Placenta
Volume 28 , Pages S64-S69 , April 2007

Human Early Placental Development: Potential Roles of the Endometrial Glands

  • G.J. Burton

      Affiliations

    • Department of Physiology, Development and Neuroscience, Physiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 1223 333 856; fax: +44 1223 333 840.
    • ,
  • E. Jauniaux

      Affiliations

    • Academic Department of Obstetrics and Gynaecology, Royal Free and University College, London, UK
    • ,
  • D.S. Charnock-Jones

      Affiliations

    • Department of Obstetrics and Gynaecology, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK

,Accepted 8 January 2007.

References 

  1. Wooding FBP, Flint APF. Placentation. In:  Lamming GE editors. Marshall's physiology of reproduction. London: Chapman & Hall; 1994;p. 233–460
  2. Hamilton WJ, Boyd JD. Development of the human placenta in the first three months of gestation. J Anat. 1960;94:297–328
  3. Hertig AT, Rock J, Adams EC. A description of 34 human ova within the first 17days of development. Am J Anat. 1956;98:435–494
  4. Enders AC, Carter AM. What can comparative studies of placental structure tell us? – A review. Placenta. 2004;25:S3–S9(Supplement A, Troph Res)
  5. Boyd JD, Hamilton WJ. The human placenta. Cambridge: Heffer and Sons; 1970;365 pp.
  6. Hamilton WJ, Gladstone RJ. A presomite human embryo (Shaw): the implantation. J Anat. 1942;76:187–203
  7. Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniaux E. Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab. 2002;87:2954–2959
  8. Hempstock J, Cindrova-Davies T, Jauniaux E, Burton GJ. Endometrial glands as a source of nutrients, growth factors and cytokines during the first trimester of human pregnancy; a morphological and immunohistochemical study. Reprod Biol Endocrinol. 2004;2:58
  9. Demir R, Kayisli UA, Celik-Ozenci C, Korgun ET, Demir-Weusten AY, Arici A. Structural differentiation of human uterine luminal and glandular epithelium during early pregnancy: an ultrastructural and immunohistochemical study. Placenta. 2002;23:672–684
  10. Bell SC. Secretory endometrial/decidual proteins and their function in early pregnancy. J Reprod Fertil 1988;Suppl. 36:109–25.
  11. Seppala M, Riittinen L, Julkunen M, Koistinen R, Wahlstrom T, Iino K, et al. Structural studies, localization in tissue and clinical aspects of human endometrial proteins. J Reprod Fertil Suppl. 1988;36:127–141
  12. Jauniaux E, Watson AL, Hempstock J, Bao Y-P, Skepper JN, Burton GJ. Onset of maternal arterial bloodflow and placental oxidative stress; a possible factor in human early pregnancy failure. Am J Pathol. 2000;157:2111–2122
  13. Beir-Hellwig K, Sterzik K, Bonn B, Beir HM. Contribution to the physiology and pathology of endometrial receptivity: the determination of protein patterns in human uterine secretions. Hum Reprod. 1989;4(Suppl.):115–120
  14. Boyd JD. Some aspects of the relationship between mother and child. Ulster Med J. 1959;28:35–46
  15. Seppälä M, Jukunen M, Riitinen L, Koistinen R. Endometrial proteins: a reappraisal. Hum Reprod. 1992;7(Suppl. 1):31–38
  16. Beckman DA, Brent RL, Lloyd JB. Sources of amino acids for protein synthesis during early organogenesis in the rat. 4. Mechanisms before envelopment of the embryo by the yolk sac. Placenta. 1996;17:635–641
  17. Jauniaux E, Cindrova-Davies T, Johns J, Dunster C, Hempstock J, Kelly FJ, et al. Distribution and transfer pathways of antioxidant molecules inside the first trimester human gestational sac. J Clin Endocrinol Metab. 2004;89:1452–1459
  18. Ladines-Llave CA, Maruo T, Manalo AS, Mochizuki M. Cytologic localization of epidermal growth factor and its receptor in developing human placenta varies over the course of pregnancy. Am J Obstet Gynecol. 1991;165:1377–1382
