Skip to main content

Advertisement

SpringerLink
Log in

Galectin-1 expression in prostate tumor-associated capillary endothelial cells is increased by prostate carcinoma cells and modulates heterotypic cell–cell adhesion

  • Published:
Angiogenesis Aims and scope Submit manuscript

Abstract

Besides providing tumors with nutrients, newly formed capillaries constitute a potential escape route for tumor cells favoring metastatic dissemination, and constitute an access for the anti-tumoral host immune cells. Galectin-1, a soluble human lectin, is involved in numerous biological functions including cell–cell and cell–substrate interactions. In addition, galectin-1 is able to induce apoptosis of activated T-lymphocytes. In this study, we have examined galectin-1 expression in capillaries associated to the carcinoma cells or present in the remote non-tumoral stroma of 100 human prostate carcinoma samples by immunoperoxidase staining. Galectin-1 was expressed by endothelial cells from capillaries infiltrating the tumor tissue in 64% (64/100) of the cases. On the contrary, endothelial cells in the adjacent non-tumoral stroma expressed galectin-1 in very few cases (7/100). Increased frequency of galectin-1-positive capillaries in the tumor-associated compared to the tumor-free areas was observed in 63% of the cases. This striking contrast led us to set up an in vitro model to test whether tumor cells could induce galectin-1 expression by endothelial cells. Incubation of human umbilical vein endothelial cells with conditioned media from PC-3 or DU 145 prostate carcinoma cells led to a significant increase of galectin-1 protein expression (+32.97% and 37.91% P < 0.01 and P < 0.05, respectively). PC-3 conditioned medium also induced increased adhesion values of PC-3 cells to the endothelial cells (53.4 ± 4.7 vs. 38.5 ± 3.5 after 30 min; 66.6 ± 7.8 vs. 46.2 ± 6.4 after 60 min). An anti-galectin-1 antiserum abolished this modulation, and recombinant galectin-1 also induced increased adhesion values in a dose-dependent fashion. This effect was specific as no such modulations were observed using normal lymphocytes instead of PC-3 cells. Preferential galectin-1 expression in the endothelial cells close to the cancer cells could provide these latter with increased abilities to interact with the endothelial cells as well as a defense against the host immune system.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Hanahan D, Folkman J. Patterns ans emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996; 86: 353–64.

    Article  PubMed  CAS  Google Scholar 

  2. Rak J, Filmus J, Kerbel RS. Reciprocal paracrine interactions between tumour cells and endothelial cells: The ‘angiogenesis progression’ hypothesis. Eur J Cancer 1996; 32A: 2438–50.

    Article  PubMed  CAS  Google Scholar 

  3. Laine RA. The information-storing potential of the sugar code. In Gabius H-J, Gabius S (eds): Glycosciences: Status and Perspectives. Weinheim, Germany: Chapman & Hall 1997; 1–14.

    Google Scholar 

  4. Barondes SH, Castronovo V, Cooper DNW et al. Galectins: A family of animal β-galactoside-binding lectins. Cell 1994; 76: 597–8.

    Article  PubMed  CAS  Google Scholar 

  5. Barondes SH, Cooper DNW, Gitt MA, Leffler H. Galectins: Structure and function of a large family of animal lectins. J Biol Chem 1994; 269: 20807–10.

    PubMed  CAS  Google Scholar 

  6. Allen HJ, Sucato D, Woynarowska B et al. Role of galaptin in ovarian carcinoma adhesion to extracellular matrix in vitro. J Cell Biochem 1990; 43: 43–57.

    Article  PubMed  CAS  Google Scholar 

  7. Skrincosky DM, Allen HJ, Bernacki RJ. Galaptin-mediated adhesion of human ovarian carcinoma A121 cells and detection of cellular galaptin-binding glycoproteins. Cancer Res 1993; 53: 2667–75.

    PubMed  CAS  Google Scholar 

  8. van den Brûle FA, Buicu C, Baldet M et al. Galectin-1 modulates human melanoma cell adhesion to laminin. Biochem Biophys Res Commun 1995; 209: 760–7.

    Article  PubMed  Google Scholar 

  9. Kaltner H, Stierstorfer B. Animal lectins as cell adhesion molecules. Acta Anat 1998; 161: 162–79.

    Article  PubMed  CAS  Google Scholar 

  10. Chiariotti L, Berlingieri MT, De Rosa P et al. Increased expression of the negative growth factor, galactoside-binding protein, gene in transformed thyroid cells and in human thyroid carcinomas. Oncogene 1992; 7: 2507–11.

    PubMed  CAS  Google Scholar 

  11. Chiariotti L, Berlingieri MT, Battaglia C et al. Expression of galectin-1 in normal human thyroid gland and in differentiated and poorly differentiated thyroid tumors. Int J Cancer 1995; 64: 171–5.

    PubMed  CAS  Google Scholar 

  12. Xu XC, el-Naggar AK, Lotan R. Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications. Am J Pathol 1995; 147: 815–22.

    PubMed  CAS  Google Scholar 

  13. van den Brûle FA, Buicu C, Berchuck A et al. Expression of the 67 kD laminin receptor, galectin-1 and galectin-3 in advanced uterine carcinoma. Hum Pathol 1996; 27: 1185–91.

