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Cell adhesion molecules acting between C6 glioma and endothelial cells

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Summary

The interactions between tumor cells and endothelium play a key role in the process of tumor growth, local invasion, and distant metastasis. In the present study, we examined the adhesion of C6 glioma cells to bovine endothelial cell (EC) monolayers and defined the cell adhesion molecules acting between these cells. Pretreatment of the EC monolayer with cytokines, tumor necrosis factor (TNF)-α, interleukin (IL)-1β, and interferon (INF)-γ, significantly increased the adhesion of C6 glioma cells to the EC monolayer. The effect lasted more than 24 hours and was protein-synthesis dependent. The adhesion of C6 glioma cells to TNF-activated ECs was blocked by the monoclonal antibody to the intercellular adhesion molecule-1 (ICAM-1) orβ 2 integrin, whereas that of melanoma cells was not. These findings provide evidence that ICAM-1 and β2 integrin function as inducible cell surface molecules that can support the adhesion of C6 glioma cells to ECs, and may contribute to the characteristic growth of glial tumorsin vivo.

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References

  1. Dustin ML, Stauton DE, Springer TA: Supergene families meet in the immune system. Immunol Today 9: 213–215, 1988

    Google Scholar 

  2. Osborn L: Leukocyte adhesion to endothelium in inflammation. Cell 62: 3–6, 1990

    Google Scholar 

  3. Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA Jr: Interleukin 1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines. J Clin Invest 76: 2003–2011, 1985

    Google Scholar 

  4. Gamble JR, Harlan JM, Klebanoff SJ, Vadas MA: Stimulation of the adherence of neutrophils to umbilical vein endothelium by human recombinant tumor necrosis factor. Proc Natl Acad Sci USA 82: 8667–8671, 1985

    Google Scholar 

  5. Pober JS, Bevilacqua MP, Mendrick DL, Lapierre LA, Fiers W, Gimbrone MA Jr: Two distinct monokines interleukin-1 and tumor necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured human vascular endothelial cells. J Immunol 136: 1680–1687, 1986

    Google Scholar 

  6. Schleimer RP, Rutledge BK: Cultured human vascular endothelial cells acquire adhesiveness for neutrophils after stimulation with interleukin 1, endotoxin, and tumor-promoting phorbol diesters. J Immunol 136: 649–654, 1986

    Google Scholar 

  7. Arfors KE, Lundberg C, Lindbom L, Lundberg K, Beatty PG, Harlan JM: A monoclonal antibody to the membrane glycoprotein complex CD18 inhibits polymorphonuclear leukocyte accumulation and plasma leakagein vivo. Blood 69: 338–340, 1987

    Google Scholar 

  8. Arnaout MA: Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75: 1037–1050, 1990

    Google Scholar 

  9. Bevilacqua MP, Stengelin S, Gimbrone MA Jr, Seed B: Endothelial leukocyte adhesion molecule 1: An inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 243: 1160–1165, 1989

    Google Scholar 

  10. Diamond MS, Staunton DE, Marlin SD, Springer TA: Binding of the integrin Mac-1 (CDllb/CD18) to the third immunoglobulin-like domain of ICAM-1 (CD54) and its regulation by glycosylation. Cell 65: 961–971, 1991

    Google Scholar 

  11. Hemler ME, Huang C, Takada Y, Schwarz L. Strominger JL, Clabby ML: Characterization of the cell surface heterodimer VLA-4 and related peptides. J Biol Chem 262: 11478–11485, 1987

    Google Scholar 

  12. Larson RS, Springer TA: Structure and function of leukocyte integrins. Immunol Rev 114: 181–217, 1990

    Google Scholar 

  13. Picker LJ, Warnock RA, Burns AR, Doerschuk CM, Berg EL, Butcher EC: The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell 66: 921–933, 1991

    Google Scholar 

  14. Rothlein R, Dustin ML, Marlin SD, Springer TA: A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J Immunol 137: 1270–1274, 1986

    Google Scholar 

  15. Staunton DE, Marlin SD, Stratowa C, Dustin ML, Springer TA: Primary structure of ICAM-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families. Cell 52: 925–933, 1988

    Google Scholar 

  16. Huber AR, Kunkel SL, Todd RF, Weiss SJ: Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 254: 99–102, 1991

    Google Scholar 

  17. Kishimoto TK, Jutila MA, Berg EL, Butcher EC: Neutrophil Mac-1 and MEL-14 adhesion proteins inversely regulated by chemotactic factors. Science 245: 1238–1241, 1989

    Google Scholar 

  18. Rice GE, Bevilacqua MP: An inducible endothelial cell surface glycoprotein mediates melanoma adhesion. Science 246: 1303–1306, 1989

    Google Scholar 

  19. Rice GE, Gimbrone MA Jr, Bevilacqua MP: Tumor cell-endothelial interactions. Am J Pathol 133: 204–210, 1988

    Google Scholar 

  20. Dejana E, Bertocchi F, Bortolami MC, Regonesi A, Tonta A,. Breviario F, Giavazzi R: Interleukin 1 promotes tumor cell adhesion to cultured human endothelial cells. J Clin Invest 82: 1466–1470, 1988

    Google Scholar 

  21. Kramer RH, Nicolson GL: Interactions of tumor cells with vascular endothelial cell monolayers: A model for metastatic invasion. Proc Natl Acad Sci USA 76: 5704–5708, 1979

    Google Scholar 

  22. Nicolson GL: Metastatic tumor cell attachment and invasion assay utilizing vascular endothelial cell monolayers. J Histochem Cytochem 30: 214–220, 1982

    Google Scholar 

  23. Stewart PA, Hayakawa K, Hayakawa E, Farrell CL, Del Maestro RF: A quantitative study of blood-brain barrier permeability ultrastructure in a new rat glioma model. Acta Neuropathol (Berl) 67: 96–102, 1985

