The hepatic sinusoidal endothelial cell: Morphology, function, and pathobiology

The Liver: Biology and Pathobiology

Volumn , Issue , 2009, Pages 371-388

  DeLeve, Laurie D ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84889838022     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470747919.ch26     Document Type: Chapter

References (161)

1. Wisse, E. (1970) An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J Ultrastruct Res, 31, 125-50.
2. Wisse, E. (1972) 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, 528-62.
3. Knook, D.L., Blansjaar, N. and Sleyster, E.C. (1977) Isolation and characterization of Kupffer and endothelial cells from the rat liver. Exp Cell Res, 109, 317-29.
4. Knook, D.L. and Sleyster, E.C. (1976) Separation of the Kupffer and endothelial cells of the rat liver by centrifugal elutriation. Exp Cell Res, 99, 444-49.
5. DeLeve, L.D., Wang, X., McCuskey, M.K. and Mc-Cuskey, R.S. (2006) Rat liver endothelial cells isolated by anti-CD31 immunomagnetic sorting lack fenestrae and sieve plates. Am J Physiol Gastrointest Liver Physiol, 291, G1187-89.
6. Elvevold, K., Smedsrod, B. and Martinez, I. (2007) The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity. Am J Physiol Gastrointest Liver Physiol, 294, 391-400.
7. Aird, W.C. (2005) Endothelial Cells in Health and Disease, Taylor & Francis, New York.
8. Aird, W.C. (2007) Endothelial Biomedicine, Cambridge University Press, New York.
9. Blue, J. and Weiss, L. (1981) Electron microscopy of the red pulp of the dog spleen including vascular arrangements, peri-arterial macrophage sheaths, ellipsoids, and the contractive reticular meshwork. Am J Anat, 161, 189-218.
10. Blue, J. and Weiss, L. (1981) Vascular pathways in nonsinusal red pulp: an electron microscopic study of the cat spleen. Am J Anat, 161, 135-68.
11. Weiss, L. and Chen, L.T. (1974) A scanning electron microscopic study of the spleen. Blood, 43, 65-91.
12. De Bruyn, P.P. and Michelson, S. (1979) Changes in the random distribution of sialic acid at the surface of the myeloid sinusoidal endothelium resulting from the presence of diaphragmed fenestrae. J Cell Biol, 82, 708-14.
13. Inoue, S. and Osmond, D.G. (2001) Basement membrane of mouse bone marrow sinusoids shows distinctive structure and proteoglycan composition: a high resolution ultrastructural study. Anat Rec, 264, 294-304.
14. Wisse, E., De Zanger, R.B., Charels, K., van der Smissen, P. and McCuskey, R.S. (1985) The liver sieve: considerations concerning the structure and function of endothelial fenestra, the sinusoidal wall and the space of Disse. Hepatology, 5, 683-92.
15. Vidal-Vanaclocha, F. and Barbera-Guillem, E. (1985) Fenestration patterns in endothelial cell of rat liver sinusoids. J Ultrastruct Res, 90, 115-23.
16. Wisse, E., Zanger, R.B. and Jacobs, R. (1982) Lobular gradient in endothelial fenestrae and sinusoidal diameter favor centriolobular exchange processes: a scanning EM study, in Sinusoidal Liver Cells (eds D.L. Knook and E. Wisse), Elsevier Biomedical Press, Amsterdam, pp. 61-7.
17. Módis, L. and Martinez-Hernandez, A. (1991) Hepatocytes modulate the hepatic microvascular phenotype. Lab Invest, 65, 661-70.
18. DeLeve, L.D., Wang, X., Hu, L., McCuskey, M.K. and McCuskey, R.S. (2004) Rat liver sinusoidal endothelial cell phenotype is under paracrine and autocrine control. Am J Physiol Gastrointest Liver Physiol, 287, G757-63.
19. Risau, W. (1995) Differentiation of endothelium. FASEB J, 9, 926-33.
20. Roberts, W.G. and Palade, G.E. (1995) Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci, 108, 2369-79.
21. Plitas, G., Burt, B.M., Stableford, J.A., Nguyen, H.M., Welles, A.P. and DeMatteo, R.P. (2008) Dendritic cells are required for effective cross-presentation in the murine liver. Hepatology, 47, 1343-51.
22. Sato, T., Yamamoto, H., Sasaki, C. and Wake, K. (1998) Maturation of rat dendritic cells during intrahepatic translocation evaluated using monoclonal antibodies and electron microscopy. Cell Tissue Res, 294, 503-14.
23. Schildberg, F.A., Hegenbarth, S.I., Schumak, B., Limmer, A. and Knolle, P.A. (2008) Liver sinusoidal endothelial cells veto CD8 T cell activation by antigen-presenting dendritic cells. Eur J Immunol, 38, 957-67.
24. Grote, J. (1980) in Physiologie der Menschen 20th edn, (eds R.F. Schmidt and G. Thews), Springer-Verlag, New York, p. 560.
