Skip to main content
Log in

Identification of G6PDH-active sinusoidal cells as Kupffer cells in the rat liver

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

Summary

The aim of this study was to identify the G6PDH-active sinusoidal cells in the rat liver described by Rieder et al. (1978). Because of their number and distribution in the liver parenchyma, endothelial cells and pit cells could be excluded. Fat-storing cells were specifically marked by vital staining with vitamin A and identified by fluorescence microscopy. Kupffer cells could be detected after vital staining with carmine. Both staining methods allowed a subsequent incubation for the demonstration of G6PDH activity in the same unfixed cryostat section. Whereas more than 80% of the fluorescent particles were found outside the enzyme-positive cells, all G6PDH-active cells contained carmine particles. After counting the G6PDH-active cells, an estimation of 0.217 × 108 cells/g liver tissue was obtained. The results indicate that high G6PDH activity is common to all Kupffer cells, and is therefore a highly specific marker enzyme for this class of sinusoidal liver cells.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aterman, K.: Some observations on the sinusoidal cells of the liver. Acta Anat. (Basel) 32, 193–213 (1958)

    Google Scholar 

  • Aterman, K.: Liver sinusoids and sinusoidal cells. In: The liver (Ch. Rouiller, ed.), Vol. 1, pp. 61–136 New York-London: Academic Press 1963

    Google Scholar 

  • Berkel, T.J.C. van, Koster, J.F.: Biochemical characteristics of non-parenchymal liver cells. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 299–306. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Berkel, T.J.C. van, Kruijt, J.K.: Distribution and some properties on NADPH and NADH oxidase in parenchymal and non-parenchymal liver cells. Arch. Biochem. Biophys. 179, 8–14 (1977)

    Google Scholar 

  • Blouin, A.: Morphometry of liver sinusoidal cells. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), 61–71. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Blouin, A., Bolender, R., Weibel, E.: Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma — a stereological study. J. Cell Biol. 72, 441–445 (1977)

    Google Scholar 

  • Bronfenmajer, S., Schaffner, F., Popper, H.: Fat storing cells (lipocytes) in human liver. Arch. Path. 82, 447–453 (1966)

    Google Scholar 

  • Carr, I.: The macrophage — a review of ultrastructure and function. London-New York: Academic Press 1973

    Google Scholar 

  • Emeis, J.J., Planqué, B.: Heterogeneity of cells isolated from rat liver by pronase digestion: ultrastructure, cytochemistry and cell structure. J. Reticuloendothel. Soc. 20, 11–29 (1976)

    Google Scholar 

  • Fahimi, H.D.: The fine structural localization of endogenous and exogenous peroxidase activity in Kupffer cells of rat liver. J. Cell Biol. 47, 247–262 (1970)

    Google Scholar 

  • Fahimi, H.D., Gray, B.A., Herzog, V.K.: Cytochemical localization of catalase and peroxidase in sinusoidal cells of rat liver. Lab. Invest. 34, 192–201 (1976)

    Google Scholar 

  • Greengard, O., Federman, M., Knox, W.E.: Cytomorphometry of developing rat liver and its application to enzymic differentiation. J. Cell Biol. 52, 261–272 (1972)

    Google Scholar 

  • Hirosawa, K., Yamada, E.: The localization of the vitamin A in the mouse liver as revealed by electron microscope radioautography. J. Electron Microsc. 22, 337–346 (1973)

    Google Scholar 

  • Ikejiri, N., Tanikawa, K.: Effects of vitamin A and oestrogen on the sinusoidal cells in rat liver. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 83–92. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Ito, T., Nemoto, M.: Über die Kupfferschen Sternzellen und die “Fettspeicherungszellen” (“fat storing cells”) in der Blutkapillarenwand der menschlichen Leber. Okajimas Folia Anat. Jap. 24, 243–258 (1952)

    Google Scholar 

  • Ito, T., Shibasaki, S.: Electron microscopic study on the hepatic sinusoidal wall and the fat storing cells in the normal human liver. Arch. Histol. Jap. 29, 137–192 (1968)

    Google Scholar 

  • Kent, G., Gay, S., Inouye, T., Bahu, R., Minick, O.T., Popper, H.: Vitamin A — containing lipocytes and formation of type III collagen in liver injury. Proc. Natl. Acad. Sci. USA 73, 3719–3722 (1976)

    Google Scholar 

  • Kent, G., Inouye, T., Minick, O.T., Bahu, R.M.: Role of lipocytes (perisinusoidal cells) in fibrogenesis. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 73–82. Elsevier: North-Holland Biomedical Press 1977b

    Google Scholar 

  • Kent, G., Minick, T., Inouye, T.: Nature and role of vitamin A — storing cells. J. Cell Biol. 75, HM 936 (1977a)

    Google Scholar 

  • Knook, D.L., Blansjaar, N., Sleyster, E.CH.: Isolation and characterization of Kupffer and endothelial cells from the rat liver. Exp. Cell Res. 109, 317–329 (1977)

