ, Thatcher WW. 2000. Intracellular regulation of endometrial PGF(2a) and PGE(2) production in dairy cows during early pregnancy and following treatment with recombinant interferon-tau. Domest Anim Endocrinol, 18:199-216.

Arosh JA, Banu SK, Kimmins S, Chapdelaine P, Maclaren LA, Fortier MA. 2004. Effect of interferon-tau on prostaglandin biosynthesis, transport, and signaling at the time of maternal recognition of pregnancy in cattle: evidence of polycrine actions of prostaglandin E2. Endocrinology, 145:5280-5293.

Arosh JA, Banu SK, McCracken JA. 2016. Novel concepts on the role of prostaglandins on luteal maintenance and maternal recognition and establishment of pregnancy in ruminants. J Dairy Sci, 99:5926-5940.

Asselin E, Lacroix D, Fortier MA. 1997. IFN-tau increases PGE(2) production and COX-2 gene expression in the bovine endometrium in vitro. Mol Cell Endocrinol, 132:117-126.

Atli MO, Bender RW, Mehta V, Bastos MR, Luo WX, Vezina CM, Wiltbank MC. 2012. Patterns of gene expression in the bovine corpus luteum following repeated intrauterine infusions of low doses of prostaglandin F2alpha. Biol Reprod, 86. doi: 10.1095/biolreprod.111.094870.

Baez GM, Barletta RV, Guenther JN, Gaska JM, Wiltbank MC. 2016. Effect of uterine size on fertility of lactating dairy cows. Theriogenology, 85:1357-1366.

Baez GM, Trevisol E, Barletta RV, Cardoso BO, Ricci A, Guenther JN, Cummings NE, Wiltbank MC. 2017. Proposal of a new model for CL regression or maintenance during pregnancy on the basis of timing of regression of contralateral, accessory CL in pregnant cows. Theriogenology, 89:214-225.

Bazer FW, Spencer TE, Ott TL. 1997. Interferon tau: a novel pregnancy recognition signal. Am J Reprod Immunol, 37:412-420.

Bonnin P, Huynh L, L'Haridon R, Chene N, Martal J. 1999. Transport of uterine PGF(2 alpha) to the ovaries by systemic circulation and local lymphovenous-arterial diffusion during luteolysis in sheep. J Reprod Fertil, 116:199-210.

Bott RC, Ashley RL, Henkes LE, Antoniazzi AQ, Bruemmer JE, Niswender GD, Bazer FW, Spencer TE, Smirnova NP, Anthony RV, Hansen TR. 2010. Uterine vein infusion of interferon Tau (IFNT) extends luteal life span in ewes. Biol Reprod, 82:725-735.

Bridges PJ, Wright DJ, Buford WI, Ahmad N, Hernandez-Fonseca H, McCormick ML, Schrick FN, Dailey RA, Lewis PE, Inskeep EK. 2000. Ability of induced corpora lutea to maintain pregnancy in beef cows. J Anim Sci, 78:2942-2949.

Burns PD, Graf GA, Hayes SH, Silvia WJ. 1997a. Cellular mechanisms by which oxytocin stimulates uterine PGF(2 alpha) synthesis in bovine endometrium: roles of phospholipases C and A(2). Domest Anim Endocrinol, 14:181-191.

Burns PD, Tsai SJ, Wiltbank MC, Hayes SH, Graf GA, Silvia WJ. 1997b. Effect of oxytocin on concentrations of prostaglandin H synthase-2 mRNA in ovine endometrial tissue in vivo. Endocrinology, 138:5637-5640.

Chang MC. 1952. Development of bovine blastocyst with a note on implantation. Anat Rec, 113:143-161.

Charpigny G, Reinaud P, Tamby J-P, Creminon C, Guillomot M. 1997. Cyclooxygenase-2 unlike cyclooxygenase-1 is highly expressed in ovine embryos during the implantation period. Biol Reprod, 57:1032-1040.

