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Trophoblast-Uterine Interactions in Implantation: Role of Transforming Growth Factor α/Epidermal Growth Factor Receptor Signaling

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Trophoblast Cells

Part of the book series: Serono Symposia, USA Norwell, Massachusetts ((SERONOSYMP))

Abstract

The uterine tissue compartments comprise heterogeneous cell types that respond uniquely toestrogen (E) andprogesterone (P4). In the adult ovariectomized mouse or rat uterus, E stimulates proliferation and differentiation of luminal and glandular epithelia, whereas in the stroma, these processes require both P4 and E (1, 2). Steroid hormonal modulation of cell-type-specific proliferation and differentiation also occurs in the mouse uterus during the periimplantation period. Preovulatory ovarian E directs epithelial cell proliferation on days 1 and 2 of pregnancy, whereas on day 3, P4 from newly formed corpora lutea initiates proliferation of stromal cells that is further accelerated by preimplantation Esecretion on day 4. During implantation, stromal cells undergo extensive proliferation and differentiation into decidual cells (1, 2). Ovariectomy during the preimplantation period before the presumedE-surge results in delayed-implantation and blastocyst dormancy (3). Delayed implantation can be maintained for several days by continued P4 treatment. However, a single injection of a small amount of E initiates implantation in P4-primed delayed-implanting mice (4, 5). In the pregnant or pseudopregnant mouse, the uterus becomes receptive only on day 4 (the day of implantation), while by day 5 (as examined in the pseudopregnant mouse by embryo transfer), the uterus becomes refractory and fails to respond to the presence of blastocysts for initiation of implantation.

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References

  1. Martin L, Finn CA. Hormonal regulation of cell division in epithelial and connective tissues of mouse uterus. J Endocrinol 1968;41:363–71.

    Article  PubMed  CAS  Google Scholar 

  2. Huet-Hudson YM, Andrews GK, Dey SK. Cell type–specific localization of c–myc protein in the mouse uterus: modulation by steroid hormones and analysis of the periimplantation period. Endocrinology 1989;125:1683–90.

    Article  PubMed  CAS  Google Scholar 

  3. McCormack JT, Greenwald GS. Evidence for a preimplantation rise in estradiol-17β levels on day 4 of pregnancy in the mouse. J Reprod Fertil 1974;41:297–301.

    Article  PubMed  CAS  Google Scholar 

  4. Yoshinaga K, Adams CE. Delayed implantation in the spayed, progesterone-treated adult mouse. J Reprod Fertil 1966;12:593–5.

    Article  PubMed  CAS  Google Scholar 

  5. Huet YM, Dey SK. Role of early and late estrogenic effects on implantation in the mouse. J Reprod Fertil 1987;81:453–8.

    Article  PubMed  CAS  Google Scholar 

  6. Dey SK, Johnson DC. Embryo-uterine interactions during implantation. Life Sci 1980;27:2381–4.

    Article  PubMed  CAS  Google Scholar 

  7. Huet-Hudson YM, Andrews GK, Dey SK. Epidermal growth factor and pregnancy in the mouse. In: Heyner S, Wiley LM, eds. Early embryo development and paracrine relationships. New York: Wiley-Liss, 1990:125–36.

    Google Scholar 

  8. Tamada H, McMaster MT, Flanders KC, Andrews GK, Dey SK. Cell type specific expression of transforming growth factor–ail in the mouse uterus during the periimplantation period. Mol Endocrinol 1990;4:965–72.

    Article  PubMed  CAS  Google Scholar 

  9. Tamada H, Das SK, Andrews GK, Dey SK. Cell type specific expression of transforming growth factor-α in the mouse uterus during the periimplantation period. Biol Reprod 1991;45:365–72.

    Article  PubMed  CAS  Google Scholar 

  10. Murphy LJ, Murphy LC, Friesen HG. Estrogen induces insulin-like growth factor-I in the rat uterus. Mol Endocrinol 1987;1:445–50.

    Article  PubMed  CAS  Google Scholar 

  11. Chakraborty C, Tawfik OW, Dey SK. Epidermal growth factor binding in rat uterus during the periimplantation period. Biochem Biophys Res Commun 1988;154:564–9.

    Article  Google Scholar 

  12. DiAugustine RP, Petrusz P, Bell GI, et al. Influence of estrogens on mouse uterine epidermal growth factor precursor protein and messenger ribonucleic acid. Endocrinology 1988;122:2355–63.

    Article  PubMed  CAS  Google Scholar 

  13. Mukku VR, Stancel GL. Regulation of epidermal growth factor receptors by estrogen. J Biol Chem 1985;260:9820–4.

    PubMed  CAS  Google Scholar 

  14. Lingham RB, Stancel GM, Loose-Mitchell DM. Estrogen regulation of epidermal growth factor receptor messenger ribonucleic acid. Mol Endocrinol 1988;2:230–5.

