Skip to main content
SpringerLink
Log in

Interferon effect on glycosaminoglycans in mouse gliomain vitro

  • Laboratory Investigation
  • Published:
Journal of Neuro-Oncology Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Summary

The effect of mouse interferon α/β (MuIFN α/β) on the production of glycosaminoglycans (GAGs) by mouse glioma G-26in vitro was evaluated. Two GAG species secreted extracellularly by the mouse glioma G-26 were isolated using cellulose acetate electrophoresis. They were identified as hyaluronic acid (HA) and chondroitin sulfate (CS) following enzymatic digestion with enzymes: hyaluronidase and chondroitinase ABC. Further characterization of CS by enzymatic digestion with specific chondroitinases for chondroitin 4-sulfate (CSA) and chondroitin 6-sulfate (CSC), revealed that the isolated CS was neither CSA nor CSC. Therefore, it may be either chondroitin sulfate B (CSB) (dermatan sulfate) or one of the ‘chontroitin sulfate isomers’ (D-H).

The three day incubation of glioma G-26 cells with 8×10-8×104 U/ml of MuIFN α/β resulted in a dose dependent inhibition of cell proliferation measured by3H-thymidine incorporation and the MTT assay. The significant decrease of the CS (p < 0.008) but not the HA level, (measured densitometrically), was observed following 72 hours (hrs) incubation of G-26 cells with 8 × 103 U/ml of MuIFN α/β (IFN treated cells: 0.03 ± 0.007 integrated optical density (IOD); control cells: 0.07 ± 0.01 IOD). The decreased CS production may be the underlying cause of IFN mediated inhibition of glioma cell proliferation.

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. Groothuis DR, Vick NA: Brain tumors and the blood-brain barrier. Trends Neurosci 5: 232–235, 1982

    Google Scholar 

  2. Neuwelt EA, Barnett PA: Blood-brain barrier disruption in the treatment of brain tumors: Animal studies. In: Implications of the blood-brain barrier and its manipulation, (ed) E.A. Neuwelt. Plenum Publ Corp, New York and London, 1989, Volume 2, pp 107–182

    Google Scholar 

  3. McBride WH, Bard JBL: Hyaluronidase-sensitive halos around adherent cells. J Exp Med 149: 507–515, 1979

    Google Scholar 

  4. Gately CL, Messler Muul L, Greenwood MA, Papazoglou S, Dick SJ, Kornblith PL, Smith BH, Gately MK:In vitro studies on the cell-mediated immune response to human brain tumors. II. Leukocyte-induced coats of glycosaminoglycan increase the resistance of glioma cells to cellular immune attack. J Immunol 133: 3387–3395, 1984

    Google Scholar 

  5. Bourin M-C, Lindahl U: Glycosaminoglycans and the regulation of blood coagulation. Biochem J 289: 313–330, 1993

    Google Scholar 

  6. Esko JD, Rostand KS, Weinke JL: Tumor formation dependent on proteoglycan biosynthesis. Science 241: 1092–1096, 1988

    Google Scholar 

  7. Bertolotto A, Magrassi ML, Orsi L, Sitia C, Schiffer D: Glycosaminoglycan changes in human gliomas. A biochemical study. J Neuro-Oncol 4: 43–48, 1986

    Google Scholar 

  8. Schrappe M, Klier FG, Spiro RC, Waltz TA, Reisfeld RA, Gladson CL: Correlation of chondroitin sulfate proteoglycan expression on proliferating brain capillary endothelial cells with malignant phenotype of astroglial cells. Cancer Res 51: 4896–4993, 1991

    Google Scholar 

  9. Murata K, Yokoyama Y: Enzymatic analysis with chondrosulf atases of constituent disaccharides of sulf ated chondroitin sulfate and dermatan sulfate isomers by high-performance liquid chromatography. Anal Biochem 149: 261–268, 1985

    Google Scholar 

  10. Elias JA, Krol RC, Freundlich B, Sampson PM: Regulation of human lung fibroblast glycosaminoglycan production by recombinant interferons, tumor necrosis factor, and lymphotoxin. Clin Invest 81: 325–333, 1988

    Google Scholar 

  11. Giordana MT, Bertolotto A, Mauro A, Migheli A, Pezzotta S, Racagni G, Schiffer D: Glycosaminoglycans in human cerebral tumors. Part II. Histochemical Findings and Correlations. Acta Neuropathol 57: 299–305, 1982

    Google Scholar 

  12. Pfeffer LM, Wang E, Tamm I: Interferon effects on microfilament organization, cellular fibronectin distribution, and cell motility in human fibroblasts. J Cell Biol 85: 9–17, 1980

    Google Scholar 

  13. Gillery P, Serpier H, Polette M, Bellon G, Clavel C, Wegrowski Y, Birembaut P, Kalis B, Cariou R, Maquart FX: Gamma-interferon inhibits extracellular matrix synthesis and remodeling in collagen lattice cultures of normal and scleroderma skin fibroblasts. Eur J Cell Biol 57: 244–253, 1992

    Google Scholar 

  14. Klein NJ, Shennan GI, Heyderman RS, Levin M: Alteration in glycosaminoglycan metabolism and surface charge on human umbilical vein endothelial cells isolated by cytokines, endotoxin and neutrophils. J Cell Sci 102: 821–832, 1992

