Structure of rat liver sinusoids and associated tissue spaces as revealed by scanning electron microscopy Article Received: 28 November 1973 DOI:
10.1007/BF00224322 Cite this article as: Motta, P. & Porter, K.R. Cell Tissue Res. (1974) 148: 111. doi:10.1007/BF00224322 Summary
The inner surface of sinusoids and adjacent hepatocytes have been examined by scanning electron microscopy. The endothelial cells lining the sinusoids show large numbers of fenestrations which vary greatly in size and arrangement. Some are very small (0.1 μm) and arranged in clusters; others that are much larger (∼1.0 μm) are subdivided by slender strands of cytoplasm. At sites where the larger fenestrae are present it is evident that the endothelial lining of the sinusoid is double. This may represent a kind of structural assurance against complete breakdown of what seems to be a very thin and fragile endothelial wall. Junctions between adjacent endothelial cells have not been found in these preparations.
The open continuity of the sinusoid is occasionally interrupted by slender extensions of cells morphologically distinct from the thin fenestrated endothelial cells. These possess a characteristically textured surface and are thought to represent stellate Kupffer cells.
The SEM images describe the subendothelial Spaces of Disse as being larger and as having more extensive ramifications than is generally evident from transmission micrographs. The space, limited on one side by the hepatocyte with numerous microvilli and on the other by endothelial cells, appears actually to be only part of an extensive labyrinth of intercellular channels. These connect the more discrete Spaces of Disse and extend into the narrower spaces between the hepatocytes. The total effect of this system is to expose the greater part of the liver cell surface to the blood filtrate. Microvilli populate the hepatocyte surfaces except for narrow margins which border the bile canaliculi. Whether their presence coincides with the adsorbing surfaces and their absence with secreting surfaces can be decided best by experimental studies.
Key words Liver Sinusoids Kupffer cells Spaces of Disse Scanning electron microscopy
This work was supported in part by a contract from the Special Virus Cancer Program, National Cancer Institute. The study was made while Dr. Motta was a guest investigator and Fulbright Scholar in the Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, Colorado.
Download to read the full article text References
Aterman, K.: The structure of the liver sinusoids and the sinusoidal cell. In: The liver, vol. I (Ch. Rouiller, ed.), p. 61–136. New York: Academic Press 1963
Barone, P., Inferrera, C., Carrozza, G.: Aspetti ultrastrutturali dell' epatocita in rapporto alla secrezione biliare ed alle sue alterazioni. Relaz. Atti X Congr. Soc. Ital. Patologia, Messina-Taormina, p. 49–211 (1967)
Bloom, W., Fawcett, D. W.: A textbook of histology, 9th ed. Philadelphia: W. B. Saunders Co. 1968
Brauer, R. W.: Liver circulation and function. Physiol. Rev.
, 115–213 (1963)
Brooks, S.E.H., Haggis, G. H.: Scanning electron microscopy of rat's liver. Application of freeze-fracture and freeze-drying techniques. Lab. Invest.
, 60–64 (1973)
Bruni, C., Porter, K. R.: The fine structure of the parenchymal cell of the normal rat liver. I. General observations. Amer. J. Path.
, 691–755 (1965)
Burkel, W. E., Low, F. N.: The fine structure of rat liver sinusoids, Spaces of Disse and associated tissue space. Amer. J. Anat.
, 769–784 (1966)
Carr, I.: The fine structure of the mammalian lymphoreticular system. Int. Rev. Cytol.
Carsten, P. M.: Elektronenmikroskopische Untersuchungen an der Sinusoidwand menschlicher fetaler Lebern. Z. Zellforsch.
, 252–261 (1961)
Cossel, L.: Die menschliche Leber im Elektronenmikroskop. Jena: Gustav Fischer 1964
David, H.: Submikroskopische Orthound Pathomorphologie der Leber. Berlin: Akademie Verlag 1964
Dogliotti, G. C.: Ricerche sull' assunzione di da parte delle cellule epatiche nei ratti albini. Monit. zool. ital.
, 100–106 (1929)
Elias, H.: A re-examination of the structure of the mammalian liver. II. The hepatic lobule and its relation to the vascular and biliary systems. Amer. J. Anat.
, 379–465 (1949)
Fawcett, D. W.: Observations on the cytology and electron microscopy of hepatic cells. J. nat. Cancer Inst.
, 1475–1502 (1955)
Ham, A. W.: Histology, 6th ed. Philadelphia: J. B. Lippincott Co. 1969
Hampton, J.: A re-evaluation of the submicroscopic structure of liver. Tex. Rep. Biol. Med.
