Skip to main content
Log in

Adhesion molecule expression on murine cerebral endothelium following the injection of a proinflammagen or during acute neuronal degeneration

  • Published:
Journal of Neurocytology

Summary

The acute inflammatory response in the murine CNS is different from that observed in other tissues. Few polymorphonuclear leukocytes are recruited to the brain parenchyma and there is a delay in the recruitment of monocytes. Leukocyte recruitment to sites of inflammation is dependent on adhesion molecules expressed on the endothelium. The atypical kinetics of leukocyte recruitment to the CNS may be the result of deficient or delayed adhesion molecule expression on the cerebral endothelium. Using immunohistochemistry, the present study demonstrates that following the intracranial injection of a proinflammagen, lipopolysaccharide, or following acute neuronal degeneration elicited with kainic acid, the adhesion molecules ICAM-1 and VCAM were readily upregulated on cerebral endothelium in a time course comparable with that demonstrated on non-CNS endothelium. Both molecules were expressed on vessels, irrespective of their size, at 24h after kainic acid or 6 h after lipopolysaccharide injection but leukocyte recruitment was negligible. The expression of ICAM-1 was demonstrated not only on endothelium but also on microglia especially in response to nerve terminal degeneration. PECAM was constitutively expressed at high levels on cerebral endothelium and did not change during brain injury. However, PECAM was induced on astrocytes after lipopolysaccharide injection or during acute neuronal degeneration, the latter providing a particularly strong stimulus. This study indicates that the expression of these adhesion molecules on CNS endothelium is neither deficient or delayed and that they are unlikely to be limiting factors in leukocyte recruitment to the CNS.

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.

Similar content being viewed by others

References

  • Akiyama, H., Kawamata, T., Yamada, T., Tooyama, I., Ishii, T. &Mcgeer, P. (1993) Expression of intercellular adhesion molecule (ICAM)-1 by a subset of astrocytes in Alzheimer Disease and some other degenerative neurological disorders.Acta Neuropathologica 85, 628–34.

    PubMed  Google Scholar 

  • Albelda, S. M., Oliver, P. D., Romer, L. H. &Buck, C. A. (1990) EndoCAM: a novel endothelial cell-cell adhesion molecule.Journal of Cell Biology 110, 1227–37.

    PubMed  Google Scholar 

  • Albelda, S. M., Muller, W. A., Buck, C. A. &Newman, P. J. (1991) Molecular and cellular properties of PECAM-1 (endo CAM/CD 31): a novel vascular cell-cell adhesion molecule.Journal of Cell Biology 114, 1059–68.

    PubMed  Google Scholar 

  • Aloisi, F., Borsellini, G., Samoggia, P., Testa, U., Chelucci, C., Russo, G., Peschle, C. &Levi, G. (1992) Astrocyte cultures from human embryonic brain: characterisation and modulation of surface molecules by inflammatory cytokines.Journal of Neuroscience Research 32, 494–506.

    PubMed  Google Scholar 

  • Anderson, D. C., Schmalstieg, F. C., Finegold, J. J., Hughes, B. J., Rothlein, R., Miler, L. J., Kohl, S., Tosi, M. F., Jacobs, R. L., Waldrop, T. C., Goldman, A. S., Shearer, W. T. &Springer, T. A. (1985) The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: their quantitative definition and relation to leukocyte dysfunction and clinical features.Journal of Infectious Diseases 152, 668–89.

    PubMed  Google Scholar 

  • Andersson, P-B., Perry, V. H. &Gordon, S. (1991) The kinetics and morphological characteristics of the macrophagemicroglial response to kainic acid-induced neuronal degeneration.Neuroscience 42, 201–14.

    PubMed  Google Scholar 

  • Andersson, P-B., Perry, V. H. &Gordon, S. (1992) The acute inflammatory response to lipopolysaccharide in the CNS parenchyma differs from that of other body tissues.Neuroscience 48, 169–86.

    PubMed  Google Scholar 

  • Austyn, J. M. &Gordon, S. (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage.European Journal of Immunology 11, 805–15.

    PubMed  Google Scholar 

  • Barton, D. M. &Ruddle, N. H. (1994) Vascular cell adhesion molecule-1 modulation by tumor necrosis factor in experimental allergic encephalomyelitis.Journal of Neuroimmunology 51, 123–33.

