Abstract
Recently, fibrinoid of the human placenta has been described as being composed of two main types differing in origin and chemical composition. Fibrin-type fibrinoid is mostly a blood clot product. Matrix-type fibrinoid was defined as the extracellular matrix secreted by extravillous trophoblast cells. The structure and composition of matrix-type fibrinoid was addressed in this study, focusing on fibronectins as one major constituent. A panel of antibodies directed against different fibronectin isoforms generated by different mRNA splicing, as well as antibodies recognizing oncofetal carbohydrate epitopes, were used on cryostat, paraffin and Lowicryl sections of placental tissue from different stages of pregnancy. The oncofetal carbohydrate epitopes studied comprised the blood group precursor antigens i and I. We identified the blood group-related antigen i as an additional marker for matrix-type fibrinoid. The antigen was detected on a glycoprotein that was also recognized by the fibronectin antibodies in western blots. Immunohistochemically this i-glycosylated oncofetal fibronectin-like molecule of about 55 kDa is expressed only by the invasive phenotype of extravillous trophoblast. Long chain carbohydrate moieties with a structure fulfilling the criteria for i reactivity on human placental fibronectin are known to have anti-adhesive properties and to enhance resistance of the protein chain to proteolysis. These properties underline the functional relevance of glycosylation of fibronectins in matrix-type fibrinoid and suggest matrix-type fibrinoid is a typical matrix of invasive cells. In contrast, the more mature blood group precursor I could be detected after sialidase pretreatment of sections. This antigen was expressed by villous, non-invasive trophoblast.
Similar content being viewed by others
References
Alitalo K, Vaheri A (1982) Pericellular matrix in malignant transformation. Adv Cancer Res 37:111–158
Amenta PS, Gay S, Vaheri A, Martinez Hernandez A (1986) The extracellular matrix is an integrated unit: ultrastructural localization of collagen types I, III, IV, V, VI, fibronectin, and laminin in human term placenta. Coll Relat Res 6:125–152
Aplin JD (1993) Expression of the integrin α6β4 in human trophoblast and its loss from extravillous cells. Placenta 14:203–215
Aplin JD, Campbell S (1985) An immunofluorescence study of extracellular matrix associated with cytotrophoblast of the chorion laeve. Placenta 6:469–479
Augustin Voss HG, Pauli BU (1992) Migrating endothelial cells are distinetly hyperglycosylated and express specific migration-associated cell surface glycoproteins. J Cell Biol 119:483–491
Benirschke K, Kaufmann P (1995) Pathology of the human placenta, 3rd edn. springer, New York
Blanchard D, Bernard D, Loirat MJ, Frioux Y, Guimbretiere J, Guimbretiere L (1992) Characterization of murine monoclonal antibodies against fetal erythrocytes. Rev Fr Transfus Hemobiol 35:239–254
Blankenship TN, King BF (1994) Identification of a 72 kD type IV collagenase at sites of trophoblastic invasion of Macaque spiral arteries. Placenta 15:177–187
Borsi L, Carnemolla B, Castellani P, Rossellini C, Vecchio D, Allemanni G, Chang SE, Taylor-Papadimitriou J, Pande H, Zardi L (1987) Monoclonal antibodies in the analysis of fibronectin isoforms generated by alternative splicing of mRNA precursors in normal and transformed human cells. J Cell Biol 104:595–600
Borsi L, Balza E, Leprini A, Ponassi M, Zardi L (1991) Procedure for the purification of the fibronectin proteolytic fragments containing the ED-B oncofetal domain. Anal Biochem 192: 372–379
Burrows TD, King A, Loke YW (1993) Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin. Hum Reprod 8:475–484
Burrows TD, King A, Loke YW (1994) Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells: implications for vascular invasion during implantation. Placenta 15:21–33
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
Carnemolla B, Balza E, Siri A, Zardi L, Nicotra MR, Bigotti A, Natali PG (1989) A tumor-associated fibronectin isoform generated by alternative splicing of messenger RNA precursors. J Cell Biol 108:1139–1148
