Summary
Protein uptake from cerebral ventricles into the epithelium of the choroid plexus, and transport across the epithelium were studied ultrastructurally in rats. Horseradish peroxidase (HRP, MW 40,000) was used as protein tracer. Steady-state ventriculo-cisternal perfusion with subatmospheric pressure (-10cm of water) in the ventricular system was applied. HRP dissolved in artificial CSF was perfused from the lateral ventricles to cisterna magna for various times, and ventriculo-cisternal perfusion, vascular perfusion or immersion fixation with a formaldehyde-glutaraldehyde solution was performed.
Coated micropinocytic vesicles containing HRP were seen both connected with the apical, lateral and basal epithelial surface and within the cells. Heavily HRP-labeled vesicles were often fused with the lining membrane of slightly labeled or unlabeled intercellular spaces. Since the apical tight junctions of the epithelium never appeared open or never contained HRP in the spaces between the fusion points, and since the intercellular spaces between adjacent epithelial cells below the junctions only infrequently contained tracer after 5 min, by increasing amounts after 15–60 min of HRP perfusion, a vesicular transport of HRP from the apical epithelial surface to the intercellular spaces, bypassing the tight junctions, is suggested.
In addition to the transepithelial transport, micropinocytic vesicles also transported HRP to the lysosomal apparatus of the epithelial cells. With increasing length of exposure to HRP, a sequence of HRP-labeled structures could be evaluated, from slightly labeled apical vacuoles and multivesicular bodies to very heavily labeled dense bodies.
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Becker, N.H., Almazon, R.: Evidence for the functional polarization of micropinocytotic vesicles in the rat choroid plexus. J. Histochem. Cytochem. 16, 278–279 (1968)
Becker, N.H., Hirano, A., Zimmerman, H.M.: Observations of the distribution of exogenous peroxidase in the rat cerebrum. J. Neuropath, exp. Neurol. 27, 439–452 (1968)
Becker, N.H., Novikoff, A.B., Zimmerman, H.M.: Fine structure observations of the uptake of intravenously injected peroxidase by the rat choroid plexus. J. Histochem. Cytochem. 15, 160–165 (1967)
Becker, N.H., Sutton, C.H.: Pathologic features of the choroid plexus. 1. Cytochemical effects of hypervitaminosis A. Amer. J. Path. 43, 1017–1030 (1963)
Bohman, S.-O., Maunsbach, A.B.: Effects on tissue fine structure of variations in colloid osmotic pressure of glutaraldehyde fixatives. J. Ultrastruct. Res. 30, 195–208 (1970)
Brightman, M.W.: Ultrastructural characteristics of adult choroid plexus: Relation to the blood-cerebrospinal fluid barrier to proteins. In: The choroid plexus in health and disease (M.G. Netsky and S. Shuangshati, eds.), pp. 86–112. Charlottesville: University Press of Virginia 1975
Brightman, M.W., Reese, T.S., Feder, N.: Assessment with the electron microscope of the permeability to peroxidase of cerebral endothelium and epithelium in mice and sharks. In: Capillary permeability. The transfer of molecules and ions between capillary blood and tissue (C. Crone and N.A. Lassen, eds.), pp. 468–476. Alfred Benzon Symposium II. Copenhagen: Munksgaard 1970
Bulger, R.E., Trump, B.F.: A mechanism for rapid transport of colloidal particles by flounder renal epithelium. J. Morph. 127, 205–224 (1969)
Cancilla, P.A., Zimmerman, H.M., Becker, N.H.: A histochemical and fine structure study of the developing rat choroid plexus. Acta neuropath. (Berl.) 6, 188–200 (1966)
Cornell, R., Walker, W.A., Isselbacher, K.J.: Small intestinal absorption of horseradish peroxidase. A cytochemical study. Lab. Invest. 25, 42–48 (1971)
Davis, D.A., Lloyd, B.J., Milhorat, T.H.: A comparative ultrastructural study of the choroid plexus of the immature pig. Anat. Rec. 176, 443–456 (1973)
Davis, D.A., Milhorat, T.H.: The blood-brain barrier of the rat choroid plexus. Anat. Rec. 181, 779–790 (1975)
Davson, H.: Physiology of the cerebrospinal fluid. London: J &A Churchill 1967
Deimann, W., Taugner, R., Fahimi, H.D.: Arterial hypotension induced by horseradish peroxidase in various rat strains. J. Histochem. Cytochem. 24, 1213–1217 (1976)
del Cerro, M.: Uptake of tracer proteins in the developing cerebellum, particularly by the growth cones and blood vessels. J. comp. Neurol. 157, 245–280 (1974)
