Skip to main content
Log in

Binding of galectin-1 (gal-1) to the Thomsen–Friedenreich (TF) antigen on trophoblast cells and inhibition of proliferation of trophoblast tumor cells in vitro by gal-1 or an anti-TF antibody

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

Abstract

Galectin-1 (gal-1), a member of the mammalian β-galactoside-binding proteins, recognizes preferentially Galβ1-4GlcNAc sequences of several cell surface oligosaccharides. We demonstrate histochemically that the lectin recognizes appropriate glycotopes on the syncytiotrophoblast and extravillous trophoblast layer from second trimester human placenta and on BeWo chorion carcinoma cells. Gal-1 binding to BeWo cells was diminished by the Thomsen–Friedreich (TF)-disaccharide (Galβ1-3GalNAc-) conjugated to polyacrylamide (TF–PAA). Gal-1 also inhibited BeWo cell proliferation in a concentration-dependent manner. Similar antiproliferative effects were also observed with an anti-TF monoclonal antibody (mAb, A78-G/A7). Therefore, we conclude that ligation of Galβ1-4GlcNAc and Galβ1-3GalNAc epitopes on BeWo cells may have regulatory effects on cell proliferation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams L, Scott GK, Weinberg CS (1996) Biphasic modulation of cell growth by recombinant human galectin-1. Biochim Biophys Acta 1312:137–144

    Article  PubMed  Google Scholar 

  • Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K, et al. (1994a) Galectins: a family of animal beta-galactoside-binding lectins. Cell 76:597–598

    Article  CAS  Google Scholar 

  • Barondes SH, Cooper DN, Gitt MA, Leffler H (1994b) Galectins. Structure and function of a large family of animal lectins. J Biol Chem 269:20807–20810

    CAS  Google Scholar 

  • Barr N, Taylor CR, Young T, Springer GF (1989) Are pancarcinoma T and Tn differentiation antigens? Cancer 64:834–841

    Article  PubMed  CAS  Google Scholar 

  • Boorsma DM, Van Bommel J, Vanden Heuvel J (1986) Avidin-HRP conjugates in biotin-avidin immunoenzyme cytochemistry. Histochemistry 84:333–337

    Article  PubMed  CAS  Google Scholar 

  • van den Brule F, Califice S, Garnier F, Fernandez PL, Berchuck A, Castronovo V (2003) Galectin-1 accumulation in the ovary carcinoma peritumoral stroma is induced by ovary carcinoma cells and affects both cancer cell proliferation and adhesion to laminin-1 and fibronectin. Lab Invest 83:377–386

    PubMed  Google Scholar 

  • van den Brule F, Califice S, Castronovo V (2004) Expression of galectins in cancer: a critical review. Glycoconj J 19:537–542

    Article  PubMed  Google Scholar 

  • Butschak G, Karsten U (2002) Isolation and characterization of thomsen–friedenreich-specific antibodies from human serum. Tumour Biol 23:113–122

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Stosiek P, Springer GF, Karsten U (1996) Thomsen–Friedenreich-related carbohydrate antigens in normal adult human tissues: a systematic and comparative study. Histochem Cell Biol 106:197–207

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Schlag PM, Karsten U (1997) Immunodetection of epithelial mucin (MUC1, MUC3) and mucin-associated glycotopes (TF, Tn, and sialosyl-Tn) in benign and malignant lesions of colonic epithelium: apolar localization corresponds to malignant transformation. Virchows Arch 431:159–166

    Article  PubMed  CAS  Google Scholar 

  • Glinsky VV, Huflejt ME, Glinsky GV, Deutscher SL, Quinn TP (2000) Effects of Thomsen–Friedenreich antigen-specific peptide P-30 on beta-galactoside-mediated homotypic aggregation and adhesion to the endothelium of MDA-MB-435 human breast carcinoma cells. Cancer Res 60:2584–2588

    PubMed  CAS  Google Scholar 

  • Glinsky VV, Glinsky GV, Rittenhouse-Olson K, Huflejt ME, Glinskii OV, Deutscher SL, Quinn TP (2001) The role of Thomsen–Friedenreich antigen in adhesion of human breast and prostate cancer cells to the endothelium. Cancer Res 61:4851–4857

    PubMed  CAS  Google Scholar 

  • Goletz S, Cao Y, Danielczyk A, Ravn P, Schoeber U, Karsten U (2003) Thomsen–Friedenreich antigen: the “hidden” tumor antigen. Adv Exp Med Biol 535:147–162

    PubMed  CAS  Google Scholar 

  • Grummer R, Hohn HP, Mareel MM, Denker HW (1994) Adhesion and invasion of three human choriocarcinoma cell lines into human endometrium in a three-dimensional organ culture system. Placenta 15:411–429