25. Mansbach, C.M.I. and Gorelick, F. (2007) Development and physiological regulation of intestinal lipid absorption. II. Dietary lipid absorption, complex lipid synthesis, and the intracellular packaging and secretion of chylomicrons. Am J Physiol Gastrointest Liver Physiol, 293, G645-50.
26. Redgrave, T.G. (1970) Formation of cholesteryl esterrich particulate lipid during metabolism of chylomicrons. J Clin Invest, 49, 465-71.
27. Fraser, R., Bosanquet, A.G. and Day, W.A. (1978) Filtration of chylomicrons by the liver may influence cholesterol metabolism and atherosclerosis. Atherosclerosis, 29, 113-23.
28. Cogger, V.C., Hilmer, S.N., Sullivan, D., Muller, M., Fraser, R. and Le Couteur, D.G. (2006) Hyperlipidemia and surfactants: the liver sieve is a link. Atherosclerosis, 189, 273-81.
29. Smedsrød, B., Pertoft, H., Gustafson, S. and Laurent, T.C. (1990) Scavenger functions of the liver endothelial. Cell, 266, 313-27.
30. Seternes, T., Dalmo, R.A., Hoffman, J., Bogwald, J., Zykova, S. and Smedsrod, B. (2001) Scavengerreceptor-mediated endocytosis of lipopolysaccharide in Atlantic cod (Gadus morhua L.). J Exp Biol, 204, 4055-64.
31. Nagelkerke, J.F., Barto, K.P. and van Berkel, T.J. (1983) In vivo and in vitro uptake and degradation of acetylated low density lipoprotein by rat liver endothelial, Kupffer, and parenchymal cells. J Biol Chem, 258, 12221-27.
32. Blomhoff, R., Drevon, C.A., Eskild, W., Helgerud, P., Norum, K.R. and Berg, T. (1984) Clearance of acetyl low density lipoprotein by rat liver endothelial cells. Implications for hepatic cholesterol metabolism. J Biol Chem, 259, 8898-903.
33. Skogh, T., Blomhoff, R., Eskild, W. and Berg, T. (1985) Hepatic uptake of circulating IgG immune complexes. Immunology, 55, 585-94.
34. Van Berkel, T.J., De Rijke, Y.B. and Kruijt, J.K. (1991) Different fate in vivo of oxidatively modified low density lipoprotein and acetylated low density lipoprotein in rats. Recognition by various scavenger receptors on Kupffer and endothelial liver cells. J Biol Chem, 266, 2282-89.
35. Smedsrod, B., Melkko, J., Araki, N., Sano, H. and Horiuchi, S. (1997) Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Biochem J, 322, 567-73.
36. Martin-Armas, M., Simon-Santamaria, J., Pettersen, I., Moens, U., Smedsrod, B. and Sveinbjornsson, B. (2006) Toll-like receptor 9 (TLR9) is present in murine liver sinusoidal endothelial cells (LSECs) and mediates the effect of CpG-oligonucleotides. J Hepatol, 44, 939-46.
37. Knook, D.L. and Sleyster, E.C. (1980) Isolated parenchymal, Kupffer and endothelial rat liver cells characterized by their lysosomal enzyme content. Biochem Biophys Res Commun, 96, 250-57.
38. Knolle, P.A. and Gerken, G. (2000) Local control of the immune response in the liver. Immunol Rev, 174, 21-34.
39. Klugewitz, K., Blumenthal-Barby, F., Schrage, A., Knolle, P.A., Hamann, A. and Crispe, I.N. (2002) Immunomodulatory effects of the liver: deletion of activated CD4+ effector cells and suppression of IFN-gamma-producing cells after intravenous protein immunization. J Immunol, 169, 2407-13.
40. Onoe, T., Ohdan, H., Tokita, D., Shishida, M., Tanaka, Y., Hara, H., Zhou, W., Ishiyama, K., Mitsuta, H., Ide, K. and Asahara, T. (2005) Liver sinusoidal endothelial cells tolerize T cells across MHC barriers in mice. J Immunol, 175, 139-46.
41. Katz, S.C., Pillarisetty, V.G., Bleier, J.I., Shah, A.B. and DeMatteo, R.P. (2004) Liver sinusoidal endothelial cells are insufficient to activate T cells. J Immunol, 173, 230-35.
42. Knolle, P.A. and Limmer, A. (2001) Neighborhood politics: the immunoregulatory function of organ-resident liver endothelial cells. Trends Immunol, 22, 432-37.
43. Horn, T., Christoffersen, P. and Henriksen, J.H. (1987) Alcoholic liver injury: defenestration in noncirrhotic livers-a scanning electron microscopic study. Hepatology, 7, 77-82.
44. Mori, T., Okanoue, T., Sawa, Y., Hori, N., Ohta, M. and Kagawa, K. (1993) Defenestration of the sinusoidal endothelial cell in a rat model of cirrhosis. Hepatology, 17, 891-97.
