Placental contribution to the endocrinology of gestation and parturition
Gerhard Schuler, Rainer Fürbass, Karl Klisch
Abstract
In addition to many other functions, the placenta is a source of a vast number of autocrine, paracrine and endocrine factors. However, the spectrum of placental regulatory factors, their concentrations, gestational profiles and roles may differ considerably even between phylogenetically closely related species. Depending on the species, placental regulatory factors of a broad range of molecule classes have been found including (glyco-)proteins, peptides, steroids and prostaglandins. Local placental regulatory factors are especially important for the dialogue between the fetal and the maternal compartment immediately at the feto-maternal borderline and for the control of growth, differentiation and functions of the placenta itself. Moreover, placental hormones in a proper sense may also have effects in more remote targets within the maternal compartment, serving functions such as pregnancy-specific adaptations of maternal circulation, provision of hemotrophe to the fetus or the development and function of the mammary gland. Functions of placental hormones in the fetus proper are less clear but may be especially important before the establishment of a functional fetal endocrine system and near term within the highly species-specific networks of signals preparing and initiating parturition. This review takes a comparative view on the situation in different domestic animals focusing on ruminants and on placental hormones occurring at significant concentrations in the maternal circulation.
Keywords
References
Aba MA, Sumar J, Kindahl H, Forsberg M, Edqvist LE. 1998. Plasma concentrations of 15-ketodihydro-PGF2 alpha, progesterone, oestrone sulphate, oestradiol-17 beta and cortisol during late gestation, parturition and the early post partum period in llamas and alpacas. Anim Reprod Sci, 50:111-121.
Abd-Elnaeim MM, Derar IR, Wilsher S, Allen WR, Leiser R, Schuler G. 2009. Immunohistochemical localization of oestrogen receptors alpha and beta, progesterone receptor and aromatase in the equine placenta. Reprod Domest Anim, 44:312-319.
Al-Gubory KH, Camous S, Germain G, Bolifraud P, Nicole A, Ceballos-Picot I. 2006. Reconsideration of the proposed luteotropic and luteoprotective actions of ovine placental lactogen in sheep: in vivo and in vitro studies. J Endocrinol, 188:559-568.
Allen WR. 2001. Fetomaternal interactions and influences during equine pregnancy. Reproduction, 121:513-527.
Alvarez-Oxiley AV, Sousa NM, Hornick JL, Touati K, van der Weijden GC, Taverne MA, Szenci O, Sulon J, Debliquy P, Beckers JF. 2007. Radioimmunoassay of bovine placental lactogen using recombinant and native preparations: determination of fetal concentrations across gestation. Reprod Fertil Dev, 19:877-885.
Anand-Ivell R, Ivell R. 2014. Regulation of the reproductive cycle and early pregnancy by relaxin family peptides. Mol Cell Endocrinol, 382:472-479.
Antczak DF, de Mestre AM, Wilsher S, Allen WR. 2013. The equine endometrial cup reaction: a fetomaternal signal of significance. Annu Rev Anim Biosci, 1:419-442.
Arck P, Hansen PJ, Mulac Jericevic B, Piccinni MP, Szekeres-Bartho J. 2007. Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress. Am J Reprod Immunol, 58:268-279.
Arosh JA, Banu SK, Chapdelaine P, Fortier MA. 2004 Temporal and tissue-specific expression of prostaglandin receptors EP2, EP3, EP4, FP, and cyclooxygenases 1 and 2 in uterus and fetal membranes during bovine pregnancy. Endocrinology, 145:407-417.
Arroyo JI, Hoffmann FG, Opazo JC. 2014. Evolution of the relaxin/insulin-like gene family in anthropoid primates. Genome Biol Evol, 6:491-499.
Bagna B, Schwabe C, Anderson LL. 1991. Effect of relaxin on facilitation of parturition in dairy heifers. J Reprod Fertil, 91:605-615.
Baker CM, Goetzmann LN, Cantlon JD, Jeckel KM, Winger QA, Anthony RV. 2016. Development of ovine chorionic somatomammotropin hormone-deficient pregnancies. Am J Physiol Regul Integr Comp Physiol, 310:R837-846.
Bathgate RA, Halls ML, van der Westhuizen ET, Callander GE, Kocan M, Summers RJ. 2013. Relaxin family peptides and their receptors. Physiol Rev, 93:405-480.
Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. 2010. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod, 16:135-152.
Bazer FW. 2015. History of maternal recognition of pregnancy. Adv Anat Embryol Cell Biol, 216:5-25.
Bosu WTK, Liptrap RM, Leslie KE. 1984. Peripartal changes in plasma progesterone and 15-keto-13,14-dihydro-prostaglandin F2α concentrations in Holstein cows with and without retained foetal membranes. Anim Reprod Sci, 7:497-510.
Buczinski S, Bélanger AM, Fecteau G, Roy JP. 2007. Prolonged gestation in two Holstein cows: transabdominal ultrasonographic findings in late pregnancy and pathologic findings in the fetuses. J Vet Med A Physiol Pathol Clin Med, 54:624-626.
