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Endothelial Vesicles in the Blood–Brain Barrier: Are They Related to Permeability?

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Abstract

1. Macromolecules cross capillary walls via large vascular pores that are thought to be formed by plasmalemmal vesicles. Early hypotheses suggested that vesicles transferred plasma constituents across the endothelial wall either by a “shuttle” mechanism or by fusing to form transient patent channels for diffusion. Recent evidence shows that the transcytotic pathway involves both movement of vesicles within the cell and a series of fusions and fissions of the vesicular and cellular membranes.

2. The transfer of macromolecules across the capillary wall is highly specific and is mediated by receptors incorporated into specific membrane domains. Therefore, despite their morphological similarity, endothelial vesicles form heterogeneous populations in which the predominant receptor proteins incorporated in their membranes define the functions of individual vesicles.

3. Blood–brain barrier capillaries have very low permeabilities to most hydrophilic molecules. Their low permeability to macromolecules has been presumed to be due to an inhibition of the transcytotic mechanism, resulting in a low density of endothelial vesicles.

4. A comparison of vesicular densities and protein permeabilities in a number of vascular beds shows only a very weak correlation, therefore vesicle numbers alone cannot be used to predict permeability to macromolecules.

5. Blood–brain barrier capillaries are fully capable of transcytosing specific proteins, for example, insulin and transferrin, although the details are still somewhat controversial.

6. It has recently been shown that the albumin binding protein gp60 (also known as albondin), which facilitates the transcytosis of native albumin in other vascular beds, is virtually absent in brain capillaries.

7. It seems likely that the low blood–brain barrier permeability to macromolecules may be due to a low level of expression of specific receptors, rather than to an inhibition of the transcytosis mechanism.

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REFERENCES

  • Balin, B. J., Broadwell, R. D., and Salcman, M. (1987). Tubular profiles do not form transendothelial channels through the blood-brain barrier. J. Neurocytol. 16:721-735.

    Google Scholar 

  • Banks, W. A., and Broadwell, R. D. (1994). Blood to brain and brain to blood passage of native horseradish peroxidase, wheat germ agglutinin, and albumin: Pharmacokinetic and morphological assessments. J. Neurochem. 62:2404-2419.

    Google Scholar 

  • Bearer, E. L., Orci, L., and Sors, P. (1985). Endothelial fenestral diaphragms: A quick-freeze, deepetch study. Cell Biol. 100:418-428.

    Google Scholar 

  • Bellhorn, R. W. (1980). Permeability of blood-ocular barriers of neonatal and adult cat to sodium fluorescein. Invest. Ophthalmol. Vis. Sci. 19:870-877.

    Google Scholar 

  • Bendayan, M., and Raskova, J. (1996). Transport of insulin and albumin by the microvascular endothelium of the rete mirabile. J. Cell Sci. 109:1857-1864.

    Google Scholar 

  • Bent-Hansen, L. (1991). Initial plasma disappearance and tissue uptake of 131I-albumin in normal rabbits. Microvasc. Res. 41:345-356.

    Google Scholar 

  • Bill, A. (1977). Plasma protein dynamics: albumin and IgG capillary permeability, extravascular movement and regional blood flow in unanesthetized rabbits. Acta Physiol. Scand. 101:28-42.

    Google Scholar 

  • Broadwell, R. D. (1989). Transcytosis of macromolecules through the blood-brain barrier: A cell biological perspective and critical appraisal. Acta Neuropathol. 79:117-128.

    Google Scholar 

  • Broadwell, R. D., Baker-Cairns, B. J., Frieden, P. M., Oliver, C., and Villegas, J. C. (1996). Transcytosis of protein through the mammalian cerebral epithelium and endothelium. III. Receptor-mediated transcytosis through the blood-brain barrier of blood-borne transferrin and antibody against the transferrin receptor. Exp. Neurol. 142:47-65.

    Google Scholar 

  • Buchanan, R. A., Wagner, R. C., Andrews, S. B., and Frokjær-Jensen, J. (1988). Effect of section thickness on the morphological characterization of the vesicular system in endothelial cells. Microvasc. Res. 36:191-196.