    Article  PubMed  Google Scholar 

  14. Cindolo L, Benvenuto G, Salvatore P et al. Galectin-1 and galectin-3 expression in human bladder transitional-cell carcinomas. Int J Cancer 1999; 84: 39–43.

    Article  PubMed  CAS  Google Scholar 

  15. Sanjuan X, Fernandez PL, Castells A et al. Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology 1997; 113: 1906–15.

    Article  PubMed  CAS  Google Scholar 

  16. Gabius HJ, Brehler R, Schauer A, Cramer F. Localization of endogenous lectins in human breast, benign breast lesions and mammary carcinomas. Virchows Arch (Cell Pathol) 1986; 52: 107–15.

    CAS  Google Scholar 

  17. Baum LG, Seilhamer JJ, Pang M et al. Synthesis of an endogenous lectin, galectin-1, by human endothelial cells, is up-regulated by endothelial cell activation. Glycoconj J 1995; 12: 63–8.

    Article  PubMed  CAS  Google Scholar 

  18. Perillo NL, Pace KE, Seilhamer JJ, Baum LG. Apoptosis of T cells mediated by galectin-1. Nature 1995; 378: 736–9.

    Article  PubMed  CAS  Google Scholar 

  19. Lehr JE, Pienta KJ. Preferential adhesion of prostate cancer cells to a human bone marrow endothelial cell line. J Natl Cancer Inst 1998; 90: 118–23.

    Article  PubMed  CAS  Google Scholar 

  20. Schroder FH, Hermanek P, Denis L et al. The TNM classification of prostate cancer. Prostate 1992; 4: 129–38.

    CAS  Google Scholar 

  21. Gleason DF, Mellinger GT. Prediction of prognosis for prostatic adenocarcinoma by combined histological grading and clinical staging. J Urol 1974; 111: 58–64.

    PubMed  CAS  Google Scholar 

  22. Waltregny D, Bellahcène A, Van Riet I et al. Prognostic value of bone sialoprotein expression in localized human prostate cancer. JNCI 1998; 13: 1000–7.

    Article  Google Scholar 

  23. Cooper DNW, Barondes SH. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol 1990; 110: 1681–91.

    Article  PubMed  CAS  Google Scholar 

  24. Jaffe EA, Nachmann RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins: Identification by morphologic and immunologic criteria. J Clin Invest 1973; 52: 2745–56.

    Article  PubMed  CAS  Google Scholar 

  25. Baijum A. Isolation of morphonuclear cells and granulocytes from human blood. Scand J Clin Lab Invest 1968; 21S: 77–89.

    Google Scholar 

  26. Cooper DN, Massa SM, Barondes SH. Endogenous muscle lectin inhibits myoblast adhesion to laminin. J Cell Biol 1991; 115: 1437–48.

    Article  PubMed  CAS  Google Scholar 

  27. Ozeki Y, Matsui T, Titani K. Cell adhesive activity of two animal lectins through different recognition mechanisms. FEBS Lett 1991; 289: 145–7.

    Article  PubMed  CAS  Google Scholar 

  28. Zhou Q, Cummings RD. L-14 lectin recognition of laminin and its promotion of in vitro cell adhesion. Arch Biochem Biophys 1993; 300: 6–17.

    Article  PubMed  CAS  Google Scholar 

  29. Mahanthappa NK, Cooper DN, Barondes SH, Schwarting GA. Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism. Development 1994; 120: 1373–84.

    PubMed  CAS  Google Scholar 

  30. Ozeki Y, Matsui T, Yamamoto Y et al. Tissue fibronectin is an endogenous ligand for galectin-1. Glycobiology 1995; 5: 255–61.

    PubMed  CAS  Google Scholar 

  31. Kopitz J, von Reitzenstein C, Burchert M et al. Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J Biol Chem 1998; 273: 11205–11.

    Article  PubMed  CAS  Google Scholar 

  32. Moiseeva EP, Spring EL, Baron JH, de Bono DP. Galectin-1 modulates attachment, spreading and migration of cultured vascular smooth muscle cells via interactions with cellular receptors and components of extracellular matrix. J Vasc Res 1999; 36: 47–58.

    Article  PubMed  CAS  Google Scholar 

  33. Lotan R, Belloni PN, Tressler RJ et al. Expression of galectins on microvessel endothelial cells and their involvement in tumour cell adhesion. Glycoconj J 1994; 11: 462–8.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Metastasis Research Laboratory, Pathology B-23, Sart Tilman, B-4000, Liège, Belgium

    Nathalie Clausse, Frédéric van den Brûle, David Waltregny, Frédérique Garnier & Vincent Castronovo

Authors
  1. Nathalie Clausse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frédéric van den Brûle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Waltregny
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Frédérique Garnier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vincent Castronovo
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clausse, N., van den Brûle, F., Waltregny, D. et al. Galectin-1 expression in prostate tumor-associated capillary endothelial cells is increased by prostate carcinoma cells and modulates heterotypic cell–cell adhesion. Angiogenesis 3, 317–325 (1999). https://doi.org/10.1023/A:1026584523789

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026584523789

Search

Navigation