1932

Abstract

All mammalian uteri contain glands that synthesize or transport and secrete substances into the uterine lumen. Uterine gland development, or adenogenesis, is uniquely a postnatal event in sheep and pigs and involves differentiation of glandular epithelium from luminal epithelium, followed by invagination and coiling morphogenesis throughout the stroma. Intrinsic transcription factors and extrinsic factors from the ovary and pituitary as well as the mammary gland (lactocrine) regulate uterine adenogenesis. Recurrent pregnancy loss is observed in the ovine uterine gland knockout sheep, providing unequivocal evidence that glands and their products are essential for fertility. Uterine gland hyperplasia and hypertrophy during pregnancy are controlled by sequential actions of hormones from the ovary and/or pituitary as well as the placenta. Gland-derived histotroph is transported by placental areolae for fetal growth. Increased knowledge of uterine gland biology is expected to improve pregnancy outcomes, as well as the health and productivity of mothers and their offspring.

Keyword(s): developmentfunctionglandpigpregnancysheeputerus
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2019-02-15
2024-06-15
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Literature Cited

  1. 1.  Wooding FBP, Burton GJ 2008. Comparative Placentation: Structures, Functions and Evolution Berlin: Springer
    [Google Scholar]
  2. 2.  Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA et al. 2001. Developmental biology of uterine glands. Biol. Reprod. 65:1311–23
    [Google Scholar]
  3. 3.  Bartol FF, Wiley AA, Floyd JG, Ott TL, Bazer FW et al. 1999. Uterine differentiation as a foundation for subsequent fertility. J. Reprod. Fertil. Suppl. 54:287–302
    [Google Scholar]
  4. 4.  Cooke PS, Spencer TE, Bartol FF, Hayashi K 2013. Uterine glands: development, function and experimental model systems. Mol. Hum. Reprod. 19:547–58
    [Google Scholar]
  5. 5.  Spencer TE, Dunlap KA, Filant J 2012. Comparative developmental biology of the uterus: insights into mechanisms and developmental disruption. Mol. Cell. Endocrinol. 354:34–53
    [Google Scholar]
  6. 6.  Spencer TE, Hayashi K, Hu J, Carpenter KD 2005. Comparative developmental biology of the mammalian uterus. Curr. Top. Dev. Biol. 68:85–122
    [Google Scholar]
  7. 7.  Needham J 1959. A History of Embryology London: Cambridge Univ. Press
    [Google Scholar]
  8. 8.  Amoroso EC 1952. Placentation. Marshall's Physiology of Reproduction AS Parkes 127–311 Boston: Little Brown
    [Google Scholar]
  9. 9.  Bazer FW 1975. Uterine protein secretions: relationship to development of the conceptus. J. Anim. Sci. 41:1376–82
    [Google Scholar]
  10. 10.  Roberts RM, Bazer FW 1988. The functions of uterine secretions. J. Reprod. Fertil. 82:875–92
    [Google Scholar]
  11. 11.  Daniel JC Jr., Krishnan RS 1969. Studies on the relationship between uterine fluid components and the diapausing state of blastocysts from mammals having delayed implantation. J. Exp. Zool. 172:267–81
    [Google Scholar]
  12. 12.  Roberts RM, Murray MK, Burke MG, Ketcham CM, Bazer FW 1987. Hormonal control and function of secretory proteins. Adv. Exp. Med. Biol. 230:137–50
    [Google Scholar]
  13. 13.  Filant J, Spencer TE 2013. Endometrial glands are essential for blastocyst implantation and decidualization in the mouse uterus. Biol. Reprod. 88:93
    [Google Scholar]
  14. 14.  Cooke PS, Ekman GC, Kaur J, Davila J, Bagchi IC et al. 2012. Brief exposure to progesterone during a critical neonatal window prevents uterine gland formation in mice. Biol. Reprod. 86:63
    [Google Scholar]
  15. 15.  Gray CA, Taylor KM, Ramsey WS, Hill JR, Bazer FW et al. 2001. Endometrial glands are required for preimplantation conceptus elongation and survival. Biol. Reprod. 64:1608–13
    [Google Scholar]