Bukovsky A, Caudle MR, Cekanova M, Fernando RI, Wimalasena J, Foster JS, Henley DC, Elder RF. 2003a. Placental expression of estrogen receptor beta and its hormone binding variant - comparison with estrogen receptor alpha and a role for estrogen receptors in asymmetric division and differentiation of estrogen-dependent cells. Reprod Biol Endocrinol, 1:36. doi: 10.1186/1477-7827-1-36.
Bukovsky A, Cekanova M, Caudle MR, Wimalasena J, Foster JS, Henley DC, Elder RF. 2003b. Expression and localization of estrogen receptor-alpha protein in normal and abnormal term placentae and stimulation of trophoblast differentiation by estradiol. Reprod Biol Endocrinol, 1:13. doi: 10.1186/1477-7827-1-13.
Bulun SE. 2014. Aromatase and estrogen receptor α deficiency. Fertil Steril, 101:323-329.
Byatt JC, Sorbet RH, Eppard PJ, Curran TL, Curran DF, Collier RJ. 1997. The effect of recombinant bovine placental lactogen on induced lactation in dairy heifers. J Dairy Sci, 80:496-503.
Cahoreau C, Klett D, Combarnous Y. 2015. Structure-function relationships of glycoprotein hormones and their subunits' ancestors. Front Endocrinol (Lausanne), 6:26.
Camacho-Arroyo I, Montor JM. 2012. Beyond reproductive effects of sex steroids. Mini Rev Med Chem, 12:1037-1039.
Carvalho AF, Klisch K, Miglino MA, Pereira FT, Bevilacqua E. 2006. Binucleate trophoblast giant cells in the water buffalo (Bubalus bubalis) placenta. J Morphol, 267:50-56.
Challis JR. 1971. Sharp increase in free circulating oestrogens immediately before parturition in sheep. Nature, 229:208.
Chan JS, Robertson HA, Friesen HG. 1978. Maternal and fetal concentrations of ovine placental lactogen measured by radioimmunoassay. Endocrinology, 102:1606-1613.
Cheskis BJ, Greger JG, Nagpal S, Freedman LP. 2007. Signaling by estrogens. J Cell Physiol, 213:610-617.
Chwalisz K, Garfield RE. 1997. Regulation of the uterus and cervix during pregnancy and labor. Role of progesterone and nitric oxide. Ann N Y Acad Sci, 828:238-253.
Comline RS, Hall LW, Lavelle RB, Nathanielsz PW, Silver M. 1974. Parturition in the cow: endocrine changes in animals with chronically implanted catheters in the foetal and maternal circulations. J Endocrinol, 63:451-472.
Conley AJ, Reynolds LP. 2014. Steroidogenesis and the initiation of parturition. In: Juengel JL, Miyamoto A, Price C, Reynolds LP, Smith MF, Webb R (Ed.). Reproduction in domestic ruminants VIII. Packington UK: SRF/Context Publishing. pp. 399-413.
Conley AJ. 2016. Review of the reproductive endocrinology of the pregnant and parturient mare. Theriogenology, 86:355-365.
Cornillie P, Van den Broeck W, Simoens P. 2007. Prolonged gestation in two Belgian blue cows due to inherited adenohypophyseal hypoplasia in the fetuses. Vet Rec, 161:388-391.
Crisci A, Rota A, Panzani D, Sgorbini M, Ousey JC, Camillo F. 2014. Clinical, ultrasonographic, and endocrinological studies on donkey pregnancy. Theriogenology, 81:275-283.
Currie WB, Cox RI, Thorburn GD. 1976. Release of prostaglandin F, regression of corpora lutea and induction of premature parturition in goats treated with estradiol-17beta. Prostaglandins, 12:1093-1103.
Currie WB, Thorburn GD. 1977a. Parturition in goats: studies on the interactions between the foetus, placenta, prostaglandin F and progesterone before parturition, at term or at parturition induced prematurely by corticotrophin infusion of the foetus. J Endocrinol, 73:263-278.
Currie WB, Thorburn GD. 1977b. The fetal role in timing the initiation of parturition in the goat. Ciba Found Symp, 47:49-72.
Currie WB, Gorewit RC, Michel FJ. 1988. Endocrine changes, with special emphasis on oestradiol-17 beta, prolactin and oxytocin, before and during labour and delivery in goats. J Reprod Fertil, 82:299-308.
Currie WB, Card CE, Michel FJ, Ignotz G. 1990. Purification, partial characterization, and development of a specific radioimmunoassay for goat placental lactogen. J Reprod Fertil, 90:25-36.
Dai Y, Ivell R, Liu X, Janowski D, Anand-Ivell R. 2017. Relaxin-family peptide receptors 1 and 2 are fully functional in the bovine. Front Physiol, 8:359.
Davey RA, Grossmann M. 2016. Androgen receptor structure, function and biology: from bench to bedside. Clin Biochem Rev, 37:3-15.
Davis KA, Klohonatz KM, Bruemmer JE, Bouma GJ. 2017. Androgen receptor in the term equine placenta. J Equine Vet Sci, 54:8-11.
Day AM. 1977. Cloprostenol for termination of pregnancy in cattle. B) The induction of abortion. N Z Vet J, 25:139-144.
