Skip to main content

Epidermal Growth Factor Up-Regulates Human Cytotrophoblast Invasion

  • Conference paper
Molecular and Cellular Aspects of Periimplantation Processes

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

  • 72 Accesses

Abstract

Successful development of the human fetus is contingent on the formation of cytotrophoblast cell columns that anchor the placenta to the uterus. Cytotrophoblasts, the specialized epithelial cells of the placenta, have the ability to differentiate along one of two pathways. In one pathway cytotrophoblasts detach from their basement membrane and fuse to form the multinucleate syncytium covering the floating chorionic villi. These cells are in direct contact with maternal blood and function in gas and nutrient exchange for the fetus. In the other pathway cytotrophoblasts also detach from their basement membrane and then aggregate to form the anchoring villi, multilayered columns of individual cells that adhere to the uterus. Cytotrophoblasts in the columns ultimately invade the decidua, the inner third of the myometrium, and the arterioles that supply these areas.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Fisher SJ, Damsky CH. Human cytotrophoblast invasion. Semin Cell Biol 1993; 4: 183–8.

    Article  PubMed  CAS  Google Scholar 

  2. Fisher SJ, Cui TY, Hartman L, et al. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 1989; 109: 891–902.

    Article  PubMed  CAS  Google Scholar 

  3. Bass KE, Morrish D, Roth I, et al. Human cytotrophoblast invasion is up-regulated by epidermal growth factor: evidence that paracrine factors modify this process. Dev Biol 1994; 164: 550–61.

    Article  PubMed  CAS  Google Scholar 

  4. Hofmann GE, Drews MR, Scott RTJ, Navot D, Heller D, Deligdisch L. Epidermal growth factor and its receptor in human implantation trophoblast: immunohistochemical evidence for autocrine/paracrine function. J Clin Endocrinol Metab 1992; 4: 981–8.

    Article  Google Scholar 

  5. 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: 1377–82.

    PubMed  CAS  Google Scholar 

  6. Hofmann GE, Horowitz GM, Scott RTJ, Navot D. Transforming growth factor-α in human implantation trophoblast: immunohistochemical evidence for autocrine/paracrine function. J Clin Endocrinol Metab 1993; 76: 781–5.

    Article  PubMed  CAS  Google Scholar 

  7. Hofmann GE, Scott RT, Bergh PA, Deligdisch L. Immunohistochemical localization of epidermal growth factor in human endometrium, decidua, and placenta. J Clin Endocrinol Metab 1991; 73: 882–7.

    Article  PubMed  CAS  Google Scholar 

  8. Hirata Y, Moore GW, Bertagna C, Orth DN. Plasma concentrations of immunoreactive human epidermal growth factor (urogastrone) in man. J Clin Endocrinol Metab 1980; 50: 440–4.

    Article  PubMed  CAS  Google Scholar 

  9. Maruo T, Matsuo H, Oishi T, Hayashi M, Nishino R, Mochizuki M. Induction of differentiated trophoblast function by epidermal growth factor, relation of immunohistochemically detected cellular epidermal growth factor receptor levels. J Clin Endocrinol Metab 1987; 64: 744–50.

    Article  PubMed  CAS  Google Scholar 

  10. Haining REB, Schofield JP, Jones D, Rajput-Williams J, Smith SK. Identification of mRNA for epidermal growth factor and transforming growth factor-a present in low copy number of human endometrium and decidua using reverse transcriptase-polymerase chain reaction. J Mol Endocrinol 1991; 6: 207–14.

    Article  PubMed  CAS  Google Scholar 

  11. Librach CL, Feigenbaum SL, Bass KE, et al. Interleukin-1β regulates human cytotrophoblast metalloproteinase activity and invasion in vitro. J Biol Chem 1994; 269: 17125–31.

    PubMed  CAS  Google Scholar 

  12. Kameda T, Matsuzaki N, Sawai K, et al. Production of interleukin-6 by normal human trophoblast. Placenta 1990; 3: 205–13.

    Article  Google Scholar 

  13. Nishino E, Matsuzaki N, Masuhiro K, et al. Trophoblast-derived interleukin-6 (IL-6) regulates human chorionic gonadotropin release through IL-6 receptors on human trophoblasts. J Clin Endocrinol Metab 1990; 71: 436–41.

    Article  PubMed  CAS  Google Scholar 

  14. Kauma S, Matt D, Strom S, Eierman D, Turner T. Interleukin-10 (IL-1ß, HLA-DR-α and transforming growth factor-β (TGF-β) expression in endometrium, placenta, and placental membranes. Am J Obstet Gynecol 1990; 163: 1430–7.

