Biochemistry (Moscow)

, 73:367 | Cite as

Mechanisms determining phenotypic heterogeneity of hepatocytes

  • I. F. UsyninEmail author
  • L. E. Panin


This review summarizes results of biochemical and immunohistochemical studies indicating the existence of functional heterogeneity of hepatocytes depending on their localization in the hepatic acinus; this determines characteristic features of metabolism of carbohydrates, lipids, and xenobiotics. The physiological significance of hepatocyte heterogeneity is discussed. According to the proposed model of intercellular communication, the metabolic specialization of hepatocytes is determined by secretory activity of hepatic resident macrophages (Kupffer cells) localized mainly in the periportal zone of the liver acinus. Macrophages participate in secretion of a wide spectrum of intercellular mediators (cytokines, prostaglandins, growth factors) and also in metabolism of numerous blood metabolites and biologically active substances (hormones, lipoproteins, etc.). In the sinusoid and in the space of Disse (also known as perisinusoidal space) they form a concentration gradient of regulatory factors and metabolites inducing the phenotypic differences between hepatocytes.

Key words

liver metabolism hepatocyte heterogeneity macrophage Kupffer cell intercellular communications 





cytochrome P450


epidermal growth factor


glucose-6-phosphate dehydrogenase


high density lipoproteins


hepatocyte growth factor


insulin-like growth factor


insulin-like growth factor binding protein




latency associated peptide


low density lipoproteins


latent TGF-binding protein




plasminogen activator inhibitor-1




phosphoenolpyruvate carboxykinase


transforming growth factor-β1


tumor necrosis factor-α


very low density lipoproteins


  1. 1.
    Wilson, J. W. (1958) in Liver Function, a Symposium on Approaches to the Quantitative Description of Liver Function, American Institute of Biological Sciences, Washington, DC, pp. 175–197.Google Scholar
  2. 2.
    Jungermann, K. (1995) Histochem. Cell Biol., 103, 81–91.PubMedCrossRefGoogle Scholar
  3. 3.
    Katz, N. (1992) J. Nutr., 122, 843–849.PubMedGoogle Scholar
  4. 4.
    Bengtsson, B. G., Smith-Killand, A., and Morland, J. (1984) Exp. Mol. Pathol., 41, 44–57.PubMedCrossRefGoogle Scholar
  5. 5.
    Panin, L. E., and Usynin, I. F. (1986) Byul. Eksp. Biol. Med., No. 6, 695–697.Google Scholar
  6. 6.
    Rappaport, A. M. (1975) in Diseases of the Liver (Schiff, L., ed.) pp. 1–50.Google Scholar
  7. 7.
    Schmucker, B. L., Mooney, J. S., and Jones, A. L. (1978) J. Cell Biol., 78, 319–337.PubMedCrossRefGoogle Scholar
  8. 8.
    Kanamura, S., Kanai, K., and Watanabe, J. (1990) J. Electron. Microsc. Tech., 14, 92–105.PubMedCrossRefGoogle Scholar
  9. 9.
    Ferri, D., Moro, L., Mastrodonato, M., Capuano, F., Marra, E., Liquori, G. E., and Greco, M. (2005) J. Biol. Cell., 97, 277–288.CrossRefGoogle Scholar
  10. 10.
    Lindauer, M., Beier, K., Volkl, A., and Fahimi, H. D. (1994) Hepatology, 20, 475–486.PubMedGoogle Scholar
  11. 11.
    Van Noorden, C. J., Vogels, I. M., and James, J. (1994) Hepatology, 20, 714–724.PubMedGoogle Scholar
  12. 12.
    Layden, T. J., and Boyer, J. L. (1978) Lab. Invest., 39, 110–119.PubMedGoogle Scholar
  13. 13.
    Blitzer, B. L., and Boyer, B. (1982) Gastroenterology, 82, 346–357.PubMedGoogle Scholar
  14. 14.