45. Schaffner, F. and Popper, H. (1963) Capillarization of hepatic sinusoids in man. Gastroenterology, 44, 239-42.
46. Xu, B., Broome, U., Uzunel, M., Nava, S., Ge, X., Kumagai-Braesch, M., Hultenby, K., Christensson, B., Ericzon, B.G., Holgersson, J. and Sumitran-Holgersson, S. (2003) Capillarization of hepatic sinusoid by liver endothelial cell-reactive autoantibodies in patients with cirrhosis and chronic hepatitis. Am J Clin Pathol, 163, 1275-89.
47. Steffan, A.M., Pereira, C.A., Bingen, A., Valle, M., Martin, J.P., Koehren, F., Royer, C., Gendrault, J.L. and Kirn, A. (1995) Mouse hepatitis virus type 3 infection provokes a decrease in the number of sinusoidal endothelial cell fenestrae both in vivo and in vitro. Hepatology, 22, 395-401.
48. Straub, A.C., Stolz, D.B., Vin, H., Ross, M.A., Soucy, N.V., Klei, L.R. and Barchowsky, A. (2007) Low level arsenic promotes progressive inflammatory angiogenesis and liver blood vessel remodeling in mice. Toxicol Appl Pharmacol, 222, 327-36.
49. Dobbs, B.R., Rogers, G.W., Xing, H.Y. and Fraser, R. (1994) Endotoxin-induced defenestration of the hepatic sinusoidal endothelium: a factor in the pathogenesis of cirrhosis? Liver, 14, 230-33.
50. Warren, A., Bertolino, P., Cogger, V.C., McLean, A.J., Fraser, R. and Le Couteur, D.G. (2005) Hepatic pseudocapillarization in aged mice. Exp Gerontol, 40, 807-12.
51. McLean, A.J., Cogger, V.C., Chong, G.C., Warren, A., Markus, A.M., Dahlstrom, J.E. and Le Couteur, D.G. (2003) Age-related pseudocapillarization of the human liver. J Clin Exp Psychopathol, 200, 112-17.
52. Cogger, V.C., Warren, A., Fraser, R., Ngu, M., McLean, A.J. and Le Couteur, D.G. (2003) Hepatic sinusoidal pseudocapillarization with aging in the non-human primate. Exp Gerontol, 38, 1101-7.
53. Le Couteur, D.G., Cogger, V.C., Markus, A.M., Harvey, P.J., Yin, Z.L., Annselin, A.D. and McLean, A.J. (2001) Pseudocapillarization and associated energy limitation in the aged rat liver. Hepatology, 33, 537-43.
54. DeLeve L.D., Wang X., Guo Y. (2008) Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology, 48 (3), 920-30.
55. Jarnagin, W.R., Rockey, D.C., Koteliansky, V.E., Wang, S.S. and Bissell, D.M. (1994) Expression of variant fibronectins in wound healing: cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis. J Cell Biol, 127, 2037-48.
56. Angulo, P., Keach, J.C., Batts, K.P. and Lindor, K.D. (1999) Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitis. Hepatology, 30, 1356-62.
57. Clark, J.M. (2006) The epidemiology of nonalcoholic fatty liver disease in adults. J Clin Gastroenterol, 40, S5-10.
58. Poynard, T., Bedossa, P. and Opolon, P. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC Groups (1997) Natural history of liver fibrosis progression in patients with chronic hepatitis C. Lancet, 349, 825-32.
59. Ratziu, V., Giral, P., Charlotte, F., Bruckert, E., Thibault, V., Theodorou, I., Khalil, L., Turpin, G., Opolon, P. and Poynard, T. (2000) Liver fibrosis in overweight patients. Gastroenterology, 118, 1117-23.
60. Froomes, P.R.A., Morgan, D.J., Smallwood, R.A. and Angus, P.W. (1999) Comparative effects of oxygen supplementation on theophylline and acetaminophen clearance in human cirrhosis. Gastroenterology, 116, 915-20.
61. Hickey, P.L., Angus, P.W., McLean, A.J. and Morgan, D.J. (1995) Oxygen supplementation restores theophylline clearance to normal in cirrhotic rats. Gastroenterology, 108, 1504-9.
62. Le Couteur, D.G., Hickey, H., Harvey, P.J., Gready, J. and McLean, A.J. (1999) Hepatic artery flow and propranolol metabolism in perfused cirrhotic rat liver. J Pharmacol Exp Ther, 289, 1553-58.
63. Proctor, S.D. and Mamo, J.C. (1998) Retention of fluorescent-labelled chylomicron remnants within the intima of the arterial wall-evidence that plaque cholesterol may be derived from post-prandial lipoproteins [see comment]. Eur J Clin Invest, 28, 497-503.
64. Yu, K.C.W. and Cooper, A.D. (2001) Postprandial lipoproteins and atherosclerosis. Front Biosci, 6, 322-54.
65. Le Couteur, D.G., Fraser, R., Cogger, V.C. and McLean, A.J. (2002) Hepatic pseudocapillarisation and atherosclerosis in ageing. Lancet, 359, 1612-15.
