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. 1992 Aug;181(Pt 1):79–87.

Distribution of anionic sites on the perineurium.

M S Bush 1, G Allt 1
PMCID: PMC1259754  PMID: 1294572

Abstract

The distribution of anionic sites on the perineurial basal lamina (BL) and plasmalemma of dorsal root ganglia and sciatic nerves was determined using cationic ferritin (CF) and cationic gold (CCG). The probes were applied to the tissue before and after resin embedding and visualised by electron microscopy. There were no apparent differences in charge distribution between the 2 tissues. At physiological pH a strong anionic charge was distributed evenly over the BL as demonstrated by pre-embedding labelling with CF; the plasmalemma was only moderately anionic. A similar application of CCG at pH 2.0 revealed a quasi-regular distribution of anionic sites (presumably due to acidic carbohydrate moieties) on the BL, whilst CCG-labelling of L. R. White sections indicated a differential distribution of these moieties on the BL of the inner and outer perineurial lamellae. Cationic ferritin (12 nm diameter) crossed the BL and entered perineurial caveolae, but CCG (effective diameter of 15 nm) did not, suggesting that the BL is a size-restrictive filter. These results are discussed with regard to the ultrastructure and function of the BL of other tissues and the possible role of perineurial BL charge as a determinant of perineurial permeability.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akert K., Sandri C., Weibel E. R., Peper K., Moor H. The fine structure of the perineural endothelium. Cell Tissue Res. 1976 Jan 27;165(3):281–295. doi: 10.1007/BF00222433. [DOI] [PubMed] [Google Scholar]
  2. Allt G. Involvement of the perineurium in experimental allergic neuritis; electron microscopic observations. Acta Neuropathol. 1972;20(2):139–149. doi: 10.1007/BF00691130. [DOI] [PubMed] [Google Scholar]
  3. Arvidson B. A study of the perineurial diffusion barrier of a peripheral ganglion. Acta Neuropathol. 1979 Apr 12;46(1-2):139–144. doi: 10.1007/BF00684815. [DOI] [PubMed] [Google Scholar]
  4. Batsford S. R., Rohrbach R., Vogt A. Size restriction in the glomerular capillary wall: importance of lamina densa. Kidney Int. 1987 Mar;31(3):710–717. doi: 10.1038/ki.1987.56. [DOI] [PubMed] [Google Scholar]
  5. Beamish N. G., Stolinski C., Thomas P. K., King R. H. Freeze-fracture observations on normal and abnormal human perineurial tight junctions: alterations in diabetic polyneuropathy. Acta Neuropathol. 1991;81(3):269–279. doi: 10.1007/BF00305868. [DOI] [PubMed] [Google Scholar]
  6. Bush M. S., Allt G. Blood-nerve barrier: distribution of anionic sites on the endothelial plasma membrane and basal lamina. Brain Res. 1990 Dec 10;535(2):181–188. doi: 10.1016/0006-8993(90)91599-c. [DOI] [PubMed] [Google Scholar]
  7. 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. 1991 Sep;20(9):759–768. doi: 10.1007/BF01187849. [DOI] [PubMed] [Google Scholar]
  8. Dermietzel R., Thürauf N., Kalweit P. Surface charges associated with fenestrated brain capillaries. II. In vivo studies on the role of molecular charge in endothelial permeability. J Ultrastruct Res. 1983 Aug;84(2):111–119. doi: 10.1016/s0022-5320(83)90122-3. [DOI] [PubMed] [Google Scholar]
  9. Eldridge C. F., Sanes J. R., Chiu A. Y., Bunge R. P., Cornbrooks C. J. Basal lamina-associated heparan sulphate proteoglycan in the rat PNS: characterization and localization using monoclonal antibodies. J Neurocytol. 1986 Feb;15(1):37–51. doi: 10.1007/BF02057903. [DOI] [PubMed] [Google Scholar]
  10. Ghabriel M. N., Jennings K. H., Allt G. Diffusion barrier properties of the perineurium: an in vivo ionic lanthanum tracer study. Anat Embryol (Berl) 1989;180(3):237–242. doi: 10.1007/BF00315882. [DOI] [PubMed] [Google Scholar]
  11. Hultström D., Malmgren L., Gilstring D., Olsson Y. FITC-Dextrans as tracers for macromolecular movements in the nervous system. A freeze-drying method for dextrans of various molecular sizes injected into normal animals. Acta Neuropathol. 1983;59(1):53–62. doi: 10.1007/BF00690317. [DOI] [PubMed] [Google Scholar]
  12. Inoue S. Ultrastructure of basement membranes. Int Rev Cytol. 1989;117:57–98. doi: 10.1016/s0074-7696(08)61334-0. [DOI] [PubMed] [Google Scholar]
  13. Kanwar Y. S. Biophysiology of glomerular filtration and proteinuria. Lab Invest. 1984 Jul;51(1):7–21. [PubMed] [Google Scholar]
  14. Kanwar Y. S., Farquhar M. G. Anionic sites in the glomerular basement membrane. In vivo and in vitro localization to the laminae rarae by cationic probes. J Cell Biol. 1979 Apr;81(1):137–153. doi: 10.1083/jcb.81.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klemm H. Das Perineurium als Diffusionsbarriere gegenüber Peroxydase bei epi- und endoneuraler Applikation. Z Zellforsch Mikrosk Anat. 1970;108(3):431–445. [PubMed] [Google Scholar]
  16. Kogaya Y., Kim S., Haruna S., Akisaka T. Heterogeneity of distribution pattern at the electron microscopic level of heparan sulfate in various basement membranes. J Histochem Cytochem. 1990 Oct;38(10):1459–1467. doi: 10.1177/38.10.1698204. [DOI] [PubMed] [Google Scholar]
  17. Kristensson K., Olsson Y. The perineurium as a diffusion barrier to protein tracers. Differences between mature and immature animals. Acta Neuropathol. 1971;17(2):127–138. doi: 10.1007/BF00687488. [DOI] [PubMed] [Google Scholar]
  18. Malmgren L. T., Olsson Y. Differences between the peripheral and the central nervous system in permeability to sodium fluorescein. J Comp Neurol. 1980 May 1;191(1):103–107. doi: 10.1002/cne.901910106. [DOI] [PubMed] [Google Scholar]
  19. Moss J., Woodrow D. F., Shore I., Gower P., Phillips M., Spiro R. G. Ultrastructural immunogold studies of heparan sulphate proteoglycan in normal human glomeruli and glomerulonephritis. J Pathol. 1990 Jun;161(2):137–143. doi: 10.1002/path.1711610208. [DOI] [PubMed] [Google Scholar]
  20. Myers R. R., Heckman H. M., Powell H. C. Endoneurial fluid is hypertonic. Results of microanalysis and its significance in neuropathy. J Neuropathol Exp Neurol. 1983 May;42(3):217–224. doi: 10.1097/00005072-198305000-00001. [DOI] [PubMed] [Google Scholar]
  21. Oldfors A., Johansson B. R. Barriers and transport properties of the perineurium. An ultrastructural study with 125I-labeled albuminin and horseradish peroxidase in normal and protein-deprived rats. Acta Neuropathol. 1979 Jul 13;47(2):139–143. doi: 10.1007/BF00717037. [DOI] [PubMed] [Google Scholar]
  22. Oldfors A. Permeability of the perineurium of small nerve fascicles: an ultrastructural study using ferritin in rats. Neuropathol Appl Neurobiol. 1981 May-Jun;7(3):183–194. doi: 10.1111/j.1365-2990.1981.tb00088.x. [DOI] [PubMed] [Google Scholar]
  23. Olsson Y. Microenvironment of the peripheral nervous system under normal and pathological conditions. Crit Rev Neurobiol. 1990;5(3):265–311. [PubMed] [Google Scholar]
  24. Olsson Y., Reese T. S. Permeability of vasa nervorum and perineurium in mouse sciatic nerve studied by fluorescence and electron microscopy. J Neuropathol Exp Neurol. 1971 Jan;30(1):105–119. doi: 10.1097/00005072-197101000-00011. [DOI] [PubMed] [Google Scholar]
  25. Pino R. M., Essner E. Permeability of rat choriocapillaris to hemeproteins. Restriction of tracers by a fenestrated endothelium. J Histochem Cytochem. 1981 Feb;29(2):281–290. doi: 10.1177/29.2.7252121. [DOI] [PubMed] [Google Scholar]
  26. Rechthand E., Rapoport S. I. Regulation of the microenvironment of peripheral nerve: role of the blood-nerve barrier. Prog Neurobiol. 1987;28(4):303–343. doi: 10.1016/0301-0082(87)90006-2. [DOI] [PubMed] [Google Scholar]
  27. Shinowara N. L., Michel M. E., Rapoport S. I. Morphological correlates of permeability in the frog perineurium: vesicles and "transcellular channels". Cell Tissue Res. 1982;227(1):11–22. doi: 10.1007/BF00206328. [DOI] [PubMed] [Google Scholar]
  28. Simionescu M., Simionescu N., Palade G. E. Preferential distribution of anionic sites on the basement membrane and the abluminal aspect of the endothelium in fenestrated capillaries. J Cell Biol. 1982 Nov;95(2 Pt 1):425–434. doi: 10.1083/jcb.95.2.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stirling J. W., Coleman M., Brennan J. The use of inert dehydration and glycol methacrylate embedding for immunogold localization of glomerular basement membrane components. Lab Invest. 1990 May;62(5):655–663. [PubMed] [Google Scholar]
  30. Weerasuriya A., Rapoport S. I., Taylor R. E. Modification of permeability of frog perineurium to [14C]-sucrose by stretch and hypertonicity. Brain Res. 1979 Sep 21;173(3):503–512. doi: 10.1016/0006-8993(79)90244-0. [DOI] [PubMed] [Google Scholar]
  31. Yoshimura A., Ohno S., Nakano K., Oniki H., Inui K., Ideura T., Koshikawa S. Three-dimensional ultrastructure of anionic sites of the glomerular basement membrane by a quick-freezing and deep-etching method using a cationic tracer. Histochemistry. 1991;96(2):107–113. doi: 10.1007/BF00315980. [DOI] [PubMed] [Google Scholar]

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