  19. Maruo T, Matsuo H, Murata K, Mochizuki M. Gestational age-dependent dual action of epidermal growth factor on human placenta early in gestation. J Clin Endocrinol Metab. 1992;75:1362–1367
  20. Lennard SN, Gerstenberg C, Allen WR, Stewart F. Expression of epidermal growth factor and its receptor in equine placental tissues. J Reprod Fertil. 1998;112:49–57
  21. Jauniaux E, Gulbis B, Burton GJ. The human first trimester gestational sac limits rather than facilitates oxygen transfer to the fetus-a review. Placenta. 2003;24(Suppl. A):S86–S93
  22. Ramsey EM, Donner MW. Placental vasculature and circulation. Anatomy, physiology, radiology, clinical aspects, atlas and textbook. Stuttgart: Georg Thieme; 1980;101 pp.
  23. Hustin J, Schaaps JP, Lambotte R. Anatomical studies of the utero-placental vascularisation in the first trimester of pregnancy. Troph Res. 1988;3:49–60
  24. Burton GJ, Jauniaux E, Watson AL. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy; the Boyd Collection revisited. Am J Obstet Gynecol. 1999;181:718–724
  25. Khong TY, Liddell HS, Robertson WB. Defective haemochorial placentation as a cause of miscarriage. A preliminary study. Br J Obstet Gynaecol. 1987;94:649–655
  26. Hustin J, Jauniaux E, Schaaps JP. Histological study of the materno-embryonic interface in spontaneous abortion. Placenta. 1990;11:477–486
  27. Bartelmez GW. Histological studies on the menstruating mucous membrane of the human uterus. Contrib Embryo. 1933;142:141–186
  28. Cooper JC, Sharkey AM, McLaren J, Charnock Jones DS, Smith SK. Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. J Reprod Fertil. 1995;105:205–213
  29. Sharkey AM, King A, Clark DE, Burrows TD, Johki PP, Charnock Jones DS, et al. Localization of leukaemia inhibitory factor and its receptor in human placenta throughout pregnancy. Biol Reprod. 1999;60:355–364
  30. Charnock Jones DS, Kaufmann P, Mayhew TM. Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular recognition. Placenta. 2004;25:103–113
  31. Okamoto N, Uchida A, Takakura K, Kariya Y, Kanzaki H, Riittinen L, et al. Suppression by human placental protein 14 of natural killer cell activity. Am J Reprod Immunol. 1991;26:137–142
  32. Pockley AG, Bolton AE. The effect of human placental protein 14 (PP14) on the production of interleukin-1 from mitogenically stimulated mononuclear cell cultures. Immunology. 1990;69:277–281
  33. Rachmilewitz J, Riely GJ, Tykocinski ML. Placental protein 14 functions as a direct T-cell inhibitor. Cell Immunol. 1999;191:26–33
  34. Mukherjee AB, Cordella-Miele E, Kikukawa T, Miele L. Modulation of cellular response to antigens by uteroglobin and transglutaminase. Adv Exp Med Biol. 1988;231:135–152
  35. Muller-Schottle F, Classen-Linke I, Alfer J, Krusche C, Beier-Hellwig K, Sterzik K, et al. Expression of uteroglobin in the human endometrium. Mol Hum Reprod. 1999;5:1155–1161
  36. Kundu GC, Mantile G, Miele L, Cordella-Miele E, Mukherjee AB. Recombinant human uteroglobin suppresses cellular invasiveness via a novel class of high-affinity cell surface binding site. Proc Nat Acad Sci USA. 1996;93:2915–2919
  37. King AE, Critchley HOD, Kelly RW. Innate immune defences in the human endometrium. Reprod Biol Endocrinol. 2003;1:116
  38. Singh PK, Tack BF, McCray PB, Welsh MJ. Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am J Physiol Lung Cell Mol Physiol. 2000;279:L799–L805
  39. Dockery P, Li TC, Rogers AW, Cooke ID, Lenton EA. The ultrastructure of the glandular epithelium in the timed endometrial biopsy. Hum Reprod. 1988;3:826–834