Costine BA, Inskeep EK, Blemings KP, Flores JA, Wilson ME. 2007. Mechanisms of reduced luteal sensitivity to prostaglandin F2alpha during maternal recognition of pregnancy in ewes. Domest Anim Endocrinol, 32:106-121.

Danet-Desnoyers G, Meyer MD, Gross TS, Johnson JW, Thatcher WW. 1995. Regulation of endometrial prostaglandin synthesis during early pregnancy in cattle: effects of phospholipases and calcium in vitro. Prostaglandins, 50:313-330.

Davis JS, Rueda BR. 2002. The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front Biosci, 7:D1949-D1978.

Del Campo MR, Rowe RF, French LR, Ginther OJ. 1977. Unilateral relationship of embryos and the corpus luteum in cattle. Biol Reprod, 16:580-585.

Del Campo MR, Mapletoft RJ, Rowe RF, Critser JK, Ginther OJ. 1980. Unilateral utero-ovarian relationship in pregnant cattle and role of uterine vein. Theriogenology, 14:185-193.

Diskin MG, Morris DG. 2008. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim, 43:260-267.

Diskin MG, Waters SM, Parr MH, Kenny DA. 2016. Pregnancy losses in cattle: potential for improvement. Reprod Fertil Dev, 28:83-93.

Dorniak P, Bazer FW, Spencer TE. 2011. Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol Reprod, 84:1119-1127.

Ealy AD, Larson SF, Liu L, Alexenko AP, Winkelman GL, Kubisch HM, Bixby JA, Roberts RM. 2001. Polymorphic forms of expressed bovine interferon-tau genes: Relative transcript abundance during early placental development, promoter sequences of genes and biological activity of protein products. Endocrinology, 142:2906-2915.

Ealy AD, Yang QE. 2009. Control of interferon-tau expression during early pregnancy in ruminants. Am J Reprod Immunol, 61:95-106.

Ezashi T, Imakawa K. 2017. Transcriptional control of IFNT expression. Reproduction, 154:F21-F31.

Farin CE, Imakawa K, Hansen TR, Mcdonnell JJ, Murphy CN, Farin PW, Roberts RM. 1990. Expression of trophoblastic interferon genes in sheep and cattle. Biol Reprod, 43:210-218.

Fleming JGW, Spencer TE, Safe SH, Bazer FW. 2006. Estrogen regulates transcription of the ovine oxytocin receptor gene through GC-rich SP1 promoter elements. Endocrinology, 147:899-911.

Fredriksson G, Kindahl H, Edqvist LE. 1984. 11-Ketotetranor PGF metabolites, a suitable indicator for measuring prostaglandin release during the normal estrous cycle and early pregnancy in the goat. Anim Reprod Sci, 7:537-545.

Fuchs AR, Behrens O, Helmer H, Liu CH, Barros CM, Fields MJ. 1990. Oxytocin and vasopressin receptors in bovine endometrium and myometrium during the estrous cycle and early pregnancy. Endocrinology, 127:629-636.

Fuchs AR, Rollyson MK, Meyer M, Fields MJ, Minix JM, Randel RD. 1996. Oxytocin induces prostaglandin F-2 alpha release in pregnant cows: Influence of gestational age and oxytocin receptor concentrations. Biol Reprod, 54:647-653.

Gifford CA, Racicot K, Clark DS, Austin KJ, Hansen TR, Lucy MC, Davies CJ, Ott TL. 2007. Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, nonpregnant dairy cows. J Dairy Sci, 90.

Ginther OJ, Delcampo CH. 1974. Vascular anatomy of uterus and ovaries and unilateral luteolytic effect of uterus - cattle. Am J Vet Res, 35:193-203.

Ginther OJ, Araujo RR, Palhao MP, Rodrigues BL, Beg MA. 2009. Necessity of sequential pulses of prostaglandin F2alpha for complete physiologic luteolysis in cattle. Biol Reprod, 80:641-648.

