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. 1977 Feb 1;72(2):441–455. doi: 10.1083/jcb.72.2.441

Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. A stereological study

PMCID: PMC2110997  PMID: 833203

Abstract

When biochemical studies on the liver are interpreted, the cells of the sinusoidal area frequently receive little attention because, compared to hepatocytes, their contribution to subcellular fractions is assumed insignificant. A systematic stereological analysis of liver parenchyma was therefore performed in order to determine the distribution of organelles and membranes between hepatocytic and nonhepatocytic cells, namely endothelial, Kupffer, and fat-storing cells. The livers were fixed by vascular perfusion and the data were corrected for systematic errors dur to section thickness and compression. The extracellular space compartment includes the lumina of sinusoids (10.6%), the space of Disse (4.9%), and the bile canaliculi (0.4%). Hepatocytes constitute 78% of parenchymal volume; the nonhepatocytes account for 6.3% and consist of 2.8% endothelial cells, 2.1% Kupffer cells, and 1.4% fat- storing cells. The nonhepatocytes contribute 55% of the volume of lipid droplets in the liver, 43% of the lysosomes, and 1.2% of the mitochondria. Although the nonhepatocytes account for only 8% of the total surface area of parenchymal membranes, they contain 26.5% of all the plasma membranes, 32.4% of the lysosomal membranes, 15.1% of the Golgi apparatus 6.4% of the endoplasmic reticulum, and 2.4% of the mitochondrial membranes. The data demonstrate the extent to which nonhepatocytic organelles can potentially contaminate subcellular fractions used for biochemical studies. Particularly important for the interpretation of studies on lysosomes, plasma membrane, and Golgi apparatus is the finding that an appreciable part of these organelles may be derived from cell types other than hepatocytes.