, 602–611 (1960)
Ito, T., Nemoto, M.: Über die Kupfferschen Sternzellen und die “Fettspeicherungszellen” in der Blutkapillarenwand der menschlichen Leber. Folia anat. jap.
, 243–258 (1952)
Jezequel, A. M., Orlandi, F.: Fine morphology of the human liver as a tool in clinical pharmacology. In: Liver and drugs (F. Orlandi and A. M. Jezequel, eds.), p. 145–188. New York: Academic Press 1972
Karnovsky, M. S.: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol.
, 213–236 (1967)
Kuhn, N., Olivier, M. L.: Ultrastructure of the hepatic sinusoid of the goat,
. J. Cell Biol.
, 977–979 (1965)
Laschi, R., Casanova, S.: Fenestrae closed by a diaphragm in the endothelium of liver sinusoids. J. Microsc.
, 1037–1040 (1969)
Leak, L. V., Burke, J. F.: Fine structure of lymphatic capillary and adjoining connective tissue area. Amer. J. Anat.
, 785–810 (1966)
Leak, L. V., Burke, J. F.: Ultrastructural studies on the lymphatic anchoring filaments. J. Cell Biol.
, 129–149 (1968)
Majno, G.: Ultrastructure of the vascular membrane. In: Handbook of physiology, vol. III/2 (W. F. Hamilton and P. Dow, eds.), p. 2293–2375. Baltimore: Williams-Wilkins Co. 1965
Nicolescu, P., Rouiller, C.: Beziehungen zwischen den Endothelzellen der Lebersinusoide und den von Kupfferschen Sternzellen. Elektronenmikroskopische Untersuchung. Z. Zellforsch.
, 313–338 (1967)
Novikoff, A., Essner, E.: The liver cell. Some new approaches to its study. Amer. J. Med.
, 102–131 (1960)
Parks, H. F.: An experimental study of microscopic and submicroscopic lipid inclusions in hepatic cells of the mouse. Amer. J. Anat.
, 253–280 (1967)
Porter, K. R., Kelley, D., Andrews, P. M.: The preparation of cultured cells and soft tissues for scanning electron microscopy. In: Proceedings of the 5th Annual Stereoscan Colloquium, p. 1–19. Chicago: Kent Cambridge Scientific Co. 1972
Porter, K. R., Todaro, G. J., Fonte, V.: A scanning electron microscope study of surface features of viral and spontaneous transformants of mouse balb/3T3 cells. J. Cell Biol. (1973) (in press)
Rouiller, C., Jezequel, A. M.: Electron microscopy of the liver. In: The liver, vol. I (Ch. Rouiller, ed.), p. 195–264. New York: Academic Press 1963
Sabatini, D. D., Bensch, K. G., Barrnett, R. J.: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol.
, 19–58 (1963)
Scott, J. F., Deane, H. W.: Liver and gallbladder. In: Histology, 2nd ed. (R. O. Greep, ed.), p. 531–553. New York: McGraw-Hill Book Co. 1966
Smith, U., Michie, D. D., Ryan, J. W., Smith, D. S.: Endothelial projections as revealed by scanning electron microscopy. Science.
, 925–927 (1971)
Stein, O., Stein, Y.: Lipid synthesis, intracellular transport, storage and secretion. I. Electron microscopic radioautographic study of liver after injection of tritiated palmitate or glycerol fasted and ethanol-treated rats. J. Cell Biol.
, 319–339 (1967)
Steiner, J. W.: Investigations of allergic liver injury. I. Light, fluorescent and electron microscopic study of the effects of soluble immune aggregates. Amer. J. Path.
, 411–436 (1961)
Tanikawa, K.: Ultrastructural aspects of the liver and its disorders. Berlin-Heidelberg-New York: Springer 1968
Wassermann, F.: The structure of the wall of the hepatic sinusoids in the electron microscope. Z. Zellforsch.
, 13–32 (1958)
Weatherford, H. W.: The Golgi apparatus and vital staining of the amphibian and reptilian liver. Z. Zellforsch.
, 343–373 (1932)
Wisse, E.: An electron microscopic study of the fenestrated endothelium lining of rat liver sinusoids. J. Ultrastruct. Res.
, 125–150 (1970)
Wisse, E.: An ultrastructural characterization of the endothelial cell in the rat sinusoid under normal and various experimental conditions, as a contribution to the distinction between endothelial and Kupffer cells. J. Ultrastruct. Res.
, 528–562 (1972)