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Animals : an open access journal from MDPI2024; 14(13); 1882; doi: 10.3390/ani14131882

Early Embryonic Development in Agriculturally Important Species.

Abstract: The fertilization of oocytes ovulated by pigs, sheep, cows, and horses is not considered a limiting factor in successful establishment of pregnancy. Pig, sheep, and cow embryos undergo cleavage to the blastocyst stage, hatch from the zona pellucida, and undergo central-type implantation. Hatched blastocysts of pigs, sheep, and cows transition from tubular to long filamentous forms to establish surface area for exchange of nutrients and gases with the uterus. The equine blastocyst, surrounded by external membranes, does not elongate but migrates throughout the uterine lumen before attaching to the uterine luminal epithelium (LE) to begin implantation. Pregnancy recognition signaling in pigs requires the trophectoderm to express interleukin 1 beta, estrogens, prostaglandin E2, and interferon gamma. Sheep and cow conceptus trophectoderm expresses interferon tau that induces interferon regulatory factor 2 that inhibits transcription of estrogen and oxytocin receptors by uterine epithelia. This prevents oxytocin-induced luteolytic pulses of prostaglandin F2-alpha from regressing the corpora lutea, as well as ensuring the secretion of progesterone required for maintenance of pregnancy. The pregnancy recognition signal produced by equine blastocysts is not known. Implantation in these species requires interactions between extracellular matrix (ECM) proteins and integrins as the conceptus undergoes apposition and firm attachment to the uterine LE. This review provides details with respect to early embryonic development and the transition from spherical to filamentous conceptuses in pigs, sheep, and cows, as well as pre-implantation development of equine blastocysts and implantation of the conceptuses.
Publication Date: 2024-06-26 PubMed ID: 38997994PubMed Central: PMC11240814DOI: 10.3390/ani14131882Google Scholar: Lookup
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  • Review

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 discusses the early embryonic development in certain agriculturally important animals, such as pigs, sheep, cows, and horses. It explains the differences in their development and implantation journeys, as well as the signaling requirements for pregnancy recognition in each species.

Embryonic Development Stages

  • This study highlights that the fertilization of oocytes in pigs, sheep, cows, and horse does not pose any limitation for a successful commencement of pregnancy.
  • The embryos of pigs, sheep, and cows proceed through a process known as cleavage until the stage known as “blastocyst,” where they hatch from their protective membrane called “zona pellucida.”
  • After hatching, these blastocysts morph from a tubular to an elongated filamentous shape. This shape shift is to increase the surface area for better exchange of essential nutrients and gases with the uterus.
  • However, equine (horse) embryos differ. Instead of elongating, the equine blastocyst, surrounded by external membranes, moves within the uterine lumen before attaching to the uterine luminal epithelium (uterine lining) to commence implantation.

Pregnancy Recognition Signaling

  • In pigs, the signal for pregnancy recognition requires the expression of several compounds from the embryo’s outer layer, known as the “trophectoderm.” These compounds include interleukin 1 beta, estrogens, prostaglandin E2, and interferon gamma.
  • Sheep and cow embryos, on the other hand, show a quite different signaling method. Their trophectoderm expresses a protein called interferon tau which, in turn, induces the production of interferon regulatory factor 2. This key player inhibits the transcription of estrogen and oxytocin receptors by uterine epithelia.
  • This inhibition prevents the rise of oxytocin-induced luteolytic bursts of prostaglandin F2-alpha that would otherwise cause the regression of the corpora lutea, a structure pivotal for the secretion of progesterone which is required for the maintenance of the pregnancy.
  • In horses, however, the mechanism for pregnancy recognition signal production is not yet understood.

Implantation Process

  • The implantation process in these species is reliant on interactions between the extracellular matrix proteins and integrins as the embryo, also known as the conceptus, prepares itself for firm attachment to the uterine luminal epithelium.
  • The review provided in the research article throws light on the fascinating early embryonic development journey and the transformation of conceptuses from spherical to filamentous shapes in pigs, sheep, and cows.
  • Additionally, it elucidates the pre-implantation development process of equine blastocysts and the procedure of implantation of the conceptuses.

Cite This Article

APA
Bazer FW, Johnson GA. (2024). Early Embryonic Development in Agriculturally Important Species. Animals (Basel), 14(13), 1882. https://doi.org/10.3390/ani14131882

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 14
Issue: 13
PII: 1882

Researcher Affiliations

Bazer, Fuller W
  • Department of Animal Science, Texas A&M University, College Station, TX 77843-2471, USA.
Johnson, Gregory A
  • Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843-2471, USA.

Grant Funding

  • Research in the laboratories of F.W.B. and G.A. J. has been supported by Agriculture and Food Research Initiative Competitive Grants 2016-67015-24958, 2018-67015-28093, and 2022-67015-36376 to F.W.B. and Grants 2016-67015-24955, 2020-67015-31136, and 2022 / United States Department of Agriculture, National Institute for Food and Agriculture

Conflict of Interest Statement

The authors declare no conflicts of interest.

