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Implantation and Placentation in Ruminants

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Placentation in Mammals

Part of the book series: Advances in Anatomy, Embryology and Cell Biology ((ADVSANAT,volume 234))

Abstract

In comparison to many other mammalian species, ruminant ungulates have a unique form of placentation. Ruminants initially display an epitheliochorial type of placentation; however, during the period of placental attachment, trophoblast giant binucleate cells (BNC) develop within the chorion to migrate and fuse with the uterine surface epithelium to form syncytial plaques. Binucleate cell migration and fusion continues throughout pregnancy but never appears to breach the basal lamina, beneath the uterine surface or luminal epithelium. Therefore, the semi-invasive type of placentation in ruminants is classified as synepitheliochorial. The endometrium of ruminant species also contains unique specialized aglandular structures termed “caruncles” in which the chorioallantois (cotyledons) interdigitates and forms highly vascularized fetal–maternal “placentomes.” This chapter will discuss the current knowledge of early conceptus development during the peri-attachment period, establishment of pregnancy, conceptus attachment, and placentation in ruminant ungulates. The features of placentomes, BNCs, fetomaternal hybrid cells, and multinucleated syncytial plaques of the cotyledonary placenta of ruminant species will be reviewed to highlight the unique form of placentation compared to the placentae of other artiodactyls.

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References

  • Amoroso EC (1952) Placentation. In: Parkes AS (ed) Marshall’s physiology of reproduction, vol 2, 3rd edn. Longmans, London, pp 127–311

    Google Scholar 

  • Assis Neto AC, Pereira FTV, Santos TC, Ambrosio CE, Leiser R, Miglino MA (2010) Morpho-physical recording of bovine conceptus (Bos indicus) and placenta from days 20 to 70 of pregnancy. Reprod Domest Anim 45:760–772

    CAS  PubMed  Google Scholar 

  • Bazer FW (1989) Allantoic fluid: regulation of volume and composition. In: Brace RA (ed) Fetal and neonatal body fluids. Perinatology Press, Cornell, NY, pp 135–157

    Google Scholar 

  • Bazer FW, Johnson GA (2018) Allantois. In: Skinner MK (ed) Encyclopedia of reproduction, vol 2. Academic Press, Elsevier, New York, NY, pp 559–561

    Chapter  Google Scholar 

  • Bazer FW, Goldstein MH, Barron DH (1981) Water and electrolyte transport by pig chorioallantois. In: Mastroianni L, Biggers JD (eds) Fertilization and embryonic development in vitro. Plenum, New York, pp 299–321

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bazer FW, Kim J, Ka H, Johnson GA, Wu G, Song G (2012) Select nutrients in the uterine lumen of sheep and pigs affect conceptus development. J Reprod Dev 58:180–188

    Article  CAS  PubMed  Google Scholar 

  • Bazer FW, Ying W, Wang X, Dunlap KA, Zhou B, Johnson JA, Wu G (2015) The many faces of interferon tau. Amino Acids 47:449–460

    Article  CAS  PubMed  Google Scholar 

  • Bazer FW, Seo H, Wu G, Johnson GA (2020) Interferon tau: influences on growth and development of the conceptus. Theriogenology 150:75–83

    Article  CAS  PubMed  Google Scholar 

  • Berg DK, Smith CS, Pearton DJ, Wells DN, Broadhurst R, Donnison M, Pfeffer PL (2011) Trophectoderm lineage determination in cattle. Dev Cell 20:244–255

    Article  CAS  PubMed  Google Scholar 

  • Betteridge KJ, Flechon JE (1988) The anatomy and physiology of the pre-attachment bovine embryos. Theriogenology 29:155–187

    Article  Google Scholar 

  • Betteridge KJ, Eaglesome MD, Randall GC, Mitchell DJ (1980) Collection, description and transfer of embryos from cattle 10-16 days after oestrus. Reprod Fertil 59:205–216

    Article  CAS  Google Scholar 

  • Black SG, Arnaud F, Palmarini M, Spencer TE (2010) Endogenous retroviruses in trophoblast differentiation and placental development. Am J Reprod Immunol 64:255–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boshier DP (1969) A histological and histochemical examination of implantation and early placentome formation in sheep. J Reprod Fertil 19:51–61