De Hertogh R, Thomas K, Bietlot Y, Vanderheyden I, Ferin J. 1975. Plasma levels of unconjugated estrone, estradiol and estriol and of HCS throughout pregnancy in normal women. J Clin Endocrinol Metab, 40:93-101.
Diczfalusy E. 1964. Endocrine fnctions of the human fetoplacental unit. Fed Proc, 23:791-798.
Edqvist LE, Kindahl H, Stabenfeldt G. 1978 Release of prostaglandin F 2alpha during the bovine peripartal period. Prostaglandins, 16:111-119.
Eley RM, Thatcher WW, Bazer FW. 1979. Hormonal and physical changes associated with bovine conceptus development. J Reprod Fertil, 55:181-190.
Engeland IV, Ropstad E, Kindahl H, Andresen O, Waldeland H, Tverdal A. 1999 Foetal loss in dairy goats: function of the adrenal glands, corpus luteum and the foetal-placental unit. Anim Reprod Sci, 55:205-222.
Esteller-Vico A, Ball BA, Troedsson MHT, Squires EL. 2017. Endocrine changes, fetal growth, and uterine artery hemodynamics after chronic estrogen suppression during the last trimester of equine pregnancy. Biol Reprod, 96:414-423.
Estergreen VL, Frost OL, Gomes WR, Erb RE, Bullard JF. 1967. Effect of ovariectomy on pregnancy maintenance and parturition in dairy cows. J Dairy Sci, 50:1293-1295.
Fairclough RJ, Hunter JT, Welch RA. 1975. Peripheral plasma progesterone and utero-ovarian prostaglandin F concentrations in the cow around parturition. Prostaglandins, 9:901-914.
Flint AP, Kingston EJ, Robinson JS, Thorburn GD. 1978. Initiation of parturition in the goat: evidence for control by foetal glucocorticoid through activation of placental C21-steroid 17alpha-hydroxylase. J Endocrinol, 78:367-378.
Ford MM, Young IR, Caddy DJ, Thorburn GD. 1998. Fetal and maternal endocrine changes approaching parturition in the goat: lack of evidence for prostaglandins E2 and F2alpha as signals for luteolysis. Biol Reprod, 58:1065-1070.
Ford MM, Thorburn GD, Caddy DJ, Young IR. 1999. Pulsatile output of prostaglandin F(2alpha) does not increase around the time of luteolysis in the pregnant goat. Biol Reprod, 61:411-415.
Fournier T, Guibourdenche J, Evain-Brion D. 2015. Review: hCGs: different sources of production, different glycoforms and functions. Placenta, 36(suppl. 1):60-65.
Fowden AL, Forhead AJ, Ousey JC. 2008. The endocrinology of equine parturition. Exp Clin Endocrinol Diabetes, 116:393-403.
Fowden AL, Forhead AJ. 2009. Hormones as epigenetic signals in developmental programming. Exp Physiol, 94:607-625.
Fuchs AR, Rust W, Fields MJ. 1999. Accumulation of cyclooxygenase-2 gene transcripts in uterine tissues of pregnant and parturient cows: stimulation by oxytocin. Biol Reprod, 60:341-348.
Garg D, Ng SSM, Baig KM, Driggers P, Segars J. 2017. Progesterone-mediated non-classical signaling. Trends Endocrinol Metab, 28:656-668.
Gootwine E. 2004. Placental hormones and fetal-placental development. Anim Reprod Sci, 82/83:551-566.
Greven H, Kowalewski MP, Hoffmann B, Geyer J, Rex-Haffner M, Ugele B, Schuler G. 2007. Bovine placental steroid sulphatase: molecular cloning and expression pattern in placentomes during gestation and at parturition. Placenta, 28:889-897.
Greven H. 2008. Hydrolysis and transport of sulfonated steroids in bovine placentomes: characterization of the expression and functions of steroid sulfatase (StS) and of the sodium-dependent organic anion transporter (SOAT) [in German]. Giessen, Germany: Faculty of Veterinary Medicine, Justus Liebig University. PhD thesis. Available on: http://geb.uni-giessen.de/geb/volltexte/2008/6029/.
Gyomorey S, Gupta S, Lye SJ, Gibb W, Labrie F, Challis JR. 2000. Temporal expression of prostaglandin H synthase type 2 (PGHS-2) and P450(C17) in ovine placentomes with the natural onset of labour. Placenta, 21:478-486.
Haig D. 2008. Placental growth hormone-related proteins and prolactin-related proteins. Placenta, 29(suppl. A):36-41.
Handwerger S, Crenshaw C Jr, Maurer WF, Barrett J, Hurley TW, Golander A, Fellows RE. 1977. Studies on ovine placental lactogen secretion by homologous radioimmunoassay. J Endocrinol, 72:27-34.
Hansen PJ. 1998. Regulation of uterine immune function by progesterone--lessons from the sheep. J Reprod Immunol, 40:63-79.
Hansen TR, Sinedino LDP, Spencer TE. 2017. Paracrine and endocrine actions of interferon tau (IFNT). Reproduction, 154:F45-F59.
Hein WR, Shelton JN, Simpson-Morgan MW, Seamark RF, Morris B. 1988. Flow and composition of lymph from the ovary and uterus of cows during pregnancy. J Reprod Fertil, 83:309-323.
