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Home / Equine Research Bank / Annu Rev Anim Biosci / The equine endometrial cup reaction: a fetomaternal signal o...
Annual review of animal biosciences2012; 1; 419-442; doi: 10.1146/annurev-animal-031412-103703

The equine endometrial cup reaction: a fetomaternal signal of significance.

Abstract: A remarkable feature of equine pregnancy is the development of the invasive trophoblast of the chorionic girdle and its formation of the gonadotrophin-secreting endometrial cup cells in early gestation. The details of this process have been revealed only slowly over the past century, since the first description of the endometrial cups in 1912. This centennial presents an opportunity to review the characteristics of the cells and molecules involved in this early, critical phase of placentation in the mare. The invasiveness of the chorionic girdle trophoblast appears to represent an atavistic attribute more commonly associated with the hemochorial placentae of primates and rodents but not with the more recently derived epitheliochorial placentae of the odd-toed ungulates. The nature of and raison d'être for the strong fetal signals transmitted to the mare by the endometrial cup reaction, and her responses to these messages, are the subject of the present review.
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Publication Date: 2012-12-13 PubMed ID: 25387026PubMed Central: PMC4641323DOI: 10.1146/annurev-animal-031412-103703Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article details the development and significance of the endometrial cup cells produced during the early stages of equine pregnancy. Key themes discussed include how characteristics of this fetomaternal signaling process have gradually been understood over the past century, and an exploration of the function and influence of these signals on the mare.

Understanding the Endometrial Cup Reaction in Horses

Early in equine gestation, a critical phase of placentation involves the endometrial cup cells. These special cells, which secrete gonadotrophin, have characteristics that are:

  • Formed from the invasive trophoblast of the chorionic girdle
  • Important for fetomaternal signaling
  • Unique to the mare, as compared to other species

These cellular processes have been under investigation since the first description of the endometrial cups in 1912. Over this period, scientists have continuously added to our understanding of the cells and molecules involved in this imperative stage of equine pregnancy.

The Invasive Nature of the Chorionic Girdle Trophoblast

The invasive nature of the chorionic girdle trophoblast is seen as an atavistic characteristic—not typically seen in the newer placentae structures found in odd-toed ungulates, but is associated with the hemochorial placentae of rodents and primates. The researchers:

  • Consider this attribute to be a throwback or reversion to earlier types found in ‘ancient’ species
  • Discuss its unique relevance to the mare and how it differentiates this species from others

Signal Transmission from the Fetus to the Mare

The core aspect covered by the review is the strong fetal signals transmitted to the mother by the endometrial cup reaction. The authors delve into:

  • Understanding the purpose, or raison d’être, for these signals
  • Investigating how the mare responds to these signals
  • The consequences of these responses on both the mother and fetus

By unraveling the nature of these signals and the mare’s responses, the researchers aim to deepen our understanding of equine reproduction and prenatal development. This could potentially provide insights that improve equine breeding practices.

Cite This Article

APA
Antczak DF, de Mestre AM, Wilsher S, Allen WR. (2012). The equine endometrial cup reaction: a fetomaternal signal of significance. Annu Rev Anim Biosci, 1, 419-442. https://doi.org/10.1146/annurev-animal-031412-103703

Publication

Annual review of animal biosciences
ISSN: 2165-8110
NlmUniqueID: 101614024
Country: United States
Language: English
Volume: 1
Pages: 419-442

Researcher Affiliations

Antczak, D F
  • Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853; email: doug.antczak@cornell.edu.
de Mestre, Amanda M
    Wilsher, Sandra
      Allen, W R

        MeSH Terms

        • Animals
        • Chorion
        • Endometrium / physiology
        • Female
        • Horses / physiology
        • Maternal-Fetal Relations / physiology
        • Pregnancy
        • Trophoblasts