References

This article includes 248 references
  1. Pohler K.G., Oliveira F.R.V.. Impact of the sire on pregnancy loss.. Vet. Clin. N. Am. Food Anim. Pract. 2024;40:121–129.
    doi: 10.1016/j.cvfa.2023.08.006pubmed: 37884437google scholar: lookup
  2. Bazer F.W., First N.L.. Pregnancy and parturition.. J. Anim. Sci. 1983;57((Suppl. 2)):425–460.
    pubmed: 6352591
  3. Murray F.A., Bazer F.W., Rundell J.W., Vincent C.K., Wallace H.D., Warnick A.C.. Developmental failure of swine embryos restricted to the oviductal environment.. J. Reprod. Fertil. 1971;24:445–448.
    doi: 10.1530/jrf.0.0240445pubmed: 5548637google scholar: lookup
  4. Pope C.E., Day B.N.. Development of pig embryos following restriction to the ampullary portion of the oviduct.. J. Reprod. Fertil. 1972;31:135–138.
    doi: 10.1530/jrf.0.0310135pubmed: 5078107google scholar: lookup
  5. Winterberger-Torres S.. Les rapports entre l’oef en segmentation et le tractus maternal chez la brebis.. Third Int. Congr. Anim. Reprod. Camb. 1956;1:62.
  6. Bazer F.W., Johnson G.A.. Pig blastocyst-uterine interactions.. Differentiation. 2014;87:52–65.
    doi: 10.1016/j.diff.2013.11.005pubmed: 24388881google scholar: lookup
  7. Johnson G.A.. Domestic Animal Placentation.. In: Skinner M.K., editor. Encyclopedia of Reproduction. Volume 2. Academic Press; Cambridge, MA, USA: Elsevier; Amsterdam, The Netherlands: 2018. pp. 448–454.
  8. Organ S.L., Tsao M.S.. An overview of c-MET signaling pathway.. Ther. Adv. Med. Oncol. 2011;3((Suppl. S1)):S7–S19.
    doi: 10.1177/1758834011422556pmc: PMC3225017pubmed: 22128289google scholar: lookup
  9. Chen C., Spencer T.E., Bazer F.W.. Expression of hepatocyte growth factor and its receptor c-met in the ovine uterus.. Biol. Reprod. 2000;62:1844–1850.
    doi: 10.1095/biolreprod62.6.1844pubmed: 10819791google scholar: lookup
  10. Chen C., Spencer T.E., Bazer F.W.. Fibroblast growth factor-10: A stromal mediator of epithelial function in the ovine uterus.. Biol. Reprod. 2000;63:959–966.
    doi: 10.1095/biolreprod63.3.959pubmed: 10952944google scholar: lookup
  11. Ka H., Al-Ramadan S., Erikson D.W., Johnson G.A., Burghardt R.C., Spencer T.E., Jaeger L.A., Bazer F.W.. Regulation of expression of fibroblast growth factor 7 in the pig uterus by progesterone and estradiol.. Biol. Reprod. 2007;77:172–180.
    doi: 10.1095/biolreprod.106.056309pubmed: 17392499google scholar: lookup
  12. Ka H., Spencer T.E., Johnson G.A., Bazer F.W.. Keratinocyte growth factor: Expression by endometrial epithelia of the porcine uterus.. Biol. Reprod. 2000;62:1772–1778.
    doi: 10.1095/biolreprod62.6.1772pubmed: 10819782google scholar: lookup
  13. Bazer F.W., Johnson G.A., Burghardt R.C.. Implantation.. In: Pond W.G., Bell A.W., editors. Encyclopedia of Animal Science. Marcel Dekker, Inc.; New York, NY, USA: 2005. pp. 555–558.
  14. Johnson G.A., Bazer F.W., Burghardt R.C., Wu G., Seo H., Kramer A.C., McLendon B.A.. Cellular events during ovine implantation and impact for gestation.. Anim. Reprod. 2018;15((Suppl. S1)):843–855.
  15. Johnson G.A., Bazer F.W., Seo H.. The Early Stages of Implantation and Placentation in the Pig.. In: Geisert R.D., Spencer T., editors. Placentation in Mammals. Volume 234. Springer; Cham, Switzerland: 2021. pp. 61–89. Advances in Anatomy, Embryology and Cell Biology.
    pubmed: 34694478
  16. Denker H.W.. Implantation: A cell biological paradox.. J. Exp. Zool. 1993;266:541–558.
    doi: 10.1002/jez.1402660606pubmed: 8371097google scholar: lookup
  17. Guillomot M.. Cellular interactions during implantation in domestic ruminants.. J. Reprod. Fertil. Suppl. 1995;49:39–51.
    doi: 10.1530/biosciprocs.3.004pubmed: 7623329google scholar: lookup
  18. Guillomot M., Guay P.. Ultrastructural features of the cell surfaces of uterine and trophoblastic epithelia during embryo attachment in the cow.. Anat. Rec. 1982;204:315–322.
    doi: 10.1002/ar.1092040404pubmed: 7181136google scholar: lookup
  19. Kimber S.J., Illingworth I.M., Glasser S.R.. Expression of carbohydrate antigens in the rat uterus during early pregnancy and after ovariectomy and steroid replacement.. J. Reprod. Fertil. 1995;103:75–87.
    doi: 10.1530/jrf.0.1030075pubmed: 7535850google scholar: lookup
  20. Aplin J.D., Meseguer M., Simon C., Ortiz M.E., Croxatto H., Jones C.J.. MUC1, glycans and the cell-surface barrier to embryo implantation.. Biochem. Soc. Trans. 2001;29:153–156.
    doi: 10.1042/bst0290153pubmed: 11356144google scholar: lookup
  21. Aplin J.D., Kimber S.J.. Trophoblast-uterine interactions at implantation.. Reprod. Biol. Endocrinol. 2004;2:48–60.
    pmc: PMC471567pubmed: 15236654
  22. Burghardt R.C., Johnson G.A., Jaeger L.A., Ka H., Garlow J.E., Spencer T.E., Bazer F.W.. Integrins and extracellular matrix proteins at the maternal/fetal interface in domestic animals.. Cells Tissues Organs. 2002;172:202–217.
    doi: 10.1159/000066969pubmed: 12476049google scholar: lookup
  23. Lessey B.A.. Adhesion molecules and implantation.. J. Reprod. Immunol. 2002;55:101–112.
    doi: 10.1016/S0165-0378(01)00139-5pubmed: 12062825google scholar: lookup
  24. Roberts R.M., Green J.A., Schulz L.C.. The evolution of the placenta.. Reproduction. 2016;152:R179–R189.
    doi: 10.1530/REP-16-0325pmc: PMC5033709pubmed: 27486265google scholar: lookup
  25. Burton G.J., Scioscia M., Rademacher T.W.. Endometrial secretions: Creating a stimulatory microenvironment within the human early placenta and implications for the aetiopathogenesis of preeclampsia.. J. Reprod. Immunol. 2011;89:118–125.
    doi: 10.1016/j.jri.2011.02.005pubmed: 21531028google scholar: lookup
  26. Burton G.J.. Benirschke’s Pathology of the Human Placenta.. Springer; Cham, Switzerland: 2022. Placental types.
  27. Mattson B.A., Overstrom E.W., Albertini D.F.. Transitions in trophectoderm cellular shape and cytoskeletal organization in the elongating pig blastocyst.. Biol. Reprod. 1990;42:195–205.
    doi: 10.1095/biolreprod42.1.195pubmed: 2310817google scholar: lookup
  28. Geisert R.D., Yelich J.V.. Regulation of conceptus development and attachment in pigs.. J. Reprod. Fertil. 1997;52:133–149.
    doi: 10.1530/biosciprocs.15.0010pubmed: 9602725google scholar: lookup
  29. Burghardt R.C., Burghardt J.R., Taylor J.D., Reeder A.T., Nguen B.T., Spencer T.E., Bayless K.J., Johnson G.A.. Enhanced focal adhesion assembly reflects increased mechanosensation and mechanotransduction at the maternal-conceptus interface and uterine wall during ovine pregnancy.. Reproduction. 2009;137:567–582.
    doi: 10.1530/REP-08-0304pubmed: 19060096google scholar: lookup
  30. Geisert R.D., Johnson G.A., Burghardt R.C.. Implantation and establishment of pregnancy in the pig.. In: Geisert R.D., Bazer F.W., editors. Regulation of Implantation and Establishment of Pregnancy in Mammals: Tribute to 45-Year Anniversary of Roger V. Short’s “Maternal Recognition of Pregnancy”. Academic Press; Cambridge, MA, USA: Elsevier; Amsterdam, The Netherlands: 2015. pp. 137–164.
  31. Johnson G.A., Burghardt R.C., Bazer F.W., Seo H., Cain J.W.. Integrins and their potential roles in mammalian pregnancy.. J. Anim. Sci. Biotechnol. 2023;14:115–134.
    doi: 10.1186/s40104-023-00918-0pmc: PMC10486019pubmed: 37679778google scholar: lookup
  32. Steinhauser C.B., Landers M., Myatt L., Burghardt R.C., Vallet J.L., Bazer F.W., Johnson G.A.. Fructose synthesis and transport at the uterine-placental interface of pigs: Cell-specific localization of SLC2A5, SLC2A8, and components of the polyol pathway.. Biol. Reprod. 2016;9:108–121.
    doi: 10.1095/biolreprod.116.142174pubmed: 27535960google scholar: lookup
  33. Seo H., Li X., Wu G., Bazer F.W., Burghardt R.C., Bayless K.J., Johnson G.A.. Mechanotransduction drives morphogenesis to develop folding at the uterine-placental interface of pigs.. Placenta. 2020;90:62–70.
  34. Seo H., Johnson G.A., Bazer F.W., Wu G., McLendon B.A., Kramer A.C.. Cell-specific expression of enzymes required for serine biosynthesis and glutaminolysis in farm animals.. Adv. Exp. Med. Biol. 2021;1285:17–28.
    pubmed: 33770400
  35. Seo H., Kramer A.C., McLendon B.A., Cain J.W., Burghardt R.C., Wu G., Bazer F.W., Johnson G.A.. Elongating porcine conceptuses utilize glutaminolysis as an anaplerotic pathway to maintain the TCA cycle.. Biol. Reprod. 2022;107:823–833.
    doi: 10.1093/biolre/ioac097pubmed: 35552608google scholar: lookup
  36. McLendon B.A., Kramer A.C., Seo H., Burghardt R.C., Bazer F.W., Wu G., Johnson G.A.. Temporal and spatial expression of aquaporins 1, 5, 8, and 9: Potential transport of water across the endometrium and chorioallantois of pigs.. Placenta. 2022;124:28–36.
  37. Johnson G.A., Seo H., Bazer F.W., Wu G., Kramer A.C., McLendon B.A., Cain J.W.. Metabolic pathways utilized by the porcine conceptus, uterus, and placenta.. Mol. Reprod. Dev. 2023;90:673–683.
    doi: 10.1002/mrd.23570pubmed: 35460118google scholar: lookup
  38. Lefevre C.M., Cain J.W., Kramer A.C., Seo H., Lopez A.N., Sah N., Wu G., Bazer F.W., Johnson G.A.. Evidence for metabolism of creatine by the conceptus, placenta, and uterus for production of ATP during conceptus development in pigs.. Biol. Reprod. 2024.
    doi: 10.1093/biolre/ioae088pubmed: 38836439google scholar: lookup
  39. Dantzer V.. Electron microscopy of the initial stages of placentation in the pig.. Anat. Embryol. 1985;172:281–293.
    doi: 10.1007/BF00318976pubmed: 4061869google scholar: lookup
  40. Brayman M., Thathiah A., Carson D.D.. MUC1: A multifunctional cell surface component of reproductive tissue epithelia.. Reprod. Biol. Endocrinol. 2004;2:4–12.
    doi: 10.1186/1477-7827-2-4pmc: PMC320498pubmed: 14711375google scholar: lookup
  41. Geisert R.D., Pratt T.N., Bazer F.W., Mayes J.S., Watson G.H.. Immunocytochemical localization and changes in endometrial progestin receptor protein during the porcine oestrous cycle and early pregnancy.. Reprod. Fertil. Dev. 1994;6:749–760.
    doi: 10.1071/RD9940749pubmed: 7624516google scholar: lookup
  42. Steinhauser C.B., Bazer F.W., Burghardt R.C., Johnson G.A.. Expression of progesterone receptor in the porcine uterus and placenta throughout gestation: Correlation with expression of uteroferrin and osteopontin.. Domest. Anim. Endocrinol. 2017;58:19–29.
  43. Bowen J.A., Bazer F.W., Burghardt R.C.. Spatial and temporal analysis of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo.. Biol. Reprod. 1996;55:1098–1106.
    doi: 10.1095/biolreprod55.5.1098pubmed: 8902223google scholar: lookup
  44. Kimber S.J., Spanswick C.. Blastocyst implantation: The adhesion cascade.. Semin. Cell Dev. Biol. 2000;11:77–92.
    doi: 10.1006/scdb.2000.0154pubmed: 10873705google scholar: lookup
  45. Spencer T.E., Johnson G.A., Bazer F.W., Burghardt R.C.. Implantation mechanisms: Insights from the sheep.. Reproduction. 2004;128:656–668.
    doi: 10.1530/rep.1.00398pubmed: 15579583google scholar: lookup