    PubMed  Google Scholar 

  • Benveniste, E. N., Sparacio, S. M., Norris, J. G., Grenett, H. E. &Fuller, G. M. (1990) Induction and regulation of interleukin-6 gene expression in rat astrocytes.Journal of Neuroimmunology 30, 201–12.

    PubMed  Google Scholar 

  • Bird, I. N., Spragg, J. H., Ager, A. &Matthews, N. (1993) Studies of lymphocyte transendothelial migration: analysis of migrated cell phenotypes with regard to CD31 (PECAM-1), CD45RA and CD45RO.Immunology 80, 553–60.

    PubMed  Google Scholar 

  • Bochner, B. S., Luscinskas, F. W., Gimbrone, Jn., M. A., Newman, W., Sterbinsky, S. A., Derseanthony, C. P., Klunk, D. &Schleimer, R. P. (1991) Adhesion of human basophils, eosinophils, and neutrophils to interleukin-1 activated human vascular endothelial cells: contributions of endothelial cell adhesion molecules.Journal of Experimental Medicine 173, 1553–7.

    PubMed  Google Scholar 

  • Cannella, B., Cross, A. H. &Raine, C. S. (1990) Upregulation and coexpression of adhesion molecules correlate with relapsing autoimmune demyelination in the central nervous system.Journal of Experimental Medicine 172, 1521–4.

    PubMed  Google Scholar 

  • Carlos, T. M. &Harlan, J. M. (1990) Membrane proteins involved in phagocyte adherence to endothelium.Immunological Reviews 114, 5–28.

    Google Scholar 

  • Choi, D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system.Neuron 1, 623–34.

    PubMed  Google Scholar 

  • Chuluyan, H. E. &Issekutz, A. C. (1993) VLA-4 Integrin can mediate CD11/CD18-independent transendothelial migration of human monocytes.Journal of Clinical Investigation 92, 2768–77.

    PubMed  Google Scholar 

  • Chung, I. Y. &Benveniste, E. N. (1990) Tumor necrosis factor-alpha production by astrocytes: induction by lipopolysaccharide, interferon-gamma and interleukin-1 beta.Journal of Immunology 144, 2999–3007.

    Google Scholar 

  • Coyle, J. T. &Schwarcz, R. (1976) Lesion of striatal neurones with kainic acid provides a model for Huntington's chorea.Nature 263, 244–6.

    PubMed  Google Scholar 

  • Davies, M. J., Gordon, J. L., Gearing, A. J., Pigott, R., Woolf, N., Katz, D. &Kyriakopoulos, A. (1993) The expression of the adhesion molecules ICAM-1, VCAM-1, PECAM and E-selectin in human atherosclerosis.Journal of Pathology 171, 223–9.

    PubMed  Google Scholar 

  • Dobrina, A., Menegazzi, R., Carlos, T. M., Nardon, E., Cramer, R., Zacchi, T., Harlan, J. M. &Patriarca, P. (1991) Mechanisms of eosinophil adherence to cultured vascular endothelial cells.Journal of Clinical Investigation 88, 20–6.

    PubMed  Google Scholar 

  • Dougherty, G., Murdoch, S. &Hogg, N. (1988) The function of human intercellular adhesion molecule-1 (ICAM-1) in the generation of an immune response.European Journal of Immunology 18, 35–9.

    PubMed  Google Scholar 

  • Dustin, M. L. &Springer, T. A. (1988) Lymphocyte function-associated antigen-1 (LFA-1) interaction with intercellular adhesion molecule-1 (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells.Journal of Cell Biology 107, 321–31.

    PubMed  Google Scholar 

  • Dustin, M. L., Staunton, D. E. &Springer, T. A. (1988) Supergene families meet in the immune system.Immunology Today 9, 213–15.

    PubMed  Google Scholar 

  • Elices, M. J., Osborn, L., Takada, Y., Grouse, S., Luhowskyj, S., Hemler, M. E. &Lobb, R. R. (1990) VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4 fibronectin binding site.Cell 60, 577–84.

    PubMed  Google Scholar 

  • Engelhardt, B., Conley, F. K. &Butcher, E. C. (1994) Cell adhesion molecules on vessels during inflammation in the mouse central nervous system.Journal of Neuroimmunology 51, 199–208.