    Google Scholar 

  • Knook, D.L., Sleyster, E.CH.: Lysosomal enzyme activities in parenchymal and nonparenchymal liver cells isolated from young, adult and old rats. Mech. Aging Development 5, 389–397 (1976a)

    Google Scholar 

  • Knook, D.L., Sleyster, E.CH.: Separating of Kupffer and endothelial cells of the rat liver by centrifugal elutriation. Exp. Cell Res. 99, 444–449 (1976b)

    Google Scholar 

  • Kobayashi, K., Takahashi, T., Shibasaki, S.: Cytological studies of fat-storing cells in the liver of rats given large doses of vitamin A. Nature New Biol. 243, 186–188 (1973)

    Google Scholar 

  • Kupffer, C. von: Ueber Sternzellen in der Leber — briefliche Mittheilung an Prof. Waldeyer. Arch. Mikr. Anat. 12, 353–358 (1876)

    Google Scholar 

  • Kusumoto, Y., Fujita, T.: Vitamin A uptake cells distributed in the liver and other organs. Arch. Histol. Jap. 40, 121–136 (1977)

    Google Scholar 

  • Linder, M.C., Anderson, G.H., Ascarelli, I.: Quantitative distribution of vitamin A in Kupffer cell and hepatic population of rat liver. J. Biol. Chem. 246, 5538–5540 (1971)

    Google Scholar 

  • Lison, L., Smulders, J.: Discriminating'athrocytes' in the reticuloendothelial system. Nature 162, 65–66 (1948)

    Google Scholar 

  • Loud, A.V.: A quantitative stereological description of the ultrastructure of normal rat liver parenchymal cells. J. Cell Biol. 37, 27–46 (1968)

    Google Scholar 

  • MacGee, J. O'D., Patrick, R.S.: The role of perisinusoidal cells in hepatic fibrogenesis, an electron microscopic study of acute carbon tetrachloride liver injury. Lab. Invest. 26, 429–440 (1972)

    Google Scholar 

  • Motta, P.: Kupffer cells as revealed by scanning electron microscopy. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 93–102. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Munthe-Kass, A.C., Berg, T., Seljelid, R.: Distribution of lysosomal enzymes in different types of rat liver cells. Exp. Cell Res. 99, 146–154 (1976)

    Google Scholar 

  • Muto, M.: A scanning electron microscopic study on endothelial cells and Kupffer cells in rat liver sinusoids. Arch. Histol. Jap. 37, 369–386 (1975)

    Google Scholar 

  • Muto, M., Fujita, T.: Phagocytic activities of the Kupffer cell: a scanning electron microscope study. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 109–119. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Muto, M., Nishi, M., Fujita, T.: Scanning electron microscopy of human liver sinusoids. Arch. Histol. Jap. 40, 137–151 (1977)

    Google Scholar 

  • Naito, M., Wisse, E.: Observations on the fine structure and cytochemistry of sinusoidal cells in fetal and neonatal rat liver. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 497–505. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Nakane, P.K.: Ito's “fat storing cell” of the mouse liver. Anat. Rec. 145, 265–266 (1963)

    Google Scholar 

  • Nicolescu, P., Rouiller, C.H.: Beziehungen zwischen den Endothelzellen der Lebersinusoide und den von Kupffer'schen Sternzellen. Z. Zellforsch. 76, 313–338 (1967)

    Google Scholar 

  • North, R.J.: The mitotic potential of fixed phagocytes in the liver as revealed during the development of cellular immunity. J. Exp. Med. 130, 315–326 (1969)

    Google Scholar 

  • Ogawa, K., Minase, T., Yokoyama, S., Onoé, T.: An ultrastructural study of peroxidatic and phagocytic activities of two types of sinusoidal lining cells in rat liver. Tohoku J. Exp. Med. 111, 253–269 (1973)

    Google Scholar 

  • Patriarca, P., Cramer, R., Moncalvo, S., Rossi, F., Romeo, D.: Enzymatic basis of metabolic stimulation. in leukocytes during phagocytosis: the role of activated NADPH oxidase. Arch. Biochem. Biophys. 145, 255–262 (1971)

    Google Scholar 

  • Popper, H.: Distribution of vitamin A in tissue as visualized by fluorescence microscopy. Physiol. Rev. 24, 205–224 (1944)

    Google Scholar 

  • Popper, H., Schaffner, F.: Die Leber, Struktur und Funktion. Stuttgart: Georg Thieme 1961

    Google Scholar 

  • Rieder, H., Teutsch, H.F., Sasse, D.: NADP-dependent dehydrogenases in rat liver parenchyma, methodological studies on the qualitative histochemistry of G6PDH, 6PGDH, malic enzyme and ICDH. Histochemistry 56, 283–298 (1978)

    Google Scholar 

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

    Google Scholar 

  • Rossi, F., Zatti, M.: Effect of phagocytosis on the carbohydrate metabolism of polymorphonuclear leukocytes. Biochim. Biophys. Acta 121, 110–119 (1966)