  46. Johnson G.A., Bazer F.W., Burghardt R.C., Spencer T.E., Wu G., Bayless K.J.. Conceptus-uterus interactions in pigs: Endometrial gene expression in response to estrogens and interferons from conceptuses.. Soc. Reprod. Fertil. Suppl. 2009;66:321–332.
    doi: 10.1530/biosciprocs.18.0037pubmed: 19848299google scholar: lookup
  47. Red-Horse K., Zhou Y., Genbacev O., Prakobphol A., Foulk R., McMaster M., Fisher S.J.. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface.. J. Clin. Investig. 2004;114:744–754.
    doi: 10.1172/JCI200422991pmc: PMC516273pubmed: 15372095google scholar: lookup
  48. Powell J.K., Glasser S.R., Woldesenbet S., Burghardt R.E., Newton G.R.. Expression of carbohydrate antigens in the goat uterus during early pregnancy and on steroid-treated polarized uterine epithelial cells in vitro.. Biol. Reprod. 2000;62:277–284.
    doi: 10.1095/biolreprod62.2.277pubmed: 10642563google scholar: lookup
  49. Spencer T.E., Bartol F.F., Bazer F.W., Johnson G.A., Joyce M.M.. Identification and characterization of glycosylation dependent cell adhesion molecule 1 (GlyCAM-1) expression in the ovine uterus.. Biol. Reprod. 1999;60:241–250.
    doi: 10.1095/biolreprod60.2.241pubmed: 9915987google scholar: lookup
  50. Johnson G.A., Burghardt R.C., Bazer F.W.. Osteopontin: A leading candidate adhesion molecule for implantation in pigs and sheep.. J. Anim. Sci. Biotechnol. 2014;5:56–70.
    doi: 10.1186/2049-1891-5-56pmc: PMC4322467pubmed: 25671104google scholar: lookup
  51. Albelda S.M., Buck C.A.. Integrins and other cell adhesion molecules.. Fed. Am. Soc. Exp. Biol. 1990;4:2868–2880.
    doi: 10.1096/fasebj.4.11.2199285pubmed: 2199285google scholar: lookup
  52. Kling D., Fingerle J., Harlan J.M.. Inhibition of leukocyte extravasation with a monoclonal antibody to CD18 during formation of experimental intimal thickening in rabbit carotid arteries.. Arterioscler. Thromb. 1992;12:997–1007.
    doi: 10.1161/01.ATV.12.9.997pubmed: 1381958google scholar: lookup
  53. Giancotti F.G., Ruoslahti E.. Integrin signaling.. Science. 1999;285:1028–1032.
    doi: 10.1126/science.285.5430.1028pubmed: 10446041google scholar: lookup
  54. Gallant N.D., Michael K.E., García A.J.. Cell adhesion strengthening: Contributions of adhesive area, integrin binding, and focal adhesion assembly.. Mol. Biol. Cell. 2005;16:4329–4340.
    doi: 10.1091/mbc.e05-02-0170pmc: PMC1196341pubmed: 16000373google scholar: lookup
  55. Humphries J.D., Byron A., Humphries M.J.. Integrin ligands at a glance.. J. Cell Sci. 2006;119:3901–3903.
    doi: 10.1242/jcs.03098pmc: PMC3380273pubmed: 16988024google scholar: lookup
  56. Gupta A., Dekaney C.M., Bazer F.W., Madrigal M.M., Jaeger L.A.. Beta transforming growth factors (TGFβs) at the porcine conceptus-maternal interface. Part II: Uterine TGFβ bioactivity and expression of immunoreactive TGFβs (TGFβ1, TGFβ2, and TGFβ3) and their receptors (Type I and Type II). Biol. Reprod. 1998;59:911–917.
    doi: 10.1095/biolreprod59.4.911pubmed: 9746743google scholar: lookup
  57. Geisert R.D., Yelich J.V., Pratt T., Pomp D.. Expression of an inter-α-trypsin inhibitor heavy chain-like protein in the pig endometrium during the oestrous cycle and early pregnancy.. J. Reprod. Fert. 1998;114:35–43.
    doi: 10.1530/jrf.0.1140035pubmed: 9875153google scholar: lookup
  58. Garlow J.E., Ka H., Johnson G.A., Burghardt R.C., Jaeger L.A., Bazer F.W.. Analysis of osteopontin at the maternal-placental interface in pigs.. Biol. Reprod. 2002;66:718–725.
    doi: 10.1095/biolreprod66.3.718pubmed: 11870079google scholar: lookup
  59. White F.J., Ross J.W., Joyce M.M., Geisert R.D., Burghardt R.C., Johnson G.A.. Steroid regulation of cell specific secreted phosphoprotein 1 (osteopontin) expression in the pregnant porcine uterus.. Biol. Reprod. 2005;73:1294–1301.
    doi: 10.1095/biolreprod.105.045153pubmed: 16120824google scholar: lookup
  60. Erikson D.W., Burghardt R.C., Bayless K.J., Johnson G.A.. Secreted phosphoprotein 1 (SPP1, osteopontin) binds to integrin alpha v beta 6 on porcine trophectoderm cells and integrin alpha v beta 3 on uterine luminal epithelial cells and promotes trophectoderm cell adhesion and migration.. Biol. Reprod. 2009;81:814–825.
    doi: 10.1095/biolreprod.109.078600pubmed: 19571258google scholar: lookup
  61. Massuto D.A., Kneese E.C., Johnson G.A., Hooper N.H., Burghardt R.C., Ing N.H., Jaeger L.A.. Transforming growth factor beta (TGFB) signaling is activated during porcine implantation: Proposed role for latency associated peptide-integrins at the conceptus-maternal interface.. Reproduction. 2009;139:465–478.
    doi: 10.1530/REP-09-0447pubmed: 19920116google scholar: lookup
  62. Frank J.W., Seo H., Burghardt R.C., Bayless K.J., Johnson G.A.. ITGAV (Alpha V Integrins) bind SPP1 (osteopontin) to support trophoblast cell adhesion.. Reproduction. 2017;153:695–706.
    doi: 10.1530/REP-17-0043pubmed: 28250242google scholar: lookup
  63. Johnson G.A., Bazer F.W., Jaeger L.A., Ka H., Garlow J.E., Pfarrer C., Spencer T.E., Burghardt R.C.. Muc-1, integrin and osteopontin expression during the implantation cascade in sheep.. Biol. Reprod. 2001;65:820–828.
    doi: 10.1095/biolreprod65.3.820pubmed: 11514347google scholar: lookup
  64. Zaidel-Bar R., Itzkovitz S., Ma’ayan A., Lyengar R., Geiger B.. Functional atlas of the integrin adhesome.. Nat. Cell Biol. 2007;9:858–867.
    doi: 10.1038/ncb0807-858pmc: PMC2735470pubmed: 17671451google scholar: lookup
  65. Ingber D.E.. Tensegrity and mechanotransduction.. J. Body Mov. Ther. 2008;12:198–200.
    doi: 10.1016/j.jbmt.2008.04.038pmc: PMC2614693pubmed: 19083675google scholar: lookup
  66. Riveline D., Zamir E., Balaban N.Q., Schwarz U.S., Ishizaki T., Narumiya S., Kam Z., Geiger B., Bershadsky A.D.. Focal contacts as mechanosensors: Externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism.. J. Cell Biol. 2001;153:1175–1186.
    doi: 10.1083/jcb.153.6.1175pmc: PMC2192034pubmed: 11402062google scholar: lookup
  67. Steven D.H.. Essays in Structure and Function.. Academic Press; London, UK: 1975. Comparative placentation; p. 315.
  68. Burghardt R.C., Bowen J.A., Newton G.R., Bazer F.W.. Extracellular matrix and the implantation cascade in pigs.. J. Reprod. Fertil. Suppl. 1997;52:151–164.
    doi: 10.1530/biosciprocs.15.0011pubmed: 9602726google scholar: lookup
  69. Dunlap K.A., Erikson D.W., Burghardt R.C., White F.J., Reed K.M., Farmer J.L., Spencer T.E., Magness R.R., Bazer F.W., Bayless K.J.. Progesterone and placentation increase secreted phosphoprotein one (SPP1 or osteopontin) in uterine glands and stroma for histotrophic and hematotrophic support of ovine pregnancy.. Biol. Reprod. 2008;79:983–990.
  70. Johnson G.A., Burghardt R.C., Bazer F.W., Spencer T.E.. Minireview: Osteopontin: Roles in implantation and placentation.. Biol. Reprod. 2003;69:1458–1471.
    doi: 10.1095/biolreprod.103.020651pubmed: 12890718google scholar: lookup
  71. Perry J.S., Heap R.B., Burton R.D., Gadsby J.E.. Endocrinology of the blastocyst and its role in the establishment of pregnancy.. J. Reprod. Fertil. Suppl. 1976;25:85–104.
    pubmed: 137974
  72. Fischer H.E., Bazer F.W., Fields M.J.. Steroid metabolism by endometrial and conceptus tissues during early pregnancy and pseudopregnancy in gilts.. J. Reprod. Fertil. 1985;75:69–78.
    doi: 10.1530/jrf.0.0750069pubmed: 4032377google scholar: lookup
  73. Zavy M.T., Bazer F.W., Thatcher W.W., Wilcox C.J.. A study of prostaglandin F2 alpha as the luteolysin in swine: V. Comparison of prostaglandin F, progestins, estrone and estradiol in uterine flushings from pregnant and nonpregnant gilts.. Prostaglandins. 1980;20:837–851.
    doi: 10.1016/0090-6980(80)90137-9pubmed: 7465869google scholar: lookup
  74. Geisert R.D., Renegar R.H., Thatcher W.W., Roberts R.M., Bazer F.W.. Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions.. Biol. Reprod. 1982;27:925–939.
    doi: 10.1095/biolreprod27.4.925pubmed: 6959653google scholar: lookup
  75. Frank M., Bazer F.W., Thatcher W.W., Wilcox C.J.. A study of prostaglandin F2α as the luteolysin in swine: III. Effects of estradiol valerate on prostaglandin F, progestins, estrone and estradiol concentrations in the utero ovarian vein of nonpregnant gilts.. Prostaglandins. 1977;14:1183–1196.
    doi: 10.1016/0090-6980(77)90295-7pubmed: 564076google scholar: lookup
  76. Geisert R.D., Zavy M.T., Wettemann R.P., Biggers B.G.. Length of pseudopregnancy and pattern of uterine protein release as influenced by time and duration of oestrogen administration in the pig.. J. Reprod. Fertil. 1987;79:163–172.
    doi: 10.1530/jrf.0.0790163pubmed: 3820168google scholar: lookup
  77. Geisert R.D., Bazer F.W., Lucas C.G., Pfeiffer C.A., Meyer A.E., Sullivan R., Johns D.N., Sponchiado M., Prather R.S.. Maternal recognition of pregnancy in the pig: A servomechanism involving sex steroids, cytokines and prostaglandins.. Anim. Reprod. Sci. 2024;12:264.
  78. Whyte J.J., Meyer A.E., Spate L.D., Benne J.A., Cecil R., Samuel M.S., Murphy C.N., Prather R.S., Geisert R.D.. Inactivation of porcine interleukin-1β results in failure of rapid conceptus elongation.. Proc. Natl. Acad. Sci. USA. 2018;115:307–312.
    doi: 10.1073/pnas.1718004115pmc: PMC5777074pubmed: 29279391google scholar: lookup
  79. Meyer A.E., Pfeiffer C.A., Brooks K.E., Spate L.D., Benne J.A., Cecil R., Samuel M.S., Murphy C.N., Behura S., McLean M.K.. New perspective on conceptus estrogens in maternal recognition and pregnancy establishment in the pig.. Biol. Reprod. 2019;101:148–161.
    doi: 10.1093/biolre/ioz058pubmed: 31066888google scholar: lookup
  80. Gomes L.C., Sullivan R.M., Pfeiffer C.A., Chen P.R., Kim J., Sponchiado M., Conley A.J., Prather R.S., Wells K.D., Geisert R.D.. Porcine-specific expression of the three functional CYP19 paralogs in early conceptus, placenta, and gonads.. Reproduction. 2023;166:263–269.
    doi: 10.1530/REP-23-0189pubmed: 37490351google scholar: lookup
  81. Bazer F.W., Thatcher W.W.. Theory of maternal recognition in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2α by the uterine endometrium.. Prostaglandins. 1977;14:397–401.
    doi: 10.1016/0090-6980(77)90185-Xpubmed: 897228google scholar: lookup
  82. Ziecik A.J., Waclawik A., Kaczmarek M.M., Blitek A., Jalali B.M., Andronoswka A.. Mechanisms for establishment of pregnancy in the pig.. Reprod. Domest. Anim. 2011;46((Suppl. S3)):31–41.
  83. Sullivan R.M., Lucas C.G., Sponchiado M., Eitel E.K., Spate L.D., Lucy M.C., Smith M.F., Wells K.D., Prather R.S., Geisert R.D.. Conceptus estrogen and prostaglandins provide the maternal recognition of pregnancy signal to prevent luteolysis during early pregnancy in the pig.. Biol. Reprod. 2024:ioae104.
    doi: 10.1093/biolre/ioae104pubmed: 38904948google scholar: lookup
  84. Seo H., Choi Y., Shim J., Yoo I., Ka H.. Prostaglandin transporters ABCC4 and SLCO2A1 in the uterine endometrium and conceptus during pregnancy in pigs.. Biol. Reprod. 2014;90:100.