Hisaw FL. 1926. Experimental relaxation of the pubic ligament of the guinea pig. Proc Soc Exp Biol Med, 23:661-663.
Hoffmann B, Schams D, Bopp R, Ender ML, Giménez T, Karg H. 1974. Luteotrophic factors in the cow: evidence for LH rather than prolactin. J Reprod Fertil, 40:77-85.
Hoffmann B, Wagner WC, Hixon JE, Bahr J. 1979. Observations concerning the functional status of the corpus luteum and the placenta around parturition in the cow. Anim Reprod Sci, 2:253-266.
Hoffmann B, Höveler R, Nohr B, Hasan SH. 1994. Investigations on hormonal changes around parturition in the dog and the occurrence of pregnancy-specific non conjugated oestrogens. Exp Clin Endocrinol, 102:185-189.
Hoffmann B, Gentz F, Failing K. 1996. Investigations into the course of progesterone-, oestrogen- and eCG-concentrations during normal and impaired pregnancy in the mare. Reprod Domest Anim, 32:717-723.
Hoffmann B, Goes de Pinho T, Schuler G. 1997. Determination of free and conjugated oestrogens in peripheral blood plasma, feces and urine of cattle throughout pregnancy. Exp Clin Endocrinol Diabetes, 105:296-303.
Hoffmann B, Bernhardt AW, Failing K, Schuler G. 2014 Profiles of estrone, estrone sulfate and progesterone in donkey (Equus asinus) mares during pregnancy. Tierärztl Prax Ausg G Grosstiere Nutztiere, 42:32-39.
Hoffmann FG, Opazo JC. 2011. Evolution of the relaxin/insulin-like gene family in placental mammals: implications for its early evolution. J Mol Evol, 72:72-79.
Holland MD, Hossner KL, Williams SE, Wallace CR, Niswender GD, Odde KG. 1997. Serum concentrations of insulin-like growth factors and placental lactogen during gestation in cattle. I. Fetal profiles. Domest Anim Endocrinol, 14:231-239.
Hradecký P, Mossman HW, Stott GG. 1988. Comparative development of ruminant placentomes. Theriogenology, 29:715-729.
Hunter JT, Fairclough RJ, Peterson AJ, Welch RA. 1977. Foetal and maternal hormonal changes preceding normal bovine parturition. Acta Endocrinol (Copenh), 84:653-662.
Illingworth DV, Challis JR, Henville A. 1971. Plasma levels of progesterone and oestrogen in the pregnant guinea-pig. J Reprod Fertil, 25:305-306.
Jackson JA, Albrecht ED. 1985. The development of placental androstenedione and testosterone production and their utilization by the ovary for aromatization to estrogen during rat pregnancy. Biol Reprod, 33:451-457.
Janowski T, Zdunczyk S, Podhalicz-Dziegielewska M, Rasz A, Chmielewski A. 1996. Effect of oestrogen antagonist (tamoxifen) on steroid hormone levels, maturation process of placentomes and course of late pregnancy in cows. Reprod Domest Anim, 31:379-384.
Janowski T, Zduńczyk S, Malecki-Tepicht J, Barański W, Raś A. 2002. Mammary secretion of oestrogens in the cow. Domest Anim Endocrinol, 23:125-137.
Jeckel KM, Boyarko AC, Bouma G, Winger Q, Anthony RV. 2018. Chorionic somatomammotropin impacts early fetal growth and placental gene expression. J Endocrinol, J Endocrinol, 237:301-310. .
Jenkin G, Young IR. 2004 Mechanisms responsible for parturition; the use of experimental models. Anim Reprod Sci, 82/83:567-581.
Johnson WH, Manns JG, Adams WM, Mapletoft RJ. 1981. Termination of pregnancy with cloprostenol and dexamethasone in intact or ovariectomized cows. Can Vet J, 22:288-290.
Kennedy PC, Kendrick JW, Stormont C. 1957. Adenohypophyseal aplasia, an inherited defect associated with abnormal gestation in Guernsey cattle. Cornell Vet, 47:160-178.
Khatri P, Frenette G, Sullivan R, Hoffmann B, Schuler G. 2011. Expression of SULT1E1 protein in bovine placentomes: evidence for localization in uninucleated trophoblast cells. Placenta, 32:431-140.
Khatri P, Hoffmann B, Schuler G. 2013. Androgen receptor is widely expressed in bovine placentomes and up-regulated during differentiation of bovine trophoblast giant cells. Placenta, 34:416-423.
Kindahl H, Edqvist LE, Granström E, Bane A. 1976. The release of prostaglandin F2alpha as reflected by 15-keto-13,14-dihydroprostaglandin F2alpha in the peripheral circulation during normal luteolysis in heifers. Prostaglandins, 11:871-878.
Kindahl H, Basu S, Fredriksson G, Goff A, Kunavongkrit A, Edqvist LE. 1984. Levels of prostaglandins F2α metabolites in blood and urine during early pregnancy. Anim Reprod Sci, 7:133-148.
Klein C. 2016. The role of relaxin in mare reproductive physiology: a comparative review with other species. Theriogenology, 86:451-456.