    Article  CAS  PubMed  Google Scholar 

  • Brackett BG, Oh YK, Evans JF, Donawick WJ (1980) Fertilization and early development of cow ova. Biol Reprod 23:189–205

    Article  CAS  PubMed  Google Scholar 

  • Brooks KE, Burns GW, Spencer TE (2015) Peroxisome proliferator activator receptor gamma (PPARG) regulates conceptus elongation in sheep. Biol Reprod 42:1–13

    Google Scholar 

  • Burghardt RC, Burghardt JR, Taylor JD II, Reeder AT, Nguyen BT, Spencer TE, Johnson GA (2009) Enhanced focal adhesion assembly reflects increased mechanosensation and mechanotransduction along the maternal/conceptus interface during pregnancy in sheep. Reproduction 137:567–582

    Article  CAS  PubMed  Google Scholar 

  • Carter AM, Enders AC (2013) The evolution of epitheliochorial placentation. Annu Rev Anim Biosci 1:443–467

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Charpigny G, Reinaud P, Tamby JP, Creminon C, Martal J, Maclouf J, Guillomot M (1997b) Expression of cyclooxygenase-1 and -2 in ovine endometrium during the estrous cycle and early pregnancy. Endocrinology 138:2163–2217

    Article  CAS  PubMed  Google Scholar 

  • Chavatte-Palmer P, Guillomot M (2007) Comparative implantation and placentation. Gynecol Obstet Invest 64:166–174

    Article  PubMed  Google Scholar 

  • Cockburn K, Rossant J (2010) Making the blastocyst: lessons from the mouse. J Clin Invest 120:995–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper DN (2002) Galectinomics: finding themes in complexity. Biochim Biophys Acta 1572:209–231

    Article  CAS  PubMed  Google Scholar 

  • Cornelis G, Heidmann O, Degrelle SA, Vernochet C, Lavialle C, Letzelter C, Bernard-Stoecklin S, Hassanin A, Mulot B, Guillomot M, Hue I, Heidmann T, Dupressoir A (2013) Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. PNAS 110:E828–E837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Duello TM, Byatt JC, Bremel RD (1986) Immunohistochemical localization of placental lactogen in binucleate cells of bovine placentomes. Endocrinology 119:1351–1355

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KA, Palmarini M, Adelson DL, Spencer TE (2005) Sheep endogenous betaretroviruses (enJSRVs) and the hyaluronidase 2 (HYAL2) receptor in the ovine uterus and conceptus. Biol Reprod 73:271–279

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KA, Palmarini M, Spencer TE (2006a) Ovine endogenous betaretroviruses (enJSRVs) and placental morphogenesis. Placenta 27(Suppl a):S135–S140

    Article  PubMed  Google Scholar 

  • Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE (2006b) Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci 103:14390–14395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eley RM, Thatcher WW, Bazer FW, Wilcox CJ, Becker RB, Head HH, Adkinson RW (1978) Development of the conceptus in the bovine. J Dairy Sci 61:467–473

    Article  CAS  PubMed  Google Scholar 

  • Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R, O'Gaora P, Roche JF, Lonergan P (2011) Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod 85:144–156

    Article  CAS  PubMed  Google Scholar 

  • Frank JW, Steinhauser CB, Wang X, Bughardt RC, Bazer FW, Johnson GA (2020) Loss of ITGB3 in ovine conceptuses decreases conceptus expression of NOS3 and SPP1: implications for the developing placental vasculature. Biol Reprod:ioaa212

    Google Scholar 

  • Galdos-Riveros AC, Favaron PO, Seal W, Miglino MA, Maria DA (2015) Bovine yolk sac: from morphology to metabolomic and proteomic profiles. Genet Mol Res 14:6223–6238

    Article  CAS  PubMed  Google Scholar 

  • Garrett JE, Geisert RD, Zavy MT, Morgan GL (1988) Evidence for maternal regulation of early conceptus growth and development in beef cattle. J Reprod Fertil 84:437–446

    Article  CAS  PubMed  Google Scholar 

  • Geisert RD, Johnson GA, Burghardt RC (2015) Implantation and establishment of pregnancy in the pig. Adv Anat Embryol Cell Biol 216:137–163

