Summary
Lanthanum, applied to the outside of the fixed sciatic nerve of Rana pipiens, did not enter the endoneurium, but was halted by functionally tight junctions at the inner layers of the perineurium. This component of the bloodnerve barrier consists of several concentric layers of cells interspersed with an extracellular matrix of amorphous ground substance, collagen fibrils, and fine filaments. Numerous vesicular profiles are closely associated with the surface membranes of all the cells. The application of lanthanum to fixed tissue revealed that these profiles are attached to the cell surface by narrow necks, and open to the extracellular space. The attenuated cells are filled by the vesicular structures, which often appear to overlap. Stereoscopic electron microscopy showed that these vesicles did not fuse with each other or with the apposing cell surface to form transcellular channels. Channel formation does not appear to contribute significantly to the permeability of any of the perineurial layers.
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References
Akert K, Sandri C, Weibel ER, Peper K, Moor H (1976) The fine structure of the perineurial endothelium. Cell Tissue Res 165:281–295
Bruns RR, Palade GE (1968) Studies on blood capillaries I. General organization of blood capillaries in muscle. J Cell Biol 37:244–276
Bundgaard M, Cserr HF (1981) Impermeability of hagfish cerebral capillaries to radiolabelled polyethylene glycols and to microperoxidase. Brain Res 206:71–81
Bundgaard M, Frøkjaer-Jensen J (1982) Functional aspects of the ultrastructure of terminal blood vessels: a quantitative study on consecutive segments of the frog mesenteric microvasculature. Microvasc Res 23:1–30
Bundgaard M, Cserr H, Murray M (1979a) Impermeability of hagfish cerebral capillaries to horseradish peroxidase. Cell Tissue Res 198:65–77
Bundgaard M, Frøkjaer-Jensen J, Crone C (1979b) Endothelial plasmalemmal vesicles as elements in a system of branching invaginations from the cell surface. Proc Natl Acad Sci USA 76:6439–6442
Burkel WE (1967) The histological fine structure of perineurium. Anat Rec 158:177–190
Curry FE, Michel CC (1980) A fiber matrix model of capillary permeability. Microvasc Res 20:96–99
Frøkjaer-Jensen J (1980) Three-dimensional organization of plasmalemmal vesicles in endothelial cells. An analysis by serial sectioning of frog mesenteric capillaries. J Ultrastruct Res 73:9–20
Karnovsky MJ (1967) The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J Cell Biol 35:213–236
Kristensson K, Olsson Y (1971) The perineurium as a diffusion barrier to protein tracers. Differences between mature and immature animals. Acta Neuropathol (Berl) 17:127–138
Kristensson K, Olsson Y (1976) Osmotic opening of perineurial diffusion barrier in peripheral nerve. Neuropath and Applied Neurobiol 2:479–488
Krnjevic D (1954) Some observations on perfused frog sciatic nerve. J Physiol (Lond) 123:338–356
Masson-Pevét M, Gros D (1980) Pinocytotic function of the membrane vesicles, or caveolae, in heart muscle cells. In: Tajuddin IM, Das PK, Tariq M, Dhalla NS (eds) Advances in Myocardiology, vol I. University Park Press, Baltimore, pp 23–31
Mazzone RW, Kornblau SM (1981) Pinocytotic vesicles in the endothelium of rapidly frozen rabbit lung. Microvasc Res 21:193–211
Olsson Y, Reese TS (1971) Permeability of vasa nervorum and perineurium in mouse sciatic nerve studied by fluorescence and electron microscopy. J Neuropath Exp Neurol 30:105–119
Palade GE, Bruns RR (1964) Structural modulations of plasmalemmal vesicles. J Cell Biol 37:633–649
Revel JP, Karnovsky M (1967) Hexogonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol 33:C7-C12
Shaklai M, Tavassoli M (1977) A modern technique to obtain uniform precipitation of lanthanum tracer in the extracellular space. J Histochem Cytochem 25:1013–1015
Shinowara NL, Michel ME, Rapoport SI (1981) Variations in vesicular morphology in the frog perineurium demonstrated with lanthanum and steroscopic electron microscopy. Soc Neurosci Astr 7:307
Shinowara NL, Michel ME, Rapoport SI (1982) Morphological correlates of tracer permeability through the perineurial barrier of frog peripheral nerve. Anat Rec Abstr 176A
Simionescu N, Simionescu M, Palade GE (1975) Permeability of muscle capillaries to small hemepeptides: Evidence for the existence of patent transendothelial channels. J Cell Biol 64:586–607
Simionescu N, Simionescu M, Palade GE (1978) Structural basis of permeability in sequential segments of the microvasculature of the diaphragm. II. Pathways followed by microperoxidase across the endothelium. Microvasc Res 15:17–36
Thomas PK (1963) The connective tissue of peripheral nerve: an electron microscope study. J Anat (Lond) 97:35–44
Waggener JD, Bunn SM, Beggs J (1965) The diffusion of ferritin within the peripheral nerve sheath: an electron microscopy study. J Neuropath Exp Neurol 24:430–443
Weerasuriya A, Rapoport SI, Taylor RE (1979a) Modification of permeability of frog perineurium to [14C] sucrose by stretch and hypertonicity. Brain Res 173:503–512
Weerasuriya A, Spangler RA, Rapoport SI, Taylor RE (1979b) Electrical impedance of the perineurium of the frog sciatic nerve. Biophys J 25:300a
Weerasuriya A, Rapoport SI, Taylor RE (1980) Ionic permeabilities of the frog perineurium. Brain Res 191:405–415
Westergaard E, Brightman MW (1973) Transport of proteins across normal cerebral arterioles. J Comp Neurol 152:17–44
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Shinowara, N.L., Michel, M.E. & Rapoport, S.I. Morphological correlates of permeability in the frog perineurium: Vesicles and “transcellular channels”. Cell Tissue Res. 227, 11–22 (1982). https://doi.org/10.1007/BF00206328
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DOI: https://doi.org/10.1007/BF00206328