        Grant Funding

        • 091581 / Wellcome Trust

        References

        This article includes 108 references
        1. Schauder W. Untersuchungen uber die eithaute und Embryotrophe des pferdes.. Arch. Anat. Physiol. 1912;192:259–302.
        2. Ewart JC. A Critical Period in the Development of the Horse.. 1897; p. 16.
        3. Hamilton DW, Allen WR, Moor RM. The origin of equine endometrial cups. 3. Light and electron microscopic study of fully developed equine endometrial cups.. Anat Rec 1973 Dec;177(4):503-17.
          pubmed: 4762727doi: 10.1002/ar.1091770404google scholar: lookup
        4. Cole HH, Goss H. The source of equine gonadotropin. Essays in Biology in Honor of Herbert M Evans Univ. Calif. Press; Berkeley: 1943; pp. 107–19.
        5. Cole HH, Hart GH. The potency of blood serum of mares in progressive stages of pregnancy in effecting the sexual maturity of the immature rat.. Am. J. Physiol. 1930;93:57–68.
        6. Ascheim S, Zondek B. Das hormone des hypophysenvorderlappens. 1. Testobjekt zum Nachweis des Hormons.. Klin. Wochenschr. 1927;6:248–52.
        7. Cole HH, Saunders FJ. The concentration of gonad-stimulating hormone in blood serum and of estrin in the urine throughout pregnancy in the mare.. Endocrinology 1935;19:199–208.
        8. Cole HH. High gonadotrophic hormone concentration in pregnant ponies.. Proc. Soc. Exp. Biol. Med. 1938;38:193–94.
        9. Evans HM, Gustus EL, Simpson ME. CONCENTRATION OF THE GONADOTROPIC HORMONE IN PREGNANT MARE'S SERUM.. J Exp Med 1933 Oct 31;58(5):569-74.
          pmc: PMC2132317pubmed: 19870216doi: 10.1084/jem.58.5.569google scholar: lookup
        10. Cole HH, Pencharz RI, Goss H. On the biological properties of highly purified gonadotropin from pregnant mare serum.. Endocrinology 1940;27:548–53.
        11. Cole HH. On the biological properties of mare gonadotropic hormone.. Am. J. Anat. 1936;59:299–332.
        12. Cole HH, Hart GH. Concerning gonadotropic substances in mare serum.. Proc. Soc. Exp. Biol. Med. 1934;32:370–73.
        13. Cole HH, Miller RF. Artificial induction of ovulation and oestrum in the ewe during anoestrum.. Am. J. Physiol. 1933;104:165–71.
        14. Catchpole HR, Cole HH, Pearson PB. Studies on the rate of disappearance and fate of mare gonadotrophic hormone following intravenous injection.. Am. J. Physiol. 1935;112:21–26.
        15. Goss H, Cole HH. Further studies on the purification of mare gonadotropic hormone.. Endocrinology 1940;26:244–49.
        16. Goss H, Cole HH. Sex hormones in the blood serum of mares. III. Some chemical properties of the ovary stimulating principle.. Endocrinology 1931;15:214–24.
        17. Saunders FJ, Cole HH. Two gonadotropic substances in mare serum.. Proc. Soc. Exp. Biol. Med. 1935;32:1476–78.
        18. Evans HM, Korpi KJ, Simpson ME, Pencharz RI. Fractionation of gonadotrophic hormones in pregnant mare serum by means of ammonium sulphate.. Univ. Calif. Publ. Anat. 1936;1:275–81.
        19. Saunders FJ, Cole HH. Means of augmenting the ovarian response to gonadotropic substances.. Proc. Soc. Exp. Biol. Med. 1936;33:505–8.
        20. Cole HH, Erway J. 48-hour assay test for equine gonadotropin with results expressed in international units.. Endocrinology 1941;29:514–19.
        21. Catchpole HR, Lyons WR. The gonad-stimulating hormone of pregnant mares.. Am. J. Anat. 1934;55:167–227.
        22. Zondek B. Hormonale Schangerschaftsreaktion aus dem Harn bei Mensch und Tier.. Klin. Wochenschr. 1930;9:2285–89.
        23. Zondek B. Hypophysenvorderlappen.. Arch. Gynaek. 1930;144:133–64.
        24. CLEGG MT, BODA JM, COLE HH. The endometrial cups and allantochorionic pouches in the mare with emphasis on the source of equine gonadotrophin.. Endocrinology 1954 Apr;54(4):448-63.
          pubmed: 13151141doi: 10.1210/endo-54-4-448google scholar: lookup
