The Cellular Basis of Hepatic Fibrosis – Mechanisms and Treatment Strategies

New England Journal of Medicine

Volumn 328, Issue 25, 1993, Pages 1828-1835

  Flier, Jeffrey S ^a   Underhill, Lisa H ^a   Friedman, Scott L ^b,c  

^a University of California ^*

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN FRANCISCO GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHELMINTIC AGENT; COLCHICINE; GAMMA INTERFERON; MESSENGER RNA; OXYGENASE INHIBITOR; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; RETINOID;

FIBROGENESIS; HUMAN; KUPFFER CELL; LIVER FIBROSIS; LIVER SINUSOID; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW;

ENDOTHELIUM; EXTRACELLULAR MATRIX; HUMAN; KUPFFER CELLS; LIVER; LIVER CIRRHOSIS; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 33746521801     PISSN: 00284793     EISSN: 15334406     Source Type: Journal    
DOI: 10.1056/NEJM199306243282508     Document Type: Review

References (74)

1. Rojkind M, Giambrone M-A, Biempica L Collagen types in normal and cirrhotic liver. Gastroenterology 1979; 76:710-719
2. Gressner AM, Bachem MG Cellular sources of noncollagenous matrix proteins: role of fat-storing cells in fibrogenesis. Semin Liver Dis 1990; 10:30-46
3. Bissell DM Cell-matrix interaction and hepatic fibrosis. Prog Liver Dis 1990; 9:143-155
4. Bissell DM, Arenson DM, Maher JJ, Roll FJ Support of cultured hepatocytes by a laminin-rich gel: evidence for a functionally significant subendothelial matrix in normal rat liver. J Clin Invest 1987; 79:801-812
5. Martinez-Hernandez A The hepatic extracellular matrix. II. Electron immunohistochemical studies in rats with CCl4-induced cirrhosis. Lab Invest 1985; 53:166-186
6. Schaffner F, Popper H Capillarization of hepatic sinusoids in man. Gastroenterology 1963; 44:239-242
7. McGuire RF, Bissell DM, Boyles J, Roll FJ Role of extracellular matrix in regulating fenestrations of sinusoidal endothelial cells isolated from normal rat liver. Hepatology 1992; 15:989-997
8. Yokoi Y, Namihisa T, Kuroda H, Immunocytochemical detection of desmin in fat-storing cells (Ito cells). Hepatology 1984; 4:709-714
9. Takahara T, Kojima T, Miyabayashi C, Collagen production in fat-storing cells after carbon tetrachloride intoxication in the rat: immunoelectron microscopic observation of type I, type III collagens, and prolyl hydroxylase. Lab Invest 1988; 59:509-521
10. Nakatsukasa H, Nagy P, Evarts RP, Hsia C-C, Marsden E, Thorgeirsson SS Cellular distribution of transforming growth factor-β 1 and procollagen types I, III, and IV transcripts in carbon tetrachloride-induced rat liver fibrosis. J Clin Invest 1990; 85:1833-1843
11. Milani S, Herbst H, Schuppan D, Riecken EO, Stein H Cellular localization of laminin gene transcripts in normal and fibrotic human liver. Am J Pathol 1989; 134:1175-1182
12. Maher JJ, McGuire RF Extracellular matrix gene expression increases preferentially in rat lipocytes and sinusoidal endothelial cells during hepatic fibrosis in vivo. J Clin Invest 1990; 86:1641-1648
13. Pietrangelo A, Gualdi R, Geerts A, De Bleser P, Casalgrandi G, Ventura E Enhanced hepatic collagen gene expression in a rodent model of hemochromatosis. Gastroenterology 1992; 102: Suppl: A868-A868 abstract.
14. Friedman SL, Roll FJ, Boyles J, Bissell DM Hepatic lipocytes: the principal collagen-producing cells of normal rat liver. Proc Natl Acad Sci U S A 1985; 82:8681-8685
15. Loreal O, Clement B, Schuppan D, Rescan PY, Rissel M, Guillouzo A Distribution and cellular origin of collagen VI during development and in cirrhosis. Gastroenterology 1992; 102:980-987
16. Arenson DM, Friedman SL, Bissell DM Formation of extracellular matrix in normal rat liver: lipocytes as a major source of proteoglycan. Gastroenterology 1988; 95:441-447
17. Maher JJ, Friedman SL, Roll FJ, Bissell DM Immunolocalization of laminin in normal rat liver and biosynthesis of laminin by hepatic lipocytes in primary culture. Gastroenterology 1988; 94:1053-1062
18. Loreal O, Levavasseur F, Rescan PY, Yamada Y, Guillouzo A, Clement B Differential expression of laminin chains in hepatic lipocytes. FEBS Lett 1991; 290:9-12
19. Ramadori G, Knittel T, Odenthal M, Schwogler S, Neubauer K, Meyer zum Buschenfelde K-H Synthesis of cellular fibronectin by rat liver fat-storing (Ito) cells: regulation by cytokines. Gastroenterology 1992; 103:1313-1321