    PubMed  Google Scholar 

  • Fabry, Z., Fitzsimmons, K. M., Herlein, J. A., Moninger, T. O., Dobbs, M. B. &Hart, M. N. (1993) Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes.Journal of Neuroimmunology 47, 23–34.

    PubMed  Google Scholar 

  • Faden, A. I. &Simon, R. P. (1988) A potential role for excitotoxins in the pathophysiology of spinal cord injury.Annals of Neurology 23, 623–6.

    PubMed  Google Scholar 

  • Frei, K., Siepl, C., Groscurth, P., Bodmer, S., Schwerdel, C. &Fontana, A. (1987) Antigen presentation and tumor cytotoxicity by interferongamma treated microglial cells.European Journal of Immunology 17, 1271–8.

    PubMed  Google Scholar 

  • Frei, K., Malipiero, U. V., Leist, T. P., Zinkernagel, R. M., Schwab, M. E. &Fontana, A. (1989) On the cellular source and function of interleukin-6 produced in the central nervous system in viral diseases.European Journal of Immunology 19, 689–94.

    PubMed  Google Scholar 

  • Frohman, E. M., Frohman, T. C., Dustin, M. L., Vayuvegula, B., Choi, B., Gupta, A., Van Den Noort, S. &Gupta, S. (1989) The induction of intercellular adhesion molecule (ICAM)-1 expression on human fetal astrocytes by IFN-gamma, TNF-α, lymphotoxin and IL-1: relevance to intracerebral antigen presentation.Journal of Neuroimmunology 23, 117–24.

    PubMed  Google Scholar 

  • Frohman, E. M., Frohman, T. C., Gupta, S., De-Fougerolles, A. &Van Den Noort, S. (1991) Expression of intercellular adhesion molecule 1 (ICAM-1) in Alzheimer's disease.Journal of the Neurological Sciences 106, 105–11.

    PubMed  Google Scholar 

  • Guilian, D., Baker, T. J., Shih, L. &Lachman, L. B. (1986) Interleukin-1 of the central nervous system is produced by amoeboid microglia.Journal of Experimental Medicine 164, 594–604.

    PubMed  Google Scholar 

  • Harlan, J. M. (1993) Leukocyte adhesion deficiency syndrome: insights into the molecular basis of leukocyte emigration.Clinical Immunology and Immunopathology 67, S16–24.

    PubMed  Google Scholar 

  • Hemler, M. E., Huang, C., Takada, Y., Schwarz, L., Strominger, J. L. &Clabby, M. L. (1987) Characterisation of the cell surface heterodimer VLA-4 and related peptides.Journal of Biological Chemistry 262, 11478–95.

    PubMed  Google Scholar 

  • Horley, K. J., Carpenito, C., Baker, B. &Takei, F. (1989) Molecular cloning of murine intercellular adhesion molecule (ICAM-1).EMBO Journal 8, 2889–96.

    PubMed  Google Scholar 

  • Hsu, S. M., Raine, L. &Fanger, H. (1981) The use of avidin-biotin-peroxidase (ABC) complex in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures.Journal of Histochemistry and Cytochemistry 29, 577–80.

    PubMed  Google Scholar 

  • Kishimoto, T. K., Larson, R. S., Corbi, A. L., Dustin, M. C., Staunton, D. E. &Springer, T. A. (1989) The leukocyte integrins.Advances in Immunology 46, 149–82.

    PubMed  Google Scholar 

  • Lieberman, A. P., Pitha, P. M., Shin, H. S. &Shin, M. L. (1989) Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus.Proceedings of the National Academy of Sciences (USA) 86, 6348–52.

    Google Scholar 

  • Locksley, R. M., Wilson, C. B. &Klebanoff, S. J. (1983) Increased respiratory burst in myeloperoxidase-deficient monocytes.Blood 62, 902–9.

    PubMed  Google Scholar 

  • McLean, I. W. &Nakane, P. K. (1974) Periodate-lysine-paraformaldehyde fixative. A new fixative for immunoelectron microscopy.Journal of Histochemistry and Cytochemistry 22, 1077–83.

    PubMed  Google Scholar 

  • Metzelaar, M. J., Korteweg, J., Sixma, J. J. &Nieuwenhuis, H. K. (1991) Biochemical characterisation of PECAM-1 (CD31 antigen) on human platelets.Thrombostasis and Haemostasis 66, 700–7.

