[en] Trophoblast differentiation is a key event in human placental development. During extravillous trophoblast (EVT) differentiation, stem cells from the anchoring villi detach from their basement membrane and proliferate to form aggregates called trophoblast cell columns (TCCs). They subsequently invade the decidua and differentiate into interstitial and endovascular trophoblasts. The influence of the decidua on EVT differentiation is controversial. We therefore compared the pattern of trophoblast differentiation marker expression in viable intrauterine and tubal pregnancies, as decidual cell markers (prolactin [PRL] and insulin-like growth factor binding Protein-1 [IGFBP1]) were only expressed in endometrial implantation sites. Extravillous trophoblast differentiation in anchoring villi from uterine and ectopic pregnancies exhibited a comparable phenotypical switch: alpha6 integrin subunit, E-cadherin, EGF receptor, Ki 67 and connexin 40 were localized in the proximal part of the TCC, while alpha5beta1 and alpha1 integrins, c-erb B2, hPL and HLA-G were expressed by invasive cytotrophoblasts. The cyclin-dependent kinase inhibitors p16 and p57 were mainly detected in invasive cytotrophoblasts some distance from the columns. However, the TCC was markedly longer in tubal pregnancy than in intrauterine pregnancy. These findings suggest that the decidua is not necessary to trigger EVT invasion, but that it is likely to limit the extent of the TCC and to accelerate the onset of EVT migration.
Disciplines :
Immunology & infectious disease
Author, co-author :
Goffin, Frédéric ; Centre Hospitalier Universitaire de Liège - CHU > Gynécologie-Obstétrique CHR
Munaut, Carine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Malassine, A.
Evain-Brion, D.
Frankenne, Francis
Fridman, Viviana ; Centre Hospitalier Universitaire de Liège - CHU > Anatomie pathologique
Dubois, Michel ; Université de Liège - ULiège > Services généraux (Faculté de médecine) > Relations académiques et scientifiques (Médecine)
Uzan, S.
Merviel, P.
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique
Language :
English
Title :
Evidence of a limited contribution of feto-maternal interactions to trophoblast differentiation along the invasive pathway
Publication date :
August 2003
Journal title :
Tissue Antigens
ISSN :
0001-2815
eISSN :
1399-0039
Publisher :
International Booksellers Publishers, Copenhagen, Denmark
Redman CW. Cytotrophoblasts: masters of disguise. Nat Med 1997: 3: 610-1.
Benirschke K, Kaufmann P. Pathology of the Human Placenta 4th edn. New York: Springer, 2000.
Aplin JD. Implantation, trophoblast differentiation and hemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 1991: 99: 681-92.
Tarrade A, Lai Kuen R, Malassine A, et al. Characterization of human villous and extravillous trophoblasts isolated from first trimester placenta. Lab Invest 2001: 81: 1199-211.
Fisher SJ. The placenta dilemma. Semin Reprod Med 2000: 18: 321-6.
Genbacev O, McMaster MT, Fisher SJ. A repertoire of cell cycle regulators whose expression is coordinated with human cytotrophoblast differentiation. Am J Pathol 2000: 157: 1337-51.
Damsky CH, Librach C, Lim KH, et al. Integrin switching regulates normal trophoblast invasion. Development 1994: 120: 3657-66.
Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: key pieces of the development puzzle. Science 1994: 266: 1508-18.
Strickland S, Richards WG. Invasion of the trophoblasts. Cell 1992: 71: 355-7.
Bischof P, Meisser A, Campana A. Biochemistry and molecular biology of trophoblast invasion. Ann N Y Acad Sci 2001: 943: 157-62.
Ramsey EM, Houston ML, Harris JW. Interactions of the trophoblast and maternal tissues in three closely related primate species. Am J Obstet Gynecol 1976: 124: 647-52.
Loke YW, King A, eds. Human Implantation. Cell Biology and Immunology, 1st edn. Cambridge, UK: Cambridge University Press, 1995.