    Castagna, M., and Chauveau, J. (1969) Exptl. Cell Res., 57, 211–222.PubMedCrossRefGoogle Scholar
  15. 15.
    Wanson, J.-C., Drochmans, P., May, C., Penasse, W., and Popowski, A. (1975) J. Cell Biol., 66, 23–41.PubMedCrossRefGoogle Scholar
  16. 16.
    Allen, C. M., and Paine, A. J. (1983) Biochem. Soc. Trans., 11, 275.Google Scholar
  17. 17.
    Baron, J., Redick, J. A., and Guengerich, P. P. (1982) J. Biol. Chem., 257, 953–957.PubMedGoogle Scholar
  18. 18.
    Moody, D. E., Taylor, L. A., Smuckler, E. A., Levin, W., and Thomas, P. E. (1983) Drug Met. Dis., 11, 339–343.Google Scholar
  19. 19.
    Tavassoli, M., Ozols, J., Sugimoto, G., Cox, K. H., and Muller-Eberhard, U. (1976) Biochem. Biophys. Res. Commun., 72, 281–287.PubMedGoogle Scholar
  20. 20.
    Panin, L. E., and Usynin, I. F. (1987) Byul. Eksp. Biol. Med., No. 2, 172–174.Google Scholar
  21. 21.
    Tordjmann, T., Berthon, B., Lardeux, B., Moreau, A., Jacquemin, E., Combettes, L., Feldmann, G., and Claret, M. (1997) Hepatology, 26, 1592–1599.PubMedCrossRefGoogle Scholar
  22. 22.
    Ugele, B., and Gebhardt, R. (2003) Hepatol. Res., 27, 238–247.PubMedCrossRefGoogle Scholar
  23. 23.
    Fisher, W., Ick, M., and Katz, N. R. (1982) Hoppe-Seyler’s Z. Physiol. Chem., 363, 375–380.Google Scholar
  24. 24.
    Usynin, I. F. (1999) The Role of Macrophages in Regulation of Metabolic Processes in the Liver during Functional Load of the Body: Doctoral dissertation [in Russian], Novosibirsk.Google Scholar
  25. 25.
    Wisse, E., Braet, F., Luo, D., Vermijlen, D., Eddouks, M., Konstandoulaki, M., Empsen, C., and de Zanger, R. B. (1999) in Liver Diseases and Hepatic Sinusoidal Cells (Tanikawa, K., and Ueno, T., eds.) Springer, Tokyo, pp. 17–55.Google Scholar
  26. 26.
    Usynin, I. F. (1987) Biochemical Analysis of Functional Heterogeneity of Hepatocytes: Candidate’s dissertation [in Russian], Novosibirsk.Google Scholar
  27. 27.
    Ikezawa, Y., Yamatani, K., Ogawa, A., Ohnuma, H., Igarashi, M., Daimon, M., Manaka, H., and Sasaki, H. (1998) J. Lab. Clin. Med., 132, 547–555.PubMedCrossRefGoogle Scholar
  28. 28.
    Giffin, B. F., Drake, R. L., Morris, R. E., and Cardell, R. R. (1993) J. Histochem. Cytochem., 41, 1849–1862.PubMedGoogle Scholar
  29. 29.
    Sasse, D., and Hoffmann, H. (1982) Histochemistry, 75, 31–42.PubMedCrossRefGoogle Scholar
  30. 30.
    Asada-Kubota, M., Kanai, K., and Kanamura, S. (1982) Anat. Rec., 202, 395–405.PubMedCrossRefGoogle Scholar
  31. 31.
    Quistorff, B., Katz, N., and Witters, L. A. (1992) Enzyme, 46, 59–71.PubMedGoogle Scholar
  32. 32.
    Rieder, H. (1981) Histochemistry, 72, 579–615.PubMedCrossRefGoogle Scholar
  33. 33.
    Aspichueta, P., Perez, S., Ochoa, B., and Fresnedo, O. (2005) J. Lipid Res., 46, 1017–1026.PubMedCrossRefGoogle Scholar
  34. 34.
    Panin, L. E., Usynin, I. F., and Polyakov, L. M. (1986) Vopr. Med. Khim., No. 4, 106–110.Google Scholar
  35. 35.
    Botham, K. M., Fresnedo, O., Romero, J. R., and Ochoa, B. (1998) Gen. Physiol. Biophys., 17, 79–94.PubMedGoogle Scholar
  36. 36.
    Voorschuur, A. H., Kuiper, J., Neelissen, J. A., Boers, W., and van Berkel, T. J. (1994) Biochem. J., 303, 809–816.PubMedGoogle Scholar
  37. 37.
    Romero, J. R., Fresnedo, O., Isusi, E., Barrionuevo, J., and Ochoa, B. (1999) Lipids, 34, 907–913.PubMedCrossRefGoogle Scholar
  38. 38.
    Gebhardt, R., Alber, J., Wegner, H., and Mecke, D. (1994) Biochem. Pharmacol., 48, 761–766.PubMedCrossRefGoogle Scholar
  39. 39.