        25. Aylward F, Ottway CW. The collection and examination of plasma from pregnant mares for gonadotrophic hormone.. J. Comp. Pathol. Theriogenology 1945;55:159–67.
        26. Gustus EL, Meyer EK, Woods OR. Preparation of the gonadotropic hormone of pregnant mare blood.. J. Biol. Chem. 1936;114:59–63.
        27. Cartland GF, Nelson JW. The preparation and purification of extracts containing the gonad-stimulating hormone of pregnant mare serum.. J. Biol. Chem. 1937;119:59–67.
        28. Li CH, Evans HM, Wonder DH. ELECTROPHORETIC HOMOGENEITY OF PREGNANT MARE SERUM GONADOTROPHIN.. J Gen Physiol 1940 Jul 20;23(6):733-9.
          pmc: PMC2237959pubmed: 19873189doi: 10.1085/jgp.23.6.733google scholar: lookup
        29. Rowson LE. The second Hammond Memorial Lecture. The role of reproductive research in animal production.. J Reprod Fertil 1971 Jul;26(1):113-26.
          pubmed: 5091291doi: 10.1530/jrf.0.0260113google scholar: lookup
        30. Schams D, Papkoff H. Chemical and immunochemical studies on pregnant mare serum gonadotropin.. Biochim Biophys Acta 1972 Mar 15;263(1):139-48.
          pubmed: 4622386doi: 10.1016/0005-2795(72)90168-7google scholar: lookup
        31. Stewart F, Allen WR, Moor RM. Pregnant mare serum gonadotrophin: ratio of follicle-stimulating hormone and luteinizing hormone activities measured by radioreceptor assay.. J Endocrinol 1976 Dec;71(3):471-82.
          pubmed: 187709doi: 10.1677/joe.0.0710371google scholar: lookup
        32. van Niekerk CH. The early diagnosis of pregnancy, the development of foetal membranes and nidation in the mare.. J. S. Afr. Vet. Med. Assoc. 1965;36:483–88.
        33. AMOROSO EC. Endocrinology of pregnancy.. Br Med Bull 1955 May;11(2):117-25.
          pubmed: 14378562doi: 10.1093/oxfordjournals.bmb.a069463google scholar: lookup
        34. Allen WR. Equine Gonadotrophins.. PhD thesis. Univ. Camb; Cambridge: 1970.
        35. Allen WR, Moor RM. The origin of the equine endometrial cups. I. Production of PMSG by fetal trophoblast cells.. J Reprod Fertil 1972 May;29(2):313-6.
          pubmed: 5023705doi: 10.1530/jrf.0.0290313google scholar: lookup
        36. Wooding FB, Morgan G, Fowden AL, Allen WR. A structural and immunological study of chorionic gonadotrophin production by equine trophoblast girdle and cup cells.. Placenta 2001 Sep-Oct;22(8-9):749-67.
          pubmed: 11597196doi: 10.1053/plac.2001.0707google scholar: lookup
        37. Allen WR, Hamilton DW, Moor RM. The origin of equine endometrial cups. II. Invasion of the endometrium by trophoblast.. Anat Rec 1973 Dec;177(4):485-501.
          pubmed: 4762726doi: 10.1002/ar.1091770403google scholar: lookup
        38. Allen WR. Immunological aspects of the equine endometrial cup reaction.. Immunobiology of Trophoblast Camb. Univ. Press; Cambridge: 1975; pp. 217–53.
        39. Evans MJ, Irvine CH. Serum concentrations of FSH, LH and progesterone during the oestrous cycle and early pregnancy in the mare.. J Reprod Fertil Suppl 1975 Oct;(23):193-200.
          pubmed: 1060778
        40. Urwin VE, Allen WR. Pituitary and chorionic gonadotrophic control of ovarian function during early pregnancy in equids.. J Reprod Fertil Suppl 1982;32:371-81.
          pubmed: 6820064
        41. AMOROSO EC, HANCOCK JL, ROWLANDS IW. Ovarian activity in the pregnant mare.. Nature 1948 Mar 6;161(4088):355.
          pubmed: 18908583doi: 10.1038/161355a0google scholar: lookup
        42. Cole HH, Howell CE, Hart GH. The changes occurring in the ovary of the mare during pregnancy.. Anat. Rec. 1931;49:199–209.
        43. Squires EL, Ginther OJ. Follicular and luteal development in pregnant mares.. J Reprod Fertil Suppl 1975 Oct;(23):429-33.
          pubmed: 1060820
        44. Lennard SN, Gerstenberg C, Allen WR, Stewart F. Expression of epidermal growth factor and its receptor in equine placental tissues.. J Reprod Fertil 1998 Jan;112(1):49-57.
