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Liver perivascular cells revealed by gold- and silver-impregnation methods and electron microscopy

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Biopathology of the Liver

Abstract

Scientific interest in the perivascular cells of the liver began over one hundred years ago, in 1876, with the discovery of ‘Sternzellen’ (stellate cells) by von Kupffer1. After much controversy through several decades, however, the theory that the perisinusoidal stellate cells play metabolic roles in retinol (vitamin A) storage and collagen synthesis in the liver, has rather recently been established (see Wake, 1980)2.

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References

  1. Kupffer, C. von. (1876). Ueber Sternzellen der Leber. Briefliche Mitteilung an Prof. Waldeyer. Arch. Mikr. Anat., 12, 353–358

    Article  Google Scholar 

  2. Wake, K. (1980). Perisinusoidal stellate cells (fat-storing cells, interstitial cells, lipocytes), their related structure in and around the liver sinusoids, and vitamin A-storing cells in extrahepatic organs. In Bourne, G. H. and Danielli, J. F. (eds.) International Review of Cytology, Vol. 66, pp. 303–353. (New York: Academic Press)

    Google Scholar 

  3. Rothe, P. (1882). Ueber die Sternzellen der Leber. Inaug.-Dissertation Munich University

    Google Scholar 

  4. Wake, K. (1964). Distribution of vitamin A in the liver. In Proceedings of The Fifth Annual General Meeting of the Japanese Histochemical Association, p. 103

    Google Scholar 

  5. Wake, K. (1971). ‘Sternzellen’ in the liver: Perisinusoidal cells with special reference to storage of vitamin A. Am. J. Anat., 132, 429–462

    Article  CAS  PubMed  Google Scholar 

  6. Kupffer, C. von. (1898). Ueber Sternzellen der Leber. Verh. Anat. Ges., 12 (Versammlung in Kiel), 80–86

    Google Scholar 

  7. Kupffer, C. von. (1899). Uber die sogenannten Sternzellen der Säugethierleber. Arch. Mikr. Anat., 54, 254–288

    Article  Google Scholar 

  8. Berkley, H.J. (1893). Studies in the histology of the liver. III. The perivascular cells of the rabbit’s liver. Anat. Anz., 8, 787–792

    Google Scholar 

  9. Dogiel, A. S. (1895). Zur Frage über die Ganglien der Darmgeflechte im den Säugetieren. Anat. Anz., 10, 517–528

    Google Scholar 

  10. Zimmermann, K.W. (1923). Der feinere Bau der Blutcapillaren, Z. Anat., 68, 29–109

    Article  Google Scholar 

  11. Suzuki, K. (1958). A silver impregnation method in histology (Japanese text). In The Experimental Therapy, No. 310–320. (Osaka: Takeda Pharmaceutical Ind.)

    Google Scholar 

  12. Suzuki, K. (1963). The end apparatus of the vegetative nervous system. In Proceedings of the sixteenth General Assembly of the Japan Medical Congress, Osaka, Vol. 4, pp. 13–28

    Google Scholar 

  13. Ito, T. (1951). Cytological studies on stellate cells of Kupffer and fat storing cells in the capillary wall of the human liver. Acta Anat. Nippon., 26, 2

    Google Scholar 

  14. Ito, T. and Nemoto, M. (1956). Morphologische Studien über die ‘Fettspeicherungszellen’ der Leber bei verschiedenen Wirbeltieren. 1. Über die Fettspeicherungszellen der Huftiere. Okajima Folia Anat. Jpn., 28, 521–542

    CAS  Google Scholar 

  15. Yamagishi, M. (1959). Electron microscope studies on the fine structure of the sinusoidal wall and fat-storing cells of rabbit livers. Arch. Histol. Jpn., 18, 223–261

    Article  Google Scholar 

  16. Nakane, P. K. (1963). Ito’s ‘fat-storing cell’ of the mouse liver. Anat. Rec., 145, 265–266

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  19. Wake, K. and Senoo, H. (1986). Morphological aspects of the differentiation of stellate cell line in the vertebrates. In Kirn, A., Knook, D. L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 215–220. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  20. Aterman, K. (1986). The parasinusoidal cells of the liver: A historical account. Histochem. J., 18, 279–305