    McKinnon, R. A., Hall, P. D., Quattrochi, L. C., Tukey, R. H., and McManus, M. E. (1991) Hepatology, 14, 848–856.PubMedCrossRefGoogle Scholar
  40. 40.
    Taira, Y., Redick, J. A., and Baron, J. (1980) Mol. Pharmacol., 17, 374–381.PubMedGoogle Scholar
  41. 41.
    Thurman, R. G., and Kauffman, B. C. (1985) Hepatology, 5, 144–151.PubMedCrossRefGoogle Scholar
  42. 42.
    Ekberg, K., Chandramouli, V., Kumaran, K., Schumann, W. C., Wahren, J., and Landau, B. R. (1995) J. Biol. Chem., 270, 21715–21717.PubMedCrossRefGoogle Scholar
  43. 43.
    Ullrich, D., Fischer, G., Katz, H., and Bock, K. W. (1984) Chem.-Biol. Interact., 48, 181–190.PubMedCrossRefGoogle Scholar
  44. 44.
    Novikoff, A. B. (1959) J. Histochem. Cytochem., 7, 240–244.PubMedGoogle Scholar
  45. 45.
    Allen, J. W., Khetani, S. R., and Bhatia, S. N. (2005) Toxicol. Sci., 84, 110–119.PubMedCrossRefGoogle Scholar
  46. 46.
    Jungermann, K., and Kietzmann, T. (2000) Hepatology, 31, 255–260.PubMedCrossRefGoogle Scholar
  47. 47.
    Gulak, P. V., Dudchenko, A. M., Zaitsev, V. V., Luk’yanova, L. D., Novikov, K. N., Orlov, S. N., Pokudin, N. I., Popova, O. A., and Ugolev, A. T. (1985) Hepatocyte: Functional and Metabolic Properties [in Russian], Nauka, Moscow.Google Scholar
  48. 48.
    Gebhardt, R., and Mecke, D. (1984) in Glutamate Metabolism in Mammalian Tissues (Haussinger, D., and Sies, H., eds.) Springer Verlag, Heidelberg, pp. 98–121.Google Scholar
  49. 49.
    Stoll, B., McNelly, S., Buscher, H. P., and Haussinger, D. (1991) Hepatology, 13, 247–253.PubMedGoogle Scholar
  50. 50.
    Wilson, D. F., Owen, C. S., and Erecinska, M. (1979) Arch. Biochem. Biophys., 195, 494–504.PubMedCrossRefGoogle Scholar
  51. 51.
    Ghosh, A. K., Finegold, D., White, W., Zawalich, K., and Matschinsky, F. N. (1982) J. Biol. Chem., 257, 5476–5481.PubMedGoogle Scholar
  52. 52.
    Jungermann, K., and Katz, N. (1982) in Metabolic Compartmentation, Academic Press, London, pp. 411–435.Google Scholar
  53. 53.
    Rossouw, J. E., Labadarios, D., Vinik, I., and de Villiers, A. S. (1978) Metabolism, 27, 1067–1073.PubMedCrossRefGoogle Scholar
  54. 54.
    Wittig, B., Zierz, S., Gubernatis, G., Nath, A., and Jungermann, K. (1985) Biol. Chem. Hoppe-Seyler, 366, 713–722.PubMedGoogle Scholar
  55. 55.
    Miethke, H., Wittig, B., Nath, A., Zierz, S., and Jungermann, K. (1985) Biol. Chem. Hoppe-Seyler, 366, 493–501.PubMedGoogle Scholar
  56. 56.
    Lee, S. M., and Clemens, M. G. (2004) Shock, 22, 82–87.PubMedCrossRefGoogle Scholar
  57. 57.
    Bouwens, L., de Bleser, P., Vanderkerken, K., Geerts, B., and Wisse, E. (1992) Enzyme, 46, 155–168.PubMedGoogle Scholar
  58. 58.
    Shin, Y. C. (1997) Anat. Rec., 247, 206–213.PubMedCrossRefGoogle Scholar
  59. 59.
    Bykov, B., Ylipaasto, P., Eerola, L., and Lindros, K. O. (2003) Scand. J. Gastroenterol., 38, 1256–1261.PubMedCrossRefGoogle Scholar
  60. 60.
    Naito, M., Hasegawa, G., Ebe, Y., and Yamamoto, T. (2004) Med. Electron. Microsc., 37, 16–28.PubMedCrossRefGoogle Scholar
  61. 61.
    Ogi, M., Yokomori, H., Oda, M., Yoshimura, K., Nomura, M., Ohshima, S., Akita, M., Toda, K., and Ishii, H. (2003) Med. Electron. Microsc., 36, 33–40.PubMedCrossRefGoogle Scholar
  62. 62.
    Theuerkauf, I., Zhou, H., and Fischer, H. P. (2001) Virchows Arch., 438, 498–504.PubMedCrossRefGoogle Scholar
  63. 63.
    Pusztaszeri, M. P., Seelentag, W., and Bosman, F. T. (2006) J. Histochem. Cytochem., 54, 385–395.PubMedCrossRefGoogle Scholar