    Article  PubMed  CAS  Google Scholar 

  15. Kapur S, Tamada H, Dey SK, Andrews GK. Expression of insulin-like growth factor-1 (IGF-1) and its receptor in the peri–implantation mouse uterus, and cell-specific regulation of IGF-1 gene expression by estradiol and progesterone. Biol Reprod 1992;46:208–19.

    Article  PubMed  CAS  Google Scholar 

  16. Brown MJ, Zogg JL, Schultz GS, Hilton FK. Increased binding of epidermal growth factor at the implantation sites in mouse uteri. Endocrinology 1989;124:2882–8.

    Article  PubMed  CAS  Google Scholar 

  17. Das S, Flanders KC, Andrews GK, Dey SK. Expression of transforming growth factor-β isoforms (P2 and 03) in the mouse uterus: analysis of the periimplantation period and effects of ovarian steroids. Endocrinology 1992;130:3459–66.

    Article  PubMed  CAS  Google Scholar 

  18. Rappolee DA, Brenner CA, Schultz R, Mark D, Werb Z. Developmental expression of PDGF, TGF-α and TGF-β genes in preimplantation mouse embryos. Science 1988;241:1823–5.

    Article  PubMed  CAS  Google Scholar 

  19. Rappolee D, Sturm KS, Schultz GA, Pedersen RA, Werb Z. The expression of growth factor ligands and receptors in preimplantation mouse embryo. In: Heyner S, Wiley L, eds. Early embryo development and paracrine relation¬ships. New York: A.R. Liss, 1990:11–25.

    Google Scholar 

  20. Watson AJ, Hogan A, Hahnel A, Weimer KE, Schultz GA. Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo. Mol Reprod Dev 1992;31:87–95.

    Article  PubMed  CAS  Google Scholar 

  21. Paria BC, Dey SK. Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc Natl Acad Sci USA 1990;87:4756–60.

    Article  PubMed  CAS  Google Scholar 

  22. Paria BC, Tsukamura H, Dey SK. Epidermal growth factor specific protein tyrosine phosphorylation in preimplantation embryo development. Biol Reprod 1991;45:711–8.

    Article  PubMed  CAS  Google Scholar 

  23. Paria BC, Jones KL, Flanders KC, Dey SK. Localization and binding of transforming growth factor-β isoforms in mouse preimplantation embryos, and in delayed and activated blastocysts. Dev Biol 1992;151:91–104.

    Article  PubMed  CAS  Google Scholar 

  24. Adamson ED, Deller MJ, Warshaw JB. Functional EGF receptors are pre¬sent on mouse embryo tissues. Nature 1981;291:656–9.

    Article  PubMed  CAS  Google Scholar 

  25. Adamson ED. EGF-receptor activity in mammalian development. Mol Reprod Dev 1990;27:16–22.

    Article  PubMed  CAS  Google Scholar 

  26. Simmen FA, Simmen RCM. Peptide growth factors and proto–oncogenes in mammalian conceptus development. Biol Reprod 1991;44:1–5.

    Article  PubMed  CAS  Google Scholar 

  27. Zhang Y, Paria BC, Dey SK, Davis DL. Characterization of the epidermal growth factor receptor in preimplantation pig conceptuses. Dev Biol 1992;151:617–21.

    Article  PubMed  CAS  Google Scholar 

  28. Wiley LM, Jie-Xin W, Harari I, Adamson ED. Epidermal growth factor receptor mRNA and protein increase after the four-cell preimplantation stage in murine development. Dev Biol 1992;149:247–60.

    Article  PubMed  CAS  Google Scholar 

  29. Heyner S, Smith RM, Schultz GA. Temporally regulated expression of insulin and insulin-like growth factors and their receptors in early mammalian development. Bioessays 1981;11:171–6.

    Article  Google Scholar 

  30. Rall LB, Scott J, Bell GI, et al. Mouse prepro-epidermal growth factor synthesis by the kidney and other tissues. Nature 1985;313:228–31.

    Article  PubMed  CAS  Google Scholar 

  31. Marquardt H, Hunkapillar MW, Hood LE, et al. Transforming growth factors produced by retrovirus transformed rodent fibroblasts and human melanoma cells: amino acid sequence homology with epidermal growth factor. Proc Natl Acad Sci USA 1983;80:4684–8.

    Article  PubMed  CAS  Google Scholar 

  32. Derynck R, Roberts AB, Winkler ME, Chen EY, Goeddel DV. Human transforming growth factor-α: precursor structure and expression in E. coli. Cell 1984;38:287–97.

    CAS  Google Scholar 

  33. Marquardt H, Hunkapiller MW, Hood LE, Todaro GJ. Rat transforming growth factor I: structure and relation to epidermal growth factor. Science 1984;223:1079–82.