    Google Scholar 

  • Bundgaard, M. (1983). Vesicular transport in capillary endothelium: Does it occur? Fed. Proc. 42:2425-2430.

    Google Scholar 

  • Bundgaard, M., and Frokjær-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.

    Google Scholar 

  • Bundgaard, M., Frokjær-Jensen, J., and Crone, C. (1979). Endothelial plasmalemmal vesicles as elements in a system of branching invaginations from the cell surface. Proc. Natl. Acad. Sci. USA 76:6439-6442.

    Google Scholar 

  • Bundgaard, M., Hagman, P., and Crone, C. (1983). The three-dimensional organization of plasmalemmal vesicular profiles in the endothelium of rat heart capillaries. Microvasc. Res. 25:358-368.

    Google Scholar 

  • Casley-Smith, J. R., Green, H. S., Harris, J. L., and Wadey, P. J. (1975). The quantitative morphology of skeletal muscle capillaries in relation to permeability. Microvasc. Res. 10:43-64.

    Google Scholar 

  • Connell, C. J., and Mercer, K. L. (1974). Freeze-fracture appearance of the capillary endothelium in the cerebral cortex of mouse brain. Am. J. Anat. 140:595-599.

    Google Scholar 

  • Coomber, B. L., and Stewart, P. A. (1985). Morphometric analysis of CNS microvascular endothelium. Microvasc. Res. 30:99-115.

    Google Scholar 

  • Coomber, B. L., Stewart, P. A., Hayakawa, E. M., Farrell, C. L., and Del Maestro, R. F. (1988). A quantitative assessment of microvessel ultrastructure in C6 astrocytoma spheroids transplanted to brain and to muscle. J. Neuropathol. Exp. Neurol. 47:29-40.

    Google Scholar 

  • Crowe, A., and Morgan, E. H. (1992). Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res. 592:8-16.

    Google Scholar 

  • Cunha-Vaz, J. G., Shakib, M., and Ashton, N. (1966). Studies on the permeability of the blood-retinal barrier. 1. On the existence, development, and site of a blood-retinal barrier. Br. J. Ophthalmol. 50:441-453.

    Google Scholar 

  • Davson, H., and Oldendorf, W. H. (1967). Transport in the central nervous system. Proc. Roy. Soc. Med. 60:326-329.

    Google Scholar 

  • DeFouw, D. O., and Shumko, J. Z. (1986). Pulmonary microcirculation: Differences in endothelia of subpleural and alveolar capillaries. Microvasc. Res. 32:348-358.

    Google Scholar 

  • De Paepe, M. E., Corriveau, M., Tannous, W. N., Seemayer, T. A., and Colle, E. (1992). Increased vascular permeability in pancreas of diabetic rats: Detection with high resolution protein A-gold cytochemistry. Diabetologia 35:1118-1124.

    Google Scholar 

  • Duffy, K. R., and Pardridge, W. M. (1987). Blood-brain barrier transcytosis of insulin in developing rabbits. Brain Res. 420:32-38.

    Google Scholar 

  • Dvorak, A. M., Kohn, S., Morgan, E. H., Fox, P., and Nagy, J. A. (1996). The vesiculo-vacuolar organelle (VV): A distinct endothelial cell structure that provides a transcellular pathway for macromolecular extravasation. J. Leucoc. Biol. 59:100-115.

    Google Scholar 

  • Dym, M., and Cavicchia, J. C. (1977). Further observations on the blood-testis barrier in monkeys. Biol. Reprod. 17:390-403.

    Google Scholar 

  • Dym, M., and Fawcett, D. W. (1970). The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol. Reprod. 38:308-326.

    Google Scholar 

  • Dziegielewska, K. M., Evans, C. A. N., Malinowska, D. H., Møllgård, K., Reynolds, M. L., and Saunders, N. R. (1980). Blood-cerebrospinal fluid transfer of plasma proteins during fetal development in the sheep. J. Physiol. 300:457-465.

    Google Scholar 

  • Dziegielewska, K. M., Habgood, M. D., Møllgård, K., Stagaard, M., and Saunders, N. R. (1991). Speciesspecific transfer of plasma albumin from blood into different cerebrospinal fluid compartments in the fetal sheep. J. Physiol. 439:215-237.