  64. 64.
    Dini, L., and Carla, E. C. (1998) Exp. Cell Res., 240, 388–393.PubMedCrossRefGoogle Scholar
  65. 65.
    Hailfinger, S., Jaworski, M., Braeuning, A., Buchmann, A., and Schwarz, M. (2006) Hepatology, 43, 407–414.PubMedCrossRefGoogle Scholar
  66. 66.
    Braeuning, A., Ittrich, C., Kohle, C., Buchmann, A., and Schwarz, M. (2007) Drug Metab. Dispos., 35, 503–507.PubMedCrossRefGoogle Scholar
  67. 67.
    Benhamouche, S., Decaens, T., Godard, C., Chambrey, R., Rickman, D. S., Moinard, C., Vasseur-Cognet, M., Kuo, C. J., Kahn, A., Perret, C., and Colnot, S. (2006) Dev. Cell, 10, 759–770.PubMedCrossRefGoogle Scholar
  68. 68.
    Burke, Z. D., and Tosh, D. (2006) BioEssays, 28, 1072–1077.PubMedCrossRefGoogle Scholar
  69. 69.
    Gumucio, J. J., and Gebhardt, R. (1992) Hepatology, 16, 843–845.CrossRefGoogle Scholar
  70. 70.
    Decker, K. (1990) Eur. J. Biochem., 192, 245–261.PubMedCrossRefGoogle Scholar
  71. 71.
    Kmiec, Z. (2001) Adv. Anat. Embryol. Cell Biol., 161, 1–151.Google Scholar
  72. 72.
    Cavaillon, J. M. (1995) Bull. Inst. Pasteur, 93, 21–41.CrossRefGoogle Scholar
  73. 73.
    Berry, L. J., Goodrum, K. J., Resnick, I. G., and Ford, C. W. (1980) in RES and Pathogenesis of Liver Diseases (Liehr, H., and Grun, M., eds.) North Holland Biomedical Press, pp. 257–266.Google Scholar
  74. 74.
    McCallum, R. E., Seale, T. W., and Stith, R. D. (1983) Infect. Immun., 39, 213–219.PubMedGoogle Scholar
  75. 75.
    Hill, M., and McCallum, R. (1991) J. Clin. Invest., 88, 811–816.PubMedCrossRefGoogle Scholar
  76. 76.
    Bernuau, D., Legres, L., Giuily, N., Fey, G., and Feldmann, G. (1989) J. Exp. Med., 170, 349–354.PubMedCrossRefGoogle Scholar
  77. 77.
    Blumberg, D., Hochwald, S., Brennan, M. F., and Burt, M. (1995) Metabolism, 44, 145–146.PubMedCrossRefGoogle Scholar
  78. 78.
    Thoresen, G. H., Refsnes, M., Dajani, O. F., Johansen, E. J., and Christoffersen, T. (1995) Pharmacol. Toxicol., 76, 163–170.PubMedGoogle Scholar
  79. 79.
    Hill, M., and McCallum, R. E. (1992) Infect. Immun., 60, 4040–4050.PubMedGoogle Scholar
  80. 80.
    Yerkovich, S. T., Rigby, P. J., Fournier, P. A., Olynyk, J. K., and Yeoh, G. C. (2004) Int. J. Biochem. Cell. Biol., 36, 1462–1472.PubMedGoogle Scholar
  81. 81.
    Miyake, H., Takehara, H., and Starnes, F. J. (1994) Clin. Biochem. Nutr., 17, 1–9.Google Scholar
  82. 82.
    Christ, B., and Nath, A. (1996) Biochem. J., 320, 161–166.PubMedGoogle Scholar
  83. 83.
    Hill, M. R., Stith, R. D., and McCallum R. E. (1986) J. Immunol., 137, 858–862.PubMedGoogle Scholar
  84. 84.
    Kanemaki, T., Kitade, H., Kaibori, M., Sakitani, K., Hiramatsu, Y., Kamiyama, Y., Ito, S., and Okumura, T. (1998) Hepatology, 27, 1296–1303.PubMedCrossRefGoogle Scholar
  85. 85.
    Sprangers, F., Sauerwein, H. P., Romijn, J. A., van Woerkom, G. M., and Meijer, A. J. (1998) Biochem. J., 330, 1045–1049.PubMedGoogle Scholar
  86. 86.
    Christ, B., Nath, A., Heinrich, P. C., and Jungermann, K. (1994) Hepatology, 20, 1577–1583.PubMedCrossRefGoogle Scholar
  87. 87.
    Kuiper, J., Casteleyn, E., and van Berkel, T. J. C. (1989) Agent. Action, 26, 201–202.CrossRefGoogle Scholar
  88. 88.
    Schieferdecker, H. L., Schlaf, G., Jungermann, K., and Gotze, O. (2001) Int. Immunopharmacol., 1, 469–481.PubMedCrossRefGoogle Scholar
  89. 89.