    Article  PubMed  CAS  Google Scholar 

  • Hafer-Macko C, Pang M, Seilhamer JJ, Baum LG (1996) Galectin-1 is expressed by thymic epithelial cells in myasthenia gravis. Glycoconj J 13:591–597

    Article  PubMed  CAS  Google Scholar 

  • Hammer A, Dohr G (1999) Apoptotic nuclei within the uterine decidua of first trimester pregnancy arise from CD45 positive leukocytes. Am J Reprod Immunol 42:88–94

    PubMed  CAS  Google Scholar 

  • Hammer A, Blaschitz A, Daxbock C, Walcher W, Dohr G (1999) Fas and Fas-ligand are expressed in the uteroplacental unit of first-trimester pregnancy. Am J Reprod Immunol 41:41–51

    PubMed  CAS  Google Scholar 

  • Hirabayashi J, Kasai K (1984) Human placenta beta-galactoside-binding lectin. Purification and some properties. Biochem Biophys Res Commun 122:938–944

    Article  PubMed  CAS  Google Scholar 

  • Hirabayashi J, Kasai K (1993) The family of metazoan metal-independent beta-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology 3:297–304

    Article  PubMed  CAS  Google Scholar 

  • Hughes RC (2001) Galectins as modulators of cell adhesion. Biochimie 83:667–676

    Article  PubMed  CAS  Google Scholar 

  • Irazoqui FJ, Jansson B, Lopez PH, Nores GA (2001) Correlative fine specificity of several Thomsen–Friedenreich disaccharide-binding proteins with an effect on tumor cell proliferation (Tokyo). J Biochem 130:33–37

    PubMed  CAS  Google Scholar 

  • Jeppesen C, Nielsen PE (1989) Photofootprinting of drug-binding sites on DNA using diazo- and azido-9-aminoacridine derivatives. Eur J Biochem 182:437–444

    Article  PubMed  CAS  Google Scholar 

  • Jeschke U, Reimer T, Bergemann C, Wiest I, Schulze S, Friese K, Walzel H (2004) Binding of galectin-1 (gal-1) on trophoblast cells and inhibition of hormone production of trophoblast tumor cells in vitro by gal-1. Histochem Cell Biol 121:501–508

    Article  PubMed  CAS  Google Scholar 

  • Jeschke U, Richter DU, Hammer A, Briese V, Friese K, Karsten U (2002) Expression of the Thomsen–Friedenreich antigen and of its putative carrier protein mucin 1 in the human placenta and in trophoblast cells in vitro. Histochem Cell Biol 117:219–226

    Article  PubMed  CAS  Google Scholar 

  • Karsten U, Butschak G, Cao Y, Goletz S, Hanisch FG (1995) A new monoclonal antibody (A78-G/A7) to the Thomsen–Friedenreich pan-tumor antigen. Hybridoma 14:37–44

    Article  PubMed  CAS  Google Scholar 

  • Khaldoyanidi SK, Glinsky VV, Sikora L, Glinskii AB, Mossine VV, Quinn TP, Glinsky GV, Sriramarao P (2003) MDA-MB-435 human breast carcinoma cell homo- and heterotypic adhesion under flow conditions is mediated in part by Thomsen–Friedenreich antigen-galectin-3 interactions. J Biol Chem 278:4127–4134

    Article  PubMed  CAS  Google Scholar 

  • Lehr JE, Pienta KJ (1998) Preferential adhesion of prostate cancer cells to a human bone marrow endothelial cell line. J Natl Cancer Inst 90:118–123

    Article  PubMed  CAS  Google Scholar 

  • Offner H, Celnik B, Bringman TS, Casentini-Borocz D, Nedwin GE, Vandenbark AA (1990) Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental autoimmune encephalomyelitis. J Neuroimmunol 28:177–184

    Article  PubMed  CAS  Google Scholar 

  • Pace KE, Hahn HP, Pang M, Nguyen JT, Baum LG (2000) CD7 delivers a pro-apoptotic signal during galectin-1-induced T cell death. J Immunol 165:2331–2334

    PubMed  CAS  Google Scholar 

  • Perillo NL, Pace KE, Seilhamer JJ, Baum LG (1995) Apoptosis of T cells mediated by galectin-1. Nature 378:736–739

    Article  PubMed  CAS  Google Scholar 

  • Poirier F, Timmons PM, Chan CT, Guenet JL, Rigby PW (1992) Expression of the L14 lectin during mouse embryogenesis suggests multiple roles during pre- and post-implantation development. Development 115:143–155