Ginther OJ, Khan FA, Hannan MA, Beg MA. 2012. Temporal interrelationships at 15-min intervals among oxytocin, LH, and progesterone during a pulse of a prostaglandin F2alpha metabolite in heifers. Anim Reprod Sci, 133:63-70.

Giordano JO, Guenther JN, Lopes G, Jr., Fricke PM. 2012. Changes in serum pregnancy-associated glycoprotein, pregnancy-specific protein B, and progesterone concentrations before and after induction of pregnancy loss in lactating dairy cows. J Dairy Sci, 95:683-697.

Godkin JD, Bazer FW, Moffatt J, Sessions F, Roberts RM. 1982. Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at day 13-21. J Reprod Fertil, 65:141-150.

Godkin JD, Bazer FW, Roberts RM. 1984a. Ovine trophoblast protein 1, an early secreted blastocyst protein, binds specifically to uterine endometrium and affects protein synthesis. Endocrinology, 114:120-130.

Godkin JD, Bazer FW, Thatcher WW, Roberts RM. 1984b. Proteins released by cultured day 15-16 conceptuses prolong luteal maintenance when introduced into the uterine lumen of cyclic ewes. J Reprod Fertil, 71:57-64.

Godkin JD, Smith SE, Johnson RD, Dore JJ. 1997. The role of trophoblast interferons in the maintenance of early pregnancy in ruminants. Am J Reprod Immunol, 37:137-143.

Guillomot M, Michel C, Gaye P, Charlier N, Trojan J, Martal J. 1990. Cellular localization of an embryonic interferon, ovine trophoblastin and its mRNA in sheep embryos during early pregnancy. Biol Cell, 68:205-211.

Hansen PJ, Anthony RV, Bazer FW, Baumbach GA, Roberts RM. 1985. In vitro synthesis and secretion of ovine trophoblast protein-1 during the period of maternal recognition of pregnancy. Endocrinology, 117:1424-1430.

Hansen TR, Romero JJ, Antoniazzi AQ, Bott RC, Ashley RL, Webb BT, Henkes LE, Smirnova NP. 2013. Endocrine conceptus signaling in ruminants. Anim Reprod, 10:311-321.

Henderson K, Scaramuzzi R, Baird D. 1977. Simultaneous infusion of prostaglandin E2 antagonizes the luteolytic action of prostaglandin F2α in vivo. J Endocrinol, 72:379-383.

Huie JM, Magness RR, Reynolds LP, Hoyer G, Huecksteadt T, Colcord M, Stalcup B, Whysong GL, Weems CW. 1981. Effect of chronic inpsilateral or contralateral intrauterine infusion of prostaglandin E1 (PGE1) on luteal function of unilaterally ovariectomized ewes. Prostaglandins, 21:945-955.

Hyland J, Manns J, Humphrey W. 1982. Prostaglandin production by ovine embryos and endometrium in vitro. J Reprod Fertil, 65:299-304.

Inskeep EK, Butcher RL. 1966. Local component of utero-ovarian relationships in ewe. J Anim Sci, 25:1164-1168.

Inskeep EK, Smutny WJ, Butcher RL, Pexton JE. 1975. Effects of intrafollicular injections of prostaglandins in non-pregnant and pregnant ewes. J Anim Sci, 41:1098-1104.

Ivell R, Fuchs AR, Bathgate R, Tillmann G, Kimura T. 2000. Regulation of the oxytocin receptor in bovine reproductive tissues and the role of steroids. Reprod Domest Anim, 35:134-141.

Jenner LJ, Parkinson TJ, Lamming GE. 1991. Uterine oxytocin receptors in cyclic and pregnant cows. J Reprod Fertil, 91:49-58.

Johnson GA, Austin KJ, Collins AM, Murdoch WJ, Hansen TR. 1999. Endometrial ISG17 mRNA and a related mRNA are induced by interferon-tau and localized to glandular epithelial and stromal cells from pregnant cows. Endocrine, 10:243-252.