    Google Scholar 

  • Everett, N. B., and Simmons, B. (1958). Measurement and radioautographic localization of albumin in rat tissues after intravenous administration. Circ. Res. 6:307-313.

    Google Scholar 

  • Fawcett, D. W., Leak, L. V., and Heidger, P. M. (1970). Electron microscopic observations on the structural components of the blood-testis barrier. J. Reprod. Fert. Suppl. 10:105-122.

    Google Scholar 

  • Frokjær-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.

    Google Scholar 

  • Frokjær-Jensen, J. (1983). The plasmalemmal vesicular system in capillary endothelium. In Mebmer, K., and Hammersen, F. (eds.), Structure and Function of Endothelial Cells. Progress in Applied Microcirculation, Vol. 1, Karger, Basel, pp. 17-34.

    Google Scholar 

  • Frokjær-Jensen, J. (1984). The plasmalemmal vesicular system in striated muscle capillaries and in pericytes. Tissue Cell 16:31-42.

    Google Scholar 

  • Frokjær-Jensen, J. (1990). Anatomical correlates of capillary permeability. In Molinatti, G. M., Bar, R. S., Belfiore, R., and Porta, M. (eds.), Diabetic Microangiopathy: Problems in Methodology and Clinical Aspects, Karger, Basel, pp. 28-42.

    Google Scholar 

  • Ghinea, N., Eskenasy, M., Simionescu, M., and Simionescu, N. (1988). Identification of albumin-binding proteins in capillary endothelial cells. J. Cell Biol. 107:231-239.

    Google Scholar 

  • Ghinea, N., Eskenasy, M., Simionescu, M., and Simionescu, N. (1989). Endothelial albumin binding proteins are membrane-associated components exposed on the cell surface. J. Biol. Chem. 264:4755-4758.

    Google Scholar 

  • Ghitescu, L., and Bendayan, M. (1992). Transendothelial transport of serum albumin: A quantitative immunocytochemical study. J. Cell Biol. 117:745-755.

    Google Scholar 

  • Gordon, S. R., and Essner, E. (1985). Plasma membrane-associated vesicles in retinal capillaries of the rat. Am. J. Anat. 174:161-172.

    Google Scholar 

  • Granger, D. N., and Taylor, E. H. (1980). Permeability of intestinal capillaries to endogenous macromolecules. Am. J. Physiol. 238:H457-H464

    Google Scholar 

  • Habgood, M. D., Sedgwick, J. E. C., Dziegielewska, K. M., and Saunders, N. R. (1992). Adevelopmentally regulated blood-cerebrospinal fluid transfer mechanism for albumin in immature rats. J. Physiol. 456:181-192.

    Google Scholar 

  • Habgood, M. D., Knott, G. W., Dziegielewska, K. M., and Saunders, N. R. (1993). The nature of the decrease in blood-cerebrospinal fluid barrier exchange during postnatal brain development in the rat. J. Physiol. 468:73-83.

    Google Scholar 

  • Hart, T. K., and Pino, R. M. (1986). Pseudoislet vascularization. Induction of diaphragm-fenestrated endothelia from the hepatic sinusoids. Lab. Invest. 54:304-313.

    Google Scholar 

  • Holash, J. A., Harik, S. I., Perry, G., and Stewart, P. A. (1993). Barrier properties of testis microvessels. Proc. Natl. Acad. Sci. USA 90:11069-11073.

    Google Scholar 

  • Horvat, R., and Palade, G. E. (1993). Thrombomodulin and thrombin localization on the vascular endothelium; Their internalization and transcytosis by plasmalemmal vesicles. Eur. J. Cell Biol. 61:299-313.

    Google Scholar 

  • Johansson, B. R. (1979). Size and distribution of endothelial plasmalemmal vesicles in consecutive segments of the microvasculature in cat skeletal muscle. Microvasc. Res. 17:107-117.

    Google Scholar 

  • Jones, W. R., O'Morchoe, P. J., and O'Morchoe, C. C. C. (1983). The organization of endocytotic vesicles in lymphatic endothelium. Microvasc. Res. 25:286-299.