    Pestel, S., Schlaf, G., Gotze, O., Jungermann, K., and Schieferdecker, H. L. (2003) Lab. Invest., 83, 1733–1741.PubMedCrossRefGoogle Scholar
  90. 90.
    Okumura, T., and Saito, K. (1990) Prostaglandins, 39, 525–540.PubMedCrossRefGoogle Scholar
  91. 91.
    Nukina, S., Fusaoka, T., and Thurman, R. G. (1994) Am. J. Physiol., 266, G99–G105.PubMedGoogle Scholar
  92. 92.
    Hardardottir, I., Grunfeld, C., and Feingold, K. R. (1995) Biochem. Soc. Trans., 23, 1013–1018.PubMedGoogle Scholar
  93. 93.
    Chajek-Shaul, T., Freidman, G., Stein, O., Etienne, J., and Stein, Y. (1989) Biochim. Biophys. Acta, 1001, 316–124.PubMedGoogle Scholar
  94. 94.
    Feingold, K. R., Soued, M., Serio, M. K., Moser, A. N., Dinarello, C. A., and Grunfeld, C. (1989) Endocrinology, 125, 267–274.PubMedGoogle Scholar
  95. 95.
    Grunfeld, C., Verdier, J. A., Neese, R., Moser, A. H., and Feingold, K. R. (1988) J. Lipid Res., 29, 1327–1335.PubMedGoogle Scholar
  96. 96.
    Nonogaki, K., Fuller, G. M., Fuentes, N. L., Moser, A. H., Staprans, I., Grunfeld, C., and Feingold, K. R. (1995) Endocrinology, 136, 2143–2149.PubMedCrossRefGoogle Scholar
  97. 97.
    Grove, R. I., Mazzucco, C., Allegretto, N., Kiener, P. A., Spitalny, G., Radka, S. F., Shoyab, M., Antonaccio, M., and Warr, G. A. (1991) J. Lipid Res., 32, 1889–1897.PubMedGoogle Scholar
  98. 98.
    Liu, J. W., Grove, R. I., and Vestal, R. E. (1994) Cell Growth Differ., 5, 1333–1338.PubMedGoogle Scholar
  99. 99.
    Rea, T. J., Bisgaier, C. L., Demattos, R. B., and Pape, M. E. (1994) J. Lipid Res., 35, 1274–1282.PubMedGoogle Scholar
  100. 100.
    Ettinger, W. H., Varma, V. K., Sorcithomas, M., Parks, J. S., Sigmon, R. C., Smith, T. K., and Verdery, P. B. (1994) Arterioscler. Thromb., 14, 8–13.PubMedGoogle Scholar
  101. 101.
    Ghezzi, P., Saccardo, B., and Bianchi, M. (1986) Biochem. Biophys. Res. Commun., 136, 316–321.PubMedCrossRefGoogle Scholar
  102. 102.
    Craig, P. I., Williams, S. J., Cantrill, E., and Farrell, G. C. (1989) Gastroenterology, 197, 999–1004.Google Scholar
  103. 103.
    Morgan, E. T., Thomas, K. B., Swanson, R., Vales, T., Hwang, J., and Wright, K. (1994) Biochim. Biophys. Acta, 1219, 475–483.PubMedGoogle Scholar
  104. 104.
    Cantoni, L., Carelli, M., Ghezzi, P., Delgado, R., Faggioni, R., and Rizzardini, M. (1995) Eur. J. Pharmacol. Environ. Toxic., 292, 257–263.CrossRefGoogle Scholar
  105. 105.
    Sunman, J. A., Hawke, R. L., LeCluyse, E. L., and Kashuba, A. D. B. (2004) Drug Metab. Dis., 32, 359–363.CrossRefGoogle Scholar
  106. 106.
    Abdel-Razzak, Z., Corcos, L., Fautrel, A., Campion, J. P., and Guillouzo, A. (1994) Mol. Pharmacol., 46, 1100–1110.PubMedGoogle Scholar
  107. 107.
    Stadler, J., Trockfeld, J., Schmalix, W. A., Brill, T., Siewert, J. R., Greim, H., and Doehmer, J. (1994) Proc. Natl. Acad. Sci. USA, 91, 3559–3563.PubMedCrossRefGoogle Scholar
  108. 108.
    Panin, L. E., Sokolova, M. V., and Usynin, I. F. (1991) Patol. Fiziol. Eksp. Ter., No. 1, 20–22.Google Scholar
  109. 109.
    Mayanski, D. N., Wisse, E., and Decker, K. (1992) New Horizons of Hepatology [in Russian], Nauka, Novosibirsk.Google Scholar
  110. 110.
    Takeishi, T., Hirano, K., Kobayashi, T., Hasegawa, G., Hatakeyama, K., and Naito, M. (1999) Arch. Histol. Cytol., 62, 413–422.PubMedCrossRefGoogle Scholar
  111. 111.
    Meijer, C., Wiezer, M. J., Diehl, A. M., Schouten, H. J., Schouten, H. J., Meijer, S., van Rooijen, N., van Lambalgen, A. A., Dijkstra, C. D., and van Leeuwen, P. A. (2000) Liver, 20, 66–77.PubMedCrossRefGoogle Scholar