Kanai N, Lu R, Satriano JA, Bao Y, Wolkoff AW, Schuster VL. 1995. Identification and characterization of a prostaglandin transporter. Science, 268:866-869.

Kieborz-Loos KR, Garverick HA, Keisler DH, Hamilton SA, Salfen BE, Youngquist RS, Smith MF. 2003. Oxytocin-induced secretion of prostaglandin F-2 alpha in postpartum beef cows: effects of progesterone and estradiol-17 beta treatment. J Anim Sci, 81:1830-1836.

Kim MS, Min KS, Seong HH, Kim CL, Jeon IS, Kim SW, Imakawa K. 2018. Regulation of conceptus interferon-tau gene subtypes expressed in the uterus

during the peri-implantation period of cattle. Anim Reprod Sci, 190:39-46.

Kindahl H, Edqvist L-E, Bane A, Granstrom E. 1976. Blood levels of progesterone and 15-keto-13,14-dihydro-prostaglandin F 2a during the normal oestrous cycle and early pregnancy in heifers. Acta Endocrinol, 82:134-149.

Kizaki K, Shichijo-Kizaki A, Furusawa T, Takahashi T, Hosoe M, Hashizume K. 2013. Differential neutrophil gene expression in early bovine pregnancy. Reprod Biol Endocrinol, 11:6. doi: 10.1186/1477-7827-11-6.

Knickerbocker JJ, Wiltbank MC, Niswender GD. 1988. Mechanisms of luteolysis in domestic livestock. Domest Anim Endocrinol, 5:91-107.

Lamond DR, Drost M, Mccracke.Ja, Lamond DR. 1973. Countercurrent transfer of prostaglandin in ewe. Prostaglandins, 3:691-702.

Lee J, McCracken JA, Banu SK, Rodriguez R, Nithy TK, Arosh JA. 2010. Transport of prostaglandin F(2alpha) pulses from the uterus to the ovary at the time of luteolysis in ruminants is regulated by prostaglandin transporter-mediated mechanisms. Endocrinology, 151:3326-3335.

Lee J, McCracken JA, Stanley JA, Nithy TK, Banu SK, Arosh JA. 2012. Intraluteal prostaglandin biosynthesis and signaling are selectively directed towards PGF(2alpha) during luteolysis but towards PGE(2) during the establishment of pregnancy in sheep. Biol Reprod, 87:97. doi: 10.1095/biolreprod.112. 100438.

Lee J, McCracken JA, Banu SK, Arosh JA. 2013. Intrauterine inhibition of prostaglandin transporter protein blocks release of luteolytic PGF2alpha pulses without suppressing endometrial expression of estradiol or oxytocin receptor in ruminants. Biol Reprod, 89:27. doi: 10.1095/biolreprod.112.106427.

Lewis GS, Wilson L, Jr., Wilks JW, Pexton JE, Fogwell RL, Ford SP, Butcher RL, Thayne WV, Inskeep EK. 1977. PGF2 alpha and its metabolites in uterine and jugular venous plasma and endometrium of ewes during early pregnancy. J Anim Sci, 45:320-327.

Loeb L. 1927. The effects of hysterectomy on the system of sex organs and on the periodicity of the sexual cycle in the guinea pig. Am J Physiol, 83:202-208.

Lulai C, Dobrinski I, Kastelic JP, Mapletoft RJ. 1994. Induction of luteal regression, ovulation and development of new luteal tissue during early pregnancy in heifers. Anim Reprod Sci, 35:163-172.

Maalouf SW, Liu WS, Albert I, Pate JL. 2014. Regulating life or death: potential role of microRNA in rescue of the corpus luteum. Mol Cell Endocrinol, 398:78-88.