    Article  CAS  PubMed  Google Scholar 

  21. Wisse, E., van’t Noordende, J. M., van der Meulen, J. and Daems, W. Th. (1976). The pit cell: Description of a new type of cell occurring in rat liver sinusoids and peripheral blood. Cell Tiss. Res., 173, 423–435

    Article  CAS  Google Scholar 

  22. Kaneda, K. and Wake, K. (1983). Distribution and morphological characteristics of the pit cells in the liver of the rat. Cell Tiss. Res., 233, 485–505

    Article  CAS  Google Scholar 

  23. Kaneda, K., Dan, C. and Wake, K. (1983). Pit cells as natural killer cells. Biomed. Res., 4, 567–576

    Google Scholar 

  24. Dan, C., Kaneda, K. and Wake, K. (1985). A striking increase in rod-cored vesicles in pit cells (natural killer cells) and augmentation of the liver-associated natural killer activity by a streptococcal preparation (OK-432). Biomed. Res., 6, 347–351

    Google Scholar 

  25. Wake, K., Motomatsu, K., Senoo, H., Masuda, A. and Adachi, E. (1986) Improved Kupffer’s gold chloride method for the demonstration of the stellate cells storing retinol (vitamin A) in the liver and extrahepatic organs of vertebrates. Stain Technol., 61, 193–200

    CAS  PubMed  Google Scholar 

  26. Wake, K. (1973). Cytochemistry of the lipid droplets containing vitamin A in the liver. In Wisse, E., Daems, W. Th., Molenaar, I. and Kuijin, P. van (eds.) Electron microscopy and Cytochemistry. Proceedings of the Second International Symposium on Electron Microscopy and Cytochemistry, p. 279. (Amsterdam: North-Holland Publishing Co.)

    Google Scholar 

  27. Wake, K. (1982). The Sternzellen of von Kupffer — After 106 years. In Knook, D. L. and Wisse, E. (eds.) Sinusoidal Liver Cells, pp. 1–12. (Amsterdam: Elsevier Biomedical Press)

    Google Scholar 

  28. Yamamoto, K., Sargent, P. A., Fisher, M. M. and Youson, J. H. (1986). Periductal fibrosis and lipocytes (fat-storing cells or Ito cells) during biliary atresia in the lamprey. Hepatology, 6, 54–59

    Article  CAS  PubMed  Google Scholar 

  29. Wake, K., Motomatsu, K. and Senoo, H. (1987). Stellate cells storing retinol in the liver of adult lamprey, Lampetra japonica. Cell Tiss. Res., 249, 289–299

    Article  CAS  Google Scholar 

  30. Bertolini, B. (1965). The structure of the liver cells during the life cycle of a brook-lamprey (Lampetra zanandreai). Z. Zeilforsch., 67, 297–318

    Article  CAS  Google Scholar 

  31. Shin, Y. C. (1977). Some observations on the fine structure of lamprey liver as revealed by electron microscopy. Okajima Fol. Anat. Jpn., 54, 25–60

    CAS  Google Scholar 

  32. Peek, W. D., Sidon, E. W., Youson, J. H. and Fisher, M. M. (1979). Fine structure of the liver in the larval lamprey, Petromyson marinus, hepatocytes and sinusoids. Am. J. Anat., 156, 231–250

    Article  CAS  PubMed  Google Scholar 

  33. Blomhoff, R., Holte, K., Naess, L. and Berg, T. (1984). Newly administered 3H-retinol is transferred from hepatocytes to stellate cells in liver for storage. Exp. Cell Res., 150, 186–193

    Article  CAS  PubMed  Google Scholar 

  34. Wake, K. and Motomatsu, K. (1986). Sinusoidal endothelial cells in rat liver made visualized individually by the Golgi method. In Kirn, A., Knook, D. L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, pp. 523–524. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  36. Ito, T. (1973). Recent advances in the study on the fine structure of the hepatic sinusoidal wall. Gumma Rep. Med. Sci., 6, 119–163