66. Hilmer, S.N., Cogger, V.C., Fraser, R., McLean, A.J., Sullivan, D. and Le Couteur, D.G. (2005) Age-related changes in the hepatic sinusoidal endothelium impede lipoprotein transfer in the rat. Hepatology, 42, 1349-54.
67. Le Couteur, D.G., Warren, A., Cogger, V.C., Smedsrod, B., Sorensen, K.K., De Cabo, R., Fraser, R. and Mc-Cuskey, R.S. (2008) Old age and the hepatic sinusoid. Anat Rec, 291, 672-83.
68. Bessey C.E. and Stalker M. (1884) Bulletin of the Iowa Agricultural College, Department of Botany, p. 111.
69. Pethick, W.H. (1907) Special Report on Pictou Cattle Disease. Department of Agriculture, Canada, Health of Animals Branch. Canadian Government Printing Bureau.
70. Cushny, A.R. (1911) On the action of senecio alkaloids and the causation of the hepatic cirrhosis of cattle (Pictou, Molteno, or Winton disease). J Pharmacol Exp Ther, 2, 531-48.
71. Willmot, F.C. and Robertson, G.W. (1920) Senecio disease, or cirrhosis of the liver due to senecio poisoning. Lancet, ii, 848-49.
72. McFarlane, A.L. and Branday, W. (1945) Hepatic enlargement with ascitic children. Br Med J, i, 838-40.
73. Bras, G., Jeliffe, D.B. and Stuart, K.L. (1954) Veno-occlusive disease of the liver with non-portal type of cirrhosis occurring in Jamaica. Arch Pathol, 57, 285-300.
74. DeLeve, L.D., Shulman, H.M. and McDonald, G.B. (2002) Toxic injury to hepatic sinusoids: sinusoidal obstruction syndrome (veno-occlusive disease). Semin Liver Dis, 22, 27-42.
75. Shulman, H.M., Fisher, L.B., Schoch, H.G., Henne, K.W. and McDonald, G.B. (1994) Veno-occlusive disease of the liver after marrow transplantation: histological correlates of clinical signs and symptoms. Hepatology, 19, 1171-80.
76. McDonald, G.B. (2006) Review article: management of hepatic disease following haematopoietic cell transplant. Aliment Pharmacol Ther, 24, 441-52.
77. DeLeve, L.D. (1994) Dacarbazine toxicity in murine liver cells: a novel model of hepatic endothelial injury and glutathione defense. J Pharmacol Exp Ther, 268, 1261-70.
78. DeLeve, L.D. (1996) Cellular target of cyclophosphamide toxicity in the murine liver: role of glutathione and site of metabolic activation. Hepatology, 24, 830-37.
79. DeLeve, L.D., Wang, X., Kuhlenkamp, J.F. and Kaplowitz, N. (1996) Toxicity of azathioprine and monocrotaline in murine sinusoidal endothelial cells and hepatocytes: the role of glutathione and relevance to hepatic veno-oclusive disease. Hepatology, 23, 589-99.
80. DeLeve, L.D., McCuskey, R.S., Wang, X., Hu, L., McCuskey, M.K., Epstein, R.B. and Kanel, G. (1999) Characterization of a reproducible rat model of hepatic veno-occlusive disease. Hepatology, 29, 1779-91.
81. DeLeve, L.D., Ito, I., Bethea, N.W., McCuskey, M.K., Wang, X. and McCuskey, R.S. (2003) Embolization by sinusoidal lining cell obstructs the microcirculation in rat sinusoidal obstruction syndrome. Am J Physiol Gastrointest Liver Physiol, 284, G1045-52.
82. Lamé, M.W., Jones, A.D., Wilson, D.W., Dunston, S.K. and Segall, H.J. (2000) Protein targets of monocrotaline pyrrole in pulmonary artery endothelial cells. J Biol Chem, 275, 29091-99.
83. DeLeve, L.D., Wang, X., Tsai, J., Kanel, G.C., Strasberg, S.M. and Tokes, Z.A. (2003) Prevention of sinusoidal obstruction syndrome (hepatic venoocclusive disease) in the rat by matrix metalloproteinase inhibitors. Gastroenterology, 125, 882-90.
84. Eagleton, M.J., Peterson, D.A., Sullivan, V.V., Roelofs, K.J., Ford, J.A., Stanley, J.C. and Upchurch, G.R., Jr. (2002) Nitric oxide inhibition increases aortic wall matrix metalloproteinase-9 expression. J Invest Surg, 104, 15-21.
85. Eberhardt, W., Beeg, T., Beck, K.F., Walpen, S., Gauer, S., Bohles, H. and Pfeilschifter, J. (2000) Nitric oxide modulates expression of matrix metalloproteinase-9 in rat mesangial cells. Kidney Int, 57, 59-69.
86. Gurjar, M.V., DeLeon, J., Sharma, R.V. and Bhalla, R.C. (2001) Mechanism of inhibition of matrix metalloproteinase-9 induction by NO in vascular smooth muscle cells. J Appl Physiol, 91, 1380-86.