Mann GE, Payne JH, Lamming GE. 2001. Hormonal regulation of oxytocin-induced prostaglandin F-2 alpha secretion by the bovine and ovine uterus in vivo. Domest Anim Endocrinol, 21:127-141.

Mann GE, Lamming GE, Scholey D, Hunter M, Pettibone DJ. 2003. Attenuation of PGF(2 alpha) release in ewes infused with the oxytocin antagonist L-368,899. Domest Anim Endocrinol, 25:255-262.

Mann GE, Lamming GE. 2006. Timing of prostaglandin F-2 alpha release episodes and oxytocin receptor development during luteolysis in the cow. Anim Reprod Sci, 93:328-336.

Mapletoft RJ, Delcampo MR, Ginther OJ. 1975. Unilateral luteotropic effect of uterine venous effluent of a gravid uterine horn in sheep. Proc Soc Exp Biol Med, 150:129-133.

Mapletoft RJ, Ginther OJ. 1975. Adequacy of main uterine vein and ovarian artery in local venoarterial pathway for uterine-induced luteolysis in ewes. Am J Vet Res, 36:957-963.

Mapletoft RJ, Delcampo MR, Ginther OJ. 1976a. Local utero-ovarian venoarterial pathway in cows. J Anim Sci, 43:295-296.

Mapletoft RJ, Lapin DR, Ginther OJ. 1976b. Ovarian artery as final component of local luteotropic pathway between a gravid uterine horn and ovary in ewes. Biol Reprod, 15:414-421.

Martal J, Lacroix MC, Loudes C, Saunier M, Wintenberger-Torres S. 1979. Trophoblastin, an antiluteolytic protein present in early pregnancy in sheep. J Reprod Fertil, 56:63-73.

McCracken JA, Schramm W, Barcikowski B, Wilson L Jr. 1981. The identification of prostaglandin F2 alpha as a uterine luteolytic hormone and the hormonal control of its synthesis. Acta Vet Scand Suppl, 77:71-88.

McCracken JA, Lee J, Yang B, Nithy TK, Banu SK, Bazer FW, Arosh JA. 2011. Inhibition of the prostaglandin transporter protein suppresses luteolytic pulses of PGF2alpha from the ovine uterus. Biol Reprod, 85. doi.org/10.1093/biolreprod/85.s1.374.

Meyer MD, Hansen PJ, Thatcher WW, Drost M, Badinga L, Roberts RM, Li J, Ott TL, Bazer FW. 1995. Extension of corpus luteum lifespan and reduction of uterine secretion of prostaglandin F2 alpha of cows in response to recombinant interferon-tau. J Dairy Sci, 78:1921-1931.

Moor RM. 1968. Effect of embryo on corpus luteum function. J Anim Sci, 27(suppl. 1):97-118.

Nancarrow CD, Evison BM, Connell PJ. 1982. Effect of embryos on luteolysis and termination of early pregnancy in sheep with cloprostenol. Biol Reprod, 26:263-269.

Nojima H, Nagaoka K, Christenson RK, Shiota K, Imakawa K. 2004. Increase in DNA methylation downregulates conceptus interferon-tau gene expression. Mol Reprod Dev, 67:396-405.

Ochoa JC, Penagaricano F, Baez GM, Melo LF, Motta JC, Guerra AG, Meidan R, Ferreira JCP, Sartori R, Wiltbank MC. 2018. Mechanisms for rescue of CL during pregnancy: gene expression in bovine CL following intrauterine pulses of prostaglandins E1 and F2alpha. Biol Reprod, 98:465-479,

Oliveira JF, Henkes LE, Ashley RL, Purcell SH, Smirnova NP, Veeramachaneni DN, Anthony RV, Hansen TR. 2008. Expression of interferon (IFN)-stimulated genes in extrauterine tissues during early pregnancy in sheep is the consequence of endocrine IFN-tau release from the uterine vein. Endocrinology, 149:1252-1259.