    Google Scholar 

  37. Yamada, E. (1982). Vitamin A storing cell. Meth. Enzymol., 81, 834–839

    CAS  PubMed  Google Scholar 

  38. Vonnahme, F.J. (1982). The structure and function of subendothelial processes of perisinusoidal cells in human liver disease. In Knook, D. L. and Wisse, E. (eds.) Sinusoidal Liver Cells, pp. 13–20. (Amsterdam: Elsevier Biomedical Press)

    Google Scholar 

  39. Takahashi-Iwanaga, H. and Fujita, T. (1986). Application of an NaOH maceration method to a scanning electron microscopic observation of Ito cells in the rat liver. Arch. Histol. Jpn., 49, 349–357

    Article  CAS  PubMed  Google Scholar 

  40. Hirosawa, K. and Yamada, E. (1975). Vitamin A storing cells; An electron microscope radioautographic study. Proceedings of The Tenth International Congress of Anatomists, p. 482

    Google Scholar 

  41. Yamada, E. and Hirosawa, K. (1976). The possible existence of a vitamin A-storing cell system. Cell Struct. Funct., 1, 201–204

    Article  Google Scholar 

  42. Hirosawa, K. (1977). A note on autoradiography: An introduction of vitamin A-storing cells. Acta Histochem. Cytochem., 10, 253–259

    Article  CAS  Google Scholar 

  43. Kusumoto, Y. and Fujita, T. (1977). Vitamin A uptake cells distributed in the liver and other organs of the rat. Arch. Histol. Jpn., 40, 121–136

    Article  CAS  PubMed  Google Scholar 

  44. Yamamoto, M. and Enzan, H. (1975). Morphology and function of Ito cell (fat-storing cell) in the liver. Recent Adv. RES Res., 15, 54–75

    Google Scholar 

  45. Yokoi, Y., Namithisa, T., Kuroda, H., Komatsu, I., Miyazaki, A., Watanabe, S. and Usui, K. (1984). Immunohistochemical detection of desmin in fat-storing cells (Ito cell). Hepatology, 4, 709–714

    Article  CAS  PubMed  Google Scholar 

  46. Uehara, Y. and Suyama, K. (1978). Visualization of the adventitial aspect of the vascular smooth muscle cells under the scanning electron microscope. J. Electron Microsc., 27, 157–159

    CAS  Google Scholar 

  47. Knook, D. L., Praaning-Van Dalen, D.P. and De Leeuw, A.M. (1986). Selection criteria for the choice of isolation methods for rat liver Kupffer, endothelial and fat-storing cells. In Kirn, A., Knook, D. L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 445–450. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  48. Pertoft, H. and Smedsrod, B. (1986). The use of percoll gradients to purify hepatocytes and sinusoidal cells from rat liver. In Kirn, A., Knook, D. L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 471–472. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  49. Tanaka, Y., Hirata, R., Minato, Y., Hasumura, Y. and Takeuchi, J. (1986). Isolation and higher purification of fat-storing cells from rat liver with flow cytometry. In Kirn, A., Knook, D.L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, p. 473. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  50. Brouwer, A., Hendriks, H. F. J., Brekelmans, P., Buijtenhek, M. and Knook, D.L. (1986). Lipid analysis of different types of isolated liver cells and their lipid droplets. In Kirn, A., Knook, D.L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 175–180. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  51. Hendriks, H. F. J., Blaner, W. S., Wennekers, H.M., Brouwer, A., De Leeuw, A. M., Goodman, D. S. and Knook, D.L. (1986). Distribution of retinoids, some retinoid binding proteins and retinyl palmitate hydrolase activity in different cell types isolated from young and old rats. In Kirn, A., Knook, D. L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 201–205. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  52. Blomhoff, R., Rasmussen, M., Nilsson, A., Norum, K. R., Berg, T., Blaner, W. S., Kato, M., Mertz, J. R., Goodman, D.S., Eriksson, U. and Peterson, P.A. (1985). Distribution of retinoids, enzymes, and binding proteins in isolated rat liver cells. J. Biol. Chem., 260, 13560–13565