    doi: 10.1095/biolreprod.113.114934pubmed: 24695625google scholar: lookup
  85. Russel F.G., Koenderink J.B., Masereeuw R.. Multidrug resistance protein 4 (MRP4/ABCC4): A versatile efflux transporter for drugs and signaling molecules.. Trends Pharmacol. Sci. 2008;29:200–207.
    doi: 10.1016/j.tips.2008.01.006pubmed: 18353444google scholar: lookup
  86. Lin Z.P., Zhu Y.L., Johnson D.R., Rice K.P., Nottoli T., Haines B.C., McGrath J., Waxman S.G., Sortorelli A.C.. Disruption of cAMP and prostaglandin E2 transport by multidrug resistance protein 4 deficiency alters cAMP-mediated signaling and nociceptive response.. Mol. Pharmacol. 2008;73:243–251.
    doi: 10.1124/mol.107.039594pmc: PMC2780335pubmed: 17959714google scholar: lookup
  87. Rius M., Thon W.F., Keppler D., Nies A.T.. Prostanoid transport by multidrug resistance protein 4 (MRP4/ABCC4) localized in tissues of the human urogenital tract.. J. Urol. 2005;174:2409–2414.
  88. Mirando M.A., Harney J.P., Beers S., Pontzer C.H., Torres B.A., Johnson H.M., Bazer F.W.. Onset of secretion of proteins with antiviral activity by pig conceptuses.. J. Reprod. Fertil. 1990;88:197–203.
    doi: 10.1530/jrf.0.0880197pubmed: 2313636google scholar: lookup
  89. La Bonnardiere C., Martinat-Botte F., Terqui M., Lefevre F., Zouari K., Martal J., Bazer F.W.. Production of two species of interferons by Large White and Meishan pig conceptuses during the peri-attachment period.. J. Reprod. Fertil. 1991;91:469–478.
    doi: 10.1530/jrf.0.0910469pubmed: 1707458google scholar: lookup
  90. La Bonnardiere C.. Nature and possible functions of interferons secreted by the preimplantation pig blastocyst.. J. Reprod. Fertil. Suppl. 1993;48:157–170.
    pubmed: 7511690
  91. Harney J.P., Bazer F.W.. Effect of porcine conceptus secretory proteins on interestrous interval and uterine secretion of prostaglandins.. Biol. Reprod. 1989;41:277–284.
    doi: 10.1095/biolreprod41.2.277pubmed: 2804221google scholar: lookup
  92. McLendon B.A., Seo H., Kramer A.C., Burghardt R.C., Bazer F.W., Johnson G.A.. Pig conceptuses secrete interferon gamma to recruit T cells to the endometrium during the peri-implantation period.. Biol. Reprod. 2020;103:1018–1029.
    doi: 10.1093/biolre/ioaa132pubmed: 32716497google scholar: lookup
  93. Cain J.W., Seo H., Bumgardner K., Lefevre C., Burghardt R.C., Bazer F.W., Johnson G.A.. Pig conceptuses release extracelluar vesicles containing IFNG for paracrine communication with the endometrium.. Biol. Reprod. 2024;19:ioae044.
    doi: 10.1093/biolre/ioae044pubmed: 38501810google scholar: lookup
  94. D’Andrea S., Chousterman S., Flechon J.E., La Bonnardiere C.. Paracrine activities of porcine trophoblastic interferons.. J. Reprod. Fertil. 1994;102:185–194.
    doi: 10.1530/jrf.0.1020185pubmed: 7799312google scholar: lookup
  95. D’Andrea S., La Bonnardiere C.. Cloning of the porcine interferon-gamma receptor and its foeto-endometrial expression in early pregnancy.. Mol. Reprod. Dev. 1998;51:225–234.
  96. Farrar M.A., Schreiber R.D.. The molecular cell biology of interferon-gamma and its receptor.. Annu. Rev. Immunol. 1993;11:571–611.
  97. Joyce M.M., Burghardt R.C., Geisert R.D., Burghardt J.R., Hooper R.N., Ross J.W., Ashworth M.D., Johnson G.A.. Pig conceptuses secrete estrogen and interferons to differentially regulate uterine STAT1 in a temporal and cell type-specific manner.. Endocrinology. 2007;148:4420–4431.
    doi: 10.1210/en.2007-0505pubmed: 17525118google scholar: lookup
  98. Joyce M.M., Burghardt J.R., Burghardt R.C., Hooper R.N., Bazer F.W., Johnson G.A.. Pig conceptuses increase uterine interferon regulatory factor 1 (IRF1), but restrict expression to stroma through estrogen-induced IRF2 in luminal epithelium.. Biol. Reprod. 2008;77:292–302.
    doi: 10.1095/biolreprod.107.060939pubmed: 17475929google scholar: lookup
  99. Joyce M.M., Burghardt J.R., Burghardt R.C., Hooper R.N., Bazer F.W., Johnson G.A.. Uterine MHC class I molecules and beta 2-microglobulin are regulated by progesterone and conceptus interferons during pig pregnancy.. J. Immunol. 2008;181:2494–2505.
    doi: 10.4049/jimmunol.181.4.2494pubmed: 18684940google scholar: lookup
  100. Yoo I., Kim D., Han J., Lee S., Hong M., Jeon B.Y., Kim J.M., Ka H.. Transcriptomic analysis of interferon-γ-regulated genes in endometrial explants and their possible role in regulating maternal endometrial immunity during the implantation period in pigs, a true epitheliochorial placentation species.. Theriogenology. 2020;155:114–124.
  101. Yoo I., Kye Y.C., Han J., Kim M., Lee S., Jung W., Hong M., Park T.S., Yun C.-H., Ka H.. Uterine epithelial expression of the tumor necrosis factor superfamily: A strategy for immune privilege during pregnancy in a true epitheliochorial placentation species.. Biol. Reprod. 2020;102:828–842.
    doi: 10.1093/biolre/ioz233pubmed: 31901087google scholar: lookup
  102. Johns D.N., Lucas C.G., Pfeiffer C.A., Chen P.R., Meyer A.E., Pery S.D., Spate L.D., Cecil R.F., Fudge M.A., Samuel M.S.. Conceptus interferon gamma is essential for establishment of pregnancy in the pig.. Biol. Reprod. 2021;105:1577–1590.
    doi: 10.1093/biolre/ioab186pubmed: 34608481google scholar: lookup
  103. Bailey D.W., Dunlap K.L., Erikson D.W., Patel A., Bazer F.W., Burghardt R.C., Johnson G.A.. Effects of long-term progesterone exposure on porcine uterine gene expression: Progesterone alone does not induce secreted phosphoprotein 1 (osteopontin) in glandular epithelium.. Reproduction. 2010;140:595–604.
    doi: 10.1530/REP-10-0169pubmed: 20705772google scholar: lookup
  104. Bazer F.W.. Contributions of an animal scientist to reproductive biology.. Biol. Reprod. 2011;85:228–242.
    doi: 10.1095/biolreprod.111.091454pubmed: 21565996google scholar: lookup
  105. Bartol F.F., Wiley A.A., Bagnell C.A.. Uterine development and endometrial programming.. Soc. Reprod. Fertil. Suppl. 2006;62:113–130.
    pubmed: 16866313
  106. Spencer T.E., Bazer F.W.. Conceptus signals for establishment and maintenance of pregnancy.. Reprod. Biol. Endocrinol. 2004;2:49.
    pmc: PMC471568pubmed: 15236653
  107. Bazer F.W., Song G., Kim J., Dunlap K.A., Satterfield M.C., Johnson G.A., Burghardt R.C., Wu G.. Uterine biology in pigs and sheep.. J. Anim. Sci. Biotechnol. 2012;3:23.
    doi: 10.1186/2049-1891-3-23pmc: PMC3436697pubmed: 22958877google scholar: lookup
  108. Gao H., Wu G., Spencer T.E., Johnson G.A., Bazer F.W.. Select nutrients in the ovine uterine lumen: VI. Expression of FK506-binding protein 12-rapamycin complex-associated protein 1 (FRAP1) and regulators and effectors of mTORC1 and mTORC2 complexes in ovine uteri and conceptuses.. Biol. Reprod. 2009;81:87–100.
    doi: 10.1095/biolreprod.109.076257pubmed: 19299312google scholar: lookup
  109. Kim J., Burghardt R.C., Wu G., Johnson G.A., Spencer T.E., Bazer F.W.. Select Nutrients in the ovine uterine lumen: VIII. Arginine stimulates proliferation of ovine trophectoderm cells through mTOR-RPS6K-RPS6 signaling cascade and synthesis of nitric oxide and polyamines.. Biol. Reprod. 2011;84:62–69.
    doi: 10.1095/biolreprod.110.085738pubmed: 20844281google scholar: lookup
  110. Spencer T.E., Johnson G.A., Bazer F.W., Burghardt R.C., Palmarini M.. Pregnancy recognition and conceptus implantation in domestic ruminants: Roles of progesterone, interferons and endogenous retroviruses.. Reprod. Fertil. Dev. 2007;19:65–78.
    doi: 10.1071/RD06102pubmed: 17389136google scholar: lookup
  111. Joyce M.M., White F.J., Burghardt R.C., Muniz J.J., Spencer T.E., Bazer F.W., Johnson G.A.. Interferon stimulated gene 15 conjugates to endometrial cytosolic proteins and is expressed at the uterine-placental interface throughout pregnancy in sheep.. Endocrinology. 2005;146:675–684.
    doi: 10.1210/en.2004-1224pubmed: 15528302google scholar: lookup
  112. Johnson G.A., Stewart M.D., Gray C.A., Choi Y., Burghardt R.C., Yu-Lee L.Y., Bazer F.W., Spencer T.E.. Effects of the estrous cycle, pregnancy, and interferon tau on 2′,5′-oligoadenylate synthetase expression in the ovine uterus.. Biol. Reprod. 2001;64:1392–1399.
    doi: 10.1095/biolreprod64.5.1392pubmed: 11319143google scholar: lookup
  113. Hansen T.R., Sinedino L.D.P., Spencer T.E.. Paracrine and endocrine actions of interferon tau (IFNT). Reproduction. 2017;154:F45–F59.
    doi: 10.1530/REP-17-0315pubmed: 28982937google scholar: lookup
  114. Johnson G.A., Spencer T.E., Hansen T.R., Austin K.J., Burghardt R.C., Bazer F.W.. Expression of the interferon inducible ubiquitin cross-reactive protein in the ovine uterus.. Biol. Reprod. 1999;61:312–318.
    doi: 10.1095/biolreprod61.1.312pubmed: 10377064google scholar: lookup
  115. Choi Y., Johnson G.A., Burghardt R.C., Berghman L.R., Joyce M.M., Taylor K.M., Stewart M.D., Bazer F.W., Spencer T.E.. Interferon regulatory factor two restricts expression of interferon-stimulated genes to the endometrial stroma and glandular epithelium of the ovine uterus.. Biol. Reprod. 2001;65:1038–1049.
    doi: 10.1095/biolreprod65.4.1038pubmed: 11566724google scholar: lookup
  116. Taniguchi T., Ogasawara K., Takaoka A., Tanaka N.. IRF family of transcription factors as regulators of host defense.. Annu. Rev. Immunol. 2001;19:623–655.
  117. Arosh J.A., Banu S.K., McCracken J.A.. Novel concepts on the role of prostaglandins on luteal maintenance and maternal recognition and establishment of pregnancy in ruminants.. J. Dairy Sci. 2016;99:5926–5940.
    doi: 10.3168/jds.2015-10335pubmed: 27179861google scholar: lookup
  118. Loeb K.R., Haas A.L.. The interferon-inducible-15-kDa-ubiquitin homolog conjugates to intracellular proteins.. Biol. Chem. 1992;267:7806–7813.
    doi: 10.1016/S0021-9258(18)42585-9pubmed: 1373138google scholar: lookup
  119. Wilkinson K.D., Gan-Erdene T., Kolli N.. Derivitization of the C-terminus of ubiquitin and ubiquitin-like proteins using intein chemistry: Methods and uses.. Methods Enzymol. 2005;399:37–51.
    pubmed: 16338347
  120. Kim J., Erikson D.W., Burghardt R.C., Spencer T.E., Wu G., Bayless K.J., Johnson G.A., Bazer F.W.. 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. 2010;29:369–382.
    doi: 10.1016/j.matbio.2010.04.001pubmed: 20385232google scholar: lookup
  121. Kim J., Burghardt R.C., Wu G., Johnson G.A., Spencer T.E., Bazer F.W.. Select nutrients in the ovine uterine lumen: VII. Effects of arginine, leucine, glutamine and glucose on trophectodem cell signaling, proliferation and migration.. Biol. Reprod. 2011;84:70–78.
    doi: 10.1095/biolreprod.110.085753pubmed: 20844282google scholar: lookup
  122. Kim J., Burghardt R.C., Wu G., Johnson G.A., Spencer T.E., Bazer F.W.. Select nutrients in the ovine uterine lumen: IX. Differential effects of arginine, leucine, glutamine and glucose on interferon tau, orinithine decarboxylase and nitric oxide synthase in the ovine conceptus.. Biol. Reprod. 2011;84:1139–1147.
    doi: 10.1095/biolreprod.110.088153pubmed: 21293034google scholar: lookup