  112. 112.
    Malik, R., Selden, C., and Hodgson, H. (2002) Semin. Cell. Dev. Biol., 13, 425–431.PubMedCrossRefGoogle Scholar
  113. 113.
    Fausto, N., and Riehle, K. J. (2005) J. Hepatobiliary Pancreat. Surg., 12, 181–189.PubMedCrossRefGoogle Scholar
  114. 114.
    Satoh, M., and Yamazaki, M. (1992) J. Cell Physiol., 150, 134–139.PubMedCrossRefGoogle Scholar
  115. 115.
    Fausto, N., Laird, A. D., and Webber, E. M. (1995) FASEB J., 9, 1527–1536.PubMedGoogle Scholar
  116. 116.
    Diehl, A. M., and Rai, R. J. (1996) Gastroenterol. Hepatol., 11, 466–470.CrossRefGoogle Scholar
  117. 117.
    Rolfe, M., James, N. H., and Roberts, R. A. (1997) Carcinogenesis, 18, 2277–2280.PubMedCrossRefGoogle Scholar
  118. 118.
    Iocca, H. A., and Isom, H. C. (2003) Am. J. Pathol., 163, 465–476.PubMedGoogle Scholar
  119. 119.
    Abshagen, K., Eipel, C., Kalff, J. C., Menger, M. D., and Vollmar, B. (2007) Am. J. Physiol. Gastrointest. Liver Physiol., 292, G1570–G1577.PubMedCrossRefGoogle Scholar
  120. 120.
    Yamada, Y., and Fausto, N. (1998) Am. J. Pathol., 152, 1577–1589.PubMedGoogle Scholar
  121. 121.
    Blindenbacher, A., Wang, X., Langer, I., Savino, R., Terracciano, L., and Heim, M. H. (2003) Hepatology, 38, 674–682.PubMedCrossRefGoogle Scholar
  122. 122.
    Galun, E., and Axelrod, J. H. (2002) Biochim. Biophys. Acta, 1592, 345–358.PubMedCrossRefGoogle Scholar
  123. 123.
    Aldeguer, X., Debonera, F., Shaked, A., Krasinkas, A. M., Gelman, A. E., Que, X., Zamir, G. A., Hiroyasu, S., Kovalovich, K. K., Taub, R., and Olthoff, K. M. (2002) Hepatology, 35, 40–48.PubMedCrossRefGoogle Scholar
  124. 124.
    Taub, R., Greenbaum, L. E., and Peng, Y. (1999) Semin. Liver Dis., 19, 117–127.PubMedGoogle Scholar
  125. 125.
    Gohda, E. (2002) Nippon. Yakurigaku. Zasshi., 119, 287–294.PubMedGoogle Scholar
  126. 126.
    Ogura, Y., Hamanoue, M., Tanabe, G., Mitsue, S., Yoshidome, S., Nuruki, K., and Aikou, T. (2001) Hepatogastroenterology, 48, 545–549.PubMedGoogle Scholar
  127. 127.
    Noji, S., Tashiro, K., Koyama, E., Nohno, T., Ohyama, K., Taniguchi, S., and Nakamura, T. (1990) Biochem. Biophys. Res. Commun., 173, 42–47.PubMedCrossRefGoogle Scholar
  128. 128.
    Hata, J., Ikeda, E., Uno, H., and Asano, S. (2002) J. Histochem. Cytochem., 50, 1461–1468.PubMedGoogle Scholar
  129. 129.
    Takeishi, T., Hirano, K., Kobayashi, T., Hasegawa, G., Hatakeyama, K., and Naito, M. (1999) Arch. Histol. Cytol., 62, 413–422.PubMedCrossRefGoogle Scholar
  130. 130.
    Iida, I., Johkura, K., Teng, R., Kubota, S., Cui, L., Zhao, X., Ogiwara, N., Okouchi, Y., Asanuma, K., Nakayama, J., and Sasaki, K. J. (2003) Histochem. Cytochem., 51, 1139–1149.Google Scholar
  131. 131.
    Pal’tsev, M. A., and Ivanov, A. A. (1995) Intercellular Interactions [in Russian], Meditsina, Moscow.Google Scholar
  132. 132.
    Kimura, M., and Ogihara, M. (1998) Eur. J. Pharmacol., 354, 271–281.PubMedCrossRefGoogle Scholar
  133. 133.
    Scott, C. D., and Baxter, R. C. (1986) Endocrinology, 119, 2346–2352.PubMedCrossRefGoogle Scholar
  134. 134.
    Pinzani, M., Abboud, H. E., and Aron, D. C. (1990) Endocrinology, 127, 2343–2349.PubMedGoogle Scholar
  135. 135.
    Scharf, J., Ramadori, G., Braulke, T., and Hartmann, H. (1996) Hepatology, 23, 818–827.PubMedCrossRefGoogle Scholar
  136. 136.