    CAS  PubMed  Google Scholar 

  53. Kato, M., Kato, K. and Goodman, D.S. (1984). Immunocytochemical studies in the localization of plasma and of cellular retinol-binding proteins and of transthyretin (prealbumin) in rat liver and kidney. J. Cell Biol., 98, 1969–1704

    Article  Google Scholar 

  54. Blomhoff, R. (1985), Transport and hepatic metabolism of retinol in the rat. Inaug.-Dissertation, Oslo University

    Google Scholar 

  55. Blomhoff, R., Eskild, W., Kindberg, G. M., Pryds, K. and Berg, T. (1985). Intracellular transport of endocytosed chylomicron [3H]retinyl ester in rat liver parenchymal cells. Evidence for translocation of a [3H]retinoid from endosomes to endoplasmic reticulum. J. Biol. Chem., 260, 13566–13570

    CAS  PubMed  Google Scholar 

  56. Blomhoff, R., Norum, K. R. and Berg, T. (1985). Hepatic uptake of [3H]retinol bound to the serum retinol binding protein involves both parenchymal and perisinusoidal stellate cells. J. Biol. Chem., 260, 13571–13575

    CAS  PubMed  Google Scholar 

  57. Senoo, H., Hata, R., Nagai, Y. and Wake, K. (1984). Stellate cells (vitamin A-storing cells) are the primary site of collagen synthesis in non-parenchymal cells in the liver. Biomed. Res., 5, 451–458

    CAS  Google Scholar 

  58. Friedman, S. L., Roll, F.J. and Bissell, D.M. (1986). Collagen phenotype of rat hepatocytes in pure primary culture. In Kirn, A., Knook, D.L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 255–256. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  59. Shiratori, Y., Geerts, A., Ichida, T. and Wisse, E. (1986). Collagen production and Kupffer cell-modulated proliferation of fat-storing cells in culture. In Kirn, A., Knook, D. L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 239–244. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  60. Senoo, H., Hata, R., Nagai, Y. and Wake, K. (1986). Assembly and metabolism of collagen in the liver. In Kirn, A., Knook, D.L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 227–232. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  61. Takahara, T., Kojima, T., Miyabayashi, C., Kubota, T., Matsui, S., Inoue, K., Sasaki, H. and Ooshima, A. (1986). Production of type I and type III collagens in fat-storing cells of the rat liver following carbon tetrachloride intoxication: Immunoelectron microscopic study. In Proceedings of the Eleventh International Congress on Electron Microscopy, Kyoto, p. 2697

    Google Scholar 

  62. Enzan, H. and Hara, H. (1986). Ito cells (fat-storing cells) and collagen formation in carbon tetrachloride-induced liver fibrosis. A light and electron microscopic autoradiographic study using 3H-proline as a tracer. In Kirn, A., Knook, D.L. and Wisse, E. (eds.) Cells of the Hepatic Sinusoid, Vol. 1, pp. 233–238. (Rijswijk: Kupffer Cell Foundation)

    Google Scholar 

  63. Senoo, H. and Wake, K. (1985). Suppression of experimental hepatic fibrosis by administration of vitamin A. Lab. Invest., 52, 182–194

    CAS  PubMed  Google Scholar 

  64. Wake, K., Kamino, T., Ueki, Y. and Nagai, Y. (1986). Endocytosis and degradation of collagen fibrils by vitamin A-storing cells in the liver and intestine of the lamprey. Proceedings of the Eleventh International Congress on Electron Microscopy, Kyoto, p. 1941

    Google Scholar 

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  1. K. Wake
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Editors and Affiliations

  1. Department of Anatomy, Faculty of Medicine, University ‘La Sapienza’, Viale Regina Elena 289, 00161, Rome, Italy

    Pietro M. Motta MD, PhD (Chairman and Professor) (Chairman and Professor)

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Wake, K. (1988). Liver perivascular cells revealed by gold- and silver-impregnation methods and electron microscopy. In: Motta, P.M. (eds) Biopathology of the Liver. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-1239-7_3

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  • DOI: https://doi.org/10.1007/978-94-009-1239-7_3

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-7049-2

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