          pubmed: 9538329doi: 10.1530/jrf.0.1120049google scholar: lookup
        45. Lennard SN, Stewart F, Allen WR. Transforming growth factor beta 1 expression in the endometrium of the mare during placentation.. Mol Reprod Dev 1995 Oct;42(2):131-40.
          pubmed: 8562058doi: 10.1002/mrd.1080420202google scholar: lookup
        46. Thway TM, Clay CM, Maher JK, Reed DK, McDowell KJ, Antczak DF, Eckert RL, Nilson JH, Wolfe MW. Immortalization of equine trophoblast cell lines of chorionic girdle cell lineage by simian virus-40 large T antigen.. J Endocrinol 2001 Oct;171(1):45-55.
          pubmed: 11572789doi: 10.1677/joe.0.1710045google scholar: lookup
        47. Allen WR, Gower S, Wilsher S. Immunohistochemical localization of vascular endothelial growth factor (VEGF) and its two receptors (Flt-I and KDR) in the endometrium and placenta of the mare during the oestrous cycle and pregnancy.. Reprod Domest Anim 2007 Oct;42(5):516-26.
          pubmed: 17845608doi: 10.1111/j.1439-0531.2006.00815.xgoogle scholar: lookup
        48. Stewart F, Lennard SN, Allen WR. Mechanisms controlling formation of the equine chorionic girdle.. Biol. Reprod. Mono. 1995;1:151–59.
        49. Gerstenberg C, Allen WR, Stewart F. Factors controlling epidermal growth factor (EGF) gene expression in the endometrium of the mare.. Mol Reprod Dev 1999 Jul;53(3):255-65.
          pubmed: 10369386doi: 10.1002/(sici)1098-2795(199907)53:3<255::aid-mrd1>3.0.co;2-dgoogle scholar: lookup
        50. de Mestre AM, Miller D, Roberson MS, Liford J, Chizmar LC, McLaughlin KE, Antczak DF. Glial cells missing homologue 1 is induced in differentiating equine chorionic girdle trophoblast cells.. Biol Reprod 2009 Feb;80(2):227-34.
          pmc: PMC2804814pubmed: 18971425doi: 10.1095/biolreprod.108.070920google scholar: lookup
        51. Brosnahan MM, Miller DC, Adams M, Antczak DF. IL-22 is expressed by the invasive trophoblast of the equine (Equus caballus) chorionic girdle.. J Immunol 2012 May 1;188(9):4181-7.
          pmc: PMC3746837pubmed: 22490443doi: 10.4049/jimmunol.1103509google scholar: lookup
        52. Sonnenberg GF, Fouser LA, Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22.. Nat Immunol 2011 May;12(5):383-90.
          pubmed: 21502992doi: 10.1038/ni.2025google scholar: lookup
        53. Wolk K, Witte E, Witte K, Warszawska K, Sabat R. Biology of interleukin-22.. Semin Immunopathol 2010 Mar;32(1):17-31.
          pubmed: 20127093doi: 10.1007/s00281-009-0188-xgoogle scholar: lookup
        54. Grünig G, Triplett L, Canady LK, Allen WR, Antczak DF. The maternal leucocyte response to the endometrial cups in horses is correlated with the developmental stages of the invasive trophoblast cells.. Placenta 1995 Sep;16(6):539-59.
          pubmed: 8570575doi: 10.1016/s0143-4004(05)80005-0google scholar: lookup
        55. Donaldson WL, Oriol JG, Plavin A, Antczak DF. Developmental regulation of class I major histocompatibility complex antigen expression by equine trophoblastic cells.. Differentiation 1992 Dec;52(1):69-78.
          pubmed: 1286777doi: 10.1111/j.1432-0436.1992.tb00501.xgoogle scholar: lookup
        56. Donaldson WL, Zhang CH, Oriol JG, Antczak DF. Invasive equine trophoblast expresses conventional class I major histocompatibility complex antigens.. Development 1990 Sep;110(1):63-71.
          pubmed: 2081471doi: 10.1242/dev.110.1.63google scholar: lookup
        57. Allen WR, Kydd J, Miller J, Antczak DF. Immunological Studies on Feto Maternal Relationships in Equine Pregnancy.. Butterworths; London: 1984.
        58. Crighton DB, editor. Proc. 38th Easter School, Univ. Nottm; London: Butterworths?; pp. 183–93.
        59. Adams AP, Oriol JG, Campbell RE, Oppenheim YC, Allen WR, Antczak DF. The effect of skin allografting on the equine endometrial cup reaction.. Theriogenology 2007 Jul 15;68(2):237-47.