  40. Spencer TE, Johnson GA, Burghardt RC, Bazer FW. Progesterone and placental hormone actions on the uterus: insights from domestic animals. Biol Reprod. 2004;71:2–10
  41. Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, et al. Developmental biology of uterine glands. Biol Reprod. 2001;65:1311–1323
  42. Noel S, Herman A, Johnson GA, Gray CA, Stewart MD, Bazer FW, et al. Ovine placental lactogen specifically binds to endometrial glands of the ovine uterus. Biol Reprod. 2003;68:772–780
  43. Stewart MD, Johnson GA, Gray CA, Burghardt RC, Schuler LA, Joyce MM, et al. Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy. Biol Reprod. 2000;62:1779–1789
  44. Kleis-SanFrancisco S, Hewetson A, Chilton BS. Prolactin augments progesterone-dependent uteroglobin gene expression by modulating promoter-binding proteins. Mol Endocrinol. 1993;7:214–223
  45. Wang H, Critchley HO, Kelly RW, Shen D, Baird DT. Progesterone receptor subtype B is differentially regulated in human endometrial stroma. Mol Hum Reprod. 1998;4:407–412
  46. Zhou XL, Lei ZM, Rao CV. Treatment of human endometrial gland epithelial cells with chorionic gonadotropin/luteinizing hormone increases the expression of the cyclooxygenase-2 gene. J Clin Endocrinol Metab. 1999;84:3364–3377
  47. Jones RL, Critchley HO, Brooks J, Jabbour HN, McNeilly AS. Localization and temporal expression of prolactin receptor in human endometrium. J Clin Endocrinol Metab. 1998;83:258–262
  48. Huang JR, Tseng L, Bischof P, Janne OA. Regulation of prolactin production by progestin, estrogen, and relaxin in human endometrial stromal cells. Endocrinology. 1987;121:2011–2017
  49. Fazleabas AT, Donnelly KM, Hild-Petito S, Hausermann HM, Verhage HG. Secretory proteins of the baboon (Papio anubis) endometrium: regulation during the menstrual cycle and early pregnancy. Hum Reprod Update. 1997;3:553–559
  50. Hausermann HM, Donnelly KM, Bell SC, Verhage HG, Fazleabas AT. Regulation of the glycosylated beta-lactoglobulin homolg, glycodelin [placental protein 14:(PP14)] in the baboon (Papio anubis) uterus. J Clin Endocrinol Metab. 1998;83:1226–1233
  51. Moffett-King A. Natural killer cells and pregnancy. Nat Rev Immunol. 2002;2:656–663
  52. Basir GS, O WS, So WW, Ng EH, Ho PC. Evaluation of cycle-to-cycle variation of endometrial responsiveness using transvaginal sonography in women undergoing assisted reproduction. Ultrasound Obstet Gynaecol. 2002;19:484–489
  53. Kolibianakis EM, Zikopoulos KA, Fatemi HM, Osmanagaoglu K, Evenpoel J, Van Steirteghem A, et al. Endometrial thickness cannot predict ongoing pregnancy achievement in cycles stimulated with clomiphene citrate for intrauterine insemination. Reprod Biomed Online. 2004;8:115–118
  54. Dalton CF, Laird SM, Estdale SE, Saravelos HG, Li TC. Endometrial protein PP14 and CA-125 in recurrent miscarriage patients; correlation with pregnancy outcome. Hum Reprod. 1998;13:3197–3202
  55. Hey NA, Li TC, Devine PL, Graham RA, Saravelos H, Aplin JD. MUC1 in secretory phase endometrium: expression in precisely dated biopsies and flushings from normal and recurrent miscarriage patients. Hum Reprod. 1995;10:2655–2662
  56. Lessey BA, Yeh I, Castelbaum AJ, Fritz MA, Ilesanmi AO, Korzeniowski P, et al. Endometrial progesterone receptors and markers of uterine receptivity in the window of implantation. Fertil Steril. 1996;65:477–483
  57. Gray CA, Taylor KM, Ramsey WS, Hill JR, Bazer FW, Bartol FF, et al. Endometrial glands are required for preimplantation conceptus elongation and survival. Biol Reprod. 2001;64:1608–1613

PII: S0143-4004(07)00010-0

doi: 10.1016/j.placenta.2007.01.007

Placenta
Volume 28 , Pages S64-S69 , April 2007

Article Tools

* Image Usage & Resolution