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Feinbau und Passageverhalten der Capillaren im Subcommissuralorgan der Ratte

Ultrastructure and vascular permeability of the capillaries in the subcommissural organ of rats

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Summary

The capillaries of the subcommissural organ (SCO) and their adjacent structures of 38 adult Sprague-Dawley rats and 6 adult Wistar rats were examined in the electron microscope after perfusion fixation. Acid mucopolysaccharides were shown by Alcian Blue and Ruthenium Red, glycoproteins were identified by the periodic acid-silver methenamine technique. Horseradish peroxidase (MRP) was used as a tracer for vascular permeability.

The subcommissural organ's capillaries are characterized by an unfenestrated, continuous endothelium, showing only few vesicles; the endothelium is surrounded by a single, continuous basal lamina. Adjacent to the capillaries wall there are “periodically structured bodies” (PSK), labyrinths of the basal lamina and irregularly arranged collagen fibrils. Glycoproteins are found in the basal lamina and within the intercellular clefts; in a few cases groups of parallel arranged, periodically banded linear structures are seen within or adjacent to the basal lamina. Acid mucopolysaccharides are found within the endocapillary layer of capillaries. It seems very likely that PSK represent an atypical arrangement of collagen fibrils. The formation of these structures is discussed.

Under normal conditions, MRP, after intravenous injection, does not enter the perivascular space surrounding the capillaries of the SCO. A blood-brain barrier exists at the level of the capillary endothelium. In a few Sprague-Dawley rats MRP seems to alter the permeability of the capillaries. Reaction product of MRP is found within endothelial vesicles and the adjacent structures. It appears that the basal lamina and the PSK are not involved in the barrier mechanism or regulation of transport. In Sprague-Dawley rats intravenous injection of MRP seems to alter the blood-brain barrier by release of endogenous biogenic amines associated with mast cell degranulation. This effect is not observed in Wistar rats.

Zusammenfassung

Die Capillaren des Subcommissuralorgans (SCO) und deren Umgebung wurden an 38 adulten Sprague-Dawley- und an 6 adulten Wistar-Ratten nach Perfusionsfixierung im Elektronenmikroskop untersucht. Saure Mucopolysaccharide wurden mit Alcianblau und Rutheniumrot, Glykoproteide mittels der Perjodsäure-Silbermethenamin-Reaktion nachgewiesen. Der Stofftransport in den Capillaren wurde mit Meerrettichperoxidase (MRP) als Tracer untersucht.

Die subcommissuralen Capillaren besitzen ein ungefenstertes, vesikelarmes Endothel, das einer einfachen, durchgehenden Basallamina aufsitzt. In der Umgebung der Capillaren finden sich neben periodisch strukturierten Körpern (PSK) vereinzelt Basallamina-Labyrinthe und regellos angeordnete kollagene Mikrofibrillen. Mit der Perjodsäure-Silbermethenamin-Reaktion lassen sich Glykoproteide im Bereich der Basallamina und der nach außen anschließenden Intercellularspalten darstellen, vereinzelt auch — teils im Bereich der Basallamina, teils ihr eng angeschlossen — Gruppen parallel angeordneter, linearer Strukturen mit einem periodischen Streifenmuster. Saure Mucopolysaccharide sind nur in der lumenseitigen Glykokalyx des Capillarendothels nachweisbar. Der Aufbau der PSK aus Kollagenfilamenten erscheint sehr wahrscheinlich. Vermutungen zur Entstehung dieser hochgeordneten Strukturen werden vorgebracht.

Die Traceruntersuchungen ergeben, daß unter normalen Bedingungen in den subcommissuralen Capillaren eine Blut-Hirn-Schranke (BHS) für MRP besteht, die im Endothel lokalisiert ist. Bei einem Teil der Sprague-Dawley-Ratten ist die Barriere geschädigt und der Tracer gelangt über cytopemptische Vesikel in Basallamina und Gefäßumgebung. Der Basallamina und den PSK kommt in solchen Fällen keine besondere Schranken- oder Verteilerfunktion zu. Offenbar bewirkt bei manchen Sprague-Dawley-Ratten die MRP-Injektion über die Freisetzung von endogenen biogenen Aminen aus Mastzellen eine Schädigung der BHS, was bei Wistar-Ratten nicht eintritt.

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Literatur

  • Andres, K. H.: Der Feinbau des Subfornikalorganes vom Hund. Z. Zellforsch. 68, 445–473 (1965)

    Google Scholar 

  • Becker, N. H., Novikoff, A. B., Zimmermann, H. M.: Fine structure observations of the uptake of intravenously injected peroxidase by the rat choroid plexus. J. Histochem. Cytochem. 15, 160–165 (1967)

    Google Scholar 

  • Behnke, O., Zelander, T.: Preservation of intercellular substances by the cationic dye alcian blue in preparative procedures for electron microscopy. J. Ultrastruct. Res. 31, 424–438 (1970)

    Google Scholar 

  • Bodenheimer, T. S., Brightman, M. W.: A blood-brain barrier to peroxidase in capillaries surrounded by perivascular spaces. Amer. J. Anat. 122, 249–268 (1968)

    Google Scholar 

  • 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)

    Google Scholar 

  • Bomhard, K. von, Köhl, W., Schinko, I.: Gefäßpassage von Markierungsstoffen im Subcommissuralorgan der Ratte. Verh. Anat. Ges., 68. Vers. Lausanne 1973. Anat. Anz., Erg.-H. (im Druck)

  • Booz, K. H., Desaga, U., Felsing, T., Franz, H., Stark, M.: Sub- und interependymale Basalmembranlabyrinthe am Zentralkanal der weißen Ratte. Z. Zellforsch. 132, 217–229 (1972)

    Google Scholar 

  • Bouteille, M., Pease, D. C.: The tridimensional structure of native collagenous fibrils, their proteinaceous filaments. J. Ultrastruct. Res. 35, 314–338 (1971)

    Google Scholar 

  • Breemen, V. L. van, Clemente, C. D.: Silver deposition in the central nervous system and the hematoencephalic barrier studied with the electron microscope. J. biophys. biochem. Cytol. 1, 161–166 (1955)

    Google Scholar 

  • Brightman, M. W.: The intracerebral movement of proteins injected into blood and cerebrospinal fluid of mice. Progr. Brain Res. 29, 19–37 (1968)

    Google Scholar 

  • Brightman, M. W., Klatzo, I., Olsson, Y., Reese, T. S.: The blood-brain barrier to proteins under normal and pathological conditions. J. neurol. Sci. 10, 215–239 (1970a)

    Google Scholar 

  • Brightman, M. W., Reese, T. S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969)

    Google Scholar 

  • 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 (Alfred Benzon Symposium II) (C. Crone, N. A. Lassen, eds.), p. 468–476. New York: Acad. Press, 1980b

    Google Scholar 

  • Bruchhausen, F. von, Merker, H.-J.: Morphologischer und chemischer Aufbau isolierter Basalmembranen aus der Nierenrinde der Ratte. Histochemie 8, 90–108 (1967)

    Google Scholar 

  • Chen, H.-C., Lin, C.-S., Lien, I.-N.: Vascular permeability in experimental kernicterus. An electron microscopic study of the blood-brain barrier. Amer. J. Path. 51, 69–87 (1967)

    Google Scholar 

  • Clawson, C. C., Hartmann, J. F., Vernier, R. L.: Electron microscopy of the effect of gram negative endotoxin on the blood-brain barrier. J. comp. Neurol. 127, 183–198 (1966)

    Google Scholar 

  • Cotran, R. S., Karnovsky, M. J.: Vascular leakage induced by horseradish peroxidase in the rat. Proc. Soc. exp. Biol. (N.Y.) 126, 557–561 (1967)

    Google Scholar 

  • Cotran, R. S., Karnovsky, M. J., Goth, A.: Resistance of Wistar/Furth rats to the mast cell-damaging effect of horseradish peroxidase. J. Histochem. Cytochem. 16, 382–383 (1968)

    Google Scholar 

  • Dempsey, E. W.: Fine-structure of the rat's intercolumnar tubercle and ist adjacent ependyma and choroid plexus, with especial reference to the appearance of its sinusoidal vessels in experimental argyria. Exp. Neurol. 22, 568–589 (1968)

    Google Scholar 

  • Dempsey, E. W., Wislocki, G. B.: An electron microscopic study of the blood-brain barrier in the rat, employing silver nitrate as a vital stain. J. biophys. biochem. Cytol. 1, 245–256 (1955)

    Google Scholar 

  • Dretzki, J.: Licht- und elektronenmikroskopische Untersuchungen zum Problem der Blut-Hirn-Schranke circumventrikulärer Organe der Ratte nach der Behandlung mit Myofer. Z. Anat. Entwickl.-Gesch. 134, 278–297 (1971)

    Google Scholar 

  • Duvernoy, H., Koritké, J. G.: The vascular architecture of the subcommissural organ. In: Zirkumventrikuläre Organe und Liquor. Bericht über das Symposium in Schloß Reinhardsbrunn vom 13.–16. Mai 1968, S. 41–43. Jena: VEB G. Fischer 1969

    Google Scholar 

  • Farquhar, M. G., Palade, G. E.: Cell junctions in amphibian skin. J. Cell Biol. 26, 263 (1965)

    Google Scholar 

  • Gabbiani, G., Badonnel, M. C., Majno, G.: Intraarterial injections of histamine, serotonin, or bradykinin: a topographic study of vascular leakage. Proc. Soc. exp. Biol. (N.Y.) 135, 447–452 (1970)

    Google Scholar 

  • Giertz, H., Hahn, F.: Die anaphylaktoide Reaktion der weißen Ratte In: Handbuch der experimentellen Pharmakologie, Bd. 18/1 (Hrsg. O. Eichler u. A. Farah), S. 481–511. Berlin-Heidelberg-New York: Springer 1966

    Google Scholar 

  • Goth, A.: Inhibition of anaphylactoid edema in the rat by 2-deoxy-glucose. Amer. J. Physiol. 197, 1056–1058 (1959)

    Google Scholar 

  • 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)

    Google Scholar 

  • Hashimoto, P. H., Hama, K.: An electron microscope study on protein uptake into brain regions devoid of the blood-brain barrier. Med. J. Osaka Univ. 18, 331–346 (1968)

    Google Scholar 

  • Hirano, A., Becker, N. H., Zimmermann, H. M.: Pathological alterations in the cerebral endothelial cell barrier to peroxidase. Arch. Neurol. (Chic.) 20, 300–308 (1969)

    Google Scholar 

  • Hirano, A., Becker N. H., Zimmermann, H. M.: The use of peroxidase as a tracer in studies of alterations in the blood-brain barrier. J. neurol. Sci. 10, 205–213 (1970)

    Google Scholar 

  • Holter, P.: Regular grid-like substructures in the midgut epithelial basement membrane of some coleoptera. Z. Zellforsch. 110, 373–385 (1970)

    Google Scholar 

  • Jakus, M.: Studies on the cornea. II. The fine structure of Descemet's membrane J. biophys. biochem. Cytol. 2 (Suppl.), 243–252 (1956)

    Google Scholar 

  • Joó, F.: Increased production of coated vesicles in the brain capillaries during enhanced permeability of the blood-brain barrier. Brit. J. exp. Path. 52, 646–649 (1971)

    Google Scholar 

  • Karnovsky, M. J.: Morphology of capillaries with special reference to muscle capillaries. In: Capillary permeability (Alfred Benzon Symposium II) (C. Crone, N. A. Lassen, eds.), p. 343–350. New York: Acad. Press 1970

    Google Scholar 

  • Köhl, W., Linderer, Th.: Zur Entwicklung des Subcommissuralorgans der Ratte. Morphologische und histochemische Untersuchungen. Histochemie 33, 349–368 (1973)

