Skip to main content
Log in

Extracellular matrix components of the placental extravillous trophoblast: immunocytochemistry and ultrastructural distribution

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Invasive extraiillous trophoblast cells of the human placenta are embedded in a self-secreted extracellular matrix, the matrix-type fibrinoid. The ultrastructure and molecular composition of the matrix-type fibrinoid of the term human placenta were studied by transmission electron microscopy and immunogold labelling. We used antibodies directed against different matrix proteins such as collagen type IV, laminin, vitronectin, heparan sulfate, various fibronectin isoforms, and against the oncofetal blood group antigen, ‘i”. Immunogold labelling patterns of matrix proteins are the basis for the subdivision of the trophoblast-derived matrix-type fibrinoid into mosaiclike patches of structurally and immunocytochemically different comparments. Firstly, fine granular patches with structural similarities to basal lamina material are composed solely of collagen type IV and laminin. Secondly, an ultrastructurally amorphous glossy substance shown reactivity with antibodies against heparan sulfate and vitronectin. A third type of patches, fine fibrillar networks embedded in the above-mentioned glossy matrix, are reactive with antibodies against normal fibronectin isoforms (IST-4, IST-6, IST-9) and oncofetal isoforms (BC-1, FDC-6). The blood group precursor antigen “i” was not only expressed on the surfaces of the extravillous trophoblast cells but was associated with the fibronectinpositive fibrils. In conclusion, within this extracellular matrix, clear compartments of different composition can be distinguished from each other. Glycosylation with “i” in this matrix may be involved in immunological masking, thus preventing rejection of placenta and fetus.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aplin JD, Campbell S (1985) An immunofluorescence study of extracellular matrix associated with cytotrophoblast of the chorion laeve. Placenta 6:469–479

    PubMed  CAS  Google Scholar 

  • Benirschke K, Kaufmann P (1995) Pathology of the human placenta, 3rd ed. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Blanchard D, Bernard D, Loirat MJ, Frioux Y, Guimbretiere J, Guimbretriere L (1992) Characterization of murine monoclonal antibodies against fetal erythrocytes. Rev Fr Transfus Hemobiol 35:239–254

    Article  PubMed  CAS  Google Scholar 

  • Blankenship TN, King BF (1993) Developmental changes in the cell columns and trophoblastic shell of the macaque placenta: an immunohistochemical study localizing type IV collagen, laminin, fibronectin and cytokeratins. Cell Tissue Res 274:457–466

    Article  PubMed  CAS  Google Scholar 

  • Blankenship TN, Enders AC, King BF (1992) Distribution of laminin, type IV collagen, and fibronectin in the cell columns and trophoblastic shell of early macaque placentas. Cell Tissue Res 270:241–248

    Article  PubMed  CAS  Google Scholar 

  • Blankenship TN, Enders AC, King BF (1993) Trophoblastic invasion and the development of uteroplacental arteries in the macaque: immunohistochemical localization of cytokeratins desmin, type IV collagen, laminin, and fibronectin. Cell Tissue Res 272:227–236

    Article  PubMed  CAS  Google Scholar 

  • Brzosko W, Nowoslawski A, Pisarski I (1965) Immunohistochemical analysis of the fibrinoid masses in human placenta. Polim Med 5:114–123

    Google Scholar 

  • Carnemolla B, Borsi L, Zardi L, Owens RJ, Baralle FE (1987) Localization of the cellular fibronectin-specific epitope recognized by the monoclonal antibody IST-9 using fusion proteins expressed inE. coli. FEBS Lett 215:269–273

    Article  PubMed  CAS  Google Scholar 

  • Carnemolla B, Balza E, Siri A, Zardi L, Nicotra MR, Bigotti A, Natalli PG (1989) A tumor-associated fibronectin isoform generated by alternative splicing of messenger RNA precursors. J Cell Biol 108:1139–1148

    Article  PubMed  CAS  Google Scholar 

  • Carnemolla B, Leprini A, Allemanni G, Saginati M, Zardi L (1992) The inclusion of the type-III repeat ED-B in the fibronectin molecule generates conformational modifications that unmask a cryptic sequence. J Biol Chem 267:24689–24692

    PubMed  CAS  Google Scholar 

  • Castellani P, Siri A, Rosellini C, Infusini E, Borsi L, Zardi L (1986) Transformed human cells release different fibronectin variants than do normal cells. J Cell Biol 103:1671–1677

    Article  PubMed  CAS  Google Scholar 

  • Castellucci M, Crescimanno C, Schröter CA, Kaufmann P, Mühlhauser J (1993) Extravillous trophoblast: immunohistochemical localization of extracellular matrix molecules, In: Genazzani AR, Petraglia F, Genazzani AD (eds) Frontiers in gynecologic and obstetric investigation. Parthenon, New York, pp 19–25

    Google Scholar 

  • Damsky CH, Fitzgerald ML, Fisher SJ (1992) 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 89:210–222

    PubMed  CAS  Google Scholar 

  • Feinberg RF, Kliman HJ (1993) Tropho-uteronectin (TUN): a unique oncofetal fibronectin deposited in the extracellular matrix of the tropho-uterine junction and regulated in vitro by cultured human trophoblast cells. Trophoblast Res 7:167–181

    CAS  Google Scholar 

  • Feinberg RF, Kliman HJ, Lockwood CJ (1991) Is oncofetal fibronectin a trophoblast glue for human implantation? Am J Pathol 138:537–543