    Article  PubMed  Google Scholar 

  • Gray CA, Adelson DL, Bazer FW, Burghardt RC, Meeusen EN, Spencer TE (2004) Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm. PNAS 101:7982–7987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green JA, Xie S, Quan X, Bao B, Gan X, Mathialagan N, Beckers J-F, Roberts RM (2000) Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biol Reprod 62:1624–1631

    Article  CAS  PubMed  Google Scholar 

  • Green JA, Parks TE, Avalle MP, Telugu BP, McLain AL, Peterson AJ, McMillan W, Mathialagan N, Xie S, Hook RR, Roberts RM (2005) The establishment of an ELISA for the detection of pregnancy-associated glycoproteins (PAGs) in the serum of pregnant cows and heifers. Theriogenology 63:1481–1503

    Article  CAS  PubMed  Google Scholar 

  • Greenstein JS, Murray RW, Foley RC (1958) Observations on the morphogenesis and histochemistry of the bovine pre-attachment placenta between 16 and 33 days of gestation. Anat Rec 132:321–341

    Article  CAS  PubMed  Google Scholar 

  • Gresham EL, Rankin JHG, Makowski EL, Meschia G, Battaglia FC (1972) An evaluation of fetal renal function in a chronic sheep preparation. J Clin Invest 51:149–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grosser O (1909) Vergleichende Anatomie und Entwicklungsgeschichte der Eihaute und der Placenta. W. Braumuller, Vienna and Leipzig

    Google Scholar 

  • Grosser O (1927) Fruhentwicklung, Eihautbidung und Placentation des Menschen und der Saugetiere. J. F. Bergmann, Munchen

    Google Scholar 

  • Guillomot M, Guay P (1982) Ultrastructural features of the cell surfaces of uterine and trophoblastic epithelia during embryo attachment in the cow. Anat Rec 204:315–322

    Article  CAS  PubMed  Google Scholar 

  • Guillomot M, Fechon JE, Wintenberger-Torres S (1981) Conceptus attachment in the ewe: an ultrastructural study. Placenta 2:169–182

    Article  CAS  PubMed  Google Scholar 

  • Guillomot M, Fléchon JE, Wintenberger-Torres S (1982) Cytochemical studies of uterine and trophoblastic surface coats during blastocyst attachment in the ewe. J Reprod Fertil 65:1–8

    Article  CAS  PubMed  Google Scholar 

  • Guillomot M, Flechon JE, Leroy F (1993) Blastocyst development and implantation. In: Thibault C, Levasseur MC, Hunter RHF (eds) Reproduction in mammals and man. Ellipses, Paris, pp 387–411

    Google Scholar 

  • Haig D (1996) Altercation of generations: genetic conflicts of pregnancy. Am J Reprod Immunol 35:226–232

    Article  CAS  PubMed  Google Scholar 

  • Hradecky P (1983) Placental morphology in African antelopes and giraffes. Theriogenology 20:725–734

    Article  Google Scholar 

  • Hradecky P, Mossman HW, Stott GG (1988) Comparative development of the ruminant placentomes. Theriogenology 29:715–7129

    Article  CAS  PubMed  Google Scholar 

  • Johnson GA, Bazer FW, Jaeger LA, Ka H, Garlow JE, Pfarrer C, Spencer TE, Burghardt RC (2001) Muc-1, integrin and osteopontin expression during the implantation cascade in sheep. Biol Reprod 65:820–828

    Article  CAS  PubMed  Google Scholar 

  • Johnson GA, Burghardt RC, Bazer FW (2014) Osteopontin: a leading candidate adhesion molecule for implantation in pigs and sheep. J Anim Sci Biotech 5:56

    Article  Google Scholar 

  • Johnson GA, Bazer FW, Burghardt RC, Wu G, Seo H, Kramer AC, McLendon BA (2018) Cellular events during ovine implantation and impact for gestation. Anim Reprod 15:843–855

    Article  Google Scholar 

  • Kelleher AK, Demayo FJ, Spencer TE (2019) Uterine glands: developmental biology and functional roles in pregnancy. Endocr Rev 40:1424–1445