    Google Scholar 

  • Miyake, K., Medina, K., Ishihara, K., Kimoto, M., Auerbach, R. &Kincade, P. (1991) A VCAM-like adhesion molecule on murine bone marrow stromal cells mediates binding of lymphocyte precursors in culture.Journal of Cell Biology 111, 557–65.

    Google Scholar 

  • Muller, W. A., Weigl, S. A., Deng, X. &Philips, D. M. (1993) PECAM-1 is required for transendothelial migration of leukocytes.Journal of Experimental Medicine 178, 449–60.

    PubMed  Google Scholar 

  • Munro, J. M., Prober, J. S. &Cotran, R. S. (1989) Tumor necrosis factor and interferon-gamma induce distinct patterns of endothelial activation and associated leukocyte accumulation in skin of Papio anubis.American Journal of Pathology 135, 121–33.

    PubMed  Google Scholar 

  • Norton, J., Sloane, J. P., Al-Saffar, N. &Haskard, D. O. (1991) Vessel associated adhesion molecules in normal skin and acute graft-versus host disease.Journal of Clinical Pathology 44, 586–91.

    PubMed  Google Scholar 

  • Ohto, H., Maeda, H., Shibata, Y., Chen, R. F., Ozaki, Y., Higashihara, M., Takeuchi, A. &Tohyama, H. (1985) A novel leukocyte differentiation antigen: two monoclonal antibodies TM2 and TM3 define a 120 Kd molecule present on neutrophils, monocytes, platelets and activated lymphoblasts.Blood 66, 873–81.

    PubMed  Google Scholar 

  • Perry, V. H. &Gordon, S. (1991) Macrophages and the nervous system.International Review of Cytology 125, 203–44.

    PubMed  Google Scholar 

  • Plaitakis, A. &Caroscio, J. T. (1987) Abnormal glutamate metabolism in amyotrophic lateral sclerosis.Annals of Neurology 22, 575–9.

    PubMed  Google Scholar 

  • Pober, J. S., Gimbrone, M. A., Jr., Lapierre, L. A., Mendrick, D. L., Fiers, W., Rothlein, R. &Springer, T. A. (1986) Overlapping patterns of activation of human endothelial cells by interleukin-1, tumor necrosis factor and immune Interferon.Journal of Immunology 137, 1893–6.

    Google Scholar 

  • Pober, J. S., Lapierre, L. A., Stolpen, A. H., Brock, T. A., Springer, T. A., Fiers, W., Bevilacqua, M. P., Mendrick, D. L. &Gimbrone, Jr. M. A. (1987) Activation of cultured human endothelial cells by recombinant lymphotoxin: comparison with tumor necrosis factor and interleukin 1 species.Journal of Immunology 138, 3319–24.

    Google Scholar 

  • Poston, R., Haskard, D., Coucher, J., Gall, N. &Johnson-Tidey, R. (1992) Expression of intercellular adhesion molecule-1 in atherosclerotic plaques.American Journal of Pathology 140, 665–73.

    PubMed  Google Scholar 

  • Printseva, O., Peclo, M. &Gown, A. (1992) Various cell types in human atherosclerotic lesions express ICAM-1: further immunocytochemical and immunochemical studies employing monoclonal antibody 10Fs.American Journal of Pathology 140, 889–96.

    PubMed  Google Scholar 

  • Reinhold, R. &Fine, J. (1971) A technique for quantitative measurement of endotoxin in human plasma.Proceedings of the Society of Experimental Biological Medicine 137, 334.

    Google Scholar 

  • Renkonen, R. (1989) Regulation of intercellular adhesion molecule-1 expression on endothelial cells with correlation to lymphocyte-endothelial binding.Scandinavian Journal of Immunology 29, 717–21.

    PubMed  Google Scholar 

  • Robbins, D. S., Shirazi, Y., Drysdale, B. E., Lieberman, A., Shin, H. S. &Shin, M. L. (1987) Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes.Journal of Immunology 139, 2593–7.

    Google Scholar 

  • Rosen, H. &Gordon, S. (1987) Monoclonal antibody to the murine type 3 complement receptor inhibits adhesion of myelomonocytic cellsin vitro and inflammatory cell recruitmentin vivo.Journal of Experimental Medicine 166, 1685–701.