    PubMed  CAS  Google Scholar 

  • Flug M, Köpf-Maier P (1995) The basement membrane and its involvement in carcinoma cell invasion. Acta Anat 152:69–84

    PubMed  CAS  Google Scholar 

  • Frank H-G, Malekzadeh F, Kertschanska S, Crescimanno C, Castellucci M, Lang I, Desoye G, Kaufmann P (1994) Immunohistochemistry of two different types of placental fibrinoid. Acta Anat 150:55–68

    PubMed  CAS  Google Scholar 

  • Frank H-G, Huppertz B, Kertschanska S, Blanchard D, Roelcke D, Kaufmann P (1995) Anti-adhesive glycosylation of fibronectin-like molecules in human placental matrix-type fibrinoid. Histochem Cell Biol 104:317–329

    Article  PubMed  CAS  Google Scholar 

  • Huppertz B, Kertschanska S, Gaus G, Frank H-G, Kaufmann P (1995) Fibronectin-like immunoreactivities in the matrix-type fibrinoid of the human placenta. Placenta 16:A30

    Google Scholar 

  • Irving JA, Lysiak JJ, Graham CH, Hearn S, Han VKM, Lala PK (1995) Characteristics of trophoblast cells migrating from first trimester chorionic villus explants and propagated in culture. Placenta 16:413–433

    Article  PubMed  CAS  Google Scholar 

  • Kertschanska S, Frank H-G, Huppertz B, Funayama H, Kaufmann P (1995) Immunocytochemistry of matrix-type fibrinoid in the human placenta. Placenta 16:A34

    Google Scholar 

  • King BF, Blakenship TN (1993) Expression of proliferating cell nuclear antigen (PCNA) in developing macaque placentas. Placenta 14:A36

    Google Scholar 

  • King BF, Blankenship TN (1994a) Ultrastructure and development of a thick basement membrane-like layer in the anchroning villi of macaque placentas. Anat Rec 238:498–506

    Article  PubMed  CAS  Google Scholar 

  • King BF, Blankenship TN (1994b) Differentiation of the chorionic plate of the placenta: cellular and extracellular matrix changes during development in the macaque, Anat Res 240:267–276

    Article  CAS  Google Scholar 

  • King BF, Blankenship TN (1996) Immunohistochemical localization of fibrillin in developing macaque and term human placentas and fetal membranes. Microsc Res Tech (in press)

  • Lang I, Hartmann M, Blaschitz A, Dohr G, Kaufmann P, Frank H-G, Skofitsch G, Desoye G (1994) Differential lectin binding to the fibrinoid of human full term placenta: correlation with a fibrin antibody and the PAF-Halmi method. Acta Anat 150:170–177

    Article  PubMed  CAS  Google Scholar 

  • Malak TM, Ockleford CD, Bell SC, Dalgleish R, Bright N, Mac-Vicar J (1993) Confocal immunofluoresence localization of collagen type-I, type-III, type-IV, type-V and type VI and their ultrastructural organization in term human fetal membranes. Placenta 14:384–406

    Google Scholar 

  • Matsuura H, Hakomori S (1985) The oncofetal domain of fibronectin defined by monoclonal antibody FDC-6: its presence in fibronectins from fetal and tumor tissues and its absence in those from normal adult tissues and plasma. Proc Natl Acad Sci USA 82:6517–6521

    Article  PubMed  CAS  Google Scholar 

  • Moe N (1969) The deposits of fibrin and fibrin-like materials in the basal plate of the normal human placenta. Acta Pathol Microbiol Scand 75:1–17

    PubMed  CAS  Google Scholar 

  • Mosher DF, Sottile J, Wu C, McDonald JA (1992) Assembly of extracellular matrix. Curr Opin Cell Biol 4:810–818

    Article  PubMed  CAS  Google Scholar 

  • Nanaev AK, Milovanov AP, Domogatsky SP (1993) Immunohistochemical localization of extracellular matrix in perivillous fibrinoid of normal human term placenta. Histochemistry 100:341–346

    Article  PubMed  CAS  Google Scholar 

  • Pesciotta-Peters DM, Portz LM, Fullenwider J, Mosher DF (1990) Co-assembly of plasma and cellular fibronectins into fibrils in human fibroblast culture. J Cell Biol 111:249–256

    Article  Google Scholar 

  • Watanabe T, Araki M, Mimuro J, Tamada T, Sakata Y (1993) Fibrinolytic components in fetal membranes and amniotic fluid. Am J Obstet Gynecol 168:1283–1289

    PubMed  CAS  Google Scholar 

  • Zhu BC, Laine RA (1985) Polylactosamine glycosylation on human fetal placental fibronectin weakens the binding affinity of fibronectin to gelatin. J Biol Chem 260:4041–4045

    PubMed  CAS  Google Scholar 

  • Zhu BC, Fisher SF, Pande H, Calaycay J, Shively JE, Laine RA (1984) Human placental (fetal) fibronectin: increased glycosylation and higher protease resistance than plasma fibronectin. J Biol Chem 259:3962–3970

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huppertz, B., Kertschanska, S., Frank, H.G. et al. Extracellular matrix components of the placental extravillous trophoblast: immunocytochemistry and ultrastructural distribution. Histochem Cell Biol 106, 291–301 (1996). https://doi.org/10.1007/BF02473239

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02473239

Keywords

Navigation