Klisch K, Hecht W, Pfarrer C, Schuler G, Hoffmann B, Leiser R. 1999. DNA content and ploidy level of bovine placentomal trophoblast giant cells. Placenta, 20:451-458.
Königsson K, Kask K, Gustafsson H, Kindahl H, Parvizi N. 2001. 15-ketodihydro-PGF2 alpha, progesterone and cortisol profiles in heifers after induction of parturition by injection of dexamethasone. Acta Vet Scand, 42:151-159.
Kowalewski MP, Beceriklisoy HB, Pfarrer C, Aslan S, Kindahl H, Kücükaslan I, Hoffmann B. 2010. Canine placenta: a source of prepartal prostaglandins during normal and antiprogestin-induced parturition. Reproduction, 139:655-664.
Kowalewski MP, Gram A, Kautz E, Graubner FR. 2015. The dog: nonconformist, not only in maternal recognition signaling. Adv Anat Embryol Cell Biol, 216:215-237.
Krzymowski T, Stefańczyk-Krzymowska S. 2008. The role of the endometrium in endocrine regulation of the animal oestrous cycle. Reprod Domest Anim, 43:80-91.
Legacki EL, Corbin CJ, Ball BA, Wynn M, Loux S, Stanley SD, Conley AJ. 2016. Progestin withdrawal at parturition in the mare. Reproduction, 152:323-231.
Legacki EL, Ball BA, Corbin CJ, Loux SC, Scoggin KE, Stanley SD, Conley AJ. 2017. Equine fetal adrenal, gonadal and placental steroidogenesis. Reproduction, 154:445-454.
Leiser R, Kaufmann P. 1994. Placental structure: in a comparative aspect. Exp Clin Endocrinol, 102:122-134.
Leo CH, Jelinic M, Ng HH, Marshall SA, Novak J, Tare M, Conrad KP, Parry LJ. 2017. Vascular actions of relaxin: nitric oxide and beyond. Br J Pharmacol, 174:1002-1014.
Leon JB, Smith BB, Timm KI, LeCren G. 1990. Endocrine changes during pregnancy, parturition and the early post-partum period in the llama (Lama glama). J Reprod Fertil, 88:503-511.
Liggins GC. 1968. Premature parturition after infusion of corticotrophin or cortisol into foetal lambs. J Endocrinol, 42:323-329.
Liggins GC. 2000. The role of the hypothalamic-pituitary-adrenal axis in preparing the fetus for birth. Am J Obstet Gynecol, 182:475-477.
Loriaux DL, Ruder HJ, Knab DR, Lipsett MB. 1972. Estrone sulfate, estrone, estradiol and estriol plasma levels in human pregnancy. J Clin Endocrinol Metab, 35:887-891.
Lykkesfeldt G, Nielsen MD, Lykkesfeldt AE. 1984. Placental steroid sulfatase deficiency: biochemical diagnosis and clinical review. Obstet Gynecol, 64:49-54.
Madore E, Harvey N, Parent J, Chapdelaine P, Arosh JA, Fortier MA. 2003. An aldose reductase with 20 alpha-hydroxysteroid dehydrogenase activity is most likely the enzyme responsible for the production of prostaglandin F2 alpha in the bovine endometrium. J Biol Chem, 278:11205-11212.
Malone L, Opazo JC, Ryan PL, Hoffmann FG. 2017. Progressive erosion of the relaxin 1 gene in bovids. Gen Comp Endocrinol, 252:12-17.
Mason JI, France JT, Magness RR, Murry BA, Rosenfeld CR. 1989. Ovine placental steroid 17 alpha-hydroxylase/C-17,20-lyase, aromatase and sulphatase in dexamethasone-induced and natural parturition. J Endocrinol, 122:351-359.
Mathew DJ, Lucy MC, D Geisert R. 2016. Interleukins, interferons, and establishment of pregnancy in pigs. Reproduction, 151:R111-122.
Maule Walker FM, Davis AJ, Fleet IR. 1983. Endocrine activity of the mammary gland: oestrogen and prostaglandin secretion by the cow and sheep mammary glands during lactogenesis. Br Vet J, 139:171-177.
McLaren WJ, Young IR, Rice GE. 2000. Immunohistochemical localization of prostaglandin G/H synthase 1 and 2 in sheep placenta after glucocorticoid-induced and spontaneous labour. J Reprod Fertil, 120:33-39.
Meyer HH. 1994. Luteal versus placental progesterone: the situation in the cow, pig and bitch. Exp Clin Endocrinol, 102:190-192.
Meyer HH, Enzenhöfer G, Feck H. 1989 Improvement of radioimmunoassays for prostaglandins in bovine blood plasma and their application to monitor reproductive functions. Theriogenology, 31:701-720.
Mitchell BF, Taggart MJ. 2009. Are animal models relevant to key aspects of human parturition? Am J Physiol Regul Integr Comp Physiol, 297:R525-545.
Mueller JW, Gilligan LC, Idkowiak J, Arlt W, Foster PA. 2015. The regulation of steroid action by sulfation and desulfation. Endocr Rev, 36:526-563.
Murphy BD, Martinuk SD. 1991. Equine chorionic gonadotropin. Endocr Rev 12:27-44.