20. Schwogler S, Odenthal M, Meyer zum Buschenfelde KH, Ramadori G Alternative splicing products of the tenascin gene distinguish rat liver fat storing cells from arterial smooth muscle cells and skin fibroblasts. Biochem Biophys Res Commun 1992; 185:768-775
21. Meyer DH, Krull N, Dreher KL, Gressner AM Biglycan and decorin gene expression in normal and fibrotic rat liver: cellular localization and regulatory factors. Hepatology 1992; 16:204-216
22. Friedman SL, Rockey DC, McGuire RF, Maher JJ, Boyles JK, Yamasaki G Isolated hepatic lipocytes and Kupffer cells from normal human liver: morphological and functional characteristics in primary culture. Hepatology 1992; 15:234-243
23. Geerts A, Lazou JM, De Bleser P, Wisse E Tissue distribution, quantitation and proliferation kinetics of fat-storing cells in carbon tetrachloride-injured rat liver. Hepatology 1991; 13:1193-1202
24. Ramadori G, Veit T, Schwogler S, Expression of the gene of the α-smooth muscle-actin isoform in rat liver and in rat fat-storing (ITO) cells. Virchows Arch B Cell Pathol 1990; 59:349-357
25. Rockey DC, Boyles JK, Gabbiani G, Friedman SL Rat hepatic lipocytes express smooth muscle actin upon activation in vivo and in culture. J Submicrosc Cytol Pathol 1992; 24:193-203
26. Pinzani M, Failli P, Ruocco C, Fat-storing cells as liver-specific pericytes: spatial dynamics of agonist-stimulated intracellular calcium transients. J Clin Invest 1992; 90:642-646
27. Kawada N, Klein H, Decker K Eicosanoid-mediated contractility of hepatic stellate cells. Biochem J 1992; 285:367-371
28. Friedman SL Cellular sources of collagen and regulation of collagen production in liver. Semin Liver Dis 1990; 10:20-29
29. Johnson SJ, Hines JE, Burt AD Macrophage and perisinusoidal cell kinetics in acute liver injury. J Pathol 1992; 166:351-358
30. 4-treated rat livers induce skin fibroblast and liver fat-storing cell proliferation in culture. Matrix 1989; 9:150-158
31. Friedman SL, Arthur MJP Activation of cultured rat hepatic lipocytes by Kupffer cell conditioned medium: direct enhancement of matrix synthesis and stimulation of cell proliferation via induction of platelet-derived growth factor receptors. J Clin Invest 1989; 84:1780-1785
32. 4-induced fibrotic livers stimulate proliferation of fat-storing cells. J Hepatol 1986; 3:294-303
33. Matsuoka M, Tsukamoto H Stimulation of hepatic lipocyte collagen production by Kupffer cell-derived transforming growth factor β: implication for a pathogenetic role in alcoholic liver fibrogenesis. Hepatology 1990; 11:599-605
34. Gressner AM, Lotfi S, Gressner G, Lahme B Identification and partial characterization of a hepatocyte-derived factor promoting proliferation of cultured fat-storing cells (parasinusoidal lipocytes). Hepatology 1992; 16:1250-1266
35. Bachem MG, Melchior R, Gressner AM The role of thrombocytes in liver fibrogenesis: effects of platelet lysate and thrombocyte-derived growth factors on the mitogenic activity and glycosaminoglycan synthesis of cultured rat liver fat storing cells. J Clin Chem Clin Biochem 1989; 27:555-565
36. Houglum K, Filip M, Witztum JL, Chojkier M Malondialdehyde and 4-hydroxynonenal protein adducts in plasma and liver of rats with iron overload. J Clin Invest 1990; 86:1991-1998
37. Kamimura S, Gaal K, Britton RS, Bacon BR, Triadafilopoulos G, Tsukamoto H Increased 4-hydroxynonenal levels in experimental alcoholic liver disease: association of lipid peroxidation with liver fibrogenesis. Hepatology 1992; 16:448-453
38. Pinzani M, Gesualdo L, Sabbah GM, Abboud HE Effects of platelet-derived growth factor and other polypeptide mitogens on DNA synthesis and growth of cultured rat liver fat-storing cells. J Clin Invest 1989; 84:1786-1793
39. Friedman SL, Yamasaki G Characterization of TGFβ receptors in cultured rat lipocytes; enhanced receptor expression accompanies cellular activation. Hepatology 1991; 14:113A-113A abstract.
40. Iida H, Seifert R, Alpers CE, Platelet-derived growth factor (PDGF) and PDGF receptor are induced in mesangial proliferative nephritis in the rat. Proc Natl Acad Sci U S A 1991; 88:6560-6564
41. Rubin K, Terracio L, Ronnstrand L, Heldin CH, Klareskog L Expression of platelet-derived growth factor receptors is induced on connective tissue cells during chronic synovial inflammation. Scand J Immunol 1988; 27:285-294
42. Rubin K, Tingstrom A, Hansson GK, Induction of B-type receptors for platelet-derived growth factor in vascular inflammation: possible implications for development of vascular proliferative lesions. Lancet 1988; 1:1353-1356