    Google Scholar 

  15. Daireaux M, Redini F, Loyau G, Pujol J-P: Effects of associated cytokines (IL-1, TNF-α, IFN-γ and TGF-β) on collagen and glycosaminoglycan production by cultured human synovial cells. Int J Tiss Reac 12: 21–31, 1990

    Google Scholar 

  16. Stratton MR, Martin JM, Lantos PL: The effects of interferon on glial cells. Br J Exp Path 68: 643–653, 1987

    Google Scholar 

  17. Wiranowska M, Gonzalvo AA, Saporta S, Gonzalez OR, Prockop LD: Evaluation of blood-brain barrier permeability and the effect of interferon in mouse glioma model. J Neuro-Oncol 14: 225–236, 1992

    Google Scholar 

  18. Mosmann T: Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Meth 65: 55–63, 1983

    Google Scholar 

  19. Nikkhah G, Tonn JC, Hoffman O, Kraemer HP, Darling JL, Schonmayr R, Schachenmayr W: The MTT assay for chemosensitivity testing of human tumors of the central nervous system Part 1: Evaluation of test-specific variables. J Neuro Oncol 13: 1–11, 1992

    Google Scholar 

  20. Sobottka SB, Berger MR: Assessment of antineoplastic agents by MTT assay: Partial underestimation of antiproliferative properties. Cancer Chemother Pharmacol 30: 385–393, 1992

    Google Scholar 

  21. Kennedy A, Frank RN, Mancini MA:In vitro production of glycosaminoglycans by retinal microvessel cells and lens epithelium. Invest Ophthalmol Vis Sci 27: 746–754, 1986

    Google Scholar 

  22. Schmidley JW, Blue P: Isolation of glycosaminoglycans from basement membranes of brain microvessels. Brain Res Bull 20: 27–31, 1988

    Google Scholar 

  23. Bitter T, Muir HM: A modified uronic acid carbazole reaction. Anal Biochem 4: 330–334, 1962

    Google Scholar 

  24. Steck PA, Moser RP, Bruner JM, Liang L, Freidman AN, Hwang T, Alfred Yung WK: Altered expression and distribution of heparan sulfate proteoglycans in human gliomas. Cancer Res 49: 2096–2103, 1989

    Google Scholar 

  25. Kanwar YS, Farquhar MG: Isolation of glycosaminoglycans (heparan sulfate) from glomerular basement membranes. Proc Natl Acad Sci USA 76: 4493–41497, 1979

    Google Scholar 

  26. Naidu AK, Wiranowska M, Kori SH, Roetzheim KC, Kulkarni AP: Inhibition of cell proliferation and glutathion S-transferase by ascorbyl esters and interferon in mouse glioma. J Neuro-Oncol 16: 1–10, 1993

    Google Scholar 

  27. Gowda DC, Bhavanandan VP, Davidson EA: Isolation and characterization of proteoglycans secreated by normal and malignant human mammary epithelial cells. J Biol Chem 11: 4926–4934, 1986

    Google Scholar 

  28. Baron S, Tyring SK, Fleishmann R, Coppenhaver DH, Niesel DW, Klimpel GR, Stanton J, Hughes TK: The interferons: Mechanisms of action and clinical application. J Amer Med Assoc 266: 1375–1383, 1991

    Google Scholar 

  29. Lundblad D, Lungren F: Block of glioma cell line in S by interferon. Int J Cancer 27: 749–754, 1981

    Google Scholar 

  30. Numa Y, Kawamoto K, Sakai N, Matsumura H: Flow cytometric analysis of antineoplastic effects of interferon-α,β and labelled with flourescein isothiocyanate on cultured brain tumors. J Neuro-Oncol 11: 225–234, 1991

    Google Scholar 

  31. Takeuchi J: Effect of chondroitinases on the growth of solid Ehrlich ascities tumor. Br J Cancer 26: 115–119, 1972

    Google Scholar 

  32. Lortat-Jacob H, Grimaud JA: Binding of interferon-gamma to heparan sulfate is restricted to the heparin-like domains and involves carboxylic — but not N-sulfated — groups. Biochim Biophys Acta 1117: 126–130, 1992

    Google Scholar 

  33. Toole BP, Biswas C, Gross J: Hyaluronate and invasiveness of the rabbit V2 carcinoma. Proc Natl Acad Sci USA 76: 6299–6303, 1979

    Google Scholar 

  34. Kuppner MC, Van Meir E, Gauthier Th, Hamou MF, de Tribolet N: Differential expression of the CD44 molecule in human brain tumors. Int J Cancer 50: 572–577, 1992

    Google Scholar 

  35. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B: CD44 is the principal cell surface receptor for hyaluronate. Cell 61: 1303–1313, 1990

    Google Scholar 

  36. Couldwell WT, de Tribolet N, Antel JP, Gauthier T, Kuppner MC: Adhesion molecules and malignant gliomas: implications for tumorigenesis. J Neurosurg 76: 782–791, 1992

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Medicine, Department of Neurology, University of South Florida, Tampa, Florida, USA

    Marzenna Wiranowska & Abhinender K. Naidu

Authors
  1. Marzenna Wiranowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abhinender K. Naidu
    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

Wiranowska, M., Naidu, A.K. Interferon effect on glycosaminoglycans in mouse gliomain vitro . J Neuro-Oncol 18, 9–17 (1994). https://doi.org/10.1007/BF01324598

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01324598

Key words

Search

Navigation