  16. 16.  Bartol FF, Wiley AA, Spencer TE, Vallet JL, Christenson RK 1993. Early uterine development in pigs. J. Reprod. Fertil. Suppl. 48:99–116
    [Google Scholar]
  17. 17.  Kobayashi A, Behringer RR 2003. Developmental genetics of the female reproductive tract in mammals. Nat. Rev. Genet. 4:969–80
    [Google Scholar]
  18. 18.  Masse J, Watrin T, Laurent A, Deschamps S, Guerrier D, Pellerin I 2009. The developing female genital tract: from genetics to epigenetics. Int. J. Dev. Biol. 53:411–24
    [Google Scholar]
  19. 19.  Bartol FF, Wiley AA, Bagnell CA 2008. Epigenetic programming of porcine endometrial function and the lactocrine hypothesis. Reprod. Domest. Anim. 43:273–79
    [Google Scholar]
  20. 20.  Bartol FF, Wiley AA, George AF, Miller DJ, Bagnell CA 2017. Physiology and endocrinology symposium: postnatal reproductive development and the lactocrine hypothesis. J. Anim. Sci. 95:2200–10
    [Google Scholar]
  21. 21.  Friess AE, Sinowatz F, Skolek-Winnisch R, Trautner W 1981. The placenta of the pig. II. The ultrastructure of the areolae. Anat. Embryol. 163:43–53
    [Google Scholar]
  22. 22.  Johnson GA, Bazer FW, Burghardt RC, Spencer TE, Wu G, Bayless KJ 2009. Conceptus-uterus interactions in pigs: endometrial gene expression in response to estrogens and interferons from conceptuses. Soc. Reprod. Fertil. Suppl. 66:321–32
    [Google Scholar]
  23. 23.  Spencer TE, Bartol FF, Wiley AA, Coleman DA, Wolfe DF 1993. Neonatal porcine endometrial development involves coordinated changes in DNA synthesis, glycosaminoglycan distribution, and 3H-glucosamine labeling. Biol. Reprod. 48:729–40
    [Google Scholar]
  24. 24.  Tarleton BJ, Wiley AA, Spencer TE, Moss AG, Bartol FF 1998. Ovary-independent estrogen receptor expression in neonatal porcine endometrium. Biol. Reprod. 58:1009–19
    [Google Scholar]
  25. 25.  Bal HS, Getty R 1970. Postnatal growth of the swine uterus from birth to six months. Growth 34:15–30
    [Google Scholar]
  26. 26.  Tarleton BJ, Wiley AA, Bartol FF 1999. Endometrial development and adenogenesis in the neonatal pig: effects of estradiol valerate and the antiestrogen ICI 182,780. Biol. Reprod. 61:253–63
    [Google Scholar]
  27. 27.  Cooke PS, Buchanan DL, Lubahn DB, Cunha GR 1998. Mechanism of estrogen action: lessons from the estrogen receptor-α knockout mouse. Biol. Reprod. 59:470–75
    [Google Scholar]
  28. 28.  Cooke PS, Buchanan DL, Young P, Setiawan T, Brody J et al. 1997. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. PNAS 94:6535–40
    [Google Scholar]
  29. 29.  Hall JM, Couse JF, Korach KS 2001. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276:36869–72
    [Google Scholar]
  30. 30.  Bigsby RM, Cunha GR 1985. Effects of progestins and glucocorticoids on deoxyribonucleic acid synthesis in the uterus of the neonatal mouse. Endocrinology 117:2520–26
    [Google Scholar]
  31. 31.  Branham WS, Sheehan DM 1995. Ovarian and adrenal contributions to postnatal growth and differentiation of the rat uterus. Biol. Reprod. 53:863–72
    [Google Scholar]
  32. 32.  Bartol FF, Wiley AA, Coleman DA, Wolfe DF, Riddell MG 1988. Ovine uterine morphogenesis: effects of age and progestin administration and withdrawal on neonatal endometrial development and DNA synthesis. J. Anim. Sci. 66:3000–9
    [Google Scholar]
  33. 33.  Bartol FF, Wiley AA, Goodlett DR 1988. Ovine uterine morphogenesis: histochemical aspects of endometrial development in the fetus and neonate. J. Anim. Sci. 66:1303–13
    [Google Scholar]
  34. 34.  Bagnell CA, Ho TY, George AF, Wiley AA, Miller DJ, Bartol FF 2017. Maternal lactocrine programming of porcine reproductive tract development. Mol. Reprod. Dev. 84:957–68
    [Google Scholar]
  35. 35.  Bartol FF, Bagnell CA 2018. Lactocrine programming. Encyclopedia of Reproduction MK Skinner 1–7 Cambridge, MA: Academic. , 2nd ed..