Parkinson TJ, Jenner LJ, Lamming GE. 1990. Comparison of oxytocin prostaglandin-F2-alpha interrelationships in cyclic and pregnant cows. J Reprod Fertil, 90:337-345.

Pate JL, Hughes CK. 2018. Integration of proteomic, transcriptomic and metabolomic data for luteal rescue in early pregnancy: role of microRNA as regulators of the corpus luteum. Anim Reprod, 15:00-00.

Pinaffi FLV, Araujo ER, Ginther OJ. 2018. Concentrations of a PGF2 alpha metabolite during pregnancy on the days that luteolysis occurs in nonbred heifers. Domest Anim Endocrinol, 62:76-82.

Plante C, Thatcher WW, Hansen PJ. 1991. Alteration of oestrous cycle length, ovarian function and oxytocin-induced release of prostaglandin F-2 alpha by intrauterine and intramuscular administration of recombinant bovine interferon-alpha to cows. J Reprod Fertil, 93:375-384.

Pratt BR, Butcher RL, Inskeep EK. 1977a. Antiluteolytic effect of the conceptus and of PGE2 in ewes. J Anim Sci, 45:784-791.

Pratt BR, Butcher RL, Inskeep EK. 1977b. Effect of continuous intrauterine administration of prostaglandin E2 on life-span of corpora lutea of nonpregnant ewes. J Anim Sci, 48:1441-1446.

Pugliesi G, Miagawa BT, Paiva YN, Franca MR, Silva LA, Binelli M. 2014. Conceptus-induced changes in the gene expression of blood immune cells and the ultrasound-accessed luteal function in beef cattle: how early can we detect pregnancy? Biol Reprod, 91:95. doi: 10.1095/biolreprod.114.121525.

Reid RND, Crothers I. 1980. Prostaglandin-F2-Alpha for estrus synchronization or bbortion in polwarth ewes. Aust Vet J, 56:22-24.

Reynolds L, Stigler J, Hoyer G, Magness R, Huie J, Huecksteadt T, Whysong G, Behrman H, Weems C. 1981. Effect of PGE 1 or PGE 2 on PGF 2α-induced luteolysis in nonbred ewes. Prostaglandins, 21:957-972.

Roberts RM. 1996. Interferon-tau and pregnancy. J Interferon Cytokine Res, 16:271-273.

Robinson RS, Mann GE, Lamming GE, Wathes DC. 1999. The effect of pregnancy on the expression of uterine oxytocin, oestrogen and progesterone receptors during early pregnancy in the cow. J Endocrinol, 160:21-33.

Romero JJ, Antoniazzi AQ, Nett TM, Ashley RL, Webb BT, Smirnova NP, Bott RC, Bruemmer JE, Bazer FW, Anthony RV, Hansen TR. 2015. Temporal release, paracrine and endocrine actions of ovine conceptus-derived interferon-tau during early pregnancy. Biol Reprod, 93. doi: 10.1095/biolreprod. 115.132860.

Rowson LE, Moor RM. 1967. The influence of embryonic tissue homogenate infused into the uterus, on the life-span of the corpus luteum in the sheep. J Reprod Fertil, 13:511-516.

Saint-Dizier M, Grimard B, Guyader-Joly C, Humblot P, Ponter AA. 2011. Expression of enzymes involved in the synthesis of prostaglandin E-2 in bovine in vitro-produced embryos. Zygote, 19:277-283.

Sakurai T, Bai H, Konno T, Ideta A, Aoyagi Y, Godkin JD, Imakawa K. 2010. Function of a transcription factor CDX2 beyond its trophectoderm lineage specification. Endocrinology, 151:5873-5881.

Sakurai T, Bai H, Bai R, Sato D, Arai M, Okuda K, Ideta A, Aoyagi Y, Godkin JD, Imakawa K. 2013. Down-regulation of interferon tau gene transcription with a transcription factor, EOMES. Mol Reprod Dev, 80:371-383.

