Skip to main content
Log in

Blood-nerve barrier: Distribution of anionic sites on the endothelial plasma membrane and basal lamina of dorsal root ganglia

  • Published:
Journal of Neurocytology

Summary

Previous investigations of the blood-nerve barrier have correlated the greater permeability of ganglionic endoneurial vessels, compared to those of nerve trunks, with the presence of fenestrations and open intercellular junctions. Recent studies have demonstrated reduced endothelial cell surface charge in blood vessels showing greater permeability. To determine the distribution of anionic sites on the plasma membranes and basal laminae of endothelial cells in dorsal root ganglia, cationic colloidal gold and cationic ferritin were used. Electron microscopy revealed the existence of endothelial microdomains with differing labelling densities. Labelling indicated that caveolar and fenestral diaphragms and basal laminae are highly anionic at physiological pH, luminal plasma membranes and endothelial processes are moderately charged and abluminal plasma membranes are weakly anionic. Tracers did not occur in caveolae or cytoplasmic vesicles.In vitro tracer experiments at pH values of 7.3, 5.0, 3.5 and 2.0 indicated that the anionic charge on the various endothelial domains was contributed by chemical groups with differing pKa values. In summary, the labelling of ganglionic and sciatic nerve vessels was similar except for the heavy labelling of diaphragms in a minority of endoneurial vessels in ganglia. This difference is likely to account in part for the greater permeability of ganglionic endoneurial vessels. The results are discussed with regard to the blood-nerve and -brain barriers and vascular permeability in other tissues and a comparison made between the ultrastructure and anionic microdomains of epi-, peri- and endoneurial vessels of dorsal root ganglia and sciatic nerves.

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

  • Arvidson, B. (1979) Distribution of intravenously injected protein tracers in peripheral ganglia of adult mice.Experimental Neurology 63, 388–410.

    Google Scholar 

  • Bearer, E. L. &Orci, L. (1985) Endothelial fenestral diaphragms: a quick-freeze, deep-etch study.Journal of Cell Biology 100, 418–28.

    Google Scholar 

  • Bush, M. S. &Allt, G. (1990) Blood-nerve barrier: distribution of anionic sites on the endothelial plasma membrane and basal lamina.Brain Research 535, 181–8.

    Google Scholar 

  • Granger, D. N., Kvietys, P. R., Perry, M. A. &Taylor, A. E. (1986) Charge selectivity of rat intestinal capillaries. Influence of polycations.Gastroenterology 91, 1443–6.

    Google Scholar 

  • Hultström, D., Malmgren, L., Gilstring, D. &Olsson, Y. (1983) FITC-dextrans as tracers for macromolecular movements in the nervous system. A freezedrying method for dextrans of various molecular sizes injected into normal animals.Acta Neuropathologica (Berlin) 59, 53–62.

    Google Scholar 

  • Jacobs, J. M. (1977) Penetration of systemically injected horseradish peroxidase into ganglia and nerves of the autonomic nervous system.Journal of Neurocytology 6, 607–18.

    Google Scholar 

  • Jacobs, J. M., Macfarlane, R. M. &Cavanagh, J. B. (1976) Vascular leakage in the dorsal root ganglia of the rat, studied with horseradish peroxidase.Journal of the Neurological Sciences 29, 95–107.

    Google Scholar 

  • Kanwar, Y. S., Linker, A. &Farquhar, M. G. (1980) Increased permeability of the glomerular basement membrane to ferritin after removal of glycosaminoglycans (heparan sulfate) by enzyme digestion.Journal of Cell Biology 86, 688–93.

    Google Scholar 

  • Leblond, C. P. &Inoue, S. (1989) Structure, composition, and assembly of basement membrane.American Journal of Anatomy 185, 367–90.

    Google Scholar 

  • Mackenzie, M. L., Ghabriel, M. N. &Allt, G. (1987) The blood-nerve barrier: anin vivo lanthanum tracer study.Journal of Anatomy 154, 27–37.

    Google Scholar 

  • Nag, S. (1984) Cerebral endothelial surface charge in hypertension.Acta Neuropathologica (Berlin) 63, 276–81.

    Google Scholar 

  • Nagy, Z. (1990) Blood-brain barrier and the cerebral endothelium. InPathophysiology of the Blood-Brain Barrier. Long Term Consequences of Barrier Dysfunction for the Brain (edited byJohansson, B. B., Owman, C. &Widner, H.) Fernström Foundation Series 14, pp. 11–29. Amsterdam: Elsevier.

    Google Scholar 

  • Olsson, Y. (1984) Vascular permeability in the peripheral nervous system.In Peripheral Neuropathy, 2nd ed. (edited byDyck, P. J., Thomas, P. K., Lambert, E. H. &Bunge, R.) pp. 579–97. Philadelphia: Saunders.

    Google Scholar 

  • Palade, G. E. (1988) The microvascular endothelium revisited. InEndothelial Cell Biology in Health and Disease (edited bySimionescu, N. &Simionescu, M.) pp. 3–22, New York: Plenum Press.