    Google Scholar 

  • Knott, G. W., Dziegielewska, K. M., Habgood, M. D., Li, Z., and Saunders, N. R. (1997). Albumin transfer across the choroid plexus of South American opossum (Monodelphis domestica). J. Physiol. 499:179-194.

    Google Scholar 

  • Kvietys, P. R., Perry, M. A., and Granger, D. N. (1983). Permeability of pancreatic capillaries to small molecules. Am. J. Physiol. 245:G519-G524.

    Google Scholar 

  • Lea, P. J. (1983). Image analysis system based on a non-dedicated microcomputer. Micron Microsc. Acta 14:301-306.

    Google Scholar 

  • Levick, J. R., and Smaje, L. H. (1987). An analysis of the permeability of a fenestra. Microvasc. Res. 33:233-256.

    Google Scholar 

  • McGuire, P. G., and Twietmeyer, T. A. (1983). Morphology of rapidly frozen aortic endothelial cells. Circ. Res. 53:424-429.

    Google Scholar 

  • Mellman, I. (1996). Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12:575-625.

    Google Scholar 

  • Milici, A. J., L'hernault, N., and Palade, G. E. (1985). Surface densities of diaphragmed fenestrae and transendothelial channels in different murine capillary beds. Circ. Res. 56:709-717.

    Google Scholar 

  • Milici, A. J., Watrous, N. E., Stukenbrok, H., and Palade, G. E. (1987). Transcytosis of albumin in capillary endothelium. J. Cell Biol. 105:2603-2612.

    Google Scholar 

  • Moos, T., and Mollgård, K. (1993). Cerebrovascular permeability to azo dyes and plasma proteins in rodents of different ages. Neuropathol. Appl. Neurobiol. 19:120-127.

    Google Scholar 

  • Morioka, T., Baba, T., Black, K. L., and Streit, W. J. (1992). Inflammatory cell infiltrates vary in experimental primary and metastatic brain tumors. Neurosurgery 30:891-896.

    Google Scholar 

  • Morris, C. M., Keith, A. B., Edwardson, J. A., and Pullen, R. G. L. (1992). Uptake and distribution of iron and transferrin in the adult rat brain. J. Neurochem. 59:300-306.

    Google Scholar 

  • Mukherjee, S., Ghosh, R. N., and Maxfield, F. R. (1997). Endocytosis. Physiol. Rev. 77:759-800.

    Google Scholar 

  • Nag, S. (1991). Protective effect of flunarizine on blood-brain barrier permeability alterations in acutely hypertensive rats. Stroke 22:1265-1269.

    Google Scholar 

  • Palade, G. E. (1961). Blood capillaries of the heart and other organs. Circulation 24:368-384.

    Google Scholar 

  • Palade, G. E., Simionescu, M., and Simionescu, N. (1979). Structural aspects of the permeability of the microvascular endothelium. Acta Physiol. Scand. 463:11-32.

    Google Scholar 

  • Pardridge, W. M., Eisenberg, J., and Cefalu, W. T. (1985). Absence of albumin receptor on brain capillaries in vivo or in vitro. Am. J. Physiol. 249:E264-E267.

    Google Scholar 

  • Pino, R. M. (1985). Restriction to endogenous plasma proteins by a fenestrated capillary endothelium: An ultrastructural immunocytochemical study of the choriocapillary endothelium. Am. J. Anat. 172:279-289.

    Google Scholar 

  • Pino, R. M., and Essner, E. (1993). Structure and permeability to ferritin of the choriocapillary endothelium of the rat eye. Cell Tissue Res. 208:21-27.

    Google Scholar 

  • Powers, R. W., Chen, L., Russell, P. T., and Larsen, W. J. (1995). Gonadotropin-stimulated regulation of blood-follicle barrier is mediated by nitric oxide. Am. J. Physiol. 269:E290-E298.

    Google Scholar 

  • Predescu, D. N., Horvat, R., Predescu, S. A., and Palade, G. E. (1994). Transcytosis in the continuous endothelium of the myocardial microvasculature is inhibited by N-ethylmaleimide. Proc. Natl. Acad. Sci. USA 91:3014-3018.