    PubMed  Google Scholar 

  • Rosenblum, W. I., Murata, S., Nelson, G. H., Werner, P. K., Ranken, R. &Harmon, R. C. (1994) Anti-CD31 delays, platelet adhesion/aggregation at sites of endothelial injury in mouse cerebral arterioles.American Journal of Pathology 145, 33–6.

    PubMed  Google Scholar 

  • Sasseville, V. G., Newman, W. A., Lackner, A. A., Smith, M. O., Lausen, N. C. G., Beall, D. &Ringler, D. J. (1992) Elevated vascular cell adhesion molecule-1 in AIDS encephalitis induced by simian immunodeficiency virus.American Journal of Pathology 141, 1021–30.

    PubMed  Google Scholar 

  • Sasseville, V. G., Newman, W., Brodie, S. J., Hesterberg, P., Pauley, D. &Ringlder, D. J. (1994) Monocyte adhesion to endothelium in simian immunodeficiency virus-induced AIDS encephalitis is mediated by vascular cell adhesion molecule-1/α4β1 integrin interactions.American Journal of Pathology 144, 27–40.

    PubMed  Google Scholar 

  • Schuermann, G. M., Aber-Bishop, A. E., Facer, P., Lee, J. C., Rampton, D. S., Dore, C. J. &Polak, J. M. (1993) Altered expression of cell adhesion molecules in uninvolved gut in inflammatory bowel disease.Clinical and Experimental Immunology 94, 341–7.

    PubMed  Google Scholar 

  • Shimizu, Y., Van Seventer, G., Horgan, K. &Shaw, S. (1990) Roles of adhesion molecules in T cell recognition: fundamental similarities between four integrins on resting human T cells (LFA-1, VLA-4, VLA-5, VLA-6) in expression, binding and co-stimulation.Immunology Review 114, 109–43.

    Google Scholar 

  • Simmons, D., Makgoba, M. W. &Seed, B. (1988) ICAM, an adhesion ligand of LFA-1 is homologous to the neural cell adhesion molecule NCAM.Nature 331, 624–7.

    PubMed  Google Scholar 

  • Smith, C. W., Marlin, S. D., Rothlein, R., Toman, C. &Anderson, D. C. (1989) Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophilsin vitro.Journal of Clinical Investigation 83, 2008–17.

    PubMed  Google Scholar 

  • Sobel, R. A., Mitchell, M. E. &Fondren, G. (1990) Intercellular adhesion molecule-1 (ICAM-1) in cellular immune reactions in the central nervous system.American Journal of Pathology 136, 1309–16.

    PubMed  Google Scholar 

  • Springer, T. A. (1990) Adhesion receptors of the immune system.Nature 346, 425–34.

    PubMed  Google Scholar 

  • Staunton, D. E., Dustin, M. L. &Springer, T. A. (1989) Functional cloning if ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1.Nature 339, 61–4.

    PubMed  Google Scholar 

  • Stockinger, H., Gadd, S. J., Eher, R., Majdic, O., Schreiber, W., Kasinrerk, W., Strass, B., Schnabl, E. &Knapp, W. (1990) Molecular characterisation and functional analysis of the leukocyte surface protein CD31.Journal of Immunology 145, 3889–97.

    Google Scholar 

  • Takei, F. (1985) Inhibition of mixed lymphocyte response by a rat monoclonal antibody to a novel murine lymphocyte activation antigen (MALA-2).Journal of Immunology 134, 1403–7.

    Google Scholar 

  • Tanaka, Y., Adams, D. H. &Shaw, S. (1993) Proteoglycans on endothelial cells present adhesion-inducing cytokines to leukocytes.Immunology Today 14, 111–15.

    PubMed  Google Scholar 

  • Van Dam, A. M., Brouns, M., Louisse, S. &Berkenbosch, F. (1992) Appearance of interleukin-1 in macrophages and in ramified microglia in the brain of endotoxin-treated rats: a pathway for the induction of non-specific symptoms of sickness?Brain Research 588, 291–6.

    PubMed  Google Scholar 

  • Vaporciyan, A. A., Delisser, H. M., Yan, H-C, Mendiguren, I. I., Thom, S. R., Jones, M. L., Ward, P. A. &Albelda, S. M. (1993) Involvement of plateletendothelial cell adhesion molecule-1 in the neutrophil recruitmentin vivo.Science 262, 1580–2.