    Google Scholar 

  24. Neichi T, Chang WC, Mitsui Y, Murota S: Comparison of prostaglandin biosynthetic activity between porcine aortic endothelial and smooth muscle cells in culture. Artery 11: 47–63, 1982

    Google Scholar 

  25. Auerbach R, Lu WC, Pardon E, Gumkowski F, Kaminska G, Kaminski M: Specificity of adhesion between murine tumor cells and capillary endothelium: anin vitro correlate of preferential metastasisin vivo. Cancer Res 47: 1492–1496, 1987

    Google Scholar 

  26. Nicolson GL, Winkelhake JL: Organ specificity of bloodborne tumour metastasis determined by cell adhesion? Nature 255: 230–232, 1975

    Google Scholar 

  27. Lauri D, Bertomeu MC, Orr FW, Bastida E, Sauder DN, Buchanan MR: Differential effects of interleukine-1 and formylmethionylleucylphenylalanine on chemotaxis and human endothelium adhesivity for A549 tumor cells. Lab Invest 60: 161–164, 1989

    Google Scholar 

  28. Anderson DC, Springer TA: Leukocyte adhesion deficiency: An inherited defect in the Mac-1, LFA-1, and p150,95 glycoproteins. Ann Rev Med 38: 175–194, 1987

    Google Scholar 

  29. Roossien FF, Rijk D, Bikker A, Roos E: Involvement of LFA-1 in lymphoma invasion and metastasis demonstrated with LFA-1-deficient mutants. J Cell Biol 108: 1979–1985, 1989

    Google Scholar 

  30. Carpén O, Pallai P, Staunton DE, Springer TA: Association of intercellular adhesion molecule-1 (ICAM-1) with actincontaining cytoskeleton and α-actinin. J Cell Biol 118: 1223–1234, 1992

    Google Scholar 

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

    Google Scholar 

  32. Nagano N, Sasaki H, Aoyagi M, Hirakawa K: Invasion of experimental rat brain tumor: early morphological changes following microinjection of C6 glioma cells. Acta Neuropathol (Berl) 86: 117–125, 1993

    Google Scholar 

  33. Lester BR, McCarthy J: Tumor cell adhesion to the extracellular matrix and signal transduction mechanisms implicated in tumor cell motility, invasion and metastasis. Cancer Metastasis Rev 11: 31–44, 1992

    Google Scholar 

  34. Brem S, Cotran R, Folkman J: Tumor angiogenesis: a quantitative method for histologie grading. J Natl Cancer Inst 48: 347–356, 1972

    Google Scholar 

  35. Feigin I, Allen LB, Lipkin L, Gross SW: The endothelial hyperplasia of the cerebral blood vessels with brain tumors, and its sarcomatous transformation. Cancer 11: 264–277, 1958

    Google Scholar 

  36. Hermansson M, Nistér M, Betsholtz C, Heldin CH, Westermark B, Funa K: Endothelial cell hyperplasia in human glioblastoma: Coexpression of mRNA for platelet-derived growth factor (PDGF) B chain and PDGF receptor suggests autocrine growth stimulation. Proc Natl Acad Sci USA 85: 7748–7752, 1988

    Google Scholar 

  37. Laerum OD, Bjerkrig R, Steinberg SK, De Ridder L: Invasiveness of primary brain tumors. Cancer Metastasis Rev 3: 223–226, 1984

    Google Scholar 

  38. Cerame MA, Guthikonda M, Kohli CM: Extraneural metastases in gliosarcoma: a case report and review of the literature. Neurosurgery 17: 413–418, 1985

    Google Scholar 

  39. Debault LE, Cancilla PA: γ-glutamil transpeptidase in isolated brain endothelial cells: Induction by glial cellsin vitro. Science 207: 653–655, 1980

    Google Scholar 

  40. Joo F: Current aspects of the development of the blood brain barrier. Int J Dev Neurosci 5: 369–372, 1987

    Google Scholar 

  41. Schneider J, Hofman FM, Apuzzo MLJ, Hinton DR: Cytokines and immunoregulatory molecules in malignant glial neoplasms. J Neurosurg 77: 265–273, 1992

    Google Scholar 

  42. Sawamura Y, Abe H, Aida T, Hosokawa M, Kobayashi H: Isolation andin vitro growth of glioma-infiltrating lymphocytes, and an analysis of their surface phenotypes. J Neurosurg 69: 745–750, 1988

    Google Scholar 

  43. Sawamura Y, Hosokawa M, Kuppner MC, Kobayashi H, Aida T, Abe H, Tribolet N: Antitumor activity and surface phenotypes of human glioma-infiltrating lymphocytes afterin vitro expansion in the presence of interleukin 2. Cancer Res 49: 1843–1849, 1989

    Google Scholar 

  44. Black KL, Chen K, Becker DP, Merrill JE: Inflammatory leukocytes associated with increased immunosuppression by glioblastoma. J Neurosurg 77: 120–126, 1992

    Google Scholar 

  45. Fontana A, Kristensen F, Dubs R, Gemsa D, Weber E: Production of prostaglandin E and an interleukin-1 like factor by cultured astrocytes and C6 glioma cells. J Immunol 129: 2413–2419, 1982

    Google Scholar 

  46. Sawada M, Kondo N, Suzumura A, Marunouchi T: Production of tumor necrosis factor-alpha by microglia and astrocytes in culture. Brain Res 491: 394–397, 1989

    Google Scholar 

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Tamaki, M., Aoyagi, M., Morita, I. et al. Cell adhesion molecules acting between C6 glioma and endothelial cells. J Neuro-Oncol 24, 181–188 (1995). https://doi.org/10.1007/BF01078488

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