87. Jurasz, P., Sawicki, G., Duszyk, M., Sawicka, J., Miranda, C., Mayers, I. and Radomski, M.W. (2001) Matrix metalloproteinase 2 in tumor cell-induced platelet aggregation: regulation by nitric oxide. Cancer Res, 61, 376-82.
88. Matsunaga, T., Weihrauch, D.W., Moniz, M.C., Tessmer, J., Warltier, D.C. and Chilian, W.M. (2002) Angiostatin inhibits coronary angiogenesis during impaired production of nitric oxide. Circulation, 105, 2185-91.
89. Mujumdar, V.S., Aru, G.M. and Tyagi, S.C. (2001) Induction of oxidative stress by homocyst(e)ine impairs endothelial function. J Cell Biochem, 82, 491-500.
90. Upchurch, G.R., Jr., Ford, J.W., Weiss, S.J., Knipp, B.S., Peterson, D.A., Thompson, R.W., Eagleton, M.J., Broady, A.J., Proctor, M.C. and Stanley, J.C. (2001) Nitric oxide inhibition increases matrix metalloproteinase-9 expression by rat aortic smooth muscle cells in vitro. J Endovasc Surg, 34, 76-83.
91. DeLeve, L.D., Wang, X., Kanel, G.C., Tokes, Z.A., Tsai, J., Ito, Y., Bethea, N.W., McCuskey, M.K. and McCuskey, R.S. (2003) Decreased hepatic nitric oxide production contributes to the development of rat sinusoidal obstruction syndrome. Hepatology, 38, 900-8.
92. Harb, R., Xie, G., Lutzko, C., Guo, Y., Wang, X., Hill, C., Kanel, G., DeLeve, L.D. (2008) Bone Marrow Progenitor Cells Repair Rat Hepatic Sinusoidal Endothelial Cells After Liver Injury, Gastroenterology, 2009 (in press).
93. Zimmerman, H.J. (1981) Effects of aspirin and acetaminophen on the liver. Arch Intern Med, 141, 333-42.
94. Thompson, R.P.H., Clark, R., Wilson, R.A., Borirakchanyavat, V., Widdop, B., Goulding, R. and Williams, R. (1972) Hepatic damage from overdose of paracetamol. Gut, 13, 836.
95. Rose, P.G. (1969) Paracetamol overdose and liver damage. Br Med J, i, 381-82.
96. Klatskin, G. and Conn, H.O. (1993) Histopathology of the Liver, Oxford University Press.
97. Zimmerman H.J. (1978) Syndromes of Environmental Hepatotoxins. Hepatotoxicity-The Adverse Effect of Drugs and Other Chemicals on the Liver. Appleton-Century-Crofts, New York, 279-302.
98. Dixon, M.F., Nimmo, J. and Prescott, L.F. (1971) Experimental paracetamol-induced hepatic necrosis: a histopathological study. J Clin Exp Psychopathol, 103, 225-29.
99. Dixon, M.F., Dixon, B., Aparicio, S.R. and Loney, D.P. (1975) Experimental paracetamol-induced hepatic necrosis: a light- and electron-microscope, and histochemical study. J Clin Exp Psychopathol, 116, 17-29.
100. Miller, D.J., Pichanick, G.G., Fiskerstrand, C. and Saunders, S. (1977) Hepatic erythrocyte sequestration as a cause of acute anaemia. Am J Dig Dis, 22, 1055-59.
101. Chiu, S. and Bhakthan, N.M.G. (1978) Experimental acetaminophen-induced hepatic necrosis: biochemical and electron microscopic study of cysteamine protection. Lab Invest, 39, 193-203.
102. Walker, R.M., Massey, T.E., McElligott, T.F. and Racz, W.J. (1981) Acetaminophen-induced hypothermia, hepatic congestion, and modification by N-acetylcysteine in mice. Toxicol Appl Pharmacol, 59, 500-7.
103. Walker, R.M., Racz, W.J. and McElligott, T.F. (1983) Scanning electron microscopic examination of acetaminophen-induced hepatotoxicity and congestion in mice. Am J Pathol, 113, 321-30.
104. Walker, R.M., Racz, W.J. and McElligott, T.F. (1985) Acetaminophen-induced hepatotoxic congestion in mice. Hepatology, 5, 233-40.
105. DeLeve, L.D., Wang, X., Kaplowitz, N., Shulman, H.M., Bart, J.A. and van der Hoek, A. (1997) Sinusoidal endothelial cells as a target for acetaminophen toxicity: direct action versus requirement for hepatocyte activation in different mouse strains. Biochem Pharmacol, 53, 1339-45.
106. Ito, Y., Bethea, N.W., Abril, E.R. and McCuskey, R.S. (2003) Early hepatic microvascular injury in response to acetaminophen toxicity. Microcirculation, 10, 391-400.
107. Liu, J., Waalkes, M.P., Clark, J., Myers, P., Saavedra, J.E. and Keefer, L.K. (2003) The nitric oxide donor, V-PYRRO/NO, protects against acetaminophen-induced hepatotoxicity in mice. Hepatology, 37, 324-33.