    PubMed  CAS  Google Scholar 

  15. Dungy LI, Siddiqui TA, Khan S. Transforming growth factor-β1 expression during placental development. Am J Obstet Gynecol 1991; 165: 853–7.

    PubMed  CAS  Google Scholar 

  16. Wang C, Daimon M, Shen S, Engelmann GL, Ilan J. Insulin-like growth factor-I messenger ribonucleic acid in the developing human placenta and in term placenta of diabetics. Mol Endocrinol 1988; 2: 217–29.

    Article  PubMed  CAS  Google Scholar 

  17. Ohlsson R, Larsson E, Nilsson O, Wahlstrom T, Sundstrom P. Blastocyst implantation precedes induction of insulin-like growth factor II gene expression in human trophoblasts. Development 1989; 106: 555–9.

    PubMed  CAS  Google Scholar 

  18. Kauma SW, Aukerman SL, Eierman D, Turner T. Colony-stimulating factor-1 and c-fms expression in human endometrial tissues and placenta during the menstrual cycle and early pregnancy. J Clin Endocrinol Metab 1991; 3: 746–51.

    Article  Google Scholar 

  19. Saji F, Azuma C, Kimura T, Koyama M, Ohashi K, Tanizawa O. Gene expression of macrophage colony-stimulating factor and its receptor in human placenta and decidua. Am J Reprod Immunol 1990; 24: 99–104.

    PubMed  CAS  Google Scholar 

  20. Starkey PM, Sargent IL, Redman CWG. Cell populations in human early pregnancy decidua, characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 1988; 65: 129–34.

    PubMed  CAS  Google Scholar 

  21. Daiter E, Pampfer S, Yeung YG, Barad D, Stanley ER, Pollard JW. Expression of colony-stimulating factor-1 in the human uterus and placenta. J Clin Endocrinol Metab 1992; 74: 850–8.

    Article  PubMed  CAS  Google Scholar 

  22. Pampfer S, Daiter E, Barad D, Pollard JW. Expression of the colony-stimulating factor-1 receptor (c-fms proto-oncogene product) in the human uterus and placenta. Biol Reprod 1992; 46: 48–57.

    Article  PubMed  CAS  Google Scholar 

  23. Morrish DW, Bhardwaj D, Dabbagh L, Marusyk H, Siy O. Epidermal growth factor induces differentiation and secretion of human chorionic gonadotropin and placental lactogen in normal human placenta. J Clin Endocrinol Metab 1987; 65: 1282–90.

    Article  PubMed  CAS  Google Scholar 

  24. Morrish DW, Bhardwaj D, Paras MT. Transforming growth factor 131 inhibits placental differentiation and human chorionic gonadotropin and human placental lactogen secretion. Endocrinology 1991; 129: 22–6.

    Article  PubMed  CAS  Google Scholar 

  25. Barnea ER, Feldman D, Kaplan M, Morrish DW. The dual effect of epidermal growth factor upon human chorionic gonadotropin secretion by the first trimester placenta in vitro. J Clin Endocrinol Metab 1990; 71: 923–8.

    Article  PubMed  CAS  Google Scholar 

  26. Morrish DW, Honore LH, Bhardwaj D. Partial hydatidiform moles have impaired differentiated function (human chorionic gonadotropin and human placental lactogen secretion) in response to epidermal growth factor and 8bromo-cyclic adenosine monophosphate. Am J Obstet Gynecol 1992; 166: 160–6.

    PubMed  CAS  Google Scholar 

  27. Librach CL, Werb Z, Fitzgerald ML, et al. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 1991; 113: 437–9.

    Article  PubMed  CAS  Google Scholar 

  28. Zhou Y, Damsky CH, Chiu K, Roberts JM, Fisher SJ. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 1993; 91: 950–60.

    Article  PubMed  CAS  Google Scholar 

  29. Callegari C, Laborde NP, Buenaflor G, Nascimento CD, Brasel, JA, Fisher DA. The source of urinary epidermal growth factor in humans. Eur J Appl Physiol 1988; 58: 26–31.

    Article  CAS  Google Scholar 

  30. Lin PH, Sellinfreund R, Wakshull E. Rapid and efficient purification of plasma membrane from cultured cells: characterization of epidermal growth factor binding. Biochemistry 1987; 26: 731–6.

    Article  PubMed  CAS  Google Scholar 

  31. Payraste B, Plantavid M, Etievan C, et al. Characterization of plasma membranes from A431 cells, isolated by self-generating Percoll gradient: a rapid isolation procedure to obtain plasma membranes with functional epidermal growth factor receptors. Biochim Biophys Acta 1988; 939: 355–65.