          pmc: PMC2259290pubmed: 17559923doi: 10.1016/j.theriogenology.2007.04.058google scholar: lookup
        60. de Mestre AM, Hanlon D, Adams AP, Runcan E, Leadbeater JC, Erb HN, Costa CC, Miller D, Allen WR, Antczak DF. Functions of ectopically transplanted invasive horse trophoblast.. Reproduction 2011 Jun;141(6):849-56.
          pmc: PMC5181105pubmed: 21389079doi: 10.1530/rep-10-0462google scholar: lookup
        61. Day FT, Rowlands IW. The time and rate of appearance of gonadotrophin in the serum of pregnant mares.. J. Endocrinol. 1940;2:255–61.
        62. Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdale PD, Fowden AL. Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero.. Reproduction 2002 Mar;123(3):445-53.
          pubmed: 11882022
        63. DAY FT, ROWLANDS IW. Serum gonadotrophin in Welsh and Shetland ponies.. J Endocrinol 1947 Feb;5(1):1-8.
          pubmed: 20292724doi: 10.1677/joe.0.0050001google scholar: lookup
        64. Manning AW, Rajkumar K, Bristol F, Flood PF, Murphy BD. Genetic and temporal variation in serum concentrations and biological activity of horse chorionic gonadotrophin.. J Reprod Fertil Suppl 1987;35:389-97.
          pubmed: 3119830
        65. ROWLANDS IW. Serum gonadotrophin and ovarian activity in the pregnant mare.. J Endocrinol 1949 Oct;6(2):184-91.
          pubmed: 15392910doi: 10.1677/joe.0.0060184google scholar: lookup
        66. Bell RJ, Bristol F. Equine chorionic gonadotrophin in mares that conceive at foal oestrus.. J. Reprod. Fertil. Suppl. 1991;44:719–21.
        67. Wilsher S, Allen WR. Factors influencing equine chorionic gonadotrophin production in the mare.. Equine Vet J 2011 Jul;43(4):430-8.
          pubmed: 21496079doi: 10.1111/j.2042-3306.2010.00309.xgoogle scholar: lookup
        68. BIELANSKI W, EWY Z, PIGONIOWA H. [Preliminary comparative investigations on endocrine secretion in mares mated with stallions and donkeys].. Folia Biol (Krakow) 1955;3(1):19-30.
          pubmed: 14391422
        69. CLEGG MT, COLE HH, HOWARD CB, PIGON H. The influence of foetal genotype on equine gonadotrophin secretion.. J Endocrinol 1962 Oct;25:245-8.
          pubmed: 14021662doi: 10.1677/joe.0.0250245google scholar: lookup
        70. Allen WR. Factors influencing pregnant mare serum gonadotrophin production.. Nature 1969 Jul 5;223(5201):64-5.
          pubmed: 5792429doi: 10.1038/223064a0google scholar: lookup
        71. Allen WR. The influence of fetal genotype upon endometrial cup development and PMSG and progestagen production in equids.. J Reprod Fertil Suppl 1975 Oct;(23):405-13.
          pubmed: 1060815
        72. Allen WR, Skidmore JA, Stewart F, Antczak DF. Effects of fetal genotype and uterine environment on placental development in equids.. J Reprod Fertil 1993 May;98(1):55-60.
          pubmed: 8345479doi: 10.1530/jrf.0.0980055google scholar: lookup
        73. Holtan DW, Squires EL, Lapin DR, Ginther OJ. Effect of ovariectomy on pregnancy in mares.. J Reprod Fertil Suppl 1979;(27):457-63.
          pubmed: 289823
        74. Terqui M, Palmer E. Oestrogen pattern during early pregnancy in the mare.. J Reprod Fertil Suppl 1979;(27):441-6.
          pubmed: 289820
        75. Daels PF, DeMoraes JJ, Stabenfeldt GH, Hughes JP, Lasley BL. The corpus luteum: source of oestrogen during early pregnancy in the mare.. J Reprod Fertil Suppl 1991;44:501-8.
          pubmed: 1665517
        76. Haig D. Genetic conflicts in human pregnancy.. Q Rev Biol 1993 Dec;68(4):495-532.
          pubmed: 8115596doi: 10.1086/418300google scholar: lookup
        77. Stewart F, Allen WR, Moor RM. Influence of foetal genotype on the follicle-stimulating hormone:luteinizing hormone ratio of pregnant mare serum gonadotrophin.. J Endocrinol 1977 Jun;73(3):419-25.