108. Ito, Y., Abril, E.R., Bethea, N.W. and McCuskey, R.S. (2004) Role of nitric oxide in hepatic microvascular injury elicited by acetaminophen in mice. Am J Physiol Gastrointest Liver Physiol, 286, G60-67.
109. Caldwell-Kenkel, C., Thurman, R.G. and Lemasters, J.J. (1988) Selective loss of nonparenchymal cell viability after cold ischemic storage of rat livers. Transplantation, 45, 834-37.
110. McKeown, C.M.B., Edwards, V., Phillips, M.J., Harvey, P.R.C., Petrunka, C.N. and Strasberg, S.M. (1988) Sinusoidal lining cell damage: the critical injury in cold preservation of liver allografts in the rat. Transplantation, 46, 178-91.
111. Caldwell-Kenkel, J.C., Currin, R.T., Tanaka, Y., Thurman, R.G. and Lemasters, J.J. (1989) Reperfusion injury to endothelial cells following cold ischemic storage of rat livers. Hepatology, 10, 292-99.
112. Imamura, H., Brault, A. and Huet, P.M. (1997) Effects of extended cold preservation and transplantation on the rat liver microcirculation. Hepatology, 25, 664-71.
113. Gao, W., Bentley, R.C., Madden, J.F. and Clavien, P.A. (1998) Apoptosis of sinusoidal endothelial cells is a critical mechanism of preservation injury in rat liver transplantation. Hepatology, 27, 1652-60.
114. Natori, S., Higuchi, H., Contreras, P. and Gores, G.J. (2003) The caspase inhibitor IDN-6556 prevents caspase activation and apoptosis in sinusoidal endothelial cells during liver preservation injury. Liver Transpl, 9, 278-84.
115. Upadhya, G.A., Harvey, R.P., Howard, T.K., Lowell, J.A., Shenoy, S. and Strasberg, S.M. (1997) Evidence of a role for matrix metalloproteinases in cold preservation injury of the liver in humans and in the rat. Hepatology, 26, 922-28.
116. Upadhya, G.A. and Strasberg, S.M. (1999) Evidence that actin disassembly is a requirement for matrix metalloproteinase secretion by sinusoidal endothelial cells during cold preservation in the rat. Hepatology, 30, 169-76.
117. Upadhya, G.A., Topp, S.A., Hotchkiss, R.S., Anagli, J. and Strasberg, S.M. (2003) Effect of cold preservation on intracellular calcium concentration and calpain activity in rat sinusoidal endothelial cells. Hepatology, 37, 313-23.
118. Aguilar, H.I., Steers, J.L., Wiesner, R.H., Krom, R.A. and Gores, G.J. (1997) Enhanced liver calpain protease activity is a risk factor for dysfunction of human liver allografts. Transplantation, 63, 612-14.
119. Kohli, V., Gao, W., Camargo, C.A. Jr. and Clavien, P.A. (1997) Calpain is a mediator of preservation-reperfusion injury in rat liver transplantation. Proc Natl Acad Sci U S A, 94, 9354-59.
120. Sindram, D., Kohli, V., Madden, J.F. and Clavien, P.A. (1999) Calpain inhibition prevents sinusoidal endothelial cell apoptosis in the cold ischemic rat liver. Transplantation, 68, 136-40.
121. Upadhya, G.A. and Strasberg, S.M. (2002) Platelet adherence to isolated rat hepatic sinusoidal endothelial cells after cold preservation. Transplantation, 73, 1764-70.
122. Topp, S.A., Upadhya, G.A. and Strasberg, S.M. (2003) Leukocyte adhesion to cold-preserved rat endothelial cells: role of actin disassembly and ICAM-1. Liver Transpl, 9, 1286-94.
123. Topp, S.A., Upadhya, G.A. and Strasberg, S.M. (2004) Cold preservation of isolated sinusoidal endothelial cells in MMP 9 knockout mice: effect on morphology and platelet adhesion. Liver Transpl, 10, 1041-48.
124. Sindram, D., Porte, R.J., Hoffman, M.R., Bentley, R.C. and Clavien, P.A. (2000) Platelets induce sinusoidal endothelial cell apoptosis upon reperfusion of the cold ischemic rat liver. Gastroenterologia, 118, 183-91.
125. Sindram, D., Porte, R.J., Hoffman, M.R., Bentley, R.C. and Clavien, P.A. (2001) Synergism between platelets and leukocytes in inducing endothelial cell apoptosis in the cold ischemic rat liver: a Kupffer cell-mediated injury. FASEB J, 15, 1230-32.
126. Cottart, C.H., Do, L., Blanc, M.C., Vaubourdolle, M., Descamps, G., Durand, D., Galen, F.X. and Clot, J.P. (1999) Hepatoprotective effect of endogenous nitric oxide during ischemia-reperfusion in the rat. Hepatology, 29, 809-13.