Musah AI, Schwabe C, Willham RL, Anderson LL. 1986. Relaxin on induction of parturition in beef heifers. Endocrinology, 118:1476-1482.
Nathanielsz PW, Elsner C, Magyar D, Fridshal D, Freeman A, Buster JE. 1982. Time trend analysis of plasma unconjugated and sulfoconjugated estrone and 3beta-delta 5-steroids in fetal and maternal sheep plasma in relation to spontaneous parturition at term. Endocrinology, 110:1402-1407.
Nishiyama T, Tsumagari S, Ito M, Kimura J, Watanabe G, Taya K, Takeishi M. 1999. Immunohistochemical study of steroidogenic enzymes in the ovary and placenta during pregnancy in the dog. Anat Histol Embryol, 28:125-129.
Nowak M, Gram A, Boos A, Aslan S, Ay SS, Önyay F, Kowalewski MP. 2017. Functional implications of the utero-placental relaxin (RLN) system in the dog throughout pregnancy and at term. Reproduction, 154:415-431.
Oh SY, Kim CJ, Park I, Romero R, Sohn YK, Moon KC, Yoon BH. 2005. Progesterone receptor isoform (A/B) ratio of human fetal membranes increases during term parturition. Am J Obstet Gynecol, 193:1156-1160.
Palejwala S, Tseng L, Wojtczuk A, Weiss G, Goldsmith LT. 2002. Relaxin gene and protein expression and its regulation of procollagenase and vascular endothelial growth factor in human endometrial cells. Biol Reprod, 66:1743-1748.
Parry LJ, Vodstrcil LA. 2007. Relaxin physiology in the female reproductive tract during pregnancy. Adv Exp Med Biol, 612:34-48.
Pashen RL, Allen WR. 1979. The role of the fetal gonads and placenta in steroid production, maintenance of pregnancy and parturition in the mare. J Reprod Fertil Suppl, 27:499-509.
Patel OV, Yamada O, Kizaki K, Todoroki J, Takahashi T, Imai K, Schuler LA, Hashizume K. 2004. Temporospatial expression of placental lactogen and prolactin-related protein-1 genes in the bovine placenta and uterus during pregnancy. Mol Reprod Dev, 69:146-152.
Peaker M, Taylor E. 1990. Oestrogen production by the goat mammary gland: transient aromatase activity during late pregnancy. J Endocrinol, 125:R1-3.
Pepe GJ, Albrecht ED. 1995. Actions of placental and fetal adrenal steroid hormones in primate pregnancy. Endocr Rev, 16:608-648.
Perrier d'Hauterive S, Berndt S, Tsampalas M, Charlet-Renard C, Dubois M, Bourgain C, Hazout A, Foidart JM, Geenen V. 2007. Dialogue between blastocyst hCG and endometrial LH/hCG receptor: which role in implantation? Gynecol Obstet Invest, 64:156-160.
Peterson AJ, Fairclough RJ, Payne E, Smith JF. 1975. Hormonal changes around bovine luteolysis. Prostaglandins, 10:675-684.
Polei M, Viergutz T, Tomek W, Schuler G, Fürbass R. 2014. Estrogen-specific sulfotransferase (SULT1E1) in bovine placentomes: inverse levels of mRNA and protein in uninucleated trophoblast cells and trophoblast giant cells. Biol Reprod, 91:48. doi: 10.1095/biolreprod.114.118760.
Probo M, Cairoli F, Kindahl H, Faustini M, Galeati G, Veronesi MC. 2011. Peripartal hormonal changes in Alpine goats: a comparison between physiological and pathological parturition. Reprod Domest Anim, 46:1004-1010.
Raeside JI. 2017. A brief account of the discovery of the fetal/placental unit for estrogen production in equine and human pregnancies: relation to human medicine. Yale J Biol Med, 90:449-461.
Reicher S, Niv-Spector L, Gertler A, Gootwine E. 2008. Pituitary and placental ovine growth hormone variants differ in their receptor-binding ability and in their biological properties. Gen Comp Endocrinol, 155:368-377.
Riveros JL, Urquieta B, Bonacic C, Hoffmann B, Bas F, Schuler G. 2009. Endocrine changes during pregnancy, parturition and post-partum in guanacos (Lama guanicoe). Anim Reprod Sci, 116:318-325.
Ryan PL, Bennett-Wimbush K, Vaala WE, Bagnell CA. 2001. Systemic relaxin in pregnant pony mares grazed on endophyte-infected fescue: effects of fluphenazine treatment. Theriogenology, 56:471-483.
Ryan PL, Christiansen DL, Hopper RM, Bagnell CA, Vaala WE, Leblanc MM. 2009. Evaluation of systemic relaxin blood profiles in horses as a means of assessing placental function in high-risk pregnancies and responsiveness to therapeutic strategies. Ann N Y Acad Sci, 1160:169-178.
Sawada T, Nakatani T, Tamada H, Mori J. 1995. Secretion of unconjugated estrone during pregnancy and around parturition in goats. Theriogenology, 44:281-286.