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Selected References

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  1. BEAUFAY H., BENDALL D. S., BAUDHUN P., WATTIAUX R., DE DUVE C. Tissue fractionation studies. 13. Analysis of mitochondrial fractions from rat liver by density-gradient centrifuging. Biochem J. 1959 Dec;73:628–637. doi: 10.1042/bj0730628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berg T., Boman D. Distribution of lysosomal enzymes between parenchymal and Kupffer cells of rat liver. Biochim Biophys Acta. 1973 Oct 10;321(2):585–596. doi: 10.1016/0005-2744(73)90201-5. [DOI] [PubMed] [Google Scholar]
  3. Bergeron J. J., Ehrenreich J. H., Siekevitz P., Palade G. E. Golgi fractions prepared from rat liver homogenates. II. Biochemical characterization. J Cell Biol. 1973 Oct;59(1):73–88. doi: 10.1083/jcb.59.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bolender R. P., Weibel E. R. A morphometric study of the removal of phenobarbital-induced membranes from hepatocytes after cessation of threatment. J Cell Biol. 1973 Mar;56(3):746–761. doi: 10.1083/jcb.56.3.746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bronfenmajer S., Schaffner F., Popper H. Fat-storing cells (lipocytes) in human liver. Arch Pathol. 1966 Nov;82(5):447–453. [PubMed] [Google Scholar]
  6. Claude A. Growth and differentiation of cytoplasmic membranes in the course of lipoprotein granule synthesis in the hepatic cell. I. Elaboration of elements of the Golgi complex. J Cell Biol. 1970 Dec;47(3):745–766. doi: 10.1083/jcb.47.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. ESSNER E., NOVIKOFF A. B. Localization of acid phosphatase activity in hepatic lysosomes by means of electron microscopy. J Biophys Biochem Cytol. 1961 Apr;9:773–784. doi: 10.1083/jcb.9.4.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ehrenreich J. H., Bergeron J. J., Siekevitz P., Palade G. E. Golgi fractions prepared from rat liver homogenates. I. Isolation procedure and morphological characterization. J Cell Biol. 1973 Oct;59(1):45–72. doi: 10.1083/jcb.59.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Farquhar M. G., Palade G. E. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. doi: 10.1083/jcb.26.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gil J., Weibel E. R. An improved apparatus for perfusion fixation with automatic pressure control. J Microsc. 1971 Dec;94(3):241–244. doi: 10.1111/j.1365-2818.1971.tb02372.x. [DOI] [PubMed] [Google Scholar]
  11. Greengard O., Federman M., Knox W. E. Cytomorphometry of developing rat liver and its application to enzymic differentiation. J Cell Biol. 1972 Feb;52(2):261–272. doi: 10.1083/jcb.52.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hughes G. M., Weibel E. R. Similarity of supporting tissue in fish gills and the mammalian reticuloendothelium. J Ultrastruct Res. 1972 Apr;39(1):106–114. doi: 10.1016/s0022-5320(72)80011-x. [DOI] [PubMed] [Google Scholar]
  13. ITO T., NEMOTO M. Uber die Kupfferschen Sternzellen und die Fettspeicherungszellen (fat storing cells) in der Blutkapillarenwand der memschlichen Leber. Okajimas Folia Anat Jpn. 1952 Oct;24(4):243–258. doi: 10.2535/ofaj1936.24.4_243. [DOI] [PubMed] [Google Scholar]
  14. Ito T., Shibasaki S. Electron microscopic study on the hepatic sinusoidal wall and the fat-storing cells in the normal human liver. Arch Histol Jpn. 1968 Mar;29(2):137–192. doi: 10.1679/aohc1950.29.137. [DOI] [PubMed] [Google Scholar]
  15. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Loud A. V. A quantitative stereological description of the ultrastructure of normal rat liver parenchymal cells. J Cell Biol. 1968 Apr;37(1):27–46. doi: 10.1083/jcb.37.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Scherle W. A simple method for volumetry of organs in quantitative stereology. Mikroskopie. 1970 Jun;26(1):57–60. [PubMed] [Google Scholar]
  19. Stäubli W., Hess R., Weibel E. R. Correlated morphometric and biochemical studies on the liver cell. II. Effects of phenobarbital on rat hepatocytes. J Cell Biol. 1969 Jul;42(1):92–112. doi: 10.1083/jcb.42.1.92. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. THORBECKE G. J., OLD L. J., BENACERRAF B., CLARKE D. A. A histochemical study of acid and alkaline phosphatase in mouse livers during various conditions modifying activity of the reticuloendothelial system. J Histochem Cytochem. 1961 Jul;9:392–399. doi: 10.1177/9.4.392. [DOI] [PubMed] [Google Scholar]
  21. Wake K. Development of vitamin A-rich lipid droplets in multivesicular bodies of rat liver stellate cells. J Cell Biol. 1974 Nov;63(2 Pt 1):683–691. doi: 10.1083/jcb.63.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Weibel E. R. Stereological principles for morphometry in electron microscopic cytology. Int Rev Cytol. 1969;26:235–302. doi: 10.1016/s0074-7696(08)61637-x. [DOI] [PubMed] [Google Scholar]
  23. Wibo M., Amar-Costesec A., Berthet J., Beaufay H. Electron microscope examination of subcellular fractions. 3. Quantitative analysis of the microsomal fraction isolated from rat liver. J Cell Biol. 1971 Oct;51(1):52–71. doi: 10.1083/jcb.51.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wisse E. An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J Ultrastruct Res. 1970 Apr;31(1):125–150. doi: 10.1016/s0022-5320(70)90150-4. [DOI] [PubMed] [Google Scholar]
  25. 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. 1972 Mar;38(5):528–562. doi: 10.1016/0022-5320(72)90089-5. [DOI] [PubMed] [Google Scholar]
  26. Wisse E. Observations on the fine structure and peroxidase cytochemistry of normal rat liver Kupffer cells. J Ultrastruct Res. 1974 Mar;46(3):393–426. doi: 10.1016/s0022-5320(74)90064-1. [DOI] [PubMed] [Google Scholar]

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