Castellucci M, Crescimanno C, Mühlhauser J, Frank H-G, Kaufmann P, Zardi L (1993a) Expression of extracellular matrix molecules related to placental development (abstract). Placenta 14:A.9
Castellucci M, Crescimanno C, Schroeter CA, Kaufmann P, Mühlhauser J (1993b) Extravillous trophoblast: immunohistochemical localization of extracellular matrix molecules. In: Genazzani AR, Petraglia F, Genazzani AD (eds) Frontiers in gynecologic and obstetric investigation. Parthenon Publishing Group. New York, pp 19–25
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
Earl U, Estlin C, Bulmer JN (1990) Fibronectin and laminin in the early human placenta. Placenta 11:223–231
Emonard H, Christiane Y, Smet M, Grimaud JA, Foidart JM (1990) Type IV and interstitial collagenolytic activities in normal and malignant trophoblast cells are specifically regulated by the extracellular matrix. Invasion Metastasis 10:170–177
Evans SC, Lopez LC, Shur BD (1993) Dominant negative mutation in cell surface beta-1,4-galactosyltransferase inhibits cell-cell and cell-matrix interactions. J Cell Biol 120:1045–1057
Feinberg RF, Kao LC, Haimowitz JE, Queenan JT Jr, Wun TC, Strauss JF, Kliman HJ (1989) Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts. Lab Invest 61:20–26
Feinberg RF, Kliman HJ, Lockwood CJ (1991) Is oncofetal fibronectin a trophoblast glue for human implantation? Am J Pathol 138:537–543
Fisher SJ, Leitch MS, Kantor MS, Basbaum CB, Kramer RH (1985) Degradation of extracellular matrix by the trophoblastic cells of first trimester human placentas. J Cell Biochem 27: 31–41
Fisher SJ, Cui TY, Zhang L, Hartman L, Grahl K, Zhang GY, Tarpey J, Damsky CH (1989) Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 109:891–902
Foxall C, Watson SR, Dowbenko D, Fennie C, Lasky LA, Kiso M, Hasegawa A, Asa D, Brandley BK (1992) The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J Cell Biol 117:895–902
Frank H-G, Malekzadeh F, Crescimanno C, Castellucci M, Desoye G, Kaufmann P (1993) Human placental fibrinoid shows a heterogenous distribution of fibrin and extracellular matrix components (abstract). Placenta 14:A.23
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
Hakomori S, Kannagi R (1983) Glycosphingolipids as tumor-associated and differentiation markers. J Natl Cancer Inst 71: 231–251
Hessle H, Engvall E (1984) Type VI collagen. Studies on its localization, structure, and biosynthetic form with monoclonal antibodies. J Biol Chem 259:3955–3961
Hormann H (1982) Fibronectin: mediator between cells and connective tissue. Klin Wochenschr 60:1265–1277
Hui KY, Haber E, Matsueda GR (1983) Monoclonal antibodies to a synthetic fibrin-like peptide bind to human fibrin but not fibrinogen. Science 222:1129–1132
Hynes RO (1985) Molecular biology of fibronectin. Annu Rev Cell Biol 1:67–90
Hynes RO, Yamada KM (1982) Fibronectins: multifunctional modular glycoproteins. J Cell Biol 95:369–377
Itzkowitz SH, Yuan M, Fukushi Y, Palekar A, Phelps PC, Shamsuddin AM, Trump BF, Hakomori S, Kim YS (1986) Lewis x-and sialylated Lewis x-related antigen expression in human malignant and nonmalignant colonic tissues. Cancer Res 46:2627–2632
Jokhi PP, King A, Loke YW (1994) Reciprocal expression of epidermal growth factor receptor (EGF-R) and c-erbB2 by non-invasive and invasive human trophoblast populations. Cytokine 6:433–442
Kim YS, Yuan M, Itzkowitz SH, Sun Q, Kaizu T, Palekar A, Trump BF, Hakomori SI (1986) Expression of Le-y and extended Le-y blood group related antigens in human malignant, premalignant and nonmalignant colonic tissues. Cancer Res 46:5985–5992
King BF, Blankenship TN (1994) Ultrastructure and development of a thick basement membrane like layer in the anchoring villi of macaque placentas. Anat Res 238:498–506
King A, Loke YW (1988) Differential expression of blood-group-related carbohydrate antigens by trophoblast subpopulations. Placenta 9:513–521
Kisalus LL, Herr JC (1988) Immunocytochemical localization of heparan sulfate proteoglycan in human decidual cell secretory bodies and placental fibrinoid. Biol Reprod 39:419–430