    Article  PubMed  CAS  Google Scholar 

  34. Brown JP, Twardzik DR, Marquardt H, Todaro GJ. Vaccinia virus encodes a polypeptide homologues to epidermal growth factor and transforming growth factor. Nature 1985;313:491–2.

    Article  PubMed  CAS  Google Scholar 

  35. Pike LJ, Marquardt H, Todaro GJ, et al. Transforming growth factor and epidermal growth factor stimulate the phosphorylation of a synthetic, tyrosine-containing peptide in a similar manner. J Biol Chem 1982;257:14628–31.

    PubMed  CAS  Google Scholar 

  36. DeLarco JE, Todaro GJ. Sarcoma growth factor (SGF): specific binding to epidermal growth factor (EGF) membrane receptors. J Cell Physiol 1980;102:267–77.

    Article  CAS  Google Scholar 

  37. Margolis BL, Lax I, Kris R, et al. All autophosphorylation sites of epidermal growth factor receptor and HER2/neuare located in their carboxy-terminal tails. J Biol Chem 1989;264:10667–71.

    PubMed  CAS  Google Scholar 

  38. Cohen S, Carpenter G, King L, Jr. Epidermal growth factor-receptor-protein kinase interactions. Copurification of receptor and epidermal growth factor enhanced phosphorylation activity. J Biol Chem 1980;255:4834–42.

    PubMed  CAS  Google Scholar 

  39. Ushiro H, Cohen S. Identification of phosphotyrosine as a product of epidermal growth factor–activated protein kinase in A-431 cell membrane. J Biol Chem 1980;255:8363–5.

    PubMed  CAS  Google Scholar 

  40. Buhrow SA, Cohen S, Staros JV. Affinity labeling of the protein kinase associated with the epidermal growth factor receptor in membrane vesicle from A431 cells. J Biol Chem 1982;257:4019–22.

    PubMed  CAS  Google Scholar 

  41. Ullrich A, Coussens L, Hayflick JS, et al. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 1984;309:418–25.

    Article  PubMed  CAS  Google Scholar 

  42. Cummings RD, Soderquist AM, Carpenter G. The oligosaccharide moieties of the epidermal growth factor receptor in A431 cells: presence of complex-type N-linked chains that contain terminal N–acetylgalactosamine residues. J Biol Chem 1985;260:11944–52.

    PubMed  CAS  Google Scholar 

  43. Weber W, Bertics PJ, Gill GN. Immunoaffinity purification of the epidermal growth factor receptor: stoichiometry of binding and kinetics of self–phosphorylation. J Biol Chem 1984;259:14631–6.

    PubMed  CAS  Google Scholar 

  44. Downward J, Parker P, Waterfield MD. Autophosphorylation sites on the epidermal growth factor receptor. Nature 1984;311:483–5.

    Article  PubMed  CAS  Google Scholar 

  45. Hunter T, Cooper JA. Epidermal growth factor induces rapid tyrosine phosphorylation of proteins in A431 human tumor cells. Cell 1981;24:741–52.

    Article  PubMed  CAS  Google Scholar 

  46. Carpenter G, King L, Jr, Cohen S. Rapid enhancement of protein phosphorylation in A431 cell membrane preparations by epidermal growth factor. J Biol Chem 1979;254:2882–91.

    Google Scholar 

  47. Schlessinger J. Allosteric regulation of the epidermal growth factor receptor kinase. J Cell Biol 1986;103:2067–72.

    Article  PubMed  CAS  Google Scholar 

  48. Wong ST, Winchell LF, McCune BK, et al. The TGF-α precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell 1989;56:495–506.

    Article  PubMed  CAS  Google Scholar 

  49. Massague J. Transforming growth factor-α: a model for membrane-anchored growth factors. J Biol Chem 1990;265:21393–6.

    PubMed  CAS  Google Scholar 

  50. Derynck R. Transforming growth factor–a. Mol Reprod Dev 1990;27:3–9.

    Article  PubMed  CAS  Google Scholar 

  51. Huet-Hudson YM, Chakraborty C, De SK, Suzuki Y, Andrews GK, Dey SK. Estrogen regulates synthesis of EGF in mouse uterine epithelial cells. Mol Endocrinol 1990;4:510–23.

    Article  PubMed  CAS  Google Scholar 

  52. Paria BC, Das SK, Andrews GK, Dey SK. Expression of the epidermal growth factor receptor gene is regulated in mouse blastocysts during delayed implantation. Proc Natl Acad Sci USA 1993;90:55–9.

    Article  PubMed  CAS  Google Scholar 

  53. McCune BK, Prokop CA, Earp HS. Transient epidermal growth factor (EGF)-dependent suppression of EGF receptor autophosphorylation during internalization. J Biol Chem 1990;265:9715–21.