    Article  Google Scholar 

  32. Berkers JA, Van Bergen en Henegouwen PM, Verkleij AJ, Boonstra J. Membrane vesicles of A431 cells contain one class of epidermal growth factor binding sites. Biochim Biophys Acta 1990; 1052: 453–60.

    Article  PubMed  CAS  Google Scholar 

  33. 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 

  34. Bass KE, Roth I, Damsky CH, Fisher SJ. The regulation of human cytotrophoblast invasion. In: Wolf DP, Stouffer RL, Brenner RM, eds. In vitro fertilization and embryo transfer in primates. New York: Springer-Verlag, 1993: 182–94.

    Chapter  Google Scholar 

  35. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979; 76: 4350–4.

    Article  PubMed  CAS  Google Scholar 

  36. Down JA, Kawakami M, Klein MH, Dorrington KJ. Proteins associated with activity of Fc receptors on isolated human placental syncytiotrophoblast microvillous plasma membranes. Placenta 1989; 10: 227–46.

    Article  PubMed  CAS  Google Scholar 

  37. Rall LR, Scott J, Bell GI, et al. Mouse preproepidermal growth factor synthesis by the kidney and other tissues. Nature 1985; 313: 228–31.

    Article  PubMed  CAS  Google Scholar 

  38. Hershman HR. Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem 1991; 60: 2811–3119.

    Google Scholar 

  39. Di Marco E, Pierce JH, Aaronson SA, Di Fiore PP. Mechanisms by which EGF and TGF-α contribute to malignant transformation. Nat Immun Cell Growth Regul 1990; 9: 209–21.

    PubMed  Google Scholar 

  40. Yasui W, Hata J, Yokozaki H, et al. Interaction between epidermal growth factor and its receptor in progression of human gastric carcinoma. Int J Cancer 1988; 41: 211–7.

    Article  PubMed  CAS  Google Scholar 

  41. Tahara E, Sumiyoshi H, Hata J, et al. Human gastric carcinoma as a biologic marker of high malignancy. Jpn J Cancer Res 1986; 77: 145–52.

    PubMed  CAS  Google Scholar 

  42. Carpenter G. Epidermal growth factor: biology and receptor metabolism. J Cell Sci Suppl 1985; 3: 1–9.

    PubMed  CAS  Google Scholar 

  43. Silver MH, Murray JC, Pratt RM. Epidermal growth factor stimulates type-V collagen synthesis in cultured murine palatal shelves. Differentiation 1984; 27: 205–8.

    Article  PubMed  CAS  Google Scholar 

  44. Yoneda T, Pratt RM. Mesenchymal cells from the human embryonic palate are highly responsive to epidermal growth factor. Science 1981; 213: 563–5.

    Article  PubMed  CAS  Google Scholar 

  45. Hertel C, Perkins JP. Sequential appearance of epidermal growth factor in plasma membrane-associated and intracellular vesicles during endocytosis. J Biol Chem 1987; 262: 11407–9.

    PubMed  CAS  Google Scholar 

  46. Carpenter G, Cohen S. Epidermal growth factor. J Biol Chem 1990; 265: 7709–12.

    PubMed  CAS  Google Scholar 

  47. Matrisian LM, Hogan BLM. Growth factor-regulated proteases and extracellular matrix remodeling during mammalian development. Curr Top Dev Biol 1990; 24: 219–59.

    Article  PubMed  CAS  Google Scholar 

  48. Adamson ED. Growth factors and their receptors in development. Dev Genet 1993; 14: 159–64.

    Article  PubMed  CAS  Google Scholar 

  49. Rappolee DA, Mark D, Banda MJ, Werb Z. Wound macrophages express TGFa and other growth factors in vivo: analysis by mRNA phenotyping. Science 1988; 24: 708–12.

    Article  Google Scholar 

  50. Wiley LM, Wu J, Harai I, Adamson ED. Initiation of epidermal growth factor-receptor gene activity occurs at the two-to four-cell preimplantation stage in murine development. Dev Biol 1992; 149: 247–60.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  52. Darkik A, Smith RM, Schultz RM. Colocalization of transforming growth factor-alpha and a functional epidermal growth factor receptor (EGFR) to the inner cell mass and preferential localization of the EGFR on the basolateral surface of the trophectoderm in the mouse blastocyst. Dev Biol 1992; 154: 396–409.

    Article  Google Scholar 

  53. 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 

  54. Wood SA, Kaye PL. Effects of epidermal growth factor on preimplantation embryos. J Reprod Fertil 1989; 85: 575–81.

    Article  PubMed  CAS  Google Scholar 

  55. 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 

  56. Brice EC, Wu JX, Muraro R, Adamson ED, Wiley LM. Modulation of mouse preimplantation development by epidermal growth factor receptor antibodies, antisense RNA, and deoxyoligonucleotides. Dev Genet 1993; 14: 174–84.