Scholtz EL, Krishnan S, Ball BA, Corbin CJ, Moeller BC, Stanley SD, McDowell, KJ, Hughes AL, McDonnell DP, Conley AJ. 2014. Pregnancy without progesterone in horses defines a second endogenous biopotent progesterone receptor agonist, 5α-dihydroprogesterone. Proc Natl Acad Sci USA, 111:3365-3370.
Schuler G, Hartung F, Hoffmann B. 1994. Investigations on the use of C-21-steroids as precursors for placental oestrogen synthesis in the cow. Exp Clin Endocrinol, 102:169-174.
Schuler G, Wirth C, Klisch K, Pfarrer C, Leiser R, Hoffmann B. 1999 Immunolocalization of progesterone receptors in bovine placentomes throughout mid and late gestation and at parturition. Biol Reprod, 61:797-801.
Schuler G, Wirth C, Klisch K, Failing K, Hoffmann B. 2000. Characterization of proliferative activity in bovine placentomes between day 150 and parturition by quantitative immunohistochemical detection of Ki67-antigen. Reprod Domest Anim, 35:157-162.
Schuler G, Wirth C, Teichmann U, Failing K, Leiser R, Thole H, Hoffmann B. 2002. Occurrence of estrogen receptor alpha in bovine placentomes throughout mid and late gestation and at parturition. Biol Reprod, 66:976-982.
Schuler G, Teichmann U, Taubert A, Failing K, Hoffmann B. 2005. Estrogen receptor beta (ERbeta) is expressed differently from ERalpha in bovine placentomes. Exp Clin Endocrinol Diabetes, 113:107-114.
Schuler G, Özalp GR, Hoffmann B, Harada N, Browne P, Conley AJ. 2006a. Reciprocal expression of 17alpha-hydroxylase-C17,20-lyase and aromatase cytochrome P450 during bovine trophoblast differentiation: a two-cell system drives placental oestrogen synthesis. Reproduction, 131:669-679.
Schuler G, Teichmann U, Kowalewski MP, Hoffmann B, Madore E, Fortier MA, Klisch K. 2006b. Expression of cyclooxygenase-II (COX-II) and 20alpha-hydroxysteroid dehydrogenase (20alpha-HSD)/prostaglandin F-synthase (PGFS) in bovine placentomes: implications for the initiation of parturition in cattle. Placenta, 27:1022-1029.
Schuler G, Greven H, Kowalewski MP, Döring B, Ozalp GR, Hoffmann B. 2008. Placental steroids in cattle: hormones, placental growth factors or by-products of trophoblast giant cell differentiation? Exp Clin Endocrinol Diabetes, 116:429-436.
Sheldrick EL, Ricketts AP, Flint AP. 1980. Placental production of progesterone in ovariectomized goats treated with a synthetic progestagen to maintain pregnancy. J Reprod Fertil, 60:339-348.
Shenavai S, Hoffmann B, Dilly M, Pfarrer C, Özalp GR, Caliskan C, Seyrek-Intas K, Schuler G. 2010. Use of the progesterone (P4) receptor antagonist aglepristone to characterize the role of P4 withdrawal for parturition and placental release in cows. Reproduction, 140:623-632.
Shenavai S, Preissing S, Hoffmann B, Dilly M, Pfarrer C, Özalp GR, Caliskan C, Seyrek-Intas K, Schuler G. 2012. Investigations into the mechanisms controlling parturition in cattle. Reproduction, 144:279-292.
Siemieniuch MJ, Jursza E, Szóstek AZ, Zschockelt L, Boos A, Kowalewski MP. 2014. Placental origin of prostaglandin F2α in the domestic cat. Mediators Inflamm, 2014:364787. doi.org/10.1155/2014/364787.
Smith DE, Hixon DL, Moore DW, Van Kirk EA, Alexander BM, Anthony RV, Moss GE. 1996. Effects of porcine relaxin on induced parturition in beef heifers. Domest Anim Endocrinol, 13:469-476.
Smith KH, Musah AI, Cho SJ, Schwabe C, Anderson LL. 1997. Continuous infusion of relaxin on periparturient progesterone, oxytocin and relaxin plasma concentrations and time of parturition in beef heifers. Anim Reprod Sci, 46:15-25.
Smith R, Smith JI, Shen X, Engel PJ, Bowman ME, McGrath SA, Bisits AM, McElduff P, Giles WB, Smith DW. 2009. Patterns of plasma corticotropin-releasing hormone, progesterone, estradiol, and estriol change and the onset of human labor. J Clin Endocrinol Metab, 94:2066-2074.
Soares MJ. 2004. The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol, 2:51. doi: 10.1186/1477-7827-2-51.
Soares MJ, Konno T, Alam SM. 2007. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol Metab, 18:114-121.
Spencer TE, Hansen TR. 2015. Implantation and establishment of pregnancy in ruminants. Adv Anat Embryol Cell Biol, 216:105-135.
Spencer TE, Burghardt RC, Johnson GA, Bazer FW. 2004a. Conceptus signals for establishment and maintenance of pregnancy. Anim Reprod Sci, 82/83:537-50.
Spencer TE, Johnson GA, Burghardt RC, Bazer FW. 2004b. Progesterone and placental hormone actions on the uterus: insights from domestic animals. Biol Reprod, 71:2-10.