    PubMed  CAS  Google Scholar 

  54. Gaudette MF, Crain WR. A simple method for quantifying specific mRNAs in small numbers of early mouse embryos. Nucleic Acids Res 1991;19:1879–84.

    Article  PubMed  CAS  Google Scholar 

  55. Andrews GK, Huet-Hudson YM, Paria BC, McMaster MT, Das SK, Dey SK. Metallothionein gene expression and metal regulation during preimplantation mouse embryo development. Dev Biol 1991; 145:13–27.

    Article  PubMed  CAS  Google Scholar 

  56. Petch LA, Harris J, Raymond VW, Blasband A, Lee D, Earp HS. A truncated, secreted form of the epidermal growth factor receptor is encoded by an alternatively spliced transcript in normal rat tissue. Mol Cell Biol 1990;10:2973–82.

    PubMed  CAS  Google Scholar 

  57. Weitlauf HM, Kiessling AA, Buschman R. Comparison of DNA polymerase activity and cell division in normal and delayed-implanting mouse embryos. J Exp Zool 1979;209:467–72.

    Article  PubMed  CAS  Google Scholar 

  58. Carpenter G. Receptors for epidermal growth factor and other polypeptide mitogens. Annu Rev Biochem 1987;56:881–914.

    Article  PubMed  CAS  Google Scholar 

  59. Decker SJ. Aspects of the metabolism of the epidermal growth factor receptor in A431 human epidermoid carcinoma cells. Mol Cell Biol 1984;4:571–5.

    PubMed  CAS  Google Scholar 

  60. Weitlauf HM. Effect of actinomycin D on protein synthesis by delayed implanting mouse embryos in vitro. J Exp Zool 1974;189:197–202.

    Article  PubMed  CAS  Google Scholar 

  61. Weitlauf HM, Kiessling AA. Comparison of overall rates of RNA synthesis in implanting and delayed implanting mouse blastocysts in vitro. Dev Biol 1980;77:116–29.

    Article  PubMed  CAS  Google Scholar 

  62. McLaren A . Blastocyst activation. In: Segal SJ, Crozier R, Corfman RA, Condliffe PG, eds. The regulation of mammalian reproduction. Springfield, CT: Thomas, 1973:321–8.

    Google Scholar 

  63. Menke TM, McLaren A. Carbon dioxide production by mouse blastocysts during lactational delay of implantation or after ovariectomy. J Endocrinol 1970;47:287–94.

    Article  PubMed  CAS  Google Scholar 

  64. Weitlauf HM. A comparison of rates of accumulation of nonpolyadenylated and polyadenylated RNA in normal and delayed implanting mouse embryos. Dev Biol 1982;93:266–71.

    Article  PubMed  CAS  Google Scholar 

  65. Giebelhaus DH, Weitlauf HM, Schultz GA. Actin mRNA content in normal and delayed implanting mouse embryos. Dev Biol 1985;107:407–13.

    Article  PubMed  CAS  Google Scholar 

  66. Weitlauf HM. Changes in the role of translation with reactivation of delayed implanting mouse embryos. J Exp Zool 1985;236:309–12.

    Article  PubMed  CAS  Google Scholar 

  67. Dardik A, Schultz RM. Blastocoel expansion in the preimplantation mouse embryo: stimulatory effect of transforming growth factor-α and epidermal growth factor. Development 1991;113:919–30.

    PubMed  CAS  Google Scholar 

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Authors
  1. S. K. Dey
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  2. B. C. Paria
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  3. S. K. Das
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  4. G. K. Andrews
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Editor information

Editors and Affiliations

  1. Department of Physiology, University of Kansas Medical Center, 66160, Kansas City, KS, USA

    Michael J. Soares Ph.D.

  2. Department of Biology, Sinsheimer Laboratories, University of California, 95064, Santa Cruz, CA, USA

    Frank Talamantes Ph.D.

  3. Division of Endocrinology, Children’s Hospital Medical Center, 45229, Cincinnati, OH, USA

    Stuart Handwerger M.D.

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© 1993 Springer-Verlag New York, Inc.

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Dey, S.K., Paria, B.C., Das, S.K., Andrews, G.K. (1993). Trophoblast-Uterine Interactions in Implantation: Role of Transforming Growth Factor α/Epidermal Growth Factor Receptor Signaling. In: Soares, M.J., Talamantes, F., Handwerger, S. (eds) Trophoblast Cells. Serono Symposia, USA Norwell, Massachusetts. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-2718-2_5

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  • DOI: https://doi.org/10.1007/978-1-4612-2718-2_5

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4612-7641-8

  • Online ISBN: 978-1-4612-2718-2

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