    PubMed  CAS  Google Scholar 

  • Rabinovich GA, Rubinstein N, Matar P, Rozados V, Gervasoni S, Scharovsky GO (2002) The antimetastatic effect of a single low dose of cyclophosphamide involves modulation of galectin-1 and Bcl-2 expression. Cancer Immunol Immunother 50:597–603

    Article  PubMed  CAS  Google Scholar 

  • Raz A, Lotan R (1987) Endogenous galactoside-binding lectins: a new class of functional tumor cell surface molecules related to metastasis. Cancer Metastasis Rev 6:433–452

    Article  PubMed  CAS  Google Scholar 

  • Richter DU, Jeschke U, Makovitzky J, Goletz S, Karsten U, Briese V, Friese K (2000) Expression of the Thomsen–Friedenreich (TF) antigen in the human placenta. Anticancer Res 20:5129–5133

    PubMed  CAS  Google Scholar 

  • van Rooijen JJ, Jeschke U, Kamerling JP, Vliegenthart JF (1998) Expression of N-linked sialyl Le(x) determinants and O-glycans in the carbohydrate moiety of human amniotic fluid transferrin during pregnancy. Glycobiology 8:1053–1064

    Article  PubMed  Google Scholar 

  • Springer GF (1984) T and Tn, general carcinoma autoantigens. Science 224:1198–1206

    Article  PubMed  CAS  Google Scholar 

  • Stillman BN, Hsu DK, Pang M, Brewer CF, Johnson P, Liu FT, Baum LG (2006) Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol 176:778–789

    PubMed  CAS  Google Scholar 

  • Tinari N, Kuwabara I, Huflejt ME, Shen PF, Iacobelli S, Liu FT (2001) Glycoprotein 90K/MAC-2BP interacts with galectin-1 and mediates galectin-1-induced cell aggregation. Int J Cancer 91:167–172

    Article  PubMed  CAS  Google Scholar 

  • Vicovac L, Jankovic M, Cuperlovic M (1998) Galectin-1 and -3 in cells of the first trimester placental bed. Hum Reprod 13:730–735

    Article  PubMed  CAS  Google Scholar 

  • Walzel H, Neels P, Bremer H, Kohler H, Raab N, Barten M, Brock J (1995) Immunohistochemical and glycohistochemical localization of the beta-galactoside-binding S-type lectin in human placenta. Acta Histochem 97:33–42

    PubMed  CAS  Google Scholar 

  • Walzel H, Schulz U, Neels P, Brock J (1999) Galectin-1, a natural ligand for the receptor-type protein tyrosine phosphatase CD45. Immunol Lett 67:193–202

    Article  PubMed  CAS  Google Scholar 

  • Walzel H, Blach M, Hirabayashi J, Kasai KI, Brock J (2000) Involvement of CD2 and CD3 in galectin-1 induced signaling in human Jurkat T-cells. Glycobiology 10:131–140

    Article  PubMed  CAS  Google Scholar 

  • Wells V, Mallucci L (1991) Identification of an autocrine negative growth factor: mouse beta-galactoside-binding protein is a cytostatic factor and cell growth regulator. Cell 64:91–97

    Article  PubMed  CAS  Google Scholar 

  • Wiest I, Seliger C, Walzel H, Friese K, Jeschke U (2005) Induction of apoptosis in human breast cancer and trophoblast tumor cells by galectin-1. Anticancer Res 25:1575–1580

    PubMed  CAS  Google Scholar 

  • Yeaman GR, Collins JE, Lang GA (2002) Autoantibody responses to carbohydrate epitopes in endometriosis. Ann N Y Acad Sci 955:174–182; discussion 199–200, 396–406

    Google Scholar 

  • Yu LG, Jansson B, Fernig DG, Milton JD, Smith JA, Gerasimenko OV, Jones M, Rhodes JM (1997) Stimulation of proliferation in human colon cancer cells by human monoclonal antibodies against the TF antigen (galactose beta1-3 N-acetyl-galactosamine). Int J Cancer 73:424–431

    Google Scholar 

Download references

Acknowledgments

We thank D.U. Richter and G. Gaede for excellent technical assistance. The study was supported by the “Deutsche Forschungsgemeinschaft” (DFG) for U. Jeschke and H. Walzel.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Udo Jeschke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jeschke, U., Karsten, U., Wiest, I. et al. Binding of galectin-1 (gal-1) to the Thomsen–Friedenreich (TF) antigen on trophoblast cells and inhibition of proliferation of trophoblast tumor cells in vitro by gal-1 or an anti-TF antibody. Histochem Cell Biol 126, 437–444 (2006). https://doi.org/10.1007/s00418-006-0178-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-006-0178-1

Keywords

Navigation