Salfen BE, Cresswell JR, Xu ZZ, Bao B, Garverick HA. 1996. Effects of presence of a dominant follicle and estradiol on length of luteal phases in estrous cycles with two or three waves of follicular development. Biol Reprod, 54:235-235.

Santos JE, Thatcher WW, Chebel RC, Cerri RL, Galvao KN. 2004. The effect of embryonic death rates in cattle on the efficacy of estrus synchronization programs. Anim Reprod Sci, 82-83:513-535.

Santos JEP, Rutigliano HM, Sa Filho MF. 2009. Risk factors for resumption of postpartum estrous cycles and embryonic survival in lactating dairy cows. Anim Reprod Sci, 110:207-221.

Schramm W, Bovaird L, Glew ME, Schramm G, Mccracken JA. 1983. Corpus luteum regression induced by ultra low pulses of prostaglandin-F2-Alpha. Prostaglandins, 26:347-364.

Schuster VL. 1998. Molecular mechanisms of prostaglandin transport. Annu Rev Physiol, 60:221-242.

Schuster VL. 2002. Prostaglandin transport. Prostaglandins & Other Lipid Mediators, 68-9:633-647.

Shirasuna K, Asaoka H, Acosta TJ, Wijayagunawardane MP, Ohtani M, Hayashi KG, Matsui M, Miyamoto A. 2004. Real-time dynamics of prostaglandin F2alpha release from uterus and corpus luteum during spontaneous luteolysis in the cow. Reproduction, 128:189-195.

Shirasuna K, Matsumoto H, Kobayashi E, Nitta A, Haneda S, Matsui M, Kawashima C, Kida K, Shimizu T, Miyamoto A. 2012. Upregulation of interferon-stimulated genes and interleukin-10 in peripheral blood immune cells during early pregnancy in dairy cows. J Reprod Dev, 58:84-90.

Silva PJ, Juengel JL, Rollyson MK, Niswender GD. 2000. Prostaglandin metabolism in the ovine corpus luteum: Catabolism of prostaglandin F-2 alpha (PGF(2 alpha)) coincides with resistance of the corpus luteum to PGF(2 alpha). Biol Reprod, 63:1229-1236.

Silvia WJ, Niswender GD. 1984. Maintenance of the corpus luteum of early pregnancy in the ewe. 3. Differences between pregnant and nonpregnant ewes in luteal responsiveness to prostaglandin F2-alpha. J Anim Sci, 59:746-753.

Silvia WJ, Niswender GD. 1986. Maintenance of the corpus luteum of early pregnancy in the ewe. 4. Changes in luteal sensitivity to prostaglandin F2-alpha throughout early pregnancy. J Anim Sci, 63:1201-1207.

Silvia WJ, Raw RE. 1993. Regulation of pulsatile secretion of prostaglandin-F2-alpha from the ovine uterus by ovarian steroids. J Reprod Fertil, 98:341-347.

Spencer TE, Bazer FW. 1996. Ovine interferon tau suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium. Endocrinology, 137:1144-1147.

Spencer TE, Mirando MA, Mayes JS, Watson GH, Ott TL, Bazer FW. 1996. Effects of interferon-tau and progesterone on oestrogen-stimulated expression of receptors for oestrogen, progesterone and oxytocin in the endometrium of ovariectomized ewes. Reprod Fertil Dev, 8:843-853.

Spencer TE, Johnson GA, Burghardt RC, Bazer FW. 2004. Progesterone and placental hormone actions on the uterus: Insights from domestic animals. Biol Reprod, 71:2-10.

Spencer TE, Johnson GA, Bazer FW, Burghardt RC, Palmarini M. 2007. Pregnancy recognition and conceptus implantation in domestic ruminants: Roles of progesterone, interferons and endogenous retroviruses. Reprod Fertil Dev, 19:65-78.