    Zimmermann, E. M., Li, L., Hoyt, E. C., Pucilowska, J. B., Lichtman, S., and Lund, P. K. (2000) Am. J. Physiol. Gastrointest. Liver Physiol., 278, G447–G457.PubMedGoogle Scholar
  137. 137.
    Villafuerte, B. C., Koop, B. L., Pao, C.-I., Gu, L., Birdsong, G. G., and Phillips, L. S. (1994) Endocrinology, 134, 2044–2050.PubMedCrossRefGoogle Scholar
  138. 138.
    Meyer, D. H., Bachem, M. G., and Gressner, A. M. (1991) FEBS Lett., 283, 150–154.PubMedCrossRefGoogle Scholar
  139. 139.
    Kimura, M., and Ogihara, M. (1999) Eur. J. Pharmacol., 386, 271–277.PubMedCrossRefGoogle Scholar
  140. 140.
    De Bleser, P. J., Niki, T., Rogiers, V., and Geerts, A. (1997) J. Hepatol., 26, 886–893.PubMedCrossRefGoogle Scholar
  141. 141.
    Roth, S., Gong, W., and Gressner, A. M. (1998) J. Hepatol., 29, 915–922.PubMedCrossRefGoogle Scholar
  142. 142.
    Breitkopf, K., Lahme, B., Tag, C. G., and Gressner, A. M. (2001) Hepatology, 33, 387–396.PubMedCrossRefGoogle Scholar
  143. 143.
    George, S. J., Johnson, J. L., Smith, M. A., Angelini, G. D., and Jackson, C. L. (2005) J. Vasc. Res., 42, 247–254.PubMedCrossRefGoogle Scholar
  144. 144.
    Gentry, J., Arthur, M. J., and Benyon, R. C. (1996) Hepatology, 24, 1172–1178.PubMedCrossRefGoogle Scholar
  145. 145.
    Fearns, C., and Loskutoff, D. J. (1997) Am. J. Pathol., 150, 579–590.PubMedGoogle Scholar
  146. 146.
    Panin, L. E., Sokolova, M. V., and Usynin, I. F. (1990) Tsitologiya, No. 5, 528–532.Google Scholar
  147. 147.
    Usynin, I. F., Panin, L. E., Kharkovski, A. V., Gorjacheva, M. V., Ostanina, L. S., Trubitsina, O. M., and Tretjakova, T. A. (1995) in Cells of the Hepatic Sinusoid (Wisse, E., Knook, D. L., and Wake, K., eds.) Vol. 5, The Kupffer Cell Foundation, Leiden, The Netherlands, pp. 297–298.Google Scholar
  148. 148.
    Panin, L. E., Usynin, I. F., Kharkovski, A. V., Gorjacheva, M. V., and Maksimov, V. F. (1997) in Cells of the Hepatic Sinusoid (Wisse, E., Knook, D. L., and Balabaud, C., eds.) Vol. 6, The Kupffer Cell Foundation, Leiden, The Netherlands, pp. 156–157.Google Scholar
  149. 149.
    Panin, L. E., Maksimov, V. F., Korostyshevskaya, I. M., and Usynin, I. F. (2002) J. Steroid Biochem. Mol. Biol., 81, 69–76.PubMedCrossRefGoogle Scholar
  150. 150.
    Usynin, I. F., Panin, L. E., Kharkovski, A. V., and Gorjacheva, M. V. (1995) Biochemistry (Moscow), 60, 399–406.Google Scholar
  151. 151.
    Miyazawa, M., Torii, T., Toshimitsu, Y., and Koyama, I. (2005) Transplant Proc., 37, 2398–2401.PubMedCrossRefGoogle Scholar
  152. 152.
    Zinchenko, Y. S., Schrum, L. W., Clemens, M., and Coger, R. N. (2006) Tissue Eng., 12, 751–761.PubMedCrossRefGoogle Scholar
  153. 153.
    Panin. L. E., Usynin, I. F., Trubytsyna, O. M., Kharkovski, A. V., Sokolova, M. V., and Ostanina, L. S. (1994) Biochemistry (Moscow), 59, 249–254.Google Scholar
  154. 154.
    Provatorov, G. V., Usynin, I. F., Polyakov, L. M., and Glazyrin, A. L. (1993) Tsytologiya, 35, 42–57.Google Scholar
  155. 155.
    Van Berkel, Th. J. C., Kruijt, J. K., van Gent, T., and van Tol, A. (1980) Biochem. Biophys. Res. Commun., 92, 1002–1008.PubMedCrossRefGoogle Scholar
  156. 156.
    Panin. L. E., Usynin, I. F., Kharkovski, A. V., and Poteryaeva, O. N. (1998) Byul. Eksp. Biol. Med., No. 7, 43–45.Google Scholar
  157. 157.
    Rahim, A. T. M. A., Miyazaki, A., Morino, Y., and Horiuchi, S. (1991) Biochim. Biophys. Acta, 1082, 195–203.PubMedGoogle Scholar
  158. 158.
    Van Berkel, Th. J. C. (1979) Trends Biochem. Sci., 9, 202–205.Google Scholar