    Google Scholar 

  • Rüttner, J.R., Brunner, H.E., Vogel, A.P.: Untersuchungen über die Kupfferschen Zellen der Rattenleber. Schweiz. Z. Path. Bakt. 19, 738–747 (1956)

    Google Scholar 

  • Satodate, R., Sasou, S., Oikawa, K., Hatakeyama, N., Katsura, S.: Scanning electron microscopical studies on the Kupffer cell in phagocytic activity. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 121–129. Elsevier: North Holland Biomedical Press 1977

    Google Scholar 

  • Schmidt, E., Schmidt, F.W., Vonnahme, F.J.: Aspekte von Struktur und Funktion der Leber. Muzed 1, 150–162 (1977)

    Google Scholar 

  • Selvaraj, R.J., Sbarra, A.J.: Relationship of glycolytic and oxidative metabolism to particle entry and destruction in phagocytosing cells. Nature 211, 1272–1276 (1966)

    Google Scholar 

  • Sleyster, E.CH., Westerhuis, F.G., Knook, D.L.: The purification of nonparenchymal liver cell classes by centrifugal elutriation. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 289–298. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Wake, K.: “Sternzellen” in the liver: perisinusoidal cells with special reference to storage of vitamin A. Am. J. Anat. 132, 429–462 (1971)

    Google Scholar 

  • Wake, K.: Development of vitamin A-rich lipid droplets in multivesicular bodies of rat liver stellate cells. J. Cell Biol. 63, 683–691 (1974)

    Google Scholar 

  • Wallraff, J.: Verdauungsapparat, Atmungsapparat: Disse'scher Raum, Lebersinusoide, von Kupffersche Sternzelle. In: Handbuch der mikroskopischen Anatomie des Menschen (J. Wallraff, ed.), Bd. V, 4. Teil, S. 178–207. Berlin-Heidelberg-New York: Springer 1969

    Google Scholar 

  • Weibel, E.R., Sträubli, W., Gnägi, H.R., Hess, F.A.: Correlated morphometric and biochemical studies on the liver cell; morphometric model, stereologic methods and normal morphometric data for rat liver cells. J. Cell Biol. 42, 68–91 (1969)

    Google Scholar 

  • Widmann, J.J., Cotran, R.S., Fahimi, H.D.: Mononuclear phagocytes (Kupffer cells) and endothelial cells — identification of two functional cell types in rat liver sinusoids by endogenous peroxidase activity. J. Cell Biol. 52, 159–170 (1972)

    Google Scholar 

  • Widmann, J.J., Fahimi, H.D.: Proliferation of mononuclear phagocytes (Kupffer cells) and endothelial cells in regenerating rat liver. Am. J. Pathol. 80, 349–366 (1975)

    Google Scholar 

  • Widmann, J.J., Fahimi, H.D.: Proliferation of endothelial cells in estrogen-stimulated rat liver — a light and electron microscopic cytochemical study. Lab. Invest. 34, 141–149 (1976)

    Google Scholar 

  • Wisse, E.: An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J. Ultrastruct. Res. 31, 125–150 (1970)

    Google Scholar 

  • Wisse, E.: An ultrastructural characterization of the endothelial cell in the rat liver sinusoid under normal and various experimental conditions, as a contribution to the distinction between endothelial and Kupffer cells. J. Ultrastruct. Res. 38, 528–562 (1972)

    Google Scholar 

  • Wisse, E.: Observations on the fine structure and peroxidase cytochemistry of normal rat liver Kupffer cells. J. Ultrastruct. Res. 46, 393–426 (1974a)

    Google Scholar 

  • Wisse, E.: Kupffer cell reactions in rat liver under various conditions as observed in the electron microscope. J. Ultrastruct. Res. 46, 499–520 (1974b)

    Google Scholar 

  • Wisse, E.: Ultrastructure and function of Kupffer cells and other sinusoidal cells in the liver. In: Kupffer cells and other liver sinusoidal cells (E. Wisse and D.L. Knook, eds.), pp. 33–60. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Wisse, E., Knook, D.L. (eds.): Kupffer cells and other liver sinusoidal cells. Elsevier: North-Holland Biomedical Press 1977

    Google Scholar 

  • Wisse, E., Noordende, J.M. van't, Meulen, J. van der, Daems, W.T.H.: The pit cell: description of a new type of cell occurring in rat liver sinusoids and peripheral blood. Cell Tissue Res. 173, 423–435 (1976)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

The essential parts of this study will be presented as an Inaugural-Dissertation to the Medical Faculty of the University of Freiburg by W. Hosemann

Supported by a grant from the SFB 46 (“Molgrudent”)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hosemann, W., Teutsch, H.F. & Sasse, D. Identification of G6PDH-active sinusoidal cells as Kupffer cells in the rat liver. Cell Tissue Res. 196, 237–247 (1979). https://doi.org/10.1007/BF00240099

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00240099

Key words

Navigation