Spencer TE, Hansen TR. 2015. Implantation and establishment of pregnancy in ruminants. Adv Anat Embryol Cel, 216:105-135.

Thain RI. 1977. Subsequent fertility in heifers aborted using prostaglandins at 45-60 days of pregnancy. Aust Vet J, 53:198-198.

Thatcher WW, Bartol FF, Knickerbocker JJ, Curl JS, Wolfenson D, Bazer FW, Roberts RM. 1984. Maternal recognition of pregnancy in cattle. J Dairy Sci, 67:2797-2811.

Thatcher WW, Hansen PJ, Gross TS, Helmer SD, Plante C, Bazer FW. 1989. Antiluteolytic effects of bovine trophoblast protein-1. J Reprod Fertil Suppl, 37:91-99.

Wathes DC, Mann GE, Payne JH, Riley PR, Stevenson KR, Lamming GE. 1996. Regulation of oxytocin, oestradiol and progesterone receptor concentrations in different uterine regions by oestradiol, progesterone and oxytocin in ovariectomized ewes. J Endocrinol, 151:375-393.

Weems YS, Arreguin-Arevalo JA, Nett TM, Vann RC, Ford SP, Bridges PJ, Welsh TH, Lewis AW, Neuendorff DA, Randel RD, Weems CW. 2011. In vivo intra-luteal implants of prostaglandin (PG) E-1 or E-2 (PGE(1), PGE(2)) prevent luteolysis in cows. I. Luteal weight, circulating progesterone, mRNA for luteal luteinizing hormone (LH) receptor, and occupied and unoccupied luteal receptors for LH. Prostaglandins Other Lipid Mediat, 95:35-44.

Wiepz GJ, Wiltbank MC, Nett TM, Niswender GD, Sawyer HR. 1992. Receptors for prostaglandins-F2-alpha and E2 in ovine corpora lutea during maternal recognition of pregnancy. Biol Reprod, 47:984-991.

Wijma R, Stangaferro ML, Kamat MM, Vasudevan S, Ott TL, Giordano JO. 2016. Embryo mortality around the period of maintenance of the corpus luteum causes alterations to the ovarian function of lactating dairy cows. Biol Reprod, 95:112. doi: 10.1095/biolreprod.116.142075.

Wiltbank JN, Casida LE. 1956. Alteration of ovarian activity by hysterectomy. J Anim Sci, 15:134-140.

Wiltbank MC, Souza AH, Carvalho PD, Cunha AP, Giordano JO, Fricke PM, Baez GM, Diskin MG. 2014. Physiological and practical effects of progesterone on reproduction in dairy cattle. Animal, 8:70-81.

Wiltbank MC, Baez GM, Garcia-Guerra A, Toledo MZ, Monteiro PLJ, Melo LF, Ochoa JC, Santos JEP, Sartori R. 2016a. Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows. Theriogenology, 86:239-253.

Wiltbank MC, Meidan R, Ochoa J, Baez GM, Giordano JO, Ferreira JCP, Sartori R. 2016b. Maintenance or regression of the corpus luteum during multiple decisive periods of bovine pregnancy. Anim Reprod, 13:217-233.

Wolfenson D, Thatcher WW, Drost M, Caton D, Foster DB, Leblanc MM. 1985. Characteristics of prostaglandin-F measurements in the ovarian iirculation during the estrous cycle and early pregnancy in the cow. J Reprod Fertil, 75:491-499.

Young CD, Schrick FN, Pohler KG, Saxton AM, Di Croce FA, Roper DA, Wilkerson JB, Edwards JL. 2017. Short communication: A reproductive tract scoring system to manage fertility in lactating dairy cows. J Dairy Sci, 100:5922-5927.

Zarco L, Stabenfeldt GH, Quirke JF, Kindahl H, Bradford GE. 1988. Release of prostaglandin-F-2-alpha and the timing of events associated with luteolysis in ewes with estrous cycles of different lengths. J Reprod Fertil, 83:517-526.

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