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim J, Erikson DW, Burghardt RC, Spencer TE, Wu G, Bayless KJ, Johnson GA, Bazer FW (2010) Secreted phosphoprotein 1 binds integrins to initiate multiple cell signaling pathways, including FRAP1/mTOR, to support attachment and force-generated migration of trophectoderm cells. Matrix Biol 29:369–382

    Article  CAS  PubMed  Google Scholar 

  • Kimura J, Sasaki M, Endo H, Fukuta K (2004) Anatomical and histological characterization of the female reproductive organs of mouse deer (Tragulidae). Placenta 25:705–711

    Article  CAS  PubMed  Google Scholar 

  • King GJ (1993) Comparative placentation in ungulates. J Exp Zool 266:588–602

    Article  CAS  PubMed  Google Scholar 

  • King GJ, Atkinson BA (1987) The bovine intercaruncular placenta throughout gestation. Anim Reprod Sci 12:241–254

    Article  Google Scholar 

  • King GJ, Atkinson BA, Robertson HA (1979) Development of the bovine placentome during the second month of gestation. J Reprod Fertil 55:173–180

    Article  CAS  PubMed  Google Scholar 

  • King GJ, Atkinson BA, Robertson HA (1980) Development of the bovine placentome from days 20 to 29 of gestation. J. Reprod Fertil 59:95–100

    Article  CAS  Google Scholar 

  • King GJ, Atkinson BA, Robertson HA (1981) Development of the intercaruncular area during early gestation and the establishment of the bovine placenta. J Reprod Fertil 61:469–474

    Article  CAS  PubMed  Google Scholar 

  • King GJ, Atkinson BA, Robertson HA (1982) Implantation and early placentation in domestic ungulates. J Reprod Fertil Suppl 31:17–30

    CAS  PubMed  Google Scholar 

  • Kritzenberger M, Wrobel K-H (2004) Histochemical in situ identification of bovine embryonic blood cells reveals differences to the adult hematopoietic system and suggests a close relationships between hematopoietic stem cells and primordial germ cells. Histochem Cell Biol 121:273–289

    Article  CAS  PubMed  Google Scholar 

  • Leiser R (1975) Development of contact between trophoblast and uterine epithelium during the early stages on implantation in the cow. Zentralbl Veterinarmed C 4:63–86

    CAS  PubMed  Google Scholar 

  • Leiser R, Pfarrer C, Abd-Elnaeim M, Dantzer V (1998) Feto-maternal anchorage in epitheliochorial and endotheliochorial placental types studied by histology and microvascular corrosion casts. Placenta 9:21–39

    Article  Google Scholar 

  • Llobat L (2020) Embryo gene expression in pig pregnancy. Reprod Domest Anim 55:523–529

    Article  CAS  PubMed  Google Scholar 

  • Lonergan P, Forde N, Spencer T (2016) Role of progesterone in embryo development in cattle. Reprod Fertil Dev 28:66–74

    Article  CAS  PubMed  Google Scholar 

  • Maddox-Hyttel P, Alexopoulos NI, Vajta G, Lewis I, Rogers P, Cann L, Callesen A, Tveden-Nyborg P, Trounson A (2003) Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125:607–623

    Article  CAS  PubMed  Google Scholar 

  • Mançanares CAF, Leiser R, Favaron PO, Carvalho AF, Oliveira VC, De Santos JM et al (2013) A morphological analysis of the transition between the embryonic primitive intestine and yolk sac in bovine embryos and fetuses. Microsc Res Tech 76:756–766

    Article  PubMed  Google Scholar 

  • Mi S, Lee X, X-p L, Veldman GM, Finnerty H, Racie L, LaVallie E, Tang X-Y, Edouard P, Howes S, Keith JC, McCoy JM (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789

    Article  CAS  PubMed  Google Scholar 

  • Moraes JGN, Behura SK, Geary TW, Hansen PJ, Neibergs HL, Spencer TE (2018) Uterine influences on conceptus development in fertility-classified animals. Proc Natl Acad Sci 115:E1749–E1758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan G, Wooding FBP (1983) Cell migration in the ruminant placenta, a freeze fracture study. J Ultrastruct Res 83:148–160

    Article  CAS  PubMed  Google Scholar 

  • Mossman HW (1937) Comparative morphogenesis of the fetal membranes and accessory uterine structures. Contr Embryol Carnegie Instn 158:129–246