  123. Wu G., Bazer F.W., Johnson G.A., Herring C., Seo H., Dai Z., Wang J., Wu Z., Wang X.. Functional amino acids in development of the pig placenta.. Mol. Reprod. Dev. 2017;84:870–882.
    doi: 10.1002/mrd.22809pubmed: 28390193google scholar: lookup
  124. Wu G., Bazer F.W., Satterfield M.C., Li X., Wang X., Johnson G.A., Burghardt R.C., Dai Z., Wang J., Wu Z.. Impacts of arginine nutrition on embryonic and fetal development in mammals.. Amino Acids. 2013;45:241–256.
    doi: 10.1007/s00726-013-1515-zpubmed: 23732998google scholar: lookup
  125. Gao H., Wu G., Spencer T.E., Johnson G.A., Bazer F.W.. Select nutrients in the ovine uterine lumen: II. Glucose transporters in the uterus and peri-implantation conceptuses.. Biol. Reprod. 2009;80:94–104.
    doi: 10.1095/biolreprod.108.071654pubmed: 18753604google scholar: lookup
  126. Moses R.M., Halloran K.M., Stenhouse C., Sah N., Kramer A.C., McLendon B.A., Seo H., Johnson G.A., Wu G., Bazer F.W.. Ovine conceptus tissue metabolizes fructose for metabolic support during the peri-implantation period of pregnancy.. Biol. Reprod. 2022;107:1084–1096.
    doi: 10.1093/biolre/ioac144pubmed: 35835585google scholar: lookup
  127. Wang X., Li D., Wu G., Bazer F.W.. Functional roles of fructose: Crosstalk between O-linked glycosylation and phosphorylation of Akt-TSC2-MTOR cell signaling cascade.. Biol. Reprod. 2016;102:102.
    doi: 10.1095/biolreprod.116.142281pubmed: 27655785google scholar: lookup
  128. Bazer F.W., Kim J., Ka H., Johnson G.A., Wu G., Song G.. Select nutrients in the uterine lumen of sheep and pigs affect conceptus development.. J. Reprod. Dev. 2012;58:180–188.
    doi: 10.1262/jrd.2011-019pubmed: 22738901google scholar: lookup
  129. Gray C.A., Burghardt R.C., Johnson G.A., Bazer F.W., Spencer T.E.. Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation.. Reproduction. 2002;124:289–300.
    doi: 10.1530/rep.0.1240289pubmed: 12141942google scholar: lookup
  130. Gao H., Wu G., Spencer T.E., Johnson G.A., Bazer F.W.. Select nutrients in the ovine uterine lumen. I. Amino acids, glucose, and ions in uterine lumenal flushings of cyclic and pregnant ewes.. Biol. Reprod. 2009;80:86–93.
    doi: 10.1095/biolreprod.108.071597pubmed: 18753605google scholar: lookup
  131. Gao H., Wu G., Spencer T.E., Johnson G.A., Bazer F.W.. Select nutrients in the ovine uterine lumen. III. Cationic amino acid transporters in the ovine uterus and peri-implantation conceptuses.. Biol. Reprod. 2009;80:602–609.
    doi: 10.1095/biolreprod.108.073890pubmed: 19038856google scholar: lookup
  132. Kramer A.C., Steinhauser C.B., Gao H., Seo H., McLendon B.A., Burghardt R.C., Wu G., Bazer F.W., Johnson G.A.. Steroids regulate expression of SLC2A1 and SLC2A3 to deliver glucose into trophectoderm for metabolism via glycolysis.. Endocrinology. 2020;161:bqaa098.
    doi: 10.1210/endocr/bqaa098pubmed: 32556218google scholar: lookup
  133. Halloran K.M., Hoskins E.C., Stenhouse C., Moses R.M., Dunlap K.A., Satterfield C.A., Johnson G.A., Wu G., Bazer F.W.. Exogenous progesterone administered to sheep during the pre-implantation period of pregnancy affects composition of maternal, fetal, and placental fluids. II. Amino acids and polyamines.. J. Anim. Sci. Biotechnol. 2021;12:46.
    doi: 10.1186/s40104-021-00567-1pmc: PMC8028684pubmed: 33827696google scholar: lookup
  134. Halloran K.M., Stenhouse C., Moses R.M., Sah N., Seo H., Burghardt R.C., Johnson G.A., Wu G., Bazer F.W.. The ovine conceptus utilizes extracellular serine, glucose, and fructose to generate formate via the one carbon metabolism pathway.. Amino Acids. 2023;55:125–137.
    doi: 10.1007/s00726-022-03212-xpubmed: 36383272google scholar: lookup
  135. Bazer F.W., Wu G., Johnson G.A., Kim J., Song G.. Uterine histotroph and conceptus development: Select nutrients and secreted phosphoprotein 1 affect mechanistic target of rapamycin cell signaling in ewes.. Biol. Reprod. 2011;85:1094–1107.
    doi: 10.1095/biolreprod.111.094722pubmed: 21865556google scholar: lookup
  136. Stenhouse C., Halloran K.M., Newton M.G., Gaddy D., Suva L.J., Bazer F.W.. Novel mineral regulatory pathways in ovine pregnancy: I. Phosphate, klotho signaling, and sodium-dependent phosphate transporters.. Biol. Reprod. 2021;104:1084–1096.
    doi: 10.1093/biolre/ioab028pubmed: 33624764google scholar: lookup
  137. Stenhouse C., Newton M.G., Halloran K.M., Moses R.M., Sah N., Suva L.J., Bazer F.W.. Phosphate, calcium, and vitamin D signaling, transport, and metabolism in the endometria of cyclic ewes.. J. Anim. Sci. Biotechnol. 2023;14:13.
    doi: 10.1186/s40104-022-00803-2pmc: PMC9835233pubmed: 36631878google scholar: lookup
  138. Sah N., Stenhouse C., Halloran K.M., Moses R.M., Seo H., Burghardt R.C., Johnson G.A., Wu G., Bazer F.W.. Creatine metabolism at the uterine-conceptus interface during early gestation in sheep.. Biol. Reprod. 2022;107:1528–1539.
    doi: 10.1093/biolre/ioac171pubmed: 36054379google scholar: lookup
  139. Wood I.S., Trayhurn P.. Glucose transporters (GLUT and SGLT): Expanded families of sugar transport proteins.. Br. J. Nutr. 2003;89:3–9.
    doi: 10.1079/BJN2002763pubmed: 12568659google scholar: lookup
  140. DeBosch B.J., Chen Z., Saben J.L., Finck B.N., Moley K.H.. Glucose transporter 8 (GLUT8) mediates fructose-induced de novo lipogenesis and macrosteatosis.. J. Biol. Chem. 2014;289:10989–10998.
    doi: 10.1074/jbc.M113.527002pmc: PMC4036240pubmed: 24519932google scholar: lookup
  141. DeBosch B.J., Chi M., Moley K.H.. Glucose transporter 8 (GLUT8) regulates enterocyte fructose transport and global mammalian fructose utilization.. Endocrinology. 2012;153:4181–4191.
    doi: 10.1210/en.2012-1541pmc: PMC3423610pubmed: 22822162google scholar: lookup
  142. Limesand S.W., Regnault T.R.H., Hay W.W., Jr.. Characterization of glucose transporter 8 GLUT8) in the ovine placenta of normal and growth restricted fetuses.. Placenta. 2004;25:70–77.
  143. Guillomot M., Flechon J.E., Wintenberger-Torres S.. Conceptus attachment in the ewe: An ultrastructural study.. Placenta. 1981;2:169–182.
    doi: 10.1016/S0143-4004(81)80021-5pubmed: 7232339google scholar: lookup
  144. Wooding F.B., Flint A.P., Heap R.B., Morgan G., Buttle H.L., Young I.R.. Control of binucleate cell migration in the placenta of sheep and goats.. J. Reprod. Fertil. 1986;76:499–512.
    doi: 10.1530/jrf.0.0760499pubmed: 3486281google scholar: lookup
  145. Wooding F.B.P.. The ruminant placental trophoblast binucleate cell: An evolutionary breakthrough.. Biol. Reprod. 2022;107:705–716.
    doi: 10.1093/biolre/ioac107pmc: PMC9476219pubmed: 35594454google scholar: lookup
  146. Seo H., Bazer F.W., Burghardt R.C., Johnson G.A.. Immunohistochemical examination of trophoblast syncytialization during early placentation in sheep.. Int. J. Mol. Sci. 2019;20:4530.
    doi: 10.3390/ijms20184530pmc: PMC6769582pubmed: 31540219google scholar: lookup
  147. Seo H., Bazer F.W., Johnson G.A.. Early syncytialization of the ovine placenta revisited.. Results Probl. Cell Differ. 2024;71:127–142.
    pubmed: 37996676
  148. Seo H., Frank J.W., Burghardt R.C., Bazer F.W., Johnson G.A.. Integrins and OPN localize to adhesion complexes during placentation in sheep.. Reproduction. 2020;160:521–532.
    doi: 10.1530/REP-20-0273pubmed: 32668403google scholar: lookup
  149. Seo H., Melo G.D., Oliveira R.V., Franco-Johannsen F.A., Bazer F.W., Pohler K.G., Johnson G.A.. Immunohistochemical examination of the utero-placental interface of cows on days 21, 31, 40, and 67 of gestation.. Reproduction. 2024;167:e230444.
    pmc: PMC10895283pubmed: 38112573
  150. Johnson G.A., Bazer F.W., Seo H., Burghardt R.C., Wu G., Pohler K.G., Cain J.W.. Understanding placentation in ruminants: A review focusing on cows and sheep.. Reprod. Fertil. Develop. 2023;36:93–111.
    doi: 10.1071/RD23119pubmed: 38064193google scholar: lookup
  151. Johnson G.A., Burghardt R.C., Spencer T.E., Newton G.R., Ott T.L., Bazer F.W.. Ovine Osteopontin: II. Osteopontin and αv,β3 integrin expression in the uterus and conceptus during the peri-implantation period.. Biol. Reprod. 1999;61:892–899.
    doi: 10.1095/biolreprod61.4.892pubmed: 10491621google scholar: lookup
  152. Muñiz J.J., Joyce M.M., Taylor J.D., Burghardt J.R., Burghardt R.C., Johnson G.A.. Glycosylation dependent cell adhesion molecule 1 (GlyCAM-1)-like protein and L-selectin expression in sheep interplacentomal and placentomal endometrium.. Reproduction. 2006;131:751–761.
    doi: 10.1530/rep.1.00855pubmed: 16595726google scholar: lookup
  153. Gray C.A., Adelson D.L., Bazer F.W., Burghardt R.C., Meeusen E.N., Spencer T.E.. Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm.. Proc. Natl. Acad. Sci. USA. 2004;101:7982–7987.
    doi: 10.1073/pnas.0402669101pmc: PMC419543pubmed: 15148380google scholar: lookup
  154. Johnson G.A., Spencer T.E., Burghardt R.C., Taylor K.M., Gray C.A., Bazer F.W.. Progesterone modulation of osteopontin gene expression in the ovine uterus.. Biol. Reprod. 2000;62:1315–1321.
    doi: 10.1095/biolreprod62.5.1315pubmed: 10775182google scholar: lookup
  155. Frank J.W., Steinhauser C.B., Wang X., Bughardt R.C., Bazer F.W., Johnson G.A.. Loss of ITGB3 in ovine conceptuses decreases conceptus expression of NOS3 and SPP1: Implications for the developing placental vasculature.. Biol. Reprod. 2021;104:657–668.
    doi: 10.1093/biolre/ioaa212pubmed: 33232974google scholar: lookup
  156. Wang X., Johnson G.A., Burghardt R.C., Wu G., Bazer F.W.. Uterine histotroph and conceptus development. II. Arginine and secreted phosphoprotein 1 cooperatively stimulate migration and adhesion of ovine trophectoderm cells via focal adhesion-MTORC2 mediated cytoskeleton reorganization.. Biol. Reprod. 2016;95:71.
    doi: 10.1095/biolreprod.115.137943pubmed: 27512152google scholar: lookup
  157. Satterfield M.C., Bazer F.W., Spencer T.E.. Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus.. Biol. Reprod. 2006;75:289–296.
    doi: 10.1095/biolreprod.106.052944pubmed: 16707766google scholar: lookup
  158. Hoskins E.C., Halloran K.M., Stenhouse C., Moses R.M., Dunlap K.A., Satterfield M.C., Seo H., Johnson G.A., Wu G., Bazer F.W.. Pre-implantation exogenous progesterone and pregnancy in sheep: I. Polyamines, nutrient transport, and progestamedins.. J. Anim. Sci. Biotechnol. 2021;12:39.
    doi: 10.1186/s40104-021-00554-6pmc: PMC7934464pubmed: 33663606google scholar: lookup
  159. Satterfield M.C., Hayashi K., Song G., Black S.G., Bazer F.W., Spencer T.E.. Progesterone regulates FGF10, MET, IGFBP1, and IGFBP3 in the endometrium of the ovine uterus.. Biol. Reprod. 2008;79:1226–1236.
    doi: 10.1095/biolreprod.108.071787pubmed: 18753603google scholar: lookup
  160. Satterfield M.C., Gao H., Li X., Wu G., Johnson G.A., Spencer T.E., Bazer F.W.. Select nutrients and their associated transporters are increased in the ovine uterus following early progesterone administration.. Biol. Reprod. 2010;82:224–231.