Streyl D, Kenngott R, Herbach N, Wanke R, Blum H, Sinowatz F, Wolf E, Zerbe H, Bauersachs S. 2012. Gene expression profiling of bovine peripartal placentomes: detection of molecular pathways potentially involved in the release of foetal membranes. Reproduction, 143:85-105.
Thorburn GD. 1993 A speculative review of parturition in the mare. Equine Vet J Suppl, 14:41-49.
Tsang CP. 1974. Changes in plasma levels of estrone sulfate and estrone in the pregnant ewe around parturition. Steroids, 23:855-868.
Tsumagari S, Kamata J, Takagi K, Tanemura K, Yosai A, Takeishi M. 1994. 3beta-Hydroxysteroid dehydrogenase activity and gestagen concentrations in bovine cotyledons and caruncles during gestation and parturition. J Reprod Fertil, 102:35-39.
Ushizawa K, Takahashi T, Hosoe M, Kizaki K, Hashizume K. 2010. Cleaved bovine prolactin-related protein-I stimulates vascular endothelial cell proliferation. Mol Cell Endocrinol, 323:277-381.
Uzelac PS, Li X, Lin J, Neese LD, Lin L, Nakajima ST, Bohler H, Lei Z. 2010. Dysregulation of leptin and testosterone production and their receptor expression in the human placenta with gestational diabetes mellitus. Placenta, 31:581-588.
Vermeirsch H, Simoens P, Lauwers H. 2000. Immunohistochemical detection of the estrogen receptor-alpha and progesterone receptor in the canine pregnant uterus and placental labyrinth. Anat Rec, 260:42-50.
Vighio GH, Liptrap RM. 1986. Plasma concentrations of oxytocin, prostaglandin and ovarian steroids during spontaneous luteolysis in the cow. Domest Anim Endocrinol, 3:209-215.
Wallace CR. 1993. Concentration of bovine placental lactogen in dairy and beef cows across gestation. Domest Anim Endocrinol, 10:67-70.
Watanabe N, Hatano J, Asahina K, Iwasaki T, Hayakawa S. 2007. Molecular cloning and histological localization of LH-like substances in a bottlenose dolphin (Tursiops truncatus) placenta. Comp Biochem Physiol A Mol Integr Physiol, 146:105-118.
Weems CW, Weems YS, Randel RD. 2006. Prostaglandins and reproduction in female farm animals. Vet J, 171:206-228.
Wehbrink D, Hässig M, Ritter N, Zerbe H, Bleul U, Boos A. 2008. Immunohistochemical demonstration of cyclooxygenase-2 (COX-2) and prostaglandin receptors EP2 and FP expression in the bovine intercaruncular uterine wall around term. Anim Reprod Sci, 106:241-254.
Whittle WL, Holloway AC, Lye SJ, Gibb W, Challis JR. 2000. Prostaglandin production at the onset of ovine parturition is regulated by both estrogen-independent and estrogen-dependent pathways. Endocrinology, 141:3783-3791.
Whittle WL, Patel FA, Alfaidy N, Holloway AC, Fraser M, Gyomorey S, Lye SJ, Gibb W, Challis JR. 2001. Glucocorticoid regulation of human and ovine parturition: the relationship between fetal hypothalamic-pituitary-adrenal axis activation and intrauterine prostaglandin production. Biol Reprod, 64:1019-1032.
Wieciech I, Durlej-Grzesiak M, Słomczyńska M. 2013. Influence of the antiandrogen flutamide on the androgen receptor gene expression in the placenta and umbilical cord during pregnancy in the pig. Acta Histochem, 115:290-295.
Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R. 2006. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci USA, 103:3203-3208.
Wooding FB, Wathes DC. 1980. Binucleate cell migration in the bovine placentome. J Reprod Fertil, 59:425-430.
Wooding FB. 1992. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta, 13:101-113.
Yamamoto Y, Yamamoto T, Yuto N, Hildebrandt TB, Lueders I, Wibbelt G, Shiina O, Mouri Y, Sugimura K, Sakamoto S, Kaewmanee S, Nagaoka K, Watanabe G, Taya K. 2012. The secretory pattern and source of immunoreactive prolactin in pregnant African (Loxodonta africana) and Asian (Elephas maximus) elephants. J Reprod Dev, 58:105-111.
Yamasato K, Tsai PS, Davis J, Yamamoto SY, Bryant-Greenwood GD. 2017. Human relaxins (RLNH1, RLNH2), their receptor (RXFP1) and fetoplacental growth. Reproduction, 154:67-77.
Yegorov S, Bogerd J, Good SV. 2014. The relaxin family peptide receptors and their ligands: new developments and paradigms in the evolution from jawless fish to mammals. Gen Comp Endocrinol, 209:93-105.
Zakar T, Hertelendy F. 2007. Progesterone withdrawal: key to parturition. Am J Obstet Gynecol, 196:289-296.
Zhu BT, Han GZ, Shim JY, Wen Y, Jiang XR. 2006. Quantitative structure-activity relationship of various endogenous estrogen metabolites for human estrogen receptor alpha and beta subtypes: Insights into the structural determinants favoring a differential subtype binding. Endocrinology, 147:4132-4150.