          pubmed: 874396doi: 10.1677/joe.0.0730419google scholar: lookup
        78. Stewart F, Allen WR. Biological functions and receptor binding activities of equine chorionic gonadotrophins.. J Reprod Fertil 1981 Jul;62(2):527-36.
          pubmed: 6265633doi: 10.1530/jrf.0.0620527google scholar: lookup
        79. Talmadge K, Boorstein WR, Fiddes JC. The human genome contains seven genes for the beta-subunit of chorionic gonadotropin but only one gene for the beta-subunit of luteinizing hormone.. DNA 1983;2(4):281-9.
          pubmed: 6319099doi: 10.1089/dna.1983.2.281google scholar: lookup
        80. Maston GA, Ruvolo M. Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection.. Mol Biol Evol 2002 Mar;19(3):320-35.
          pubmed: 11861891doi: 10.1093/oxfordjournals.molbev.a004085google scholar: lookup
        81. Policastro PF, Daniels-McQueen S, Carle G, Boime I. A map of the hCG beta-LH beta gene cluster.. J Biol Chem 1986 May 5;261(13):5907-16.
          pubmed: 2422163
        82. Policastro P, Ovitt CE, Hoshina M, Fukuoka H, Boothby MR, Boime I. The beta subunit of human chorionic gonadotropin is encoded by multiple genes.. J Biol Chem 1983 Oct 10;258(19):11492-9.
          pubmed: 6194155
        83. Bousfield GR, Liu WK, Sugino H, Ward DN. Structural studies on equine glycoprotein hormones. Amino acid sequence of equine lutropin beta-subunit.. J Biol Chem 1987 Jun 25;262(18):8610-20.
          pubmed: 3298239
        84. Murphy BD, Martinuk SD. Equine chorionic gonadotropin.. Endocr Rev 1991 Feb;12(1):27-44.
          pubmed: 2026120doi: 10.1210/edrv-12-1-27google scholar: lookup
        85. Galet C, Guillou F, Foulon-Gauze F, Combarnous Y, Chopineau M. The beta104-109 sequence is essential for the secretion of correctly folded single-chain beta alpha horse LH/CG and for its FSH activity.. J Endocrinol 2009 Oct;203(1):167-74.
          pubmed: 19589909doi: 10.1677/joe-09-0141google scholar: lookup
        86. Sherman GB, Wolfe MW, Farmerie TA, Clay CM, Threadgill DS, Sharp DC, Nilson JH. A single gene encodes the beta-subunits of equine luteinizing hormone and chorionic gonadotropin.. Mol Endocrinol 1992 Jun;6(6):951-9.
          pubmed: 1379674doi: 10.1210/mend.6.6.1379674google scholar: lookup
        87. Stewart F, Maher JK. Analysis of horse and donkey gonadotrophin genes using Southern blotting and DNA hybridization techniques.. J Reprod Fertil Suppl 1991;44:19-25.
          pubmed: 1686622
        88. Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R. Evolution of the mammalian placenta revealed by phylogenetic analysis.. Proc Natl Acad Sci U S A 2006 Feb 28;103(9):3203-8.
          pmc: PMC1413940pubmed: 16492730doi: 10.1073/pnas.0511344103google scholar: lookup
        89. Mess A, Carter AM. Evolution of the placenta during the early radiation of placental mammals.. Comp Biochem Physiol A Mol Integr Physiol 2007 Dec;148(4):769-79.
          pubmed: 17347003doi: 10.1016/j.cbpa.2007.01.029google scholar: lookup
        90. Noronha LE, Antczak DF. Maternal immune responses to trophoblast: the contribution of the horse to pregnancy immunology.. Am J Reprod Immunol 2010 Oct;64(4):231-44.
          pubmed: 20618178doi: 10.1111/j.1600-0897.2010.00895.xgoogle scholar: lookup
        91. Antczak DF, Bright SM, Remick LH, Bauman BE. Lymphocyte alloantigens of the horse. I. Serologic and genetic studies.. Tissue Antigens 1982 Sep;20(3):172-87.
          pubmed: 6182639doi: 10.1111/j.1399-0039.1982.tb00343.xgoogle scholar: lookup
        92. Antczak DF, Miller JM, Remick LH. Lymphocyte alloantigens of the horse. II. Antibodies to ELA antigens produced during equine pregnancy.. J Reprod Immunol 1984 Aug;6(5):283-97.
          pubmed: 6481697doi: 10.1016/0165-0378(84)90028-7google scholar: lookup