    doi: 10.1095/biolreprod.109.076729pubmed: 19696016google scholar: lookup
  161. Satterfield M.C., Song G., Hayashi K., Bazer F.W., Spencer T.E.. Progesterone regulation of the endometrial WNT system in the ovine uterus.. Reprod. Fertil. Dev. 2008;20:935–946.
    doi: 10.1071/RD08069pubmed: 19007558google scholar: lookup
  162. Satterfield M.C., Dunlap K.A., Hayashi K., Burghardt R.C., Spencer T.E., Bazer F.W.. Tight and adherens junctions in the ovine uterus: Differential regulation by pregnancy, progesterone, and interferon tau.. Endocrinology. 2007;148:3922–3931.
    doi: 10.1210/en.2007-0321pubmed: 17478549google scholar: lookup
  163. Chang M.C.. Development of bovine blastocyst with a note on implantation.. Anat. Rec. 1952;113:143.
    doi: 10.1002/ar.1091130203pubmed: 14933807google scholar: lookup
  164. Shemesh M.F., Milaguir F., Aylon N., Hansel W.. Steroidogenesis and prostaglandin synthesis by cultured bovine blastocysts.. J. Reprod. Fertil. 1979;56:181–185.
    doi: 10.1530/jrf.0.0560181pubmed: 469839google scholar: lookup
  165. Eley R.M., Thatcher W.W., Bazer F.W., Fields M.C.. Metabolism of progesterone and androstenedione in vitro by bovine endometrium and conceptus.. J. Anim. Sci. 1979;49((Suppl. S1)):294.
  166. Eley R.M., Thatcher W.W., Bazer F.W., Fields M.J.. Steroid metabolism by the bovine uterine endometrium and conceptus.. Biol. Reprod. 1983;28:804–816.
    doi: 10.1095/biolreprod28.4.804pubmed: 6860739google scholar: lookup
  167. Lonergan P., Fair T., Forde N., Rizos D.. Embryo development in dairy cattle.. Theriogenology. 2016;86:270–277.
  168. Degrelle S.A., Campion E., Cabau C., Piumi F., Reinaud P., Richard C., Renard J.P., Hue I.. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts.. Devel. Biol. 2005;288:448–460.
    doi: 10.1016/j.ydbio.2005.09.043pubmed: 16289134google scholar: lookup
  169. Rizos D., Ward F., Duffy P., Boland M.P., Lonergan P.. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: Implications for blastocyst yield and blastocyst quality.. Mol. Reprod. Dev. 2002;61:234–248.
    doi: 10.1002/mrd.1153pubmed: 11803560google scholar: lookup
  170. Betteridge K.J., Eaglesome M.D., Randall G.C., Mitchell D.. Collection, description and transfer of embryos from cattle 10-16 days after oestrus.. J. Reprod. Fertil. 1980;59:205–216.
    doi: 10.1530/jrf.0.0590205pubmed: 7401037google scholar: lookup
  171. Grealy M., Diskin M.G., Sreenan J.M.. Protein content of cattle oocytes and embryos from the two-cell to the elongated blastocyst stage at day 16.. J. Reprod. Fertil. 1996;107:229–233.
    doi: 10.1530/jrf.0.1070229pubmed: 8882289google scholar: lookup
  172. Morris D.G., Diskin M.G., Sreenan J.M.. Protein synthesis and phosphorylation by elongating 13–15-day-old cattle blastocysts.. Reprod. Fertil. Dev. 2000;12:39–44.
    doi: 10.1071/RD00008pubmed: 11194555google scholar: lookup
  173. Watson A.J., Hogan A., Hahnel A., Wiemer K.E., Schultz G.A.. Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo.. Mol. Reprod. Dev. 1992;31:87–95.
    doi: 10.1002/mrd.1080310202pubmed: 1318055google scholar: lookup
  174. Larson R.C., Ignotz G.G., Currie W.B.. Platelet derived growth factor (PDGF) stimulates development of bovine embryos during the fourth cell cycle.. Development. 1992;115:821–826.
    doi: 10.1242/dev.115.3.821pubmed: 1425356google scholar: lookup
  175. Larson R.C., Ignotz G.G., Currie W.B.. Transforming growth factor beta and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle.. Mol. Reprod. Dev. 1992;33:432–435.
    doi: 10.1002/mrd.1080330409pubmed: 1472373google scholar: lookup
  176. Flood M.R., Gage T.L., Bunch T.D.. Effect of various growth-promoting factors on preimplantation bovine embryo development in vitro.. Theriogenology. 1993;39:823–833.
    doi: 10.1016/0093-691X(93)90421-Zpubmed: 16727256google scholar: lookup
  177. Thibodeaux J.K., Menezo Y., Roussel J.D., Hansel W., Goodeaux L.L., Thompson D.L., Godke R.A.. Coculture of in vitro fertilized bovine embryos with oviductal epithelial cells originating from different stages of the estrous cycle.. J. Dairy Sci. 1992;75:1448–1455.
  178. Shamsuddin M., Larsson B., Gustafsson H., Rodriguez-Martinez H.. In vitro development up to hatching of bovine in-vitro matured and fertilized oocytes with or without support from somatic cells.. Theriogenology. 1993;39:1067–1079.
    doi: 10.1016/0093-691X(93)90007-Rpubmed: 16727277google scholar: lookup
  179. Gandolfi F., Brevini T.A.L., Richardson L., Brown C.R., Moor R.M.. Characterization of proteins secreted by sheep oviduct epithelial cells and their function in embryonic development.. Development. 1989;106:303–312.
    doi: 10.1242/dev.106.2.303pubmed: 2591316google scholar: lookup
  180. Keefer C.L., Stice S.L., Paprocki A.M., Golueke P.. In vitro culture of bovine IVM-IVF embryos: Cooperative interaction among embryos and the role of growth factors.. Theriogenology. 1994;41:1323–1331.
    doi: 10.1016/0093-691X(94)90491-Zpubmed: 16727487google scholar: lookup
  181. Lonergan P.. Influence of progesterone on oocyte quality and embryo development in cows.. Theriogenology. 2011;76:1594–1601.
  182. Lonergan P., Forde N., Spencer T.. Role of progesterone in embryo development in cattle.. Reprod. Fertil. Dev. 2016;28:66–74.
    doi: 10.1071/RD15326pubmed: 27062875google scholar: lookup
  183. Forde N., Carter F., Fair T., Crowe M.A., Evans A.C., Spencer T.E., Bazer F.W., McBride R., Boland M.P., O’Gaora P.. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle.. Biol. Reprod. 2009;81:784–794.
    doi: 10.1095/biolreprod.108.074336pubmed: 19553605google scholar: lookup
  184. Garrett J.E., Geisert R.D., Zavy M.T., Gries L.K., Wettemann R.P., Buchanan D.S.. Effect of exogenous progesterone on prostaglandin F2 alpha release and the interestrous interval in the bovine.. Prostaglandins. 1988;36:85–96.
    doi: 10.1016/0090-6980(88)90104-9pubmed: 3175025google scholar: lookup
  185. Carter F., Rings F., Mamo S., Holker M., Kuzmany A., Besenfelder U., Havlicek V., Mehta J.P., Tesfaye D., Schellander K.. Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers.. Reprod. Fertil. Dev. 2008;20:368–375.
    doi: 10.1071/RD07204pubmed: 18402756google scholar: lookup
  186. Brooks K., Burns G., Spencer T.E.. Conceptus elongation in ruminants: Roles of progesterone, prostaglandin, interferon tau and cortisol.. J. Anim. Sci. Biotechnol. 2014;5:53.
    doi: 10.1186/2049-1891-5-53pmc: PMC4373033pubmed: 25810904google scholar: lookup
  187. Lonergan P., Forde N.. Maternal-embryo interaction leading up to the initiation of implantation of pregnancy in cattle.. Animal. 2014;8((Suppl. S1)):64–69.
    doi: 10.1017/S1751731114000470pubmed: 24679216google scholar: lookup
  188. Faulkner S., Elia G., O’ Boyle P., Dunn M., Morris D.. Composition of the bovine uterine proteome is associated with stage of cycle and concentration of systemic progesterone.. Proteomics. 2013;13:3333–3353.
    doi: 10.1002/pmic.201300204pubmed: 24115321google scholar: lookup
  189. Forde N., McGettigan P.A., Mehta J.P., O’Hara L., Mamo S., Bazer F.W., Spencer T.E., Lonergan P.. Proteomic analysis of uterine fluid during the pre-implantation period of pregnancy in cattle.. Reproduction. 2014;147:575–587.
    doi: 10.1530/REP-13-0010pubmed: 24478148google scholar: lookup
  190. Clemente M., de La Fuente J., Fair T., Al Naib A., Gutierrez-Adan A., Roche J.F., Rizos D., Lonergan P.. Progesterone and conceptus elongation in cattle: A direct effect on the embryo or an indirect effect via the endometrium?. Reproduction. 2009;138:507–517.
    doi: 10.1530/REP-09-0152pubmed: 19556439google scholar: lookup
  191. Larson J.E., Krisher R.L., Lamb G.C.. Effects of supplemental progesterone on the development, metabolism and blastocyst cell number of bovine embryos produced in vitro.. Reprod. Fertil. Dev. 2011;23:311–318.
    doi: 10.1071/RD10106pubmed: 21211464google scholar: lookup
  192. Carter F., Rings F., Mamo S., Holker M., Kuzmany A., Besenfelder U., Havlicek V., Mehta J.P., Tesfaye D., Schellander K.. Effect of elevated circulating progesterone concentration on bovine blastocyst development and global transcriptome following endoscopic transfer of in vitro produced embryos to the bovine oviduct.. Biol. Reprod. 2010;83:707–719.
    doi: 10.1095/biolreprod.109.082354pubmed: 20631399google scholar: lookup
  193. King G.J., Atkinson B.A., Robertson H.A.. Development of the bovine placentome from days 20 to 29 of gestation.. J. Reprod. Fertil. 1980;59:95–100.
    doi: 10.1530/jrf.0.0590095pubmed: 7401049google scholar: lookup
  194. King G.J., Atkinson B.A., Robertson H.A.. Development of the intercaruncular areas during early gestation and establishment of the bovine placenta.. J. Reprod. Fertil. 1981;61:469–474.
    doi: 10.1530/jrf.0.0610469pubmed: 7205793google scholar: lookup
  195. Wooding F.B.. The role of the binucleate cell in ruminant placental structure.. J. Reprod. Fertil. Suppl. 1982;31:31–39.
    pubmed: 6762432
  196. Davenport K.M., Johnson G.A., Seo H., Ortega M.S., Spencer T.E.. Implantation and placentation in ruminants.. Animal. 2023;17((Suppl. S1)):100796.
    doi: 10.1016/j.animal.2023.100796pubmed: 37567669google scholar: lookup
  197. Freeman D.A., Weber J.A., Geary R.T., Woods G.L.. Time of embryo transport through the mare’s oviduct.. Theriogenology. 1991;36:823–830.
    doi: 10.1016/0093-691X(91)90348-Hpubmed: 16727051google scholar: lookup
  198. Grøndahl C., Hyttel P.. Nucleologenesis and ribonucleic acid synthesis in preimplantation equine embryos.. Biol. Reprod. 1996;55:769–774.
    doi: 10.1095/biolreprod55.4.769pubmed: 8879488google scholar: lookup
  199. van Niekerk C.H., Gerneke W.H.. Persistence and parthenogenetic cleavage of tubal ova in the mare.. Onderstepoort J. Vet. Res. 1966;31:195–232.
    pubmed: 6007779
  200. Betteridge K.J., Mitchell D.. Direct evidence of retention of unfertilized ova in the oviduct of the mare.. J. Reprod. Fertil. 1974;39:145–148.
    doi: 10.1530/jrf.0.0390145pubmed: 4604330google scholar: lookup
  201. Weber J.A., Freeman D.A., Vanderwall D.K., Woods G.L.. Prostaglandin E2 hastens oviductal transport of equine embryos.. Biol. Reprod. 1991;45:544–546.
    doi: 10.1095/biolreprod45.4.544pubmed: 1751628google scholar: lookup
  202. Weber J.A., Freeman D.A., Vanderwall D.K., Woods G.L.. Prostaglandin E2 secretion by oviductal transport-stage equine embryos.. Biol. Reprod. 1991;45:540–543.
    doi: 10.1095/biolreprod45.4.540pubmed: 1751627google scholar: lookup
  203. Weber J.A., Woods G.L., Lichtenwalner A.B.. Relaxatory effect of prostaglandin E2 on circular smooth muscle isolated from the equine oviductal isthmus.. Biol. Reprod. 1995;1:125–130.
  204. Flood P.F., Betteridge K.J., Diocee M.S.. Transmission electron microscopy of horse embryos three to 16 days after ovulation.. J. Reprod. Fertil. Suppl. 1982;32:319–327.