    Article  PubMed  CAS  Google Scholar 

  57. Haimovici F, Anderson DJ. Effects of growth factors and growth factorextracellular matrix interactions on mouse trophoblast outgrowth in vitro. Biol Reprod 1993; 49: 124–30.

    Article  PubMed  CAS  Google Scholar 

  58. Tavare JM, Holmes CH. Differential expression of the receptors for epidermal growth factor and insulin in the developing human placenta. Cell Signal 1989; 1: 55–64.

    Article  PubMed  CAS  Google Scholar 

  59. Muhlhauser J, Crescimanno C, Kaufmann P, Höfler H, Zaccheo D, Castellucci M. Differentiation and proliferation patterns in human trophoblast revealed by c-erbB-2 oncogene product and EGF-R. J Histochem Cytochem 1993; 41: 165–73.

    Article  PubMed  CAS  Google Scholar 

  60. Bissonnette F, Cook C, Geoghegan T, et al. Transforming growth factor-a and epidermal growth factor messenger ribonucleic acid and protein levels in human placentas from early, mid, and late gestation. Am J Obstet Gynecol 1992; 166: 192–9.

    PubMed  CAS  Google Scholar 

  61. Arnholdt H, Diebold J, Kuhlmann B, Lohrs U. Receptor-mediated processing of epidermal growth factor in the trophoblast of the human placenta. Virchows Arch [B] 1991; 61: 75–80.

    Article  CAS  Google Scholar 

  62. Mirlesse V, Alsat E, Fondacci C, Evain-Brion D. Epidermal growth factor receptors in cultured human trophoblast cells from first-and third-trimester placentas. Horm Res 1990; 34: 234–9.

    Article  PubMed  CAS  Google Scholar 

  63. Alsat E, Mirlesse V, Fondacci C, Dodeur M, Evain-Brion D. Parathyroid hormone increases epidermal growth factor receptors in cultured human trophoblastic cells from early and term placenta. J Clin Endocrinol Metab 1991; 73: 288–95.

    Article  PubMed  CAS  Google Scholar 

  64. Alsat E, Haziza J, Evain-Brion D. Increase in epidermal growth factor receptor and its messenger ribonucleic acid levels with differentiation of human trophoblast cells in culture. J Cell Physiol 1993; 154: 122–8.

    Article  PubMed  CAS  Google Scholar 

  65. Lei ZM, Rao CV. Expression of epidermal growth factor (EGF) receptor and its ligands, EGF and transforming growth factor-a, in human fallopian tubes. Endocrinology 1992; 131: 947–57.

    Article  PubMed  CAS  Google Scholar 

  66. Haining REB, Schofield JP, Jones DSC, Rajput-Williams J, Smith SK. Identification of mRNA for epidermal growth factor and transforming growth factor-α present in low copy number of human endometrium and decidua using reverse transcriptase-polymerase chain reaction. J Mol Endocrinol 1991; 6: 207–14.

    Article  PubMed  CAS  Google Scholar 

  67. Chegini N, Rossi MJ, Masterson BJ. Platelet-derived growth factor (PDGF), epidermal growth factor (EGF), and EGF and PDGF β-receptors in human endometrial tissue: localization and in vitro action. Endocrinology 1992; 30: 2373–85.

    Article  Google Scholar 

  68. Genbacev O, Powlin SS, Miller RK. Regulation of human extravillous trophoblast (EVT) cell differentiation and proliferation in vitro: role of epidermal growth factor (EGF). In: Miller RK, Thiede HA, eds. HIV, perinatal infections and therapy: the role of the placenta. Trophoblast Research; vol 8. Rochester, NY: University of Rochester Press, 1994: 427–42.

    Google Scholar 

  69. Truman P, Ford HC. The effect of substrate and epidermal growth factors on human placental trophoblast cells in culture. In Vitro Cell Dev Biol 1986; 22: 525–8.

    Article  PubMed  CAS  Google Scholar 

  70. 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: 1362–7.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer-Verlag New York, Inc.

About this paper

Cite this paper

Bass, K.E., Morrish, D.W., Roth, I., Bhardwaj, D., Taylor, R.N., Fisher, S.J. (1995). Epidermal Growth Factor Up-Regulates Human Cytotrophoblast Invasion. In: Dey, S.K. (eds) Molecular and Cellular Aspects of Periimplantation Processes. Serono Symposia USA. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-2548-5_20

Download citation

  • DOI: https://doi.org/10.1007/978-1-4612-2548-5_20

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4612-7575-6

  • Online ISBN: 978-1-4612-2548-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics