Skip to main content
SpringerLink
Log in

Ultrastructural and histochemical investigation of the terminal capillaries in the spleen of the carp (Cyprinus carpio L.)

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

In the spleen of the carp arterial capillaries of a highly differentiated structure have been studied by light and electron microscopy. These capillaries share various structural characteristics with the sheathed capillaries (ellipsoids of Schweigger-Seidel) of higher vertebrates. The long arterial capillaries of the carp spleen are provided with cuboidal endothelial cells containing filaments approximately 7 nm in diameter. There is no basal lamina. The endothelial cells form various types of cell junctions, but there are also extensive areas without any junctions. Here, a free passage is possible between the capillary lumen and the subendothelial space. The capillaries possess a single-layered sheath of macrophages. Characteristically, the sheath macrophages possess long and slender cell processes forming a loose framework, the meshes of which are filled with lymphocytes and spindle cells. The sheath macrophages show a zone of ectoplasm rich in filaments. They also contain numerous phagolysosomes rich in hydrolytic enzymes, as identified histochemically. The sheath is sharply limited against the pulp by a thick layer of collagen fibers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Axline, S.G., Reaven, E.P.: Inhibition of phagocytosis and plasma membrane mobility of the cultivated macrophage by cytochalasin B. Role of subplasmalemmal microfilaments. J. Cell Biol. 62, 647–659 (1974)

    Google Scholar 

  • Bargmann, W.: Zur Kenntnis der Hülsenkapillaren der Milz. Z. Zellforsch. 31, 630–647 (1941)

    Google Scholar 

  • Barka, T.: A simple azo-dye method for histochemical demonstration of acid phosphatase. Nature 187, 248 (1960)

    Google Scholar 

  • Barka, T., Anderson, P.J.: Histochemistry. Theory, practice and bibliography. New York-EvanstonLondon: Hoeber Medical Division, Harper and Row 1963

    Google Scholar 

  • Baum, H., Dodgson, K.S., Spencer, B.: The assay of arylsulfatase A and B in human urine. Clin. Chim. Acta 4, 453 (1959)

    Google Scholar 

  • Bowers, W.E., Duve, C. de: Lysosomes in lymphoid tissue. II. Intracellular distribution of acid hydrolases. J. Cell Biol 32, 339–348 (1967a)

    Google Scholar 

  • Bowers, W.E., Duve, C. de: Lysosomes in lymphoid tissue. III. Influence of various treatments of the animals on the distribution of acid hydrolases. J. Cell Biol. 32, 349–364 (1967b)

    Google Scholar 

  • Braunsteiner, H., Schmalzl, F.: Cytochemistry of monocytes and macrophages. In: Mononuclear phagocytes (R. van Furth, ed.). Oxford-Edinburgh: Blackwell Scientific Publications 1970

    Google Scholar 

  • Carr, J.: The fine structure of microfibrils and microtubules in macrophages and other lymphoreticular cells in relation to cytoplasmic movement. J. Anat. 112, 383–389 (1972)

    Google Scholar 

  • Carr, J.: The macrophage. A review of ultrastructure and function. London-New York: Academic Press 1973

    Google Scholar 

  • Cohn, Z.A.: The structure and function of monocytes and macrophages. Adv. Immunol. 9, 163–214 (1968)

    Google Scholar 

  • Cohn, Z.A.: Properties of macrophages. In: Phagocytic mechanisms in health and disease (R.C. Williams and H.H. Fudenberg, eds.). Stuttgart: Georg Thieme 1972

    Google Scholar 

  • Connock, M.J., Sturdee, A.P.: Acid hydrolases in the suckling rat small intestine. II. On the importance of alkaline phosphatase inhibition in the histochemical localization of acid phosphatase activity. Histochem. J. 7, 103–114 (1975)

    Google Scholar 

  • Daems, W.Th., Brederoo, P.: Electron microscopical studies on the structure, phagocytic properties and peroxidatic activity of resident and exudate peritoneal macrophages in the guinea pig. Z. Zellforsch. 144, 247–297 (1973)

    Google Scholar 

  • Davis, B.J., Ornstein, L.: High resolution enzyme localization with a new diazo reagent “hexazonium pararosaniline”. J. Histochem. Cytochem. 7, 297–298 (1959)

    Google Scholar 

  • Dustin, P., Jr.: Les housses spléniques de Schweigger-Seidel. Étude d'histologie et d'histophysiologie comparées. Arch. Biol. (Paris) 49, 1–99 (1938)

    Google Scholar 

  • Ellis, A.E., Munroe, A.L.S., Roberts, R.J.: Defence mechanisms in fish. I. A study of the phagocytic system and the fate of intraperitoneally injected particulate material in the plaice (Pleuronectes platessa L.). J. Fish Biol. 8, 67–78 (1976)

    Google Scholar 

  • Farquhar, M.G., Palade, G.E.: Cell junctions in amphibian skin. J. Cell Biol. 26, 263–291 (1965)

    Google Scholar 

  • Ferguson, H.W.: The relationship between ellipsoids and melano-macrophage centres in the spleen of turbot (Scophthalmus maximus). J. Comp. Pathol. 86, 377–380 (1976)

    Google Scholar 

  • Goldfischer, S.: The cytochemical demonstration of lysosomal arylsulfatase activity by light and electron microscopy. J. Histochem. Cytochem. 13, 520–523 (1965)

    Google Scholar 

  • Gröschel-Stewart, U., Gröschel, D.: Immunological evidence for the presence of smooth muscle-type contractile fibres in mouse macrophages. Experientia 30, 1152–1153 (1974)

    Google Scholar 

  • Haider, G.: Beitrag zur Kenntnis der mikroskopischen Anatomie der Milz einiger Teleostier. Zool. Anz. 177, 348–367 (1966)

    Google Scholar 

  • Hammersen, F.: Anatomie der terminalen Strombahn. Muster-Feinbau-Funktion. München-BerlinWien: Urban & Schwarzenberg 1971

    Google Scholar 

  • Hartmann, A.: Die Milz. In: Handbuch der mikroskopischen Anatomie des Menschen, Bd VI/I (W. v. Möllendorff, ed.). Berlin: J. Springer 1930

    Google Scholar 

  • Hayashi, M.: Histochemical demonstration of N-acetyl-β-glucosaminidase employing naphthol-AS-BI-N-acetyl-β-glucosaminide as substrate. J. Histochem. Cytochem. 13, 355–360 (1965)

    Google Scholar 

  • Hayashi, M., Nakajima, Y., Fishman, W.H.: The cytologic demonstration of β-glucuronidase employing naphthol-AS-BI-glucuronide and hexazonium pararosaniline, a preliminary report. J. Histochem. Cytochem. 12, 293–297 (1964)

    Google Scholar 

  • Hayes, T.G.: Structure of the ellipsoid sheath in the spleen of the Armadillo (Dasypus novemcinctus). A light and electron microscopic study. J. Morphol. 132, 207–224 (1970)

    Google Scholar 

  • Herrath, E. v.: Bau und Funktion der normalen Milz. Berlin: Walter de Gruyter & Co 1958

    Google Scholar 

  • Hoffmann-Ostenhof, O.: Schwefelsäureester-Hydrolasen (Sulfatasen; Schwefelsäure-Esterasen). In: Hoppe-Seyler und Thierfelder, Handbuch der physiologisch-und pathologisch-chemischen Analyse. Bd. 6, Teil B: Enzyme, 10. Aufl. Berlin-Heidelberg-New York: Springer 1966

    Google Scholar 

  • Holt, S.J.: Factors governing the validity of staining methods for enzymes, and their bearing upon the Gomori acid phosphatase technique. Exp. Cell Res., Suppl. 7, 1–27 (1959)

    Google Scholar 

  • Hopsu-Havu, V.K., Arstila, A.U., Helminen, H.J., Kalimo, H.O.: Improvements in the method for the electron microscopic localization of arylsulphatase activity. Histochemie 8, 54–64 (1967)

    Google Scholar 

  • Karnovsky, M.J.: A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137A-138A (1965)

    Google Scholar 

  • Koyama, S., Aoki, S., Deguchi, K.: Electron microscopic observations of the splenic red pulp with special reference to the pitting function. Mie med. J. 14, 143–188 (1964)

    Google Scholar 

  • Li, C.Y., Yam, L.T., Crosby, W.: Histochemical characterization of cellular and structural elements of the human spleen. J. Histochem. Cytochem. 20, 1049–1058 (1972)

    Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J.: Protein measurements with the folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951)

    Google Scholar 

  • Nachlas, M.M., Tsou, K.-C., de Souza, E., Cheng, C.-S., Seligman, A.M.: Cytochemical demonstration of succinic dehydrogenase by the use of a new p-nitrophenyl substituted ditetrazole. J. Histochem. Cytochem. 5, 420–436 (1957)

    Google Scholar 

  • Nelson, D.S.: Macrophages and Immunity. Amsterdam-London: North-Holland Publishing Company 1969

    Google Scholar 

  • Nicholls, R.G., Roy, A.B.: Arylsulfatases. In: The enzymes, 3rd ed., Vol. 5 (P.D. Boyer, ed.). New-York-London: Academic Press 1971

    Google Scholar 

  • Novikoff, P.M., Novikoff, A.B., Quintana, N., Hauw, J.J.: Golgi apparatus, gerl and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry. J. Cell Biol. 50, 859–886 (1971)

    Google Scholar 

  • Petris, S. de, Karlsbad, G., Pernis, B.: Filamentous structures in the cytoplasm of normal mononuclear phagocytes. J. Ultrastruct. Res. 7, 39–55 (1962)

    Google Scholar 

  • Robinson, D., Sterling, J.L.: N-acetyl-β-glucosaminidases in human spleen. Biochem. J. 107, 321–327 (1968)

    Google Scholar 

  • Romeis, B.: Mikroskopische Technik, 16. Aufl. München-Wien: R. Oldenbourg Verlag 1968

    Google Scholar 

  • Schlüns, J., Rother, H., Tiedemann, M.: Untersuchungen zur Feinstruktur und Ultrahistochemie der Schweigger-Seidelschen Kapillarhülsen der Milz des Schweines. Verh. Anat. Ges. 68, 529–538 (1974)

    Google Scholar 

  • Schweigger-Seidel, F.: Untersuchungen über die Milz. Virchows Arch. path. Anat. 27, 460–504 (1863)

    Google Scholar 

  • Stutte, H.J.: Hexazotiertes Triaminotritolyl-methanchlorid (Neufuchsin) als Kupplungssalz in der Fermenthistochemie. Histochemie 8, 327–331 (1967)

    Google Scholar 

  • Stutte, H.J.: Nature of human spleen red pulp cells with special reference to sinus lining cells. Z. Zellforsch. 91, 300–314 (1968)

    Google Scholar 

  • Tischendorf, F.: Die Milz. In: Handbuch der mikroskopischen Anatomie des Menschen, Bd. VI/6 (W. Bargmann, ed.). Berlin-Heidelberg-New York: Springer 1969

    Google Scholar 

  • Weischer, C.H.: Histologische, histochemische und fluoreszenzmikroskopische Untersuchungen über die formale Genese des Ceroidpigments. Dissertation, Fachbereich Tiermedizin. München: LudwigMaximilians-Universität 1975

    Google Scholar 

  • Weiss, L.: Observations on the red pulp of the spleen of rabbits and dogs by electron and light microscopy. Anat. Rec. 139, 286 (1961)

    Google Scholar 

  • Weiss, L.: The structure of the fine splenic arterial vessels in relation to hemoconcentration and red cell destruction. Am. J. Anat. 111, 131–179 (1962)

    Google Scholar 

  • White, R.G., Henderson, D.C., Eslami, M.B., Nielsen, K.H.: Effect of various manipulative procedures on the morphogenesis of the germinal centre. Immunology 28, 1–21 (1975)

    Google Scholar 

  • Wolman, M., Bubis, J.J.: Ubiquinone and phospholipids as limiting factors in the histochemical demonstration of succinic dehydrogenase activity. J. Histochem. Cytochem. 15, 79–82 (1967)

    Google Scholar 

  • Yoffey, J.M.: A contribution to the study of the comparative histology and physiology of the spleen, with reference chiefly to its cellular constituents. J. Anat. 63, 314–344 (1929)

    Google Scholar 

  • Zwillenberg, H.H.L.: Bau und Funktion der Forellenmilz. Bern-Stuttgart: Hans Huber 1964

    Google Scholar 

  • Zwillenberg, H.H.L., Zwillenberg, L.O.: Über den Erythrozytenabbau in der Forellenmilz, unter besonderer Berücksichtigung der Erythrozytenfeinstruktur. Z. Zellforsch. 60, 313–324 (1963a)

    Google Scholar 

  • Zwillenberg, L.O., Zwillenberg, H.H.L.: Elektronenmikroskopische Beobachtungen an den Hülsenarteriolen in der Milz des Hundes. Experientia 18, 136–137 (1962)

    Google Scholar 

  • Zwillenberg, L.O., Zwillenberg, H.H.L.: Zur Struktur und Funktion der Hülsencapillaren in der Milz. Z. Zellforsch. 59, 908–921 (1963b)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fachrichtung Histologie und Embryologie der Freien Universität, Institut für Veterinär-Anatomie, Berlin, Bundesrepublik Deutschland

    R. Graf Dipl.-Biol. & J. Schlüns

Authors
  1. R. Graf Dipl.-Biol.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Schlüns
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Graf, R., Schlüns, J. Ultrastructural and histochemical investigation of the terminal capillaries in the spleen of the carp (Cyprinus carpio L.). Cell Tissue Res. 196, 289–306 (1979). https://doi.org/10.1007/BF00240103

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00240103

Key words

Search

Navigation