    Google Scholar 

  • Krstić, R.: Ultrastrukturelle Lokalisation von Mukosubstanzen der Zellhülle im Subcommissuralorgan der Ratte. Z. Zellforsch. 139, 237–252 (1973)

    Google Scholar 

  • Largiadèr, F.: The transplant. In: Organ transplantation (ed. F. Largiadèr), p. 154. Stuttgart: Thieme 1970

    Google Scholar 

  • Laurent, T. C.: The ultrastructure and physical-chemical properties of interstitial connective tissue. Pflügers Arch. 336, (Suppl.), S21-S42 (1972)

    Google Scholar 

  • Leonhardt, H.: Über die Blutkapillaren und perivaskulären Strukturen der Area postrema des Kaninchens und über ihr Verhalten im Pentamethylentetrazol-(Cardiazol-) Krampf. Z. Zellforsch. 76, 511–524 (1967)

    Google Scholar 

  • Leonhardt, H.: Über Hirnödem bei unterschiedlichen perikapillären Strukturen verschiedener Grisea des Kaninchens, hervorgerufen durch Pentamethylentetrazol (Cardiazol). Z. Zellforsch. 84, 199–218 (1968)

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961)

    Google Scholar 

  • Luft, J. H.: Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat. Rec. 171, 348–368 (1971a)

    Google Scholar 

  • Luft, J. H.: Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat. Rec. 171, 369–416 (1971b)

    Google Scholar 

  • Majno, G., Leventhal, M.: Pathogenesis of histamine-type vascular leakage. Lancet 1967 II, 99

    Google Scholar 

  • Majno, G., Palade, G. E.: Studies on inflammation: I. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J. biophys. biochem. Cytol. 11, 571–605 (1961a)

    Google Scholar 

  • Majno, G., Palade, G. E., Schoefl, G. I.: Studies on inflammation. II. The site of action of histamine and serotonin along the vascular tree: a topographic study. J. biophys. biochem. Cytol. 11, 607–626 (1961b)

    Google Scholar 

  • Majno, G., Shea, S. M., Leventhal, M.: Endothelial contraction induced by histamine-type mediators. J. Cell Biol. 42, 647–672 (1969)

    Google Scholar 

  • Manz, H. J., Robertson, D. M.: Vascular permeability to horseradish peroxidase in brain stem lesions of thiamine-deficient rats. Amer. J. Path. 66, 565–572 (1972)

    Google Scholar 

  • Merker, H. J., Struwe, K.: Elektronenmikroskopische Untersuchungen zum Problem der Sekretion der bindegewebigen Interzellularsubstanz. Z. Zellforsch. 115, 212–225 (1971)

    Google Scholar 

  • Møllgård, K.: Histochemical investigations on the human foetal subcommissural organ. I. Carbohydrates and mucosubstances, proteins and nucleoproteins, esterase, acid and alkaline phosphatase. Histochemie 32, 31–48 (1972)

    Google Scholar 

  • Murakami, M., Nakayama N., Tanaka, H.: Fine structure of the perivascular space of the Gecko japonicus subcommissural organ. Experientia (Basel) 25, 522–523 (1969)

    Google Scholar 

  • Papacharalampous, N. X., Schwink, A., Wetzstein, R.: Elektronenmikroskopische Untersuchungen am Subcommissuralorgan des Meerschweinchens. Z. Zellforsch. 90, 202–229 (1968)

    Google Scholar 

  • Rambourg, A.: An improved silver methenamine technique for the detection of periodic acid-reactive complex carbohydrates with the electron microscope. J. Histochem. Cytochem. 15, 409–412 (1967)

    Google Scholar 

  • Rambourg, A., Leblond, C. P.: Electron microscope observations on the carbohydrate-rich cell coat present at the surface of cells in the rat. J. Cell Biol. 32, 27–53 (1967)

    Google Scholar 

  • Reese, T. S., Brightman, M. W.: Similarity in structure and permeability to peroxidase of epithelia overlying fenestrated cerebral capillaries. Anat. Rec. 160, 414 (Abstr.) (1968)

    Google Scholar 

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

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)