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
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
Laureti E, Onisto M, Caenazzo C, Garbisa S (1992) Collagenase IV and laminin receptors in cultured trophoblast cells. Minerva Ginecol 44:423–427
Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ (1991) 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 113:437–449
Lim KH, Bass K, Kosten K, Damsky C, Fisher S (1993) Developmental delay of cytotrophoblast differentiation along the invasive pathway (abstract). Am J Obstet Gynecol 1993:151
Malak TM, Ockleford CD, Bell SC, Dalgleish R, Bright N, Macvicar J (1993) Confocal immunofluorescence localization of collagen types I, III, IV, V and VI and their ultrastructural organization in term human fetal membranes. Placenta 14:385–406
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
Matsuura H, Takio K, Titani K, Greene T, Levery SB, Salyan MEK, Hakomori S (1988) The oncofetal structure of human fibronectin defined by monoclonal antibody FDC-6. J Biol Chem 263:3314–3322
Matsuura H, Greene T, Hakomori S (1989) An alpha-N-acetylgalactosaminylation at the threonine residue of a defined peptide sequence creates the oncofetal peptide epitope in human fibronectin. J Biol Chem 264:10472–10476
Moll UM, Lane BL (1990) Proteolytic activity of first trimester human placenta: localization of interstitial collagenase in villous and extravillous trophoblast. Histochemistry 94:555–560
Morla A, Zhang Z, Ruoslahti E (1994) Superfibronectin is a functionally distinct from of fibronectin. Nature 367:193–194
Mühlhauser J, Crescimanno C, Kaufmann P, Hofler H, Zaccheo D, Castellucci M (1993) Differentiation and proliferation patterns in human trophoblast revealed by c-erbB-2 oncogene product an EGF-R. J Histochem Cytochem 41:165–173
Nanaev AK, Milovanov AP, Domogatsky SP (1993) Immunohistochemical localization of extracellular matrix in perivillous fibrinoid of normal human term placenta. Histochemistry 100: 341–346
Niemann H, Watanabe K, Hakomori S (1978) Blood group i and I activities of “lacto-N-norhexaosylceramide” and its analogues: the structural requirements for i-specificities. Biochem Biophys Res Commun 81:1286–1293
Nudelman ED, Mandel U, Levery SB, Kaizu T, Hakomori S (1989) A series of disialogangliosides with binary 2–3 sialosyllactosamine structure, defined by monoclonal antibody NUH2, are oncodevelopmentally regulated antigens. J Biol Chem 264:18719–18725
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
Roelcke D (1989) Cold agglutination. Transfus Med Rev 3: 140–166
Sekiguchi K, Siri A, Zardi L, Hakomori S (1985) Differences in domain structure between human fibronectins isolated from plasma and from culture supernatants of normal and transformed fibroblasts. J Biol Chem 260:5105–5114
Sell S (1990) Cancer-associated carbohydrates identified by monoclonal antibodies. Hum Pathol 21:1003–1019
Singhas CA (1992) Lectin histochemistry of the human amniochorionic membrane complex. Placenta 13:523–534
Stetler Stevenson WG, Aznavoorian S, Liotta LA (1993) Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol 9:541–573
Taki T, Matsuo K, Yamamoto K, Matsubara T, Hayashi A, Abe T, Matsumoto M (1988) Human placenta gangliosides. Lipids 23: 192–198
Towbin H, Staehelin T, Gordon J (1979) Elecrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350–4354
Watanabe K, Hakomori SI (1976) Status of blood group carbohydrate chains in ontogenesis and in oncogenesis. J Exp Med 144:645–653
Watanabe K, Hakomori SI, Childs RA, Feizi T (1979) Characterization of a blood group I-active ganglioside. Structural requirements for I and i specificities. J Biol Chem 254: 3221–3228
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
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
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Frank, HG., Huppertz, B., Kertschanska, S. et al. Anti-adhesive glycosylation of fibronectin-like molecules in human placental matrix-type fibrinoid. Histochem Cell Biol 104, 317–329 (1995). https://doi.org/10.1007/BF01464328
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01464328