Graham, R.C., Karnovsky, M.J.: The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14, 291–302 (1966)
Hochwald, G.M., Wallenstein, M.: Exchange of albumin between blood, cerebrospinal fluid, and brain in the cat. Amer. J. Physiol. 212, 1199–1204 (1967)
Mata, L.R.: Dynamics of HRPase absorption in the epithelial cells of the hamster seminal vesicles. J. Microscopic Biol. Cell. 25, 127–132 (1976)
Maunsbach, A.B., Christensen, E.I., Ottosen, P.D., Larsson, L.: Uptake, transport and digestion of proteins in kidney cells. In: Proc. IV Internat. Congr. Histochem. Cytochem. (T. Takevchi, K. Ogawa, S. Fujita, eds.), p. 65. Kyoto: Nakanishi Printing Co. 1972
Møller, M., van Deurs, B., Westergaard, E.: Transendothelial pathways for horseradisch peroxidase in fenestrated capillaries. J. Ultrastruct. Res. 57, 227 (1976) (Abstract)
Møllgård, K., Malinowska, D.H., Saunders, N.R.: Lack of correlation between tight junction morphology and permeability properties in developing choroid plexus. Nature (Lond.) 264, 293–294 (1976)
Møllgård, K., Saunders, N.R.: Complex tight junctions of epithelial and of endothelial cells in early foetal brain. J. Neurocytol. 4, 453–468 (1975)
Moxon, L.A., Wild, A.E., Slade, B.S.: Localisation of proteins in coated micropinocytic vesicles during transport across rabbit yolk sac endoderm. Cell Tiss. Res. 171, 175–193 (1976)
Orlic, D., Lev, R.: Fetal rat intestinal absorption of horseradish peroxidase from swallowed amniotic fluid. J. Cell Biol. 56, 106–119 (1973)
Ottosen, P.D.: Effect of intraluminal pressure on the ultrastructure and protein transport in the proximal tubule. Kidney Int. 9, 252–263 (1976)
Ottosen, P.D., Maunsbach, A.B.: Transport of peroxidase in flounder kidney tubules studied by electron microscope histochemistry. Kidney Int. 3, 315–326 (1973)
Rodewald, R.: Intestinal transport of antibodies in the newborn rat. J. Cell Biol. 58, 189–211 (1973)
Simionescu, N., Simionescu, M., Palade, G.E.: Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J. Cell Biol. 64, 586–607 (1975)
Smith, D.E., Streicher, E., Milković, K., Klatzo, I.: Observations on the transport of proteins by the isolated choroid plexus. Acta neuropath. (Berl.) 3, 372–386 (1964)
Straus, W.: Altered renal cortical reabsorption of protein and urinary excretion of sodium in relation to vascular leakage induced by horseradish peroxidase. J. Histochem. Cytochem. 25, 215–225 (1977)
Tennyson, V.M., Pappas, G.D.: Electromicroscope studies of the developing telencephalic choroid plexus in normal and hydrocephalic rabbits. In: Disorders of the developing nervous system (W.S. Fields and M.M. Desmond, eds.), pp. 267–318. Springfield: Charles C. Thomas 1961
van Deurs, B.: Choroid plexus absorption of horseradish peroxidase from the cerebral ventricles. J. Ultrastruct. Res. 55, 400–416 (1976a)
van Deurs, B.: Observations on the blood-brain barrier in hypertensive rats, with particular reference to phagocytic pericytes. J. Ultrastruct. Res. 56, 65–77 (1976b)
van Deurs, B.: Vesicular transport of horseradish peroxidase from brain to blood in segments of the cerebral microvasculature in adult mice. Brain Res. 124, 1–8 (1977)
van Deurs, B.: Horseradish peroxidase uptake into the rat choroid plexus epithelium, with special reference to the lysosomal system. J. Ultrastruct. Res., in Press (1978a)
van Deurs, B.: Microperoxidase uptake into the rat choroid plexus epithelium. J. Ultrastruct. Res., in Press (1978b)
van Deurs, B., Møller, M., Amtorp, O.: CSF to blood transport of protein in the choroid plexus. Vesicular bypass of epithelial tight junctions. J. Ultrastruct. Res., in Press (1978) (Abstract)
Wagner, H.J., Pilgrim, Ch., Brandi, J.: Penetration and removal of horseradish peroxidase injected into the cerebrospinal fluid: role of cerebral perivascular spaces, endothelium and microglia. Acta neuropath. (Berl.) 27, 299–315 (1974)
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van Deurs, B., Møller, M. & Amtorp, O. Uptake of horseradish peroxidase from CSF into the choroid plexus of the rat, with special reference to transepithelial transport. Cell Tissue Res. 187, 215–234 (1978). https://doi.org/10.1007/BF00224366
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DOI: https://doi.org/10.1007/BF00224366