        93. Donaldson WL, Oriol JG, Pelkaus CL, Antczak DF. Paternal and maternal major histocompatibility complex class I antigens are expressed co-dominantly by equine trophoblast.. Placenta 1994 Feb-Mar;15(2):123-35.
          pubmed: 8008728doi: 10.1016/s0143-4004(05)80449-7google scholar: lookup
        94. Adams AP, Antczak DF. Ectopic transplantation of equine invasive trophoblast.. Biol Reprod 2001 Mar;64(3):753-63.
          pubmed: 11207188doi: 10.1095/biolreprod64.3.753google scholar: lookup
        95. Maher JK, Tresnan DB, Deacon S, Hannah L, Antczak DF. Analysis of MHC class I expression in equine trophoblast cells using in situ hybridization.. Placenta 1996 Jul-Aug;17(5-6):351-9.
          pubmed: 8829219doi: 10.1016/s0143-4004(96)90060-0google scholar: lookup
        96. Antczak DF. T-cell tolerance to the developing equine conceptus.. Reprod Domest Anim 2012 Aug;47 Suppl 4:376-83.
          pubmed: 22827395doi: 10.1111/j.1439-0531.2012.02101.xgoogle scholar: lookup
        97. Madeja Z, Yadi H, Apps R, Boulenouar S, Roper SJ, Gardner L, Moffett A, Colucci F, Hemberger M. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth.. Proc Natl Acad Sci U S A 2011 Mar 8;108(10):4012-7.
          pmc: PMC3053985pubmed: 21300875doi: 10.1073/pnas.1005342108google scholar: lookup
        98. Samstein RM, Josefowicz SZ, Arvey A, Treuting PM, Rudensky AY. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict.. Cell 2012 Jul 6;150(1):29-38.
          pmc: PMC3422629pubmed: 22770213doi: 10.1016/j.cell.2012.05.031google scholar: lookup
        99. Rowe JH, Ertelt JM, Xin L, Way SS. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen.. Nature 2012 Oct 4;490(7418):102-6.
          pmc: PMC3465465pubmed: 23023128doi: 10.1038/nature11462google scholar: lookup
        100. Regateiro FS, Chen Y, Kendal AR, Hilbrands R, Adams E, Cobbold SP, Ma J, Andersen KG, Betz AG, Zhang M, Madhiwalla S, Roberts B, Waldmann H, Nolan KF, Howie D. Foxp3 expression is required for the induction of therapeutic tissue tolerance.. J Immunol 2012 Oct 15;189(8):3947-56.
          pmc: PMC3467196pubmed: 22988034doi: 10.4049/jimmunol.1200449google scholar: lookup
        101. de Mestre A, Noronha L, Wagner B, Antczak DF. Split immunological tolerance to trophoblast.. Int J Dev Biol 2010;54(2-3):445-55.
          pmc: PMC2879498pubmed: 19876828doi: 10.1387/ijdb.082795adgoogle scholar: lookup
        102. Baker JM, Bamford AI, Antczak DF. Modulation of allospecific CTL responses during pregnancy in equids: an immunological barrier to interspecies matings?. J Immunol 1999 Apr 15;162(8):4496-501.
          pubmed: 10201987
        103. Noronha LE, Antczak DF. Modulation of T-cell reactivity during equine pregnancy is antigen independent.. Am J Reprod Immunol 2012 Aug;68(2):107-15.
          pubmed: 22587222doi: 10.1111/j.1600-0897.2012.01154.xgoogle scholar: lookup
        104. Allen WR. Immunological aspects of the endometrial cup reaction and the effect of xenogeneic pregnancy in horses and donkeys.. J Reprod Fertil Suppl 1982 Nov;31:57-94.
          pubmed: 6962845
        105. Allen WR, Kydd JH, Boyle MS, Antczak DF. Extraspecific donkey-in-horse pregnancy as a model of early fetal death.. J Reprod Fertil Suppl 1987;35:197-209.
          pubmed: 3479576
        106. Betteridge KJ. The structure and function of the equine capsule in relation to embryo manipulation and transfer.. Equine Vet. J. Suppl. 1989;8:92–100.
        107. Oriol JG, Sharom FJ, Betteridge KJ. Developmentally regulated changes in the glycoproteins of the equine embryonic capsule.. J Reprod Fertil 1993 Nov;99(2):653-64.
          pubmed: 8107051doi: 10.1530/jrf.0.0990653google scholar: lookup
        108. Wilsher S, Allen WR. The effects of maternal age and parity on placental and fetal development in the mare.. Equine Vet J 2003 Jul;35(5):476-83.
          pubmed: 12875326doi: 10.2746/042516403775600550google scholar: lookup

        Citations

        This article has been cited 14 times.
        1. Diessler ME, Hernández R, Gomez Castro G, Barbeito CG. Decidual cells and decidualization in the carnivoran endotheliochorial placenta. Front Cell Dev Biol 2023;11:1134874.
          doi: 10.3389/fcell.2023.1134874pubmed: 37009475google scholar: lookup
        2. Schuler G, Fürbass R, Klisch K. Placental contribution to the endocrinology of gestation and parturition. Anim Reprod 2018 Jul-Sep;15(Suppl 1):822-842.
          doi: 10.21451/1984-3143-AR2018-0015pubmed: 36249837google scholar: lookup
        3. Shen Y, Ren H, Davshilt T, Tian S, Wang X, Yi M, Ulaangerel T, Li B, Dugarjav M, Bou G. The transcriptome landscapes of allantochorion and vitelline-chorion in equine day 30 conceptus. Front Cell Dev Biol 2022;10:958205.
          doi: 10.3389/fcell.2022.958205pubmed: 35990610google scholar: lookup
        4. Deng L, Han Y, Tang C, Liao Q, Li Z. Label-Free Mass Spectrometry-Based Quantitative Proteomics Analysis of Serum Proteins During Early Pregnancy in Jennies (Equus asinus). Front Vet Sci 2020;7:569587.
          doi: 10.3389/fvets.2020.569587pubmed: 33195553google scholar: lookup
        5. Loux SC, Dini P, El-Sheikh Ali H, Kalbfleisch T, Ball BA. Characterization of the placental transcriptome through mid to late gestation in the mare. PLoS One 2019;14(11):e0224497.
          doi: 10.1371/journal.pone.0224497pubmed: 31725741google scholar: lookup
        6. Aurich J, Köhne M, Wulf M, Nagel C, Beythien E, Gautier C, Zentek J, Aurich C. Effects of dietary L-arginine supplementation to early pregnant mares on conceptus diameter-Preliminary findings. Reprod Domest Anim 2019 May;54(5):772-778.
          doi: 10.1111/rda.13422pubmed: 30809848google scholar: lookup
        7. Read JE, Cabrera-Sharp V, Offord V, Mirczuk SM, Allen SP, Fowkes RC, de Mestre AM. Dynamic changes in gene expression and signalling during trophoblast development in the horse. Reproduction 2018 Oct 1;156(4):313–330.
          doi: 10.1530/REP-18-0270pubmed: 30306765google scholar: lookup
        8. Read JE, Cabrera-Sharp V, Offord V, Mirczuk SM, Allen SP, Fowkes RC, de Mestre AM. Dynamic changes in gene expression and signalling during trophoblast development in the horse. Reproduction 2018 Oct 1;156(4):313-330.
          doi: 10.1530/REP-18-0270pubmed: 29991567google scholar: lookup
        9. Read JE, Cabrera-Sharp V, Kitscha P, Cartwright JE, King PJ, Fowkes RC, de Mestre AM. Glial Cells Missing 1 Regulates Equine Chorionic Gonadotrophin Beta Subunit via Binding to the Proximal Promoter. Front Endocrinol (Lausanne) 2018;9:195.
          doi: 10.3389/fendo.2018.00195pubmed: 29755409google scholar: lookup
        10. Cabrera-Sharp V, Read JE, Richardson S, Kowalski AA, Antczak DF, Cartwright JE, Mukherjee A, de Mestre AM. SMAD1/5 signaling in the early equine placenta regulates trophoblast differentiation and chorionic gonadotropin secretion. Endocrinology 2014 Aug;155(8):3054-64.
          doi: 10.1210/en.2013-2116pubmed: 24848867google scholar: lookup
        11. Wang X, Miller DC, Harman R, Antczak DF, Clark AG. Paternally expressed genes predominate in the placenta. Proc Natl Acad Sci U S A 2013 Jun 25;110(26):10705-10.
          doi: 10.1073/pnas.1308998110pubmed: 23754418google scholar: lookup
        12. Satué K, La Fauci D, Medica P, Damiá Gímenez E, Cravana C, Fazio E. Shifts between pro-inflammatory and anti-inflammatory profiles in pregnant mares: a review of physiological functions. Front Vet Sci 2025;12:1660759.
          doi: 10.3389/fvets.2025.1660759pubmed: 41049139google scholar: lookup
        13. Carter AM. Evolution of Placental Hormones: Implications for Animal Models. Front Endocrinol (Lausanne) 2022;13:891927.
          doi: 10.3389/fendo.2022.891927pubmed: 35692413google scholar: lookup
        14. Kammerer R, Ballesteros A, Bonsor D, Warren J, Williams JM, Moore T, Dveksler G. Equine pregnancy-specific glycoprotein CEACAM49 secreted by endometrial cup cells activates TGFB. Reproduction 2020 Nov;160(5):685-694.
          doi: 10.1530/REP-20-0277pubmed: 33065543google scholar: lookup
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