    Google Scholar 

  • Raviola, G., and Butler, J. M. (1984). Unidirectional transport mechanism of horseradish peroxidase in the vessels of the iris. Invest. Ophthalmol. Vis. Sci. 25:827-836.

    Google Scholar 

  • Reese, T. S., and Karnovsky, M. J. (1967). Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell Biol. 34:207-217.

    Google Scholar 

  • Roberts, R., Sandra, A., Siek, G. C., Lucas, J. J., and Fine, R. E. (1992). Studies of the mechanism of iron transport across the blood-brain barrier. Ann. Neurol. 32 (Suppl.):S43-S50.

    Google Scholar 

  • Roberts, R. L., Fine, R. E., and Sandra, A. (1993). Receptor-mediated endocytosis of transferrin at the blood-brain barrier. J. Cell Sci. 104:521-532.

    Google Scholar 

  • Sadasivudu, B., Murthy, C. R. K., Roa, G. N., and Swamy, M. (1983). Studies on acetylcholinesterase and gamma-glutamyltranspeptidase in mouse brain in ammonia toxicity. J. Neurosci. Res. 9:127-134.

    Google Scholar 

  • Schnitzer, J. E. (1992). gp60 is an albumin-binding glycoprotein expressed by continuous endothelium involved in albumin transcytosis. Am. J. Physiol. 262:H246-H254.

    Google Scholar 

  • Schnitzer, J. E., and Oh, P. (1994). Albondin-mediated capillary permeability to albumin. Differential role of receptors in endothelial transcytosis and endocytosis of native and modified albumins. J. Biol. Chem. 269:6072-6082.

    Google Scholar 

  • Schnitzer, J., Oh, P., Pinney, E., and Allard, J. (1994). Filipin-sensitive caveolae-mediated transport in endothelium: Reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127:1217-1232.

    Google Scholar 

  • Schnitzer, J. E., Allard, J., and Oh, P. (1995). NEM inhibits transcytosis, endocytosis, and capillary permeability: Implication of caveolae fusion in endothelia. Am. J. Physiol. 268:H48-H55.

    Google Scholar 

  • Schwartz, M. W., Sipols, A., Kahn, S. E., Lattemann, D. F., Taborsky, G. J., Jr., Bergman, R. N., Woods, S. C., and Porte, D., Jr. (1990). Kinetics and specificity of insulin uptake from plasma into cerebrospinal fluid. Am. J. Physiol. Endocrinol. Metab. 259:E378-E383.

    Google Scholar 

  • Sejrsen, P., Paaske, W. P., and Henriksen, O. (1985). Capillary permeability of 131I-albumin in skeletal muscle. Microvasc. Res. 29:265-281.

    Google Scholar 

  • Setchell, B. P., Pöllänen, P., and Zupp, J. L. (1988). Development of the blood-testis barrier and changes in vascular permeability at puberty in rats. Int. J. Androl. 11:225-253.

    Google Scholar 

  • Simionescu, M., Simionescu, N., and Palade, G. E. (1974). Morphometric data on the endothelium of blood capillaries. J. Cell Biol. 60:128-152.

    Google Scholar 

  • Simionescu, N., Simionescu, M., and Palade, G. E. (1975). Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J. Cell Biol. 64:586-607.

    Google Scholar 

  • Simionescu, N., Simionescu, M., and Palade, G. E. (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.

    Google Scholar 

  • Smith, R. S., and Rudt, L. A. (1975). Ocular vascular and epithelial barriers to microperoxidase. Invest. Ophthalmol. Vis. Sci. 14:556-560.

    Google Scholar 

  • Stewart, P. A., and Hayakawa, K. (1994). Early ultrastructural changes in blood-brain barrier vessels of the rat embryo. Dev. Brain Res. 78:25-34.

    Google Scholar 

  • Stewart, P. A., and Tuor, U. I. (1994). Blood-eye barriers in the rat: Correlation of ultrastructure with function. J. Comp. Neurol. 340:566-576.