    Google Scholar 

  • Mossman HW (1974) Structural changes in vertebrate fetal membranes associated with the adoption of viviparity. Obstet Gynecol Annu 3:7–32

    CAS  PubMed  Google Scholar 

  • Mossman HW (1987) Vertebrate fetal membranes. Rutgers University Press, München, p 383

    Google Scholar 

  • Negrón-Pérez VM, Rodrigues LT, Mingoti GZ, Hansen PJ (2018) Role of ROCK signaling in formation of the trophectoderm of the bovine preimplantation embryo. Mol Reprod Dev 85:374–375

    Article  PubMed  Google Scholar 

  • Palmarini M, Gray CA, Carpenter K, Fan H, Bazer FW, Spencer TE (2001) Expression of endogenous betaretroviruses in the ovine uterus: effects of neonatal age, estrous cycle, pregnancy, and progesterone. J Virol 75:11319–11327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perry JS (1981) The mammalian fetal membranes. J Reprod Fertil 62:321–335

    Article  CAS  PubMed  Google Scholar 

  • Pohler KG, Geary TW, Johnson CL, Atkins JA, Jinks EM, Busch DC, Green JA, MacNeil MD, Smith MF (2013) Circulating bovine pregnancy associated glycoproteins are associated with late embryonic/fetal survival but not ovulatory follicle size in suckled beef cows. J Anim Sci 91:4158–4167

    Article  CAS  PubMed  Google Scholar 

  • Pohler KG, Pereira MHC, Lopes FR, Lawrence JC, Keisler DH, Smith MF, Vasconcelos JLM, Green JA (2016a) Circulating concentrations of bovine pregnancy-associated glycoproteins and late embryonic mortality in lactating dairy herds. J Dairy Sci 99:1584–1594

    Article  CAS  PubMed  Google Scholar 

  • Pohler KG, Peres RFG, Green JA, Graff H, Martins T, Vasconcelos JLM, Smith MF (2016b) Use of bovine pregnancy-associated glycoproteins to predict late embryonic mortality in postpartum Nelore beef cows. Theriogenology 85:1652–1659

    Article  CAS  PubMed  Google Scholar 

  • Raheem KA, Marei WFA, Campbell BK, Fouladi-Nashta AA (2016) In vivo and in vitro studies of MUC1 regulation in sheep endometrium. Theriogenology 85:1635–1643

    Article  CAS  PubMed  Google Scholar 

  • Rasby RJ, Wettemann RP, Geisert RD, Rice LE, Wallace CR (1990) Nutrition, body condition and reproduction in beef cows: fetal and placental development, and estrogens and progesterone in plasma. J Anim Sci 68:4267–4276

    Article  CAS  PubMed  Google Scholar 

  • Reimers T, Ullmann M, Hansel W (1985) Progesterone and prostanoid production by bovine binucleate trophoblastic cells. Biol Reprod 33:1227–1236

    Article  CAS  PubMed  Google Scholar 

  • Roberts RM, Green JA, Schulz LC (2016) The evolution of the placenta. Reproduction 152:R179–R189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowson LEA, Moore RM (1966) Embryo transfer in sheep; the significance of synchronizing oestrus in the donor and recipient animal. J Reprod Fertil 11:207–212

    Article  CAS  PubMed  Google Scholar 

  • Sasser RG, Ruder CA, Ivani KA, Butler JE, Hamilton WC (1986) Detection of pregnancy by radioimmunoassay of a novel pregnancy-specific protein in serum of cows and a profile of serum concentrations during gestation. Biol Reprod 35:936–942

    Article  CAS  PubMed  Google Scholar 

  • Satterfield MC, Bazer FW, Spencer TE (2006) Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biol Reprod 75:289–296

    Article  CAS  PubMed  Google Scholar 

  • Seo H, Bazer FW, Burghardt RC, Johnson GA (2019) Immunohistochemical examination of trophoblast syncytialization during early placentation in sheep. Int J Mol Sci 20:4530–4543

    Article  CAS  PubMed Central  Google Scholar 

  • Seo H, James W, Frank JW, Robert C, Burghardt RC, Fuller W, Bazer FW, Johnson GA (2020) Integrins and OPN localize to adhesion complexes during placentation in sheep. Reproduction 160:521–532