    PubMed  Google Scholar 

  • Vecchi, A., Garlanda, C., Lampugnani, M. G., Resnati, M., Matteucci, C., Stoppacciaro, A., Schnurch, H., Risau, W., Ruco, L., Mantovani, A. &Dejana, E. (1994) Monoclonal antibodies specific for endothelial cells of mouse blood vessels. Their application in the identification of adult and embryonic endothelium.European Journal of Cell Biology 63, 247–54.

    PubMed  Google Scholar 

  • Verbeek, M. M., Otte-Holler, I., Westphal, J. R., Wesseling, P., Ruiter, D. J. &De Waal, R. M. W. (1994) Accumulation of intercellular adhesion molecule-1 in senile plaques in brain tissue of patients with Alzheimer's Disease.American Journal of Pathology 144, 104–16.

    PubMed  Google Scholar 

  • Viale, G., Gambacorta, M., Coggi, G., Dell'orto, P., Milani, M. &Doglioni, C. (1991) Glial fibrillary acidic protein immunoreactivity in normal and diseased human breast.Virchows Archives. A. Pathol Anat. 418, 339–48.

    Google Scholar 

  • Walsh, G. M., Mermod, J-J, Hartnell, A., Kay, A. B. &Wardlaw, A. J. (1991) Human eosinophil, but not neutrophil, adherence to IL-1 stimulated human umbilical vascular endothelial cells is α4β1 (very late antigen-4) dependent.Journal of Immunology 146, 3419–23.

    Google Scholar 

  • Wellicome, S. M., Thornhill, M. H., Pitzalis, C., Thomas, D. S., Lanchbury, S., Panayi, G. S. &Haskard, D. O. (1990) A monoclonal antibody that detects a novel antigen on endothelial cells that is induced by tumour necrosis factor, IL-1, or lipopolysaccharide.Journal of Immunology 144, 2558–65.

    Google Scholar 

  • Wilkinson, L. S., Edwards, J. C. W., Poston, R. N. &Haskard, D. O. (1993) Expression of vascular cell adhesion molecule-1 in normal and inflamed synovium.Laboratory Investigation 68, 82–8.

    PubMed  Google Scholar 

  • Wilcox, C. E., Ward, A. M. V., Evans, A., Baker, B., Rothlein, R. &Turk, J. L. (1990) Endothelial cell expression of the intercellular adhesion molecule (ICAM-1) in the central nervous system of guinea pigs during acute an chronic relapsing experimental allergic encephalomyelitis.Journal of Neuroimmunology 30, 43–51.

    PubMed  Google Scholar 

  • Willenborg, D. O., Simmons, R. D., Tamatani, T. &Miyasaka, M. (1993) ICAM-1 dependent pathway is not critically involved in the inflammatory process of autoimmune encephalomyelitis or in cytokine induced inflammation of the central nervous system.Journal of Neuroimmunology 45, 147–54.

    PubMed  Google Scholar 

  • Wong, D. &Dorovini-Zis, K. (1992a) Upregulation of intercellular adhesion molecule-1 (ICAM-1) expression in primary cultures of human brain microvessel endothelial cells by cytokines and lipopolysaccharide.Journal of Neuroimmunology 39, 11–22.

    PubMed  Google Scholar 

  • Wong, D. &Dorovini-Zis, K. (1992b) Upregulation of vascular cell adhesion molecule-1 (VCAM-1) in primary cultures of human brain microvessel endothelial cells by cytokine and lipopolysaccharide.Journal of Neuropathology and Experimental Neurology 51, 378.

    Google Scholar 

  • Wuthrich, R. P., Jenkins, T. A. &Snyder, T. L. (1993) Regulation of cytokine-stimulated vascular cell adhesion molecule-1 expression in renal tubular epithelial cells.Transplantation 55, 172–7.

    PubMed  Google Scholar 

  • Yednock, T. A., Cannon, C., Fritz, L. C., Sanchez-Madrid, F., Steinman, L. &Karin, N. (1992) Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 Beta 1 integrin.Nature 356, 63–6.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bell, M.D., Perry, V.H. Adhesion molecule expression on murine cerebral endothelium following the injection of a proinflammagen or during acute neuronal degeneration. J Neurocytol 24, 695–710 (1995). https://doi.org/10.1007/BF01179819

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01179819

Keywords

Navigation