  159. 159.
    Favre, G., Blancy, E., Tournier, J. F., and Soula, G. (1989) Biochim. Biophys. Acta, 1013, 118–124.PubMedCrossRefGoogle Scholar
  160. 160.
    Gospodarowicz, D., Massoglia, D. S., and Cheng, D. K. (1986) J. Cell Physiol., 127, 121–136.PubMedCrossRefGoogle Scholar
  161. 161.
    Nofer, J. R., Junker, R., Pulawski, E., Fobker, M., Levkau, B., von Eckardstein, A., Seedorf, U., Assmann, G., and Walter, M. (2001) Thromb. Haemost., 85, 730–735.PubMedGoogle Scholar
  162. 162.
    Favre, G., Tazi, K. A., Le Gaillard, F., Bennis, F., Hachem, H., and Soula, G. (1993) J. Lipid Res., 34, 1093–1106.PubMedGoogle Scholar
  163. 163.
    Libby, P., Miao, P., Ordovas, J. M., and Schaffer, E. J. (1985) J. Cell. Physiol., 124, 1–8.PubMedCrossRefGoogle Scholar
  164. 164.
    Handwerger, S., Myers, S., Richards, R., Richardson, B., Turzai, L., Moeykins, C., Meyer, T., and Anantharamahiah, G. M. (1995) Endocrinology, 136, 5555–5560.PubMedCrossRefGoogle Scholar
  165. 165.
    Zhou, X., and von Eckardstein, A. (2002) J. Huazhong. Univ. Sci. Technol. Med. Sci., 22, 270–272.PubMedGoogle Scholar
  166. 166.
    Kockx, M., Rye, K. A., Gaus, K., Quinn, C. M., Wright, J., Sloane, T., Sviridov, D., Fu, Y., Sullivan, D., Burnett, J. R., Rust, S., Assmann, G., Anantharamaiah, G. M., Palgunachari, M. N., Katz, S. L., Phillips, M. C., Dean, R. T., Jessup, W., and Kritharides, L. (2004) J. Biol. Chem., 279, 25966–25977.PubMedCrossRefGoogle Scholar
  167. 167.
    Yamato, K., Tamasawa, N., Murakami, H., Matsui, J., Tanabe, J., Suda, T., and Yasujima, M. (2005) Diabetes Res. Clin. Pract., 69, 124–128.PubMedCrossRefGoogle Scholar
  168. 168.
    Hyka, N., Dayer, J.-M., Modoux, C., Kohno, T., Edwards, III, C. K., Roux-Lombard, P., and Burger, D. (2001) Blood, 97, 2381–2389.PubMedCrossRefGoogle Scholar
  169. 169.
    Araneo, B. A., Dowell, T., Diegel, M., and Daynes, R. A. (1991) Blood, 78, 688–699.PubMedGoogle Scholar
  170. 170.
    Mekata, H. (1971) Nagoya J. Med. Sci., 34, 89–99.PubMedGoogle Scholar
  171. 171.
    Panin, L. E., Kharkovski, A. V., and Usynin, I. F. (2000) Byul. Eksp. Biol. Med., 129, 171–173.CrossRefGoogle Scholar
  172. 172.
    Brix, K., Wirtz, R., and Herzog, V. (1997) Hepatology, 26, 1232–1240.PubMedGoogle Scholar
  173. 173.
    Watanabe, J., Kanai, K., and Kanamura, S. (1988) J. Histochem. Cytochem., 36, 1081–1089.PubMedGoogle Scholar
  174. 174.
    Soda, R., and Tavassoli, M. (1983) Exp. Cell Res., 145, 389–395.PubMedCrossRefGoogle Scholar
  175. 175.
    Ansorge, S., Wiederanders, B., Riemann, S., Brouwer, A., and Knook, D. (1984) Biomed. Biochim. Acta, 11, 1213–1221.Google Scholar
  176. 176.
    Terpstra, V., and van Berkel, T. J. (2000) Blood, 95, 2157–2163.PubMedGoogle Scholar
  177. 177.
    LeBouton, A. V. (1968) Curr. Mod. Biol., 2, 111–114.PubMedGoogle Scholar
  178. 178.
    LeBouton, A. V. (1976) Anat. Rec., 184, 679–687.PubMedCrossRefGoogle Scholar
  179. 179.
    Pyatnitskii, N. N., Zhminchenko, V. M., Sugonyaeva, N. P., Ottesyan, B. V., Kas’yanenko, V. V., and Akhmetaliev, S. G. (1977) Byul. Eksp. Biol. Med., No. 2, 214–216.Google Scholar
  180. 180.
    Minuk, G. Y. (2003) Can. J. Gastroenterol., 17, 418–424.PubMedGoogle Scholar

Copyright information

© MAIK Nauka 2008

Authors and Affiliations

  1. 1.Institute of BiochemistrySiberian Division of the Russian Academy of Medical SciencesNovosibirskRussia

Personalised recommendations