    Article  CAS  PubMed  Google Scholar 

  • Simmons RM, Erikson DW, Kim J, Burghardt RC, Bazer FW, Johnson GA, Spencer TE (2009) Insulin-like growth factor binding protein-1 in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation. Endocrinology 150:4295–4305

    Article  CAS  PubMed  Google Scholar 

  • Skidmore JA, Wooding FBP, Allen WR (1996) Implantation and early placentation in the one-humped camel (Camelus dromedarius). Placenta 17:253–262

    Article  CAS  PubMed  Google Scholar 

  • Spencer TE, Hansen TR (2015) Implantation and establishment of pregnancy in ruminants. Adv Anat Embryol Cell Biol 216:105–135

    Article  PubMed  Google Scholar 

  • Spencer TE, Bartol FF, Bazer FW, Johnson GA, Joyce MM (1999a) Identification and characterization of glycosylation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus. Biol Reprod 60:241–250

    Article  CAS  PubMed  Google Scholar 

  • Spencer TE, Stagg AG, Taylor KM, Johnson GA, Gertler A, Gootwine E, Bazer FW (1999b) Effects of recombinant ovine interferon tau, placental lactogen and growth hormone on ovine endometrial function. Biol Reprod 61:1409–1418

    Article  CAS  PubMed  Google Scholar 

  • Spencer TE, Johnson GA, Bazer FW, Burghardt RC (2004a) Implantation mechanisms: insights from the sheep. Reproduction 128:657–668

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Spencer DS, Ross JW, Ashworth MD, Geisert RD, Rickords LF (2006) Porcine conceptus Oct-4 mRNA expression during peri-implantation development. Reprod Domest Anim 41:571–572

    Article  CAS  PubMed  Google Scholar 

  • Spencer TE, Black SG, Arnaud F, Palmarini M (2010) Endogenous retroviruses of sheep: a model system for understanding physiological adaptation to an evolving ruminant genome. Soc Reprod Fertil Suppl 67:95–104

    CAS  PubMed  Google Scholar 

  • Spencer TE, Forde N, Lonergan P (2016) The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants. J Dairy Sci 99:5941–5950

    Article  CAS  PubMed  Google Scholar 

  • Surveyor GA, Gendler SJ, Pemberton L, Das SK, Chakraborty I, Julian J, Pimental RA, Wegner CC, Dey SK, Carson DD (1995) Expression and steroid hormonal control of Muc-1 in the mouse uterus. Endocrinology 136:3639–3647

    Article  CAS  PubMed  Google Scholar 

  • Telugu BP, Green JA (2007) Comparative placentation. In: Constantinescu G, Schatten H (eds) Veterinary reproductive biology. Chapter 12. Blackwell, Ames, IA

    Google Scholar 

  • Wallace RM, Pohler KG, Smith MF, Green JA (2015) Placental PAGs: gene origins, expression patterns and use as markers of pregnancy. Reproduction 149:R115–R126

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Guillomot M, Hue I (2009) Cellular organization of the trophoblastic epithelium in elongating conceptuses of ruminants. C R Biol 332:986–997. https://doi.org/10.1016/j.crvi.2009.09.004

  • Wango EO, Wooding FBP, Heap RB (1990) The role of trophoblastic cells in implantation in the goat: a quantitative study. Placenta 11:381–394

    Article  CAS  PubMed  Google Scholar 

  • Wathes DC, Wooding FBP (1980) An electron microscopic study of implantation in the cow. Am J Anat 159:285–306

    Article  CAS  PubMed  Google Scholar 

  • Wiley AA, Bartol FF, Barron DH (1987) Histogenesis of the ovine uterus. J Anim Sci 64:1262–1269

    Article  CAS  PubMed  Google Scholar 

  • Wimsatt WA (1974) Some comparative aspects of implantation. Biol Reprod 12:1–40

    Article  Google Scholar 

  • Wooding FBP (1982a) Structure and function of placental binucleate (giant) cells. Bibl Anat 22:134–139

    Google Scholar 

  • Wooding FBP (1982b) The role of binucleate cell in ruminant placental structure. Reprod Fertil Suppl 31:31–39