    Google Scholar 

  • Stewart, P. A., Hayakawa, K., Hayakawa, E. M., Farrell, C. L., and Del Maestro, R. F. (1985). A quantitative study of blood-brain barrier permeability ultrastructure in a new rat glioma model. Acta Neuropathol. 67:96-102.

    Google Scholar 

  • Stewart, P. A., Magliocco, M., Hayakawa, K., Farrell, C. L., Del Maestro, R. F., Girvin, J., Kaufmann, J. C. E., Vinters, H. V., and Gilbert, J. J. (1987). A quantitative analysis of blood-brain barrier ultrastructure in the aging human. Microvasc. Res. 33:270-282.

    Google Scholar 

  • Stewart, P. A., Farrell, C. R., Farrell, C. L., and Hayakawa, E. M. (1992). Horseradish peroxidase retention and washout in blood-brain barrier lesions. J. Neurosci. Methods 41:75-84.

    Google Scholar 

  • Stewart, P. A., Isaacs, H., LaManna, J. C., and Harik, S. I. (1997). Ultrastructural concomitants of hypoxia-induced angiogenesis. Acta Neuropathol. 93:579-584.

    Google Scholar 

  • Svendsen, J. H., Paaske, W. P., Sejrsen, P., and Haunsø, S. (1989). Capillary permeability of 131Ialbumin in canine myocardium as determined by bolus injection, residue detection. Microvasc. Res. 37:352-356.

    Google Scholar 

  • Szalay, J., Nunziata, B., and Henkind, P. (1975). Permeability of iridial blood vessels. Exp. Eye Res. 21:531-543.

    Google Scholar 

  • Tiruppathi, C., Finnegan, A., and Malik, A. B. (1996). Isolation and characterization of a cell surface albumin-binding protein from vascular endothelial cells. Proc. Natl. Acad. Sci. USA 93:250-254.

    Google Scholar 

  • Villegas, J. C., and Broadwell, R. D. (1993). Transcytosis of protein through the mammalian cerebral epithelium and endothelium. 11. Adsorptive transcytosis of WGA-HRP and the blood-brain and brain-blood barriers. J. Neurocytol. 22:67-80.

    Google Scholar 

  • Vorbrodt, A. W., and Dobrogowska, D. H. (1994). Immunocytochemical evaluation of blood-brain barrier to endogenous albumin in adult, newborn and aged mice. Folia Histochem. Cytobiol. 32:63-70.

    Google Scholar 

  • Vorbrodt, A. W., Dobrogowska, D. H., and Lossinsky, A. S. (1994). Ultrastructural study on the interaction of insulin-albumin-gold complex with mouse brain microvascular endothelial cells. J. Neurocytol. 23:201-208.

    Google Scholar 

  • Wagner, R. C. (1984). Application of high voltage electron microscopy to visualize the three-dimensional structure of the vesicular system in thick sections. Int. J. Microcirc. Clin. Exp. 3:413-413.

    Google Scholar 

  • Wagner, R. C., and Andrews, S. B. (1985). Ultrastructure of the vesicular system in rapidly frozen capillary endothelium of the rete mirabile. J. Ultrastruct. Res. 90:172.

    Google Scholar 

  • Wagner, R. C., and Casley-Smith, J. R. (1981). The quantitative morphometry of capillaries isolated from fat. Microcirculation 1:177-197.

    Google Scholar 

  • Wagner, R. C., and Robinson, C. S. (1982). Tannic acid tracer analysis of permeability pathways in the capillaries of the rete mirabile: Demonstration of the discreteness of endothelial vesicles. J. Ultrastruct. Res. 81:37-46.

    Google Scholar 

  • Wagner, R. C., and Robinson, C. S. (1984). High-voltage electron microscopy of capillary endothelial vesicles. Microvasc. Res. 28:197-205.

    Google Scholar 

  • Weibel, E. R. (1979). Stereological Methods, Vol. 1. Practical Methods for Biological Morphometry, 1st ed., Academic Press, Toronto.

    Google Scholar 

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Stewart, P.A. Endothelial Vesicles in the Blood–Brain Barrier: Are They Related to Permeability?. Cell Mol Neurobiol 20, 149–163 (2000). https://doi.org/10.1023/A:1007026504843

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