    Google Scholar 

  • Pino, R. M. (1986) The cell surface of a restricted fenestrated endothelium. II. Dynamics of cationic ferritin binding and the identification of heparin and heparan sulfate domains on the choriocapillaris.Cell and Tissue Research 243, 157–64.

    Google Scholar 

  • Pino, R. M. &Essner, E. (1981) Permeability of rat choriocapillaris to hemeproteins. Restriction of tracers by a fenestrated endothelium.Journal of Histochemistry and Cytochemistry 29, 281–90.

    Google Scholar 

  • Renkin, E. M. (1988) Transport pathways and processes. InEndothelial Cell Biology in Health and Disease (edited bySimionescu, N. &Simionescu, M.) pp. 51–68. New York: Plenum Press.

    Google Scholar 

  • Schmidley, J. W. &Wissig, S. L. (1986) Anionic sites on the luminal surface of fenestrated and continuous capillaries of the CNS.Brain Research 363, 265–71.

    Google Scholar 

  • Schneeberger, E. (1988) Interaction of plasma proteins with negatively charged sites on the pulmonary capillary endothelium of the rat.Cell and Tissue Research 251, 417–23.

    Google Scholar 

  • Seno, S. (1987) Ionized groups on the cell surface: their cytochemical detection and related cell function.International Review of Cytology 100, 203–48.

    Google Scholar 

  • Simionescu, N. &Simionescu, M. (1983) The cardiovascular system. InHistology: Cell and Tissue Biology (edited byWeiss, L.) pp. 371–433. New York: Elsevier.

    Google Scholar 

  • Simionescu, N., Simionescu, M., Palade, G. E. (1981) Differentiated microdomains on the luminal surface of the capillary endothelium. I. Preferential distribution of anionic sites.Journal of Cell Biology 90, 605–13.

    Google Scholar 

  • Taylor, A. E. &Granger, D. N. (1984) Exchange of macromolecules across the microcirculation. InHandbook of Physiology, Section 2:The Cardiovascular System, vol. IV,Microcirculation, Part I (edited byRenkin, E. M. &Michel, C. C.) pp. 467–520. Bethesda, Maryland: American Physiological Society.

    Google Scholar 

  • Thürauf, N., Dermietzel, R. &Kalweit, P. (1983) Surface charges associated with fenestrated brain capillaries. I.In vitro labelling of anionic sites.Journal of Ultrastructure Research 84, 103–110.

    Google Scholar 

  • Vorbrodt, A. W. (1986) Changes in the distribution of endothelial surface glycoconjugates associated with altered permeability of brain micro-blood vessels.Acta Neuropathologica (Berlin) 70, 103–11.

    Google Scholar 

  • Vorbrodt, A. W. (1987) Demonstration of anionic sites on the luminal and abluminal fronts of endothelial cells with poly-L-lysine-gold complex.Journal of Histochemistry and Cytochemistry 35, 1261–6.

    Google Scholar 

  • Vorbrodt, A. W. (1989) Ultracytochemical characterization of anionic sites in the wall of brain capillaries.Journal of Neurocytology 18, 359–68.

    Google Scholar 

  • Vorbrodt, A. W., Lossinsky, A. S., Wisniewski, H. M., Suzuki, R., Yamaguchi, T., Masaoka, H. &Klatzo, I. (1985) Ultrastructural observations on the transvascular route of protein removal in vasogenic brain edema.Acta Neuropathologica (Berlin) 66, 265–73.

    Google Scholar 

  • Vorbrodt, A. W., Dobrogowska, D. H., Kim, Y. S., Lossinsky, A. S. &Wisniewski, H. M. (1988) Ultrastructural studies of glycoconjugates in brain micro-blood vessels and amyloid plaques of scrapie-infected mice.Acta Neuropathologica (Berlin) 75, 277–87.

    Google Scholar 

  • Vorbrodt, A. W., Dobrogowska, D. H., Lossinsky, A. S. &Wisniewski, H. M. (1990) Changes in the distribution of anionic sites in brain micro-blood vessels with and without amyloid deposits in scrapie-infected mice.Acta Neuropathologica (Berlin) 79, 355–63.

    Google Scholar 

  • Weiss, L. &Zeigel, R. (1971) Cell surface negativity and the binding of positively charged particles.Journal of Cellular Physiology 77, 179–86.

    Google Scholar 

  • Wisniewski, H. M. &Kozlowski, P. B. (1982) Evidence for blood-brain barrier changes in senile dementia of the Alzheimer type (SDAT).Annals of the New York Academy of Sciences 396, 119–29.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bush, M.S., Reid, A.R. & Allt, G. Blood-nerve barrier: Distribution of anionic sites on the endothelial plasma membrane and basal lamina of dorsal root ganglia. J Neurocytol 20, 759–768 (1991). https://doi.org/10.1007/BF01187849

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01187849

Keywords

Navigation