    CAS  Google Scholar 

  • Wooding FBP (1984) Role of binucleate cells in fetomaternal cell fusion at implantation in the sheep. Am J Anat 170:233–250

    Article  CAS  PubMed  Google Scholar 

  • Wooding FBP (1987) Ultrastructural evidence for placental lactogen transport and secretion in ruminants. J Physiol 386:26

    Google Scholar 

  • Wooding FBP (1992) Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta 13:101–113

    Article  CAS  PubMed  Google Scholar 

  • Wooding FBP, Flint APF (1994) Placentation. In: Lamming GE (ed) Marshall’s physiology of reproduction. Chapman and Hall, London, pp 233–460

    Chapter  Google Scholar 

  • Wooding FBP, Wathes DC (1980) Binucleate cell migration in the bovine placentome. J Reprod Fertil 59:425–430

    Article  CAS  PubMed  Google Scholar 

  • Wooding FBP, Flint APF, Heap RB, Morgan G, Buttle HL, Young IR (1986) Control of binucleate cell migration in the placenta of ruminants. J Reprod Fertil 76:499–512

    Article  CAS  PubMed  Google Scholar 

  • Wooding FB (1992) Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. 13:101–113

    Google Scholar 

  • Wooding FBP, Morgan G, Adam CL (1997) Structure and function in the ruminant synepitheliochorial placenta: central role of the trophoblast binucleate cell in deer. Microsc Res Tech 38:88–99

    Article  CAS  PubMed  Google Scholar 

  • Wooding FBP, Roberts RM, Green JA (2005) Light and electron microscope immunocytochemical studies of the distribution of pregnancy-associated glycoproteins (PAGs) throughout pregnancy in the cow: possible functional implications. Placenta 26:807–827

    Article  CAS  PubMed  Google Scholar 

  • Wrobel K-H, Suess F (1998) Identification and temporospatial distribution of bovine primordial germ cells prior to gonadal sexual differentiation. Anat Embryol 197:451–467

    Article  CAS  Google Scholar 

  • Xie SC, Low BG, Nagel RJ, Kramer KK, Anthony RV, Zoli AP, Beckers JF, Roberts RM (1991) Identification of the major pregnancy-specific antigens of cattle and sheep as inactive members of the aspartic proteinase family. Proc Natl Acad Sci 88:10247–10251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Jiang Z, Bazer FW, Johnson GA, Burghardt RC, Wu G (2015) Aquaporins in the female reproductive system of mammals. Front Biosci 20:838–871

    Article  CAS  Google Scholar 

  • Zoli AP, Guilbault LA, Delahaut P, Ortiz WB, Beckers JF (1992) Radioimmunoassay of a bovine pregnancy-associated glycoprotein in serum: its application for pregnancy diagnosis. Biol Reprod 46:83–92

    Article  CAS  PubMed  Google Scholar 

Download references

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  1. Division of Animal Sciences, College of Agriculture, Food, Natural Resources, S138 Animal Science Research Center, University of Missouri, Columbia, MO, USA

    Jonathan A. Green

  2. Division of Animal Sciences, College of Agriculture, Food, Natural Resources, S121 Animal Science Research Center, University of Missouri, Columbia, MO, USA

    Rodney D. Geisert

  3. Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, USA

    Greg A. Johnson

  4. Division of Animal Sciences, College of Agriculture, Food, Natural Resources, S135 Animal Science Research Center, University of Missouri, Columbia, MO, USA

    Thomas E. Spencer

Authors
  1. Jonathan A. Green
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  2. Rodney D. Geisert
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  3. Greg A. Johnson
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  4. Thomas E. Spencer
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Correspondence to Jonathan A. Green .

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Editors and Affiliations

  1. Division of Animal Sciences, University of Missouri, Columbia, MO, USA

    Rodney D. Geisert

  2. Division of Animal Sciences, University of Missouri, Columbia, MO, USA

    Thomas Spencer

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Green, J.A., Geisert, R.D., Johnson, G.A., Spencer, T.E. (2021). Implantation and Placentation in Ruminants. In: Geisert, R.D., Spencer, T. (eds) Placentation in Mammals. Advances in Anatomy, Embryology and Cell Biology, vol 234. Springer, Cham. https://doi.org/10.1007/978-3-030-77360-1_7

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