127. Morisue, A., Wakabayashi, G., Shimazu, M., Tanabe, M., Mukai, M., Matsumoto, K., Kawachi, S., Yoshida, M., Yamamoto, S. and Kitajima, M. (2003) The role of nitric oxide after a short period of liver ischemia-reperfusion. J Surg Res, 109, 101-9.
128. Serracino-Inglott, F., Virlos, I.T., Habib, N.A., Williamson, R.C. and Mathie, R.T. (2003) Differential nitric oxide synthase expression during hepatic ischemia-reperfusion. Am J Surg, 185, 589-95.
129. Oishi, A., Inagaki, M. and Tanaka, N. (1997) Correlation between nitric oxide production and preservation injury of sinusoidal endothelial cells during cold ischemia. Transplant Proc, 29, 1338-39.
130. Ohmori, H., Dhar, D.K., Nakashima, Y., Hashimoto, M., Masumura, S. and Nagasue, N. (1998) Beneficial effects of FK409, a novel nitric oxide donor, on reperfusion injury of rat liver. Transplantation, 66, 579-85.
131. Peralta, C., Rull, R., Rimola, A., Deulofeu, R., Rosello-Catafau, J., Gelpi, E. and Rodes, J. (2001) Endogenous nitric oxide and exogenous nitric oxide supplementation in hepatic ischemia-reperfusion injury in the rat. Transplantation, 71, 529-36.
132. Geller, D.A., Chia, S.H., Takahashi, Y., Yagnik, G.P., Tsoulfas, G. and Murase, N. (2001) Protective role of the L-arginine-nitric oxide synthase pathway on preservation injury after rat liver transplantation. J Parenter Enteral Nutr, 25, 142-47.
133. Man, K., Fan, S.T., Lo, C.M., Liu, C.L., Fung, P.C., Liang, T.B., Lee, T.K., Tsui, S.H., Ng, I.O., Zhang, Z.W. and Wong, J. (2003) Graft injury in relation to graft size in right lobe live donor liver transplantation: a study of hepatic sinusoidal injury in correlation with portal hemodynamics and intragraft gene expression. Ann Surg, 237, 256-64.
134. Man, K., Lo, C.M., Ng, I.O., Wong, Y.C., Qin, L.F., Fan, S.T. and Wong, J. (2001) Liver transplantation in rats using small-for-size grafts: a study of hemodynamic and morphological changes. Arch Facial Plast Surg, 136, 280-85.
135. Leong, S.S., Cazen, R.A., Yu, G.S., LeFevre, L. and Carson, J.W. (1992) Abdominal visceral peliosis associated with bacillary angiomatosis. Ultrastructural evidence of endothelial destruction by bacilli. Arch Pathol Lab Med, 116, 866-71.
136. Goerdt, S. and Sorg, C. (1992) Endothelial heterogeneity and the acquired immunodeficiency syndrome: a paradigm for the pathogenesis of vascular disorders. Clin Oral Investig, 70, 89-98.
137. Scoazec, J.Y., Marche, C., Girard, P.M., Houtmann, J., Durand-Schneider, A.M., Saimot, A.G., Benhamou, J.P. and Feldmann, G. (1988) Peliosis hepatis and sinusoidal dilation during infection by the human immunodeficiency virus (HIV). An ultrastructural study. Am J Pathol, 131, 38-47.
138. Wanless, I.R. (1990) Micronodular transformation (nodular regenerative hyperplasia) of the liver: a report of 64 cases among 2, 500 autopsies and a new classification of benign hepatocellular nodules. Hepatology, 11, 787-97.
139. Hillaire, S., Bonte, E., Denninger, M.H., Casadevall, N., Cadranel, J.F., Lebrec, D., Valla, D. and Degott, C. (2002) Idiopathic non-cirrhotic intrahepatic portal hypertension in the West: a re-evaluation in 28 patients. Gut, 51, 275-80.
140. Ibarrola, C. and Colina, F. (2003) Clinicopathological features of nine cases of non-cirrhotic portal hypertension: current definitions and criteria are inadequate. Histopathology, 42, 251-64.
141. Nakanuma, Y., Hoso, M., Sasaki, M., Terada, T., Katayanagi, K., Nonomura, A., Kurumaya, H., Harada, A. and Obata, H. (1996) Histopathology of the liver in non-cirrhotic portal hypertension of unknown aetiology. Histopathology, 28, 195-204.
142. Shedlofsky, S., Koehler, R.E., DeSchryver-Kecskemeti, K. and Alpers, D.H. (1980) Noncirrhotic nodular transformation of the liver with portal hypertension: clinical, angiographic, and pathological correlation. Gastroenterology, 79, 938-43.
143. Wanless, I.R., Godwin, T.A., Allen, F. and Feder, A. (1980) Nodular regenerative hyperplasia of the liver in hematologic disorders: a possible response to obliterative portal venopathy. A morphometric study of nine cases with an hypothesis on the pathogenesis. Medicine, 59, 367-79.
144. Shimamatsu, K. and Wanless, I.R. (1997) Role of ischemia in causing apoptosis, atrophy, and nodular hyperplasia in human liver. Hepatology, 26, 343-50.