    pubmed: 6962867
  205. Oriol J.G., Betteridge K.J., Clarke A.J., Sharom F.J.. Mucin-like glycoproteins in the equine embryonic capsule.. Mol. Reprod. Dev. 1993;34:255–265.
    doi: 10.1002/mrd.1080340305pubmed: 8471247google scholar: lookup
  206. Albihn A., Waelchli R.O., Samper J., Oriol J.G., Croy B.A., Betteridge K.J.. Production of capsular material by equine trophoblast transplanted into immunodeficient mice.. Reproduction. 2003;125:855–863.
    doi: 10.1530/rep.0.1250855pubmed: 12773108google scholar: lookup
  207. Smits K., Govaere J., Peelman L.J., Goossens K., de Graaf D.C., Vercauteren D., Vandaele L., Hoogewijs M., Wydooghe E., Stout T.. Influence of the uterine environment on the development of in vitro-produced equine embryos.. Reproduction. 2012;143:173–181.
    doi: 10.1530/REP-11-0217pubmed: 22089531google scholar: lookup
  208. Stewart F., Charleston B., Crossett B., Barker P.J., Allen W.R.. A novel uterine protein that associates with the embryonic capsule in equids.. J. Reprod. Fertil. 1995;105:65–70.
    doi: 10.1530/jrf.0.1050065pubmed: 7490716google scholar: lookup
  209. Oriol J.G., Sharom F.J., Betteridge K.J.. Developmentally regulated changes in the glycoproteins of the equine embryonic capsule.. J. Reprod. Fertil. 1993;99:653–664.
    doi: 10.1530/jrf.0.0990653pubmed: 8107051google scholar: lookup
  210. Chu J.W., Sharom F.J., Oriol J.G., Betteridge K.J., Cleaver B.D., Sharp D.C.. Biochemical changes in the equine capsule following prostaglandin-induced pregnancy failure.. Mol. Reprod. Dev. 1997;46:286–295.
  211. Quinn B.A., Hayes M.A., Waelchli R.O., Kennedy M.W., Betteridge K.J.. Changes in major proteins in the embryonic capsule during immobilization (fixation) of the conceptus in the third week of pregnancy in the mare.. Reproduction. 2007;134:161–170.
    doi: 10.1530/REP-06-0241pubmed: 17641098google scholar: lookup
  212. Stout T.A.E., Meadows S., Allen W.R.. Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo.. Anim. Reprod. Sci. 2005;87:269–281.
  213. Arar S., Chan K.H., Quinn B.A., Waelchli R.O., Hayes M.A., Betteridge K.J., Monteiro M.A.. Desialylation of core type 1 O-glycan in the equine embryonic capsule coincides with immobilization of the conceptus in the uterus.. Carbohydr. Res. 2007;342:1110–1115.
    doi: 10.1016/j.carres.2007.02.016pubmed: 17335787google scholar: lookup
  214. Crossett B., Suire S., Herrler A., Allen W.R., Stewart F.. Transfer of a uterine lipocalin from the endometrium of the mare to the developing equine conceptus.. Biol. Reprod. 1998;59:483–490.
    doi: 10.1095/biolreprod59.3.483pubmed: 9716544google scholar: lookup
  215. Squire S., Stewart F., Beachamp J., Kennedy M.W.. Uterocalin, a lipocalin provisioning the preattachment equine conceptus: Fatty acid and retinol binding properties, and structural characterization.. Biochem. J. 2001;356:369–376.
    pmc: PMC1221847pubmed: 11368763
  216. Hayes M.A., Quinn B.A., Keirstead N.D., Katavolos P., Waelchli R.O., Betteridge K.J.. Proteins associated with the early intrauterine equine conceptus.. Reprod. Domest. Anim. 2008;43:232–237.
  217. Short R.V.. Implantation and the maternal recognition of pregnancy.. In: Wolstenholme G.E.W., O’Connor M., editors. Ciba Foundation Symposium on Foetal Autonomy. J and A Churchill Ltd.; London, UK: 1966. pp. 2–26.
  218. McDowell K.J., Sharp D.C., Peck L.S., Cheves L.L.. Effect of restricted conceptus mobility on maternal recognition of pregnancy in mares.. Equine Vet. J. Suppl. 1985;3:23–24.
  219. Stout T.A.E., Allen W.R.. Role of prostaglandins in intrauterine migration of the equine conceptus.. Reproduction. 2001;121:771–775.
    doi: 10.1530/rep.0.1210771pubmed: 11427165google scholar: lookup
  220. Vanderwall D.K., Silvia W.J., Fitzgerald B.P.. Concentrations of oxytocin in the cavernous sinus of mares during luteolysis: Temporal relationships with concentrations of 13,14-dihydro-15-ketoprostaglandin F2-alpha.. J. Reprod. Fertil. 1998;112:337–346.
    doi: 10.1530/jrf.0.1120337pubmed: 9640273google scholar: lookup
  221. Stout T.A.E., Lamming G.E., Allen W.R.. The uterus as a source of oxytocin in the cycling mare.. J. Reprod. Fertil. Suppl. 2000;56:281–287.
    pubmed: 20681139
  222. Goff A.K., Pontbriand D., Sirois J.. Oxytocin stimulation of plasma 15-keto-13,14-dihydro prostaglandin F2a during the oestrous cycle and early pregnancy in the mare.. J. Reprod. Fertil. Suppl. 1987;35:253–260.
    pubmed: 3479581
  223. Klein C., Troedsson M.H.. Maternal recognition of pregnancy in the horse: A mystery still to be solved.. Reprod. Fertil. Dev. 2011;23:952–963.
    doi: 10.1071/RD10294pubmed: 22127001google scholar: lookup
  224. Boerboom D., Brown K.A., Vaillancourt D., Poitras P., Goff A.K., Watanabe K., Dore M., Sirois J.. Expression of key prostaglandin synthases in equine endometrium during late diestrus and early pregnancy.. Biol. Reprod. 2004;70:391–399.
    doi: 10.1095/biolreprod.103.020800pubmed: 14561653google scholar: lookup
  225. Ealy A.D., Eroh M.L., Sharp D.C.. Prostglandin H synthase type 2 is differentially expressed in endometrium based on pregnancy status in pony mares and responds to oxytocin and conceptus secretions in explant culture.. Anim. Reprod. Sci. 2010;117:99–105.
  226. Starbuck G.R., Stout T.A.E., Lamming G.E., Allen W.R., Flint A.P.F.. Endometrial oxytocin receptor and uterine prostaglandin secretion in mares during oestrous cycle and early pregnancy.. J. Reprod. Fertil. 1998;113:173–179.
    doi: 10.1530/jrf.0.1130173pubmed: 9861156google scholar: lookup
  227. Stout T.A.E., Lamming G.E., Allen W.R.. Oxytocin administration prolongs luteal function in cyclic mares.. J. Reprod. Fertil. 1999;116:315–320.
    doi: 10.1530/jrf.0.1160315pubmed: 10615256google scholar: lookup
  228. de Ruijter-Villani M., Stout T.. The role of conceptus-maternal signaling in the acquisition of uterine receptivity to implantation in mammals.. Reprod. Domest. Anim. 2015;50:7–14.
    doi: 10.1111/rda.12527pubmed: 26382023google scholar: lookup
  229. Lefèvre F., Guillomot M., D’Andréa S., Battegay S., La Bonnardière C.. Interferon-delta: The first member of a novel type I interferon family.. Biochimie. 1998;80:779–788.
    doi: 10.1016/S0300-9084(99)80030-3pubmed: 9865499google scholar: lookup
  230. Stout T.A.E., Allen W.R.. Prostaglandin E2 and F2a production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares.. Reproduction. 2002;123:261–268.
    doi: 10.1530/rep.0.1230261pubmed: 11866693google scholar: lookup
  231. Sharp D.C., McDowell K.J., Weithenauer J., Thatcher W.W.. The continuum of events leading to maternal recognition of pregnancy in mares.. J. Reprod. Fertil. Suppl. 1989;37:101–107.
    pubmed: 2810225
  232. Zavy M.T., Mayer R., Vernon M.W., Bazer F.W., Sharp D.C.. An investigation of the uterine luminal environment of non-pregnant and pregnant pony mares.. J. Reprod. Fertil. Suppl. 1979;27:403–411.
    pubmed: 289817
  233. Silva L.A., Gastal E.L., Beg M.A., Ginther O.J.. Changes in vascular perfusion of the endometrium in association with changes in location of the embryonic vesicle in mares.. Biol. Reprod. 2005;72:755–761.
    doi: 10.1095/biolreprod.104.036384pubmed: 15576822google scholar: lookup
  234. Zavy M.T., Sharp D.C., Bazer F.W., Fazleabas A., Sessions F., Roberts R.M.. Identification of stage-specific hormonally induced polypeptides in the uterine protein secretions of the mare during the oestrous cycle and pregnancy.. J. Reprod. Fertil. 1982;64:199–207.
    doi: 10.1530/jrf.0.0640199pubmed: 7198687google scholar: lookup
  235. Klein C., Scoggin K.E., Ealy A.D., Troedsson M.H.. Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy.. Biol. Reprod. 2010;83:102–113.
    doi: 10.1095/biolreprod.109.081612pubmed: 20335638google scholar: lookup
  236. Merkl M., Ulbrich S.E., Otzdorff C., Herbach N., Wanke R., Wolf E., Handler J., Bauersachs S.. Microarray analysis of equine endometrium at days 8 and 12 of pregnancy.. Biol. Reprod. 2010;83:874–886.
    doi: 10.1095/biolreprod.110.085233pubmed: 20631402google scholar: lookup
  237. Bazer F.W., Spencer T.E., Johnson G.A., Burghardt R.C., Wu G.. Comparative aspects of implantation.. Reproduction. 2009;138:195–209.
    doi: 10.1530/REP-09-0158pubmed: 19502456google scholar: lookup
  238. Cochet M., Vaiman D., Lefèvre F.. Novel interferon delta genes in mammals: Cloning of one gene from the sheep, two genes expressed by the horse conceptus and discovery of related sequences in several taxa by genomic database screening.. Gene. 2009;433:88–99.
    doi: 10.1016/j.gene.2008.11.026pubmed: 19110041google scholar: lookup
  239. Carson D.D., DeSouza M.M., Kardon R., Zhou X., Lagow E., Julian J.. Mucin expression and function in the female reproductive tract.. Hum. Reprod. Update. 1998;4:459–464.
    doi: 10.1093/humupd/4.5.459pubmed: 10027596google scholar: lookup
  240. Dy S.K., Lim H., Das S.K., Reese J., Paria B.C., Daikoku T., Wang H.. Molecular cues to implantation.. Endocr. Rev. 2004;25:341–373.
    doi: 10.1210/er.2003-0020pubmed: 15180948google scholar: lookup
  241. Wilsher S., Gower S., Allen W.R.. Persistence of an immunoreactive MUC1 protein at the feto-maternal interface throughout pregnancy in the mare.. Reprod. Fertil. Dev. 2013;25:753–761.
    doi: 10.1071/RD12152pubmed: 22951049google scholar: lookup
  242. Klein C.. Novel equine conceptus/endometrial interactions on Day 16 of pregnancy based on RNA sequencing.. Reprod. Fertil. Dev. 2015;28:1712–1720.
    doi: 10.1071/RD14489pubmed: 25940503google scholar: lookup
  243. de Ruijter-Villani M., van Boxtel P.R., Stout T.A.. Fibroblast growth factor-2 expression in the preimplantation equine conceptus and endometrium of pregnant and cyclic mares.. Theriogenology. 2013;80:979–989.
  244. Herrler A., Pell J.M., Allen W.R., Beier H.M., Stewart F.. Horse conceptuses secrete insulin-like growth factor-binding protein 3.. Biol. Reprod. 2000;62:1804–1811.
    doi: 10.1095/biolreprod62.6.1804pubmed: 10819785google scholar: lookup
  245. Allen W.R., Wilsher S.. A review of implantation and early placentation in the mare.. Placenta. 2009;30:1005–1015.
  246. Allen W.R.. Luteal deficiency and embryo mortality in the mare.. Reprod. Domest. Anim. 2001;36:121–131.
  247. Lawson E.F., Grupen G.G., Baker M.A., Aitken R.J., Swegen A., Pollard C.L., Gibb Z.. Conception and early pregnancy in the mare: Lipidomics the unexplored frontier.. Reprod. Fertil. 2022;3:R1–R18.
    doi: 10.1530/RAF-21-0104pmc: PMC8956829pubmed: 35350651google scholar: lookup
  248. Smits K., Willems S., Van Steendam K., Van de Velde M., De Lange V., Ververs C., Roles K., Govaere J., Van Nieuwerburgh F., Peelman L.. Proteins involved in embryo-maternal interaction around the signalling of maternal recognition of pregnancy in the horse.. Sci. Rep. 2018;8:5249.
    doi: 10.1038/s41598-018-23537-6pmc: PMC5869742pubmed: 29588480google scholar: lookup