Enders AC. Current topic: structural responses of the primate endometrium to implantation. Placenta 1991: 12: 309-25.
Wewer UM, Faber M, Liotta LA, Albrechtsen R. Immunochemical and ultrastructural assessment of the nature of the pericellular basement membrane of human decidual cells. Lab Invest 1985: 53: 624-33.
Aplin JD, Charlton AK, Ayad S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy. Cell Tissue Res 1988: 253: 231-40.
Loke YW, King A, Burrows TD. Decidua in human implantation. Hum Reprod 1995: 10: 14-21.
Aplin J. Maternal influences on placental development. Semin Cell Dev Biol 2000: 11: 115-25.
Irwin JC, Giudice LC. Insulin-like growth factor binding protein-1 binds to placental cytotrophoblast alpha5beta1 integrin and inhibits cytotrophoblast invasion into decidualized endometrial stromal cultures. Growth Horm IGF Res 1998: 8: 21-31.
Schatz F, Papp C, Toth-Pal E et al. Protease and protease inhibitor expression during in vitro decidualization of human endometrial stromal cells. Ann N Y Acad Sci 1994: 734: 33-42.
Gleeson LM, Chakraborty C, McKinnon T, Lala PK. Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through alpha 5 beta 1 integrin via mitogen-activated protein Kinase pathway. J Clin Endocrinol Metab 2001: 86: 2484-93.
Bischof P, Meisser A, Campana A, Tseng L. Effects of decidua-conditioned medium and insulin-like growth factor binding protein-1 on trophoblastic matrix metalloproteinases and their inhibitors. Placenta 1998: 19: 457-64.
Bischof P, Meisser A, Campana A. Paracrine and autocrine regulators of trophoblast invasion - a review. Placenta 2000: 21: S55-60.
Spornitz UM. Pseudo-decidualization at the site of implantation in tubal pregnancy. Arch Gynecol Obstet 1993: 253: 85-95.
Proll J, Bensussan A, Coffin F, Foidart JM, Berrebi A, Le Bouteiller P. Tubal versus uterine placentation: similar HLA-G expressing extravillous cytotrophoblast invasion but different maternal leukocyte recruitment. Tissue Antigens 2000: 56: 479-91.
Floridon C, Nielsen O, Holund B et al. Does plasminogen activator inhibitor-1 (PAI-1) control trophoblast Invasion? A study of fetal and maternal tissue in intrauterine, tubal and molar pregnancies. Placenta 2000: 21: 754-62.
Ali SM, Sakbun V, Hansell DJ, Jara CS, Greenwood FC, Bryant-Greenwood GD. The localization of prolactin and its mRNA in the human fetal membranes, decidua and placenta. Trophoblast Res 1991: 5: 89-102.
Sakbun V, Koay ES, Bryant-Greenwood GD. Immunocytochemical localization of prolactin and relaxin C-peptide in human decidua and placenta. J Clin Endocrinol Metab 1987: 65: 339-43.
Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 1992: 89: 210-22.
Bulmer JN, Morrison L, Johnson PM. Expression of the proliferation markers Ki67 and transferrin receptor by human trophoblast populations. J Reprod Immunol 1988: 14: 291-302.
Muhlhauser J, Crescimanno C, Kaufmann P, Hofler 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.
Jokhi PP, King A, Loke YW. Reciprocal expression of epidermal growth factor receptor (EGF-R) and c-erbB2 by non-invasive and invasive human trophoblast populations. Cytokine 1994: 6: 433-42.
Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990: 248: 220-3.
McMaster MT, Librach CL, Zhou Y et al. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol 1995: 154: 3771-8.
Kurman RJ, Main CS, Chen HC. Intermediate trophoblast: a distinctive form of trophoblast with specific morphological, biochemical and functional features. Placenta 1984: 5: 349-69.
Earl U, Wells M, Bulmer JN. Immunohistochemical characterisation of trophoblast antigens and secretory products in ectopic tubal pregnancy. Int J Gynecol Pathol 1986: 5: 132-42.
Chemnitz J, Tornehave D, Teisner B, Poulsen HK, Westergaard JG. The localization of pregnancy proteins (hPL, SP1 and PAPP-A) in intra- and extrauterine pregnancies. Placenta 1984: 5: 489-94.
Lala PK, Hamilton GS. Growth factors, proteases and protease inhibitors in the maternal-fetal dialogue. Placenta 1996: 17: 545-55.
Kirby DR. Development of mouse eggs beneath the kidney capsule. Nature 1960: 187: 707-8.
Bevilacqua E, Abrahamsohn PA. Invasiveness of mouse trophoblastic cells in connective tissue. Acta Anat 1994: 150: 246-52.
Bevilacqua EM, Abrahamsohn PA. Growth of mouse embryos implanted in the subcutaneous tissue of recipient mice. J Exp Zool 1991: 257: 386-400.
Robb L, Li R, Hartley L, Nandurkar HH, Koentgen F, Begley CG. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat Med 1998: 4: 303-8.
Aplin JD, Haigh T, Lacey H, Chen CP, Jones CJ. Tissue interactions in the control of trophoblast invasion. J Reprod Fertil Suppl 2000: 55: 57-64.
Lala PK, Graham CH. Mechanisms of trophoblast invasiveness and their control: the role of proteases and protease inhibitors. Cancer Metastasis Rev 1990: 9: 369-79.
Graham CH, Lala PK. Mechanism of control of trophoblast invasion in situ. J Cell Physiol 1991: 148: 228-34.
Aplin JD, Lacey H, Haigh T, Jones CJ, Chen CP, Westwood M. Growth factor-extracellular matrix synergy in the control of trophoblast invasion. Biochem Soc Trans 2000: 28: 199-202.
Pauerstein CJ, Croxatto HB, Eddy CA, Ramzy I, Waiters MD. Anatomy and pathology of tubal pregnancy. Obstet Gynecol 1986: 67: 301-8.
Randall S, Buckley CH, Fox H. Placentation in the fallopian tube. Int J Gynecol Pathol 1987: 6: 132-9.
Senterman M, Jibodh R, Tulandi T. Histopathologic study of ampullary and isthmic tubal ectopic pregnancy. Am J Obstet Gynecol 1988: 159: 939-41.
Fox H. Ectopic pregnancy. In: Fox H, Haines & Taylor eds. Obstetrical and Gynecologic Pathology, 4th edn, vol. 2. New York: Churchill Livingstone, 1995: 1113-36.
Loke YW, King A. Immunology of implantation. Baillieres Best Practice Residential Clinic. Obstet Gynaecol 2000: 14: 827-37.
Aplin JD. Expression of integrin alpha 6 beta 4 in human trophoblast and its loss from extravillous cells. Placenta 1993: 14: 203-15.
Babawale MO, Van Noorden S, Pignatelli M, Stamp GW, Elder MG, Sullivan MH. Morphological interactions of human first trimester placental villi co- cultured with decidual explants. Hum Reprod 1996: 11: 444-50.
Winterhager E, Von Ostau C, Gerke M, Gruemmer R, Traub O, Kaufmann P. Connexin expression patterns in human trophoblast cells during placental development. Placenta 1999: 20: 627-38.
Cronier L, Bastide B, Defamie N et al. Involvement of gap junctional communication and connexin expression in trophoblast differentiation of the human placenta. Histol Histopathol 2001: 16: 285-95.
Vicovac L, Jones CJ, Aplin JD. Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro. Placenta 1995: 16: 41-56.
Genbacev O, Schubach SA, Miller RK. Villous culture of first trimester human placenta - model to study extravillous trophoblast (EVT) differentiation. Placenta 1992: 13: 439-61.