    [Google Scholar]
  36. 36.  Bartol FF, Wiley AA, Bagnell CA 2008. Epigenetic programming of porcine endometrial function and the lactocrine hypothesis. Reprod. Domest. Anim. 43:Suppl. 2273–79
    [Google Scholar]
  37. 37.  Yan W, Wiley AA, Bathgate RA, Frankshun AL, Lasano S et al. 2006. Expression of LGR7 and LGR8 by neonatal porcine uterine tissues and transmission of milk-borne relaxin into the neonatal circulation by suckling. Endocrinology 147:4303–10
    [Google Scholar]
  38. 38.  Masters RA, Crean BD, Yan W, Moss AG, Ryan PL et al. 2007. Neonatal porcine endometrial development and epithelial proliferation affected by age and exposure to estrogen and relaxin. Domest. Anim. Endocrinol. 33:335–46
    [Google Scholar]
  39. 39.  Klobasa F, Werhahn E, Butler JE 1987. Composition of sow milk during lactation. J. Anim. Sci. 64:1458–66
    [Google Scholar]
  40. 40.  Lecce JG, Morgan DO 1962. Effect of dietary regimen on cessation of intestinal absorption of large molecules (closure) in the neonatal pig and lamb. J. Nutr. 78:263–68
    [Google Scholar]
  41. 41.  George AF, Rahman KM, Miller DJ, Wiley AA, Camp ME et al. 2018. Effects of colostrum, feeding method and oral IGF1 on porcine uterine development. Reproduction 155:259–71
    [Google Scholar]
  42. 42.  Ho TY, Rahman KM, Camp ME, Wiley AA, Bartol FF, Bagnell CA 2017. Timing and duration of nursing from birth affect neonatal porcine uterine matrix metalloproteinase 9 and tissue inhibitor of metalloproteinase 1. Domest. Anim. Endocrinol. 59:1–10
    [Google Scholar]
  43. 43.  Coalson JA, Lecce JG 1973. Influence of nursing intervals on changes in serum proteins (immunoglobulins) in neonatal pigs. J. Anim. Sci. 36:381–85
    [Google Scholar]
  44. 44.  George AF, Rahman KM, Camp ME, Prasad N, Bartol FF, Bagnell CA 2017. Defining age- and lactocrine-sensitive elements of the neonatal porcine uterine microRNA-mRNA interactome. Biol. Reprod. 96:327–40
    [Google Scholar]
  45. 45.  Rahman KM, Camp ME, Prasad N, McNeel AK, Levy SE et al. 2016. Age and nursing affect the neonatal porcine uterine transcriptome. Biol. Reprod. 94:46
    [Google Scholar]
  46. 46.  Miller DJ, Wiley AA, Chen JC, Bagnell CA, Bartol FF 2013. Nursing for 48 hours from birth supports porcine uterine gland development and endometrial cell compartment-specific gene expression. Biol. Reprod. 88:4
    [Google Scholar]
  47. 47.  Kraeling RR, Webel SK 2015. Current strategies for reproductive management of gilts and sows in North America. J. Anim. Sci. Biotechnol. 6:3
    [Google Scholar]
  48. 48.  Vallet JL, Miles JR, Rempel LA, Nonneman DJ, Lents CA 2015. Relationships between day one piglet serum immunoglobulin immunocrit and subsequent growth, puberty attainment, litter size, and lactation performance. J. Anim. Sci. 93:2722–29
    [Google Scholar]
  49. 49.  Wu WZ, Wang XQ, Wu GY, Kim SW, Chen F, Wang JJ 2010. Differential composition of proteomes in sow colostrum and milk from anterior and posterior mammary glands. J. Anim. Sci. 88:2657–64
    [Google Scholar]
  50. 50.  Vallet JL, Miles JR, Rempel LA 2013. A simple novel measure of passive transfer of maternal immunoglobulin is predictive of preweaning mortality in piglets. Vet. J. 195:91–97
    [Google Scholar]
  51. 51.  Bartol FF, Wiley AA, Miller DJ, Silva AJ, Roberts KE et al. 2013. Lactation biology symposium: lactocrine signaling and developmental programming. J. Anim. Sci. 91:696–705
    [Google Scholar]
  52. 52.  Wimsatt WA 1950. New histological observations on the placenta of the sheep. Am. J. Anat. 87:391–436
    [Google Scholar]
  53. 53.  Atkinson BA, King GJ, Amoroso EC 1984. Development of the caruncular and intercaruncular regions in the bovine endometrium. Biol. Reprod. 30:763–74
    [Google Scholar]
  54. 54.  Wooding FB 1992. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta 13:101–13
    [Google Scholar]
  55. 55.  Carpenter KD, Gray CA, Bryan TM, Welsh TH Jr., Spencer TE 2003. Estrogen and antiestrogen effects on neonatal ovine uterine development. Biol. Reprod. 69:708–17
    [Google Scholar]
  56. 56.  Gray CA, Taylor KM, Bazer FW, Spencer TE 2000. Mechanisms regulating norgestomet inhibition of endometrial gland morphogenesis in the neonatal ovine uterus. Mol. Reprod. Dev. 57:67–78
    [Google Scholar]
  57. 57.  Gray CA, Bazer FW, Spencer TE 2001. Effects of neonatal progestin exposure on female reproductive tract structure and function in the adult ewe. Biol. Reprod. 64:797–804
    [Google Scholar]
  58. 58.  Wiley AA, Bartol FF, Barron DH 1987. Histogenesis of the ovine uterus. J. Anim. Sci. 64:1262–69
    [Google Scholar]
  59. 59.  Taylor KM, Gray CA, Joyce MM, Stewart MD, Bazer FW, Spencer TE 2000. Neonatal ovine uterine development involves alterations in expression of receptors for estrogen, progesterone, and prolactin. Biol. Reprod. 63:1192–204
    [Google Scholar]
  60. 60.  Hayashi K, Spencer TE 2006. WNT pathways in the neonatal ovine uterus: potential specification of endometrial gland morphogenesis by SFRP2. Biol. Reprod. 74:721–33
    [Google Scholar]
  61. 61.  Hayashi K, Carpenter KD, Spencer TE 2004. Neonatal estrogen exposure disrupts uterine development in the postnatal sheep. Endocrinology 145:3247–57
    [Google Scholar]
  62. 62.  Goad J, Ko YA, Kumar M, Syed SM, Tanwar PS 2017. Differential Wnt signaling activity limits epithelial gland development to the anti-mesometrial side of the mouse uterus. Dev. Biol. 423:138–51
    [Google Scholar]
  63. 63.  Cunha GR, Chung LW, Shannon JM, Taguchi O, Fujii H 1983. Hormone-induced morphogenesis and growth: role of mesenchymal-epithelial interactions. Recent Prog. Horm. Res. 39:559–98
    [Google Scholar]
  64. 64.  Cunha GR, Lung B 1979. The importance of stroma in morphogenesis and functional activity of urogenital epithelium. In Vitro 15:50–71
    [Google Scholar]
  65. 65.  Sato T, Wang G, Hardy MP, Kurita T, Cunha GR, Cooke PS 2002. Role of systemic and local IGF-I in the effects of estrogen on growth and epithelial proliferation of mouse uterus. Endocrinology 143:2673–79
    [Google Scholar]
  66. 66.  Taylor KM, Chen C, Gray CA, Bazer FW, Spencer TE 2001. Expression of messenger ribonucleic acids for fibroblast growth factors 7 and 10, hepatocyte growth factor, and insulin-like growth factors and their receptors in the neonatal ovine uterus. Biol. Reprod. 64:1236–46
    [Google Scholar]
  67. 67.  Friedman JR, Kaestner KH 2006. The Foxa family of transcription factors in development and metabolism. Cell. Mol. Life Sci. 63:2317–28
    [Google Scholar]
  68. 68.  Kaestner KH 2010. The FoxA factors in organogenesis and differentiation. Curr. Opin. Genet. Dev. 20:527–32
    [Google Scholar]
  69. 69.  Besnard V, Wert SE, Hull WM, Whitsett JA 2004. Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr. Patterns 5:193–208
    [Google Scholar]
  70. 70.  Filant J, Spencer TE 2013. Cell-specific transcriptional profiling reveals candidate mechanisms regulating development and function of uterine epithelia in mice. Biol. Reprod. 89:86
    [Google Scholar]
  71. 71.  Jeong JW, Kwak I, Lee KY, Kim TH, Large MJ et al. 2010. Foxa2 is essential for mouse endometrial gland development and fertility. Biol. Reprod. 83:396–403
    [Google Scholar]
  72. 72.  Kelleher AM, Peng W, Pru JK, Pru CA, DeMayo FJ, Spencer TE 2017. Forkhead box a2 (FOXA2) is essential for uterine function and fertility. PNAS 114:E1018–E26
    [Google Scholar]
  73. 73.  Gertler A, Djiane J 2002. Mechanism of ruminant placental lactogen action: molecular and in vivo studies. Mol. Genet. Metab. 75:189–201
    [Google Scholar]
  74. 74.  Anthony RV, Limesand SW, Fanning MD, Liang R 1998. Placental lactogen and growth hormone: regulation and action. The Endocrinology of Pregnancy FW Bazer 461–90 Totowa, NJ: Humana
    [Google Scholar]
  75. 75.  Freeman ME, Kanyicska B, Lerant A, Nagy G 2000. Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 80:1523–631
    [Google Scholar]
  76. 76.  Carpenter KD, Gray CA, Noel S, Gertler A, Bazer FW, Spencer TE 2003. Prolactin regulation of neonatal ovine uterine gland morphogenesis. Endocrinology 144:110–20
    [Google Scholar]
  77. 77.  Jost A, Vigier B, Prepin J, Perchellet JP 1973. Studies on sex differentiation in mammals. Recent Prog. Horm. Res. 29:1–41
    [Google Scholar]
  78. 78.  Kennedy JP, Worthington CA, Cole ER 1974. The post-natal development of the ovary and uterus of the Merino lamb. J. Reprod. Fertil. 36:275–82
    [Google Scholar]
  79. 79.  Hayashi K, Carpenter KD, Gray CA, Spencer TE 2003. The activin-follistatin system in the neonatal ovine uterus. Biol. Reprod. 69:843–50
    [Google Scholar]
  80. 80.  Carpenter KD, Hayashi K, Spencer TE 2003. Ovarian regulation of endometrial gland morphogenesis and activin-follistatin system in the neonatal ovine uterus. Biol. Reprod. 69:851–60
    [Google Scholar]
  81. 81.  Hayashi K, O'Connell AR, Juengel JL, McNatty KP, Davis GH et al. 2008. Postnatal uterine development in Inverdale ewe lambs. Reproduction 135:357–65
    [Google Scholar]
  82. 82.  Montgomery GW, Galloway SM, Davis GH, McNatty KP 2001. Genes controlling ovulation rate in sheep. Reproduction 121:843–52
    [Google Scholar]
  83. 83.  Knight JW, Bazer FW, Thatcher WW, Franke DE, Wallace HD 1977. Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: interrelations among hormonal status, placental development, fetal fluids and fetal growth. J. Anim. Sci. 44:620–37
    [Google Scholar]
  84. 84.  Perry JS, Crombie PR 1982. Ultrastructure of the uterine glands of the pig. J. Anat. 134:339–50
    [Google Scholar]
  85. 85.  Sinowatz F, Friess AE 1983. Uterine glands of the pig during pregnancy: an ultrastructural and cytochemical study. Anat. Embryol. 166:121–34
    [Google Scholar]
  86. 86.  Basha SM, Bazer FW, Roberts RM 1980. Effect of the conceptus on quantitative and qualitative aspects of uterine secretion in pigs. J. Reprod. Fertil. 60:41–48
    [Google Scholar]
  87. 87.  Ducsay CA, Buhi WC, Bazer FW, Roberts RM 1982. Role of uteroferrin in iron transport and macromolecular uptake by allantoic epithelium of the porcine conceptus. Biol. Reprod. 26:729–43
    [Google Scholar]
  88. 88.  Renegar RH, Bazer FW, Roberts RM 1982. Placental transport and distribution of uteroferrin in the fetal pig. Biol. Reprod. 27:1247–60
    [Google Scholar]
  89. 89.  Kim YJ, Lee GS, Hyun SH, Ka HH, Choi KC et al. 2009. Uterine expression of epidermal growth factor family during the course of pregnancy in pigs. Reprod. Domest. Anim. 44:797–804
    [Google Scholar]
  90. 90.  Song G, Bailey DW, Dunlap KA, Burghardt RC, Spencer TE et al. 2010. Cathepsin B, cathepsin L, and cystatin C in the porcine uterus and placenta: potential roles in endometrial/placental remodeling and in fluid-phase transport of proteins secreted by uterine epithelia across placental areolae. Biol. Reprod. 82:854–64
    [Google Scholar]
  91. 91.  Ka H, Spencer TE, Johnson GA, Bazer FW 2000. Keratinocyte growth factor: expression by endometrial epithelia of the porcine uterus. Biol. Reprod. 62:1772–78
    [Google Scholar]
  92. 92.  Jang H, Choi Y, Yoo I, Han J, Kim M, Ka H 2017. Characterization of interferon α and β receptor IFNAR1 and IFNAR2 expression and regulation in the uterine endometrium during the estrous cycle and pregnancy in pigs. Theriogenology 88:166–73
    [Google Scholar]
  93. 93.  Seo H, Kim M, Choi Y, Ka H 2011. Salivary lipocalin is uniquely expressed in the uterine endometrial glands at the time of conceptus implantation and induced by interleukin 1beta in pigs. Biol. Reprod. 84:279–87
    [Google Scholar]
  94. 94.  Shim J, Seo H, Choi Y, Yoo I, Lee CK et al. 2013. Analysis of legumain and cystatin 6 expression at the maternal-fetal interface in pigs. Mol. Reprod. Dev. 80:570–80
    [Google Scholar]
  95. 95.  Bailey DW, Dunlap KA, Erikson DW, Patel AK, Bazer FW et al. 2010. Effects of long-term progesterone exposure on porcine uterine gene expression: Progesterone alone does not induce secreted phosphoprotein 1 (osteopontin) in glandular epithelium. Reproduction 140:595–604
    [Google Scholar]
  96. 96.  Bailey DW, Dunlap KA, Frank JW, Erikson DW, White BG et al. 2010. Effects of long-term progesterone on developmental and functional aspects of porcine uterine epithelia and vasculature: Progesterone alone does not support development of uterine glands comparable to that of pregnancy. Reproduction 140:583–94
    [Google Scholar]
  97. 97.  Garlow JE, Ka H, Johnson GA, Burghardt RC, Jaeger LA, Bazer FW 2002. Analysis of osteopontin at the maternal-placental interface in pigs. Biol. Reprod. 66:718–25
    [Google Scholar]
  98. 98.  Ka H, Al-Ramadan S, Erikson DW, Johnson GA, Burghardt RC et al. 2007. Regulation of expression of fibroblast growth factor 7 in the pig uterus by progesterone and estradiol. Biol. Reprod. 77:172–80
    [Google Scholar]
  99. 99.  White FJ, Ross JW, Joyce MM, Geisert RD, Burghardt RC, Johnson GA 2005. Steroid regulation of cell specific secreted phosphoprotein 1 (osteopontin) expression in the pregnant porcine uterus. Biol. Reprod. 73:1294–301
    [Google Scholar]
  100. 100.  Steinhauser CB, Landers M, Myatt L, Burghardt RC, Vallet JL et al. 2016. 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. 95:108
    [Google Scholar]
  101. 101.  Steinhauser CB, Bazer FW, Burghardt RC, Johnson GA 2017. Expression of progesterone receptor in the porcine uterus and placenta throughout gestation: correlation with expression of uteroferrin and osteopontin. Domest. Anim. Endocrinol. 58:19–29
    [Google Scholar]
  102. 102.  Steinhauser CB, Wing TT, Gao H, Li X, Burghardt RC et al. 2017. Identification of appropriate reference genes for qPCR analyses of placental expression of SLC7A3 and induction of SLC5A1 in porcine endometrium. Placenta 52:1–9
    [Google Scholar]
  103. 103.  Knight JW, Bazer FW, Wallace HD 1974. Effect of progesterone induced increase in uterine secretory activity of development of the porcine conceptus. J. Anim. Sci. 39:743–46
    [Google Scholar]
  104. 104.  Knight JW, Bazer FW, Wallace HD, Wilcox CJ 1974. Dose-response relationships between exogenous progesterone and estradiol and porcine uterine protein secretions. J. Anim. Sci. 39:747–51
    [Google Scholar]
  105. 105.  Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K 2010. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol. Hum. Reprod. 16:135–52
    [Google Scholar]
  106. 106.  Knight JW, Bazer FW, Wallace HD 1973. Hormonal regulation of porcine uterine protein secretion. J. Anim. Sci. 36:546–53
    [Google Scholar]
  107. 107.  Young KH, Kraeling RR, Bazer FW 1990. Effect of pregnancy and exogenous ovarian steroids on endometrial prolactin receptor ontogeny and uterine secretory response in pigs. Biol. Reprod. 43:592–99
    [Google Scholar]
  108. 108.  Basha SM, Bazer FW, Geisert RD, Roberts RM 1980. Progesterone-induced uterine secretions in pigs. Recovery from pseudopregnant and unilaterally pregnant gilts. J. Anim. Sci. 50:113–23
    [Google Scholar]
  109. 109.  Spencer TE, Johnson GA, Bazer FW, Burghardt RC 2004. Implantation mechanisms: insights from the sheep. Reproduction 128:657–68
    [Google Scholar]
  110. 110.  Spencer TE, Sandra O, Wolf E 2008. Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction 135:165–79
    [Google Scholar]
  111. 111.  Hue I, Degrelle SA, Turenne N 2012. Conceptus elongation in cattle: genes, models and questions. Anim. Reprod. Sci. 134:19–28
    [Google Scholar]
  112. 112.  Guillomot M 1995. Cellular interactions during implantation in domestic ruminants. J. Reprod. Fertil. Suppl. 49:39–51
    [Google Scholar]
  113. 113.  Sandra O, Charpigny G, Galio L, Hue I 2017. Preattachment embryos of domestic animals: insights into development and paracrine secretions. Annu. Rev. Anim. Biosci. 5:205–28
    [Google Scholar]
  114. 114.  Ogasawara Y, Okamoto S, Kitamura Y, Matsumoto K 1983. Proliferative pattern of uterine cells from birth to adulthood in intact, neonatally castrated, and/or adrenalectomized mice, assayed by incorporation of [125I]iododeoxyuridine. Endocrinology 113:582–87
    [Google Scholar]
  115. 115.  Allison Gray C, Bartol FF, Taylor KM, Wiley AA, Ramsey WS et al. 2000. Ovine uterine gland knock-out model: effects of gland ablation on the estrous cycle. Biol. Reprod. 62:448–56
    [Google Scholar]
  116. 116.  Gray CA, Burghardt RC, Johnson GA, Bazer FW, Spencer TE 2002. Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 124:289–300
    [Google Scholar]
  117. 117.  Stewart MD, Johnson GA, Gray CA, Burghardt RC, Schuler LA et al. 2000. Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy. Biol. Reprod. 62:1779–89
    [Google Scholar]
  118. 118.  Koch JM, Ramadoss J, Magness RR 2010. Proteomic profile of uterine luminal fluid from early pregnant ewes. J. Proteome Res. 9:3878–85
    [Google Scholar]
  119. 119.  Brooks K, Burns GW, Moraes JG, Spencer TE 2016. Analysis of the uterine epithelial and conceptus transcriptome and luminal fluid proteome during the peri-implantation period of pregnancy in sheep. Biol. Reprod. 95:88
    [Google Scholar]
  120. 120.  Romero JJ, Liebig BE, Broeckling CD, Prenni JE, Hansen TR 2017. Pregnancy-induced changes in metabolome and proteome in ovine uterine flushings. Biol. Reprod. 97:273–87
    [Google Scholar]
  121. 121.  Song G, Satterfield MC, Kim J, Bazer FW, Spencer TE 2008. Gastrin-releasing peptide (GRP) in the ovine uterus: regulation by interferon tau and progesterone. Biol. Reprod. 79:376–86
    [Google Scholar]
  122. 122.  Hayashi K, Burghardt RC, Bazer FW, Spencer TE 2007. WNTs in the ovine uterus: potential regulation of periimplantation ovine conceptus development. Endocrinology 148:3496–506
    [Google Scholar]
  123. 123.  Gao H, Wu G, Spencer TE, Johnson GA, Bazer FW 2009. Select nutrients in the ovine uterine lumen. IV. Expression of neutral and acidic amino acid transporters in ovine uteri and peri-implantation conceptuses. Biol. Reprod. 80:1196–208
    [Google Scholar]
  124. 124.  Gao H, Wu G, Spencer TE, Johnson GA, Bazer FW 2009. Select nutrients in the ovine uterine lumen. III. Cationic amino acid transporters in the ovine uterus and peri-implantation conceptuses. Biol. Reprod. 80:602–9
    [Google Scholar]
  125. 125.  Gao H, Wu G, Spencer TE, Johnson GA, Bazer FW 2009. Select nutrients in the ovine uterine lumen. II. Glucose transporters in the uterus and peri-implantation conceptuses. Biol. Reprod. 80:94–104
    [Google Scholar]
  126. 126.  Gray CA, Adelson DL, Bazer FW, Burghardt RC, Meeusen EN, Spencer TE 2004. Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm. PNAS 101:7982–87
    [Google Scholar]
  127. 127.  Gray CA, Dunlap KA, Burghardt RC, Spencer TE 2005. Galectin-15 in ovine uteroplacental tissues. Reproduction 130:231–40
    [Google Scholar]
  128. 128.  Johnson GA, Burghardt RC, Joyce MM, Spencer TE, Bazer FW et al. 2003. Osteopontin is synthesized by uterine glands and a 45-kDa cleavage fragment is localized at the uterine-placental interface throughout ovine pregnancy. Biol. Reprod. 69:92–98
    [Google Scholar]
  129. 129.  Song G, Bazer FW, Wagner GF, Spencer TE 2006. Stanniocalcin (STC) in the endometrial glands of the ovine uterus: regulation by progesterone and placental hormones. Biol. Reprod. 74:913–22
    [Google Scholar]
  130. 130.  Song G, Bazer FW, Spencer TE 2007. Differential expression of cathepsins and cystatin C in ovine uteroplacental tissues. Placenta 28:1091–98
    [Google Scholar]
  131. 131.  Moffatt RJ, Bazer FW, Roberts RM, Thatcher WW 1987. Secretory function of the ovine uterus: effects of gestation and steroid replacement therapy. J. Anim. Sci. 65:1400–10
    [Google Scholar]
  132. 132.  Dorniak P, Bazer FW, Spencer TE 2013. Physiology and endocrinology symposium: biological role of interferon tau in endometrial function and conceptus elongation. J. Anim. Sci. 91:1627–38
    [Google Scholar]
  133. 133.  Forde N, Lonergan P 2012. Transcriptomic analysis of the bovine endometrium: What is required to establish uterine receptivity to implantation in cattle?. J. Reprod. Dev. 58:189–95
    [Google Scholar]
  134. 134.  Spencer TE, Johnson GA, Bazer FW, Burghardt RC 2007. Fetal-maternal interactions during the establishment of pregnancy in ruminants. Soc. Reprod. Fertil. Suppl. 64:379–96
    [Google Scholar]
  135. 135.  Hansen TR, Sinedino LDP, Spencer TE 2017. Paracrine and endocrine actions of interferon tau (IFNT). Reproduction 154:F45–F59
    [Google Scholar]
  136. 136.  Spencer TE, Hansen TR 2015. Implantation and establishment of pregnancy in ruminants. Adv. Anat. Embryol. Cell Biol. 216:105–35
    [Google Scholar]
  137. 137.  Johnson GA, Burghardt RC, Spencer TE, Newton GR, Ott TL, Bazer FW 1999. Ovine osteopontin: II. Osteopontin and αvβ3 integrin expression in the uterus and conceptus during the periimplantation period. Biol. Reprod. 61:892–99
    [Google Scholar]
  138. 138.  Johnson GA, Spencer TE, Burghardt RC, Bazer FW 1999. Ovine osteopontin: I. Cloning and expression of messenger ribonucleic acid in the uterus during the periimplantation period. Biol. Reprod. 61:884–91
    [Google Scholar]
  139. 139.  Noel S, Herman A, Johnson GA, Gray CA, Stewart MD et al. 2003. Ovine placental lactogen specifically binds to endometrial glands of the ovine uterus. Biol. Reprod. 68:772–80
    [Google Scholar]
  140. 140.  Lacroix MC, Devinoy E, Servely JL, Puissant C, Kann G 1996. Expression of the growth hormone gene in ovine placenta: detection and cellular localization of the protein. Endocrinology 137:4886–92
    [Google Scholar]
  141. 141.  Spencer TE, Gray A, Johnson GA, Taylor KM, Gertler A et al. 1999. Effects of recombinant ovine interferon tau, placental lactogen, and growth hormone on the ovine uterus. Biol. Reprod. 61:1409–18
    [Google Scholar]
  142. 142.  Choi Y, Johnson GA, Burghardt RC, Berghman LR, Joyce MM et al. 2001. Interferon regulatory factor-two restricts expression of interferon-stimulated genes to the endometrial stroma and glandular epithelium of the ovine uterus. Biol. Reprod. 65:1038–49
    [Google Scholar]
  143. 143.  Johnson GA, Stewart MD, Gray CA, Choi Y, Burghardt RC et al. 2001. Effects of the estrous cycle, pregnancy, and interferon tau on 2′,5′-oligoadenylate synthetase expression in the ovine uterus. Biol. Reprod. 64:1392–99
    [Google Scholar]
  144. 144.  Martin C, Pessemesse L, De La Llosa-Hermier MP, Martal J, Djiane J, Charlier M 2004. Interferon-tau upregulates prolactin receptor mRNA in the ovine endometrium during the peri-implantation period. Reproduction 128:99–105
    [Google Scholar]
  145. 145.  Yuan J, Deng W, Cha J, Sun X, Borg JP, Dey SK 2018. Tridimensional visualization reveals direct communication between the embryo and glands critical for implantation. Nat. Commun. 9:603
    [Google Scholar]
  146. 146.  Arora R, Fries A, Oelerich K, Marchuk K, Sabeur K et al. 2016. Insights from imaging the implanting embryo and the uterine environment in three dimensions. Development 143:4749–54
    [Google Scholar]
  147. 147.  Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ et al. 2017. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat. Cell Biol. 19:568–77
    [Google Scholar]
  148. 148.  Boretto M, Cox B, Noben M, Hendriks N, Fassbender A et al. 2017. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development 144:1775–86
    [Google Scholar]
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