    Google Scholar 

  • Rohr, V. U.: Zum Feinbau des Subfornical-Organs der Katze. I. Der Gefäß-Apparat. Z. Zellforsch. 73, 246–271 (1966)

    Google Scholar 

  • Rowley, D. A.: Mast cell damage and vascular injury in the rat: an electron microscopic study of a reaction produced by thorotrast. Brit. J. exp. Path. 44, 284–290 (1963)

    Google Scholar 

  • Rudert, H., Schwink, A., Wetzstein, R.: Die Feinstruktur des Subfornikalorgans beim Kaninchen. I. Die Blutgefäße. Z. Zellforsch. 74, 252–270 (1966)

    Google Scholar 

  • Saunders, B. C.: Peroxidase. London: Butterworths 1964

    Google Scholar 

  • Schinko, I., Rohrschneider, I., Wetzstein, R.: Elektronenmikroskopische Untersuchungen am Subfornikalorgan der Maus. Z. Zellforsch. 123, 277–294 (1972)

    Google Scholar 

  • Schmidt, W. R., D'Agostino, A. N.: The subcommissural organ of the adult rabbit. Neurology (Minneap.) 16, 373–379 (1966)

    Google Scholar 

  • Schwink, A., Wetzstein, R.: Die Capillaren im Subcommissuralorgan der Ratte. Elektronenmikroskopische Untersuchungen and Tieren verschiedenen Lebensalters. Z. Zellforsch. 73, 56–88 (1966)

    Google Scholar 

  • Sparrow, E. M., Wilhelm, D. L.: Species differences in susceptibility to capillary permeability factors: histamine, 5-hydroxytryptamine and compound 48/80. J. Physiol. (Lond.) 137, 51–65 (1957)

    Google Scholar 

  • Stanka, P., Schwink, A., Wetzstein, R.: Elektronenmikroskopische Untersuchung des Subcommissuralorgans der Ratte. Z. Zellforsch. 63, 277–301 (1964)

    Google Scholar 

  • Terzakis, J. A.: Substructure in an epithelial basal lamina. J. Cell Biol. 35, 237–278 (1967)

    Google Scholar 

  • Weindl, A.: Verhalten der circumventriculären Organe des Kaninchens nach intravenöser Trypanblauzufuhr. Naturwissenschaften 54, 342 (1967)

    Google Scholar 

  • Weindl, A., Joynt, R. J.: Electron microscopic observations on the organum vasculosum of the lamina terminalis (OVLT) after intravenous injection of horseradish peroxidase. Neurology (Minneap.) 13, 295 (1969)

    Google Scholar 

  • Weindl, A., Joynt, R. J.: Barrier properties of the subcommissural organ. Arch. Neurol. (Chic.) 29, 16–22 (1973)

    Google Scholar 

  • Wetzstein, R., Schwink, A., Stanka, P.: Die periodisch strukturierten Körper im Subcomissuralorgan der Ratte. Z. Zellforsch. 61, 493–523 (1963)

    Google Scholar 

  • Wislocki, G. B., King, L. S.: The permeability of hypophysis and hypothalamus to vital dyes, with a study of the hypophyseal vascular supply. Amer. J. Anat. 58, 421–472 (1936)

    Google Scholar 

  • Wislocki, G. B., Leduc, E. H.: The cytology and histochemistry of the subcommissural organ and Reissner's fiber in rodents. J. comp. Neurol. 97, 515–543 (1952)

    Google Scholar 

  • Wolff, J.: Persönliche Mitteilung, 1973

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Die Untersuchung wurde mit Unterstützung durch den Sonderforschungsbereich 51 (Medizinische Molekularbiologie und Biochemie) der DFG ausgeführt. — Frau H. Asam danken wir für hervorragende technische Hilfe.

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von Bomhard, K., Köhl, W., Schinko, I. et al. Feinbau und Passageverhalten der Capillaren im Subcommissuralorgan der Ratte. Z. Anat. Entwickl. Gesch. 144, 101–122 (1974). https://doi.org/10.1007/BF00518636

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