43. Casscells W, Lappi DA, Olwin BB, Elimination of smooth muscle cells in experimental restenosis: targeting of fibroblast growth factor receptors. Proc Natl Acad Sci U S A 1992; 89:7159-7163
44. Matsuoka M, Pham N-T, Tsukamoto H Differential effects of interleukin-1 α, tumor necrosis factor α, and transforming growth factor β 1 on cell proliferation and collagen formation by cultured fat-storing cells. Liver 1989; 9:71-78
45. Bachem MG, Meyer D, Melchior R, Sell K-M, Gressner AM Activation of rat liver perisinusoidal lipocytes by transforming growth factors derived from myofibroblastlike cells: a potential mechanism of self perpetuation in liver fibrogenesis. J Clin Invest 1992; 89:19-27
46. Casini A, Cunningham M, Rojkind M, Lieber CS Acetaldehyde increases procollagen type I and fibronectin gene transcription in cultured rat fat-storing cells through a protein synthesis-dependent mechanism. Hepatology 1991; 13:758-765
47. Friedman SL Acetaldehyde and alcoholic fibrogenesis: fuel to the fire, but not the spark. Hepatology 1990; 12:609-612
48. Chojkier M, Houglum K, Solis-Herruzo J, Brenner DA Stimulation of collagen gene expression by ascorbic acid in cultured human fibroblasts: a role for lipid peroxidation? J Biol Chem 1989; 264:16957-16962
49. Inuzuka S, Ueno T, Torimura T, Sata M, Abe H, Tanikawa K Immunohistochemistry of the hepatic extracellular matrix in acute viral hepatitis. Hepatology 1990; 12:249-256
50. Davis BH, Pratt BM, Madri JA Retinol and extracellular collagen matrices modulate hepatic Ito cell collagen phenotype and cellular retinol binding protein levels. J Biol Chem 1987; 262:10280-10286
51. Friedman SL, Roll FJ, Boyles J, Arenson DM, Bissell DM Maintenance of differentiated phenotype of cultured rat hepatic lipocytes by basement membrane matrix. J Biol Chem 1989; 264:10756-10762
52. Arthur MJP, Friedman SL, Roll FJ, Bissell DM Lipocytes from normal rat liver release a neutral metalloproteinase that degrades basement membrane (type IV) collagen. J Clin Invest 1989; 84:1076-1085
53. Winwood PJ, Schuppan D, Arthur MJP Partial purification and biochemical characterisation of Kupffer cell-derived 95 KD gelatinase. Hepatology 1992; 16:606-606 abstract.
54. Iredale JP, Murphy G, Hembry RM, Friedman SL, Arthur MJP Human hepatic lipocytes synthesize tissue inhibitor of metalloproteinases-1: implications for regulation of matrix degradation in liver. J Clin Invest 1992; 90:282-287
55. Friedman SL, Wei S, Blaner WS Retinol release by activated rat hepatic lipocytes: regulation by Kupffer cell-conditioned medium and PDGF. Am J Physiol 1993; 264: G947-G952
56. Tsukamoto H, Matsuoka M, Blaner W, Cheng S. Ito cell activation during progression of alcoholic liver fibrosis. In: Wisse E, Knook DL, McCuskey RS, eds. Cells of the hepatic sinusoid. Leiden, the Netherlands: Kupffer Cell Foundation, 1991:453-6.
57. Leo MA, Lieber CS Hepatic vitamin A depletion in alcoholic liver injury. N Engl J Med 1982; 307:597-601
58. Geubel AP, De Galocsy C, Alves N, Rahier J, Dive C Liver damage caused by therapeutic vitamin A administration: estimate of dose-related toxicity in 41 cases. Gastroenterology 1991; 100:1701-1709
59. Lieber CS Interaction of ethanol with drugs, hepatotoxic agents, carcinogens and vitamins. Alcohol Alcohol 1990; 25:157-176
60. Niederau C, Fischer R, Sonnenberg A, Stremmel W, Trampisch HJ, Strohmeyer G Survival and causes of death in cirrhotic and in noncirrhotic patients with primary hemochromatosis. N Engl J Med 1985; 313:1256-1262
61. Sternlieb I, Scheinberg IH Prevention of Wilson's disease in asymptomatic patients. N Engl J Med 1968; 278:352-359
62. Kirk AP, Jain S, Pocock S, Thomas HC, Sherlock S Late results of the Royal Free Hospital prospective controlled trial of prednisolone therapy in hepatitis B surface antigen negative chronic active hepatitis. Gut 1980; 21:78-83
63. 4-induced lipid peroxidation in rat liver and its significance for hepatoprotection. Hepatology 1989; 9:830-838
64. Sinclair SB, Greig PD, Blendis LM, Biochemical and clinical response of fulminant viral hepatitis to administration of prostaglandin E: a preliminary report. J Clin Invest 1989; 84:1063-1069
65. Kershenobich D, Vargas F, Garcia-Tsao G, Tamayo RP, Gent M, Rojkind M Colchicine in the treatment of cirrhosis of the liver. N Engl J Med 1988; 318:1709-1713
66. Rockey