Citations

This article has been cited 8 times.
  1. Sun Z, Zhao J, Liao Y, Cheng Y, Yu H, Wang M, Fang X, Yang S, Zhao Y. Multi-omics profiling of chromatin accessibility and H3K27ac reveals super-enhancer-mediated regulatory networks governing endometrial receptivity in goats. J Anim Sci Biotechnol 2026 Jan 9;17(1):4.
    doi: 10.1186/s40104-025-01318-2pubmed: 41514467google scholar: lookup
  2. Fan Z, Li Z, Jin Y, Chandrasekaran AP, Shakir IM, Zhang Y, Siddique A, Wang M, Zhou X, Tian Y, Wonka P, Li M. deepBlastoid: a deep learning model for automated and efficient evaluation of human blastoids. Life Med 2025 Dec;4(6):lnaf026.
    doi: 10.1093/lifemedi/lnaf026pubmed: 41450875google scholar: lookup
  3. Ryabchenko AS, Abdyev VK, Vorotelyak EA, Vasiliev AV. Human Blastoid: A Next-Generation Model for Reproductive Medicine?. Biology (Basel) 2025 Oct 18;14(10).
    doi: 10.3390/biology14101439pubmed: 41154841google scholar: lookup
  4. Paudel S, Wang X, Yu H, Wang T, Peng X, Bazer FW, Burghardt RC, Hu G, Wang X. Uterine histotroph and conceptus development. V. Comparative analyses of arginine-mediated transcriptomic reprogramming in conceptus trophectoderm of pigs and sheep†. Biol Reprod 2025 Dec 16;113(6):1475-1489.
    doi: 10.1093/biolre/ioaf226pubmed: 41055590google scholar: lookup
  5. Han A, Qamar AY, Bang S, Kang H, Kim H, Saadeldin IM, Lee S, Cho J. Steroid hormone-treated endometrial organoids enhance implantation of in vitro-produced porcine embryos. J Vet Sci 2025 Sep;26(5):e56.
    doi: 10.4142/jvs.25027pubmed: 40936272google scholar: lookup
  6. Halloran KM, Stenhouse C. Key biochemical pathways during pregnancy in livestock: mechanisms regulating uterine and placental development and function. Reprod Fertil 2025 Jul 1;6(3).
    doi: 10.1530/RAF-25-0056pubmed: 40569626google scholar: lookup
  7. Siemieniuch-Tartanus M. The early pregnancy in mares - What do we still not know?. Vet Anim Sci 2025 Jun;28:100441.
    doi: 10.1016/j.vas.2025.100441pubmed: 40129505google scholar: lookup
  8. Matsuno Y, Kusama K, Kimura K, Imakawa K. Ovine conceptuses express phospholipase inhibitory genes on days 14-15 of pregnancy, interacting with IFNT pathways. Reproduction 2024 Feb 1;169(2).
    doi: 10.1530/REP-24-0286pubmed: 39606929google scholar: lookup