145. Bioulac Sage, P., Dubuisson, L., Bedin, C., Gonzalez, P., de Tinguy Moreaud, E., Garcin, H. and Balabaud, C. (1992) Nodular regenerative hyperplasia in the rat induced by a selenium-enriched diet: study of a model. Hepatology, 16, 418-25.
146. Croquelois, A., Blindenbacher, A., Terracciano, L., Wang, X., Langer, I., Radtke, F., Heim M.H. (2005) Inducible inactivation of Notch1 causes nodular regenerative hyperplasia in mice. Hepatology, 41, 487-496.
147. Maione, D., Di Carlo, E., Li, W., Musiani, P., Modesti, A., Peters, M., Rose-John, S., Della Rocca, C., Tripodi, M., Lazzaro, D., Taub, R., Savino, R. and Ciliberto, G. (1998) Coexpression of IL-6 and soluble IL-6R causes nodular regenerative hyperplasia and adenomas of the liver. EMBO J, 17, 5588-97.
148. McEntee, M.F., Wright, K.N., Wanless, I., DeVovo, R., Schneider, J.F. and Shull, R. (1998) Noncirrhotic portal hypertension and nodular regenerative hyperplasia of the liver in dogs with mucopolysaccharidosis type I. Hepatology, 28, 385-90.
149. Snover, D.C., Weisdorf, S., Bloomer, J., McGlave, P. and Weisdorf, D. (1989) Nodular regenerative hyperplasia of the liver following bone marrow transplantation. Hepatology, 9, 443-48.
150. Haboubi, N.Y., Ali, H.H., Whitwell, H.L. and Ackrill, P. (1988) Role of endothelial cell injury in the spectrum of azathioprine-induced liver disease after renal transplant: light microscopy and ultrastructural observations. Am J Proctol Gastroenterol Colon Rectal Surg, 83, 256-61.
151. Mion, F., Napoleon, B., Berger, F., Chevallier, M., Bonvoisin, S. and Descos, L. (1991) Azathioprine induced liver disease: nodular regenerative hyperplasia of the liver and perivenous fibrosis in a patient treated for multiple sclerosis. Gut, 32, 715-17.
152. Russmann, S., Zimmermann, A., Krahenbuhl, S., Kern, B. and Reichen, J. (2001) Veno-occlusive disease, nodular regenerative hyperplasia and hepatocellular carcinoma after azathioprine treatment in a patient with ulcerative colitis. Eur J Gastroenterol Hepatol, 13, 287-90.
153. Vora, A., Mitchell, C.D., Lennard, L., Eden, T.O.B., Kinsey, S.E., Lilleyman, J. and Richards, S.M. (2006) Toxicity and efficacy of 6-thioguanine versus 6-mercaptopurine in childhood lymphoblastic leukaemia: a randomised trial [see comment]. Lancet, 368, 1339-48.
154. Dubinsky, M.C., Vasiliauskas, E.A., Singh, H., Abreu, M.T., Papadakis, K.A., Tran, T., Martin, P., Vierling, J.M., Geller, S.A., Targan, S.R. and Poordad, F.F. (2003) 6-thioguanine can cause serious liver injury in inflammatory bowel disease patients. Gastroenterology, 125, 298-303.
155. Arotcarena, R., Cales, V., Berthelemy, P., Parent, Y., Malet, M., Etcharry, F., Ferrari, S. and Pariente, A. (2006) Severe sinusoidal lesions: a serious and overlooked complication of oxaliplatin-containing chemotherapy? Gastroenterol Clin Biol, 30, 1313-16.
156. Steensma, A., Beamand, J.A., Walters, D.G., Price, R.J. and Lake, B.G. (1994) Metabolism of coumarin and 7-ethoxycoumarin by rat, mouse, guinea pig, cynomolgus monkey and human precision-cut liver slices. Xenobiotica, 24, 893-907.
157. Smedsrød, B. and Pertoft, H. (1985) Preparation of pure hepatocytes and reticuloendothelial cells in high yield from a single rat liver by means of Percoll centrifugation and selective adherence. J Leukocyte Biol, 38, 213-30.
158. Hansen, B., Arteta, B. and Smedsrød, B. (2002) The physiological scavenger receptor function of hepatic sinusoidal endothelial and Kupffer cells is independent of scavenger receptor class A type I and II. Mol Cell Biochem, 240, 1-8.
159. Eriksson, S., Fraser, J.R.E., Laurent, T.C., Pertoft, H. and Smedsrød, B. (1983) Endothelial cells are a site of uptake and degradation of hyaluronic acid in the liver. Exp Cell Res, 144, 223-28.
160. Pertoft, H. and Smedsrød, B. (1987) Separation and characterization of liver cells, in Cell Separation: Methods and Selected Applications (eds T.G.I. Pretlow and T.P. Pretlow), Academic Press, pp. 1-24.
161. Laakso, T. and Smedsrød, B. (1987) Cellular distribution in rat liver of intravenously administered polyacryl starch and chondroitin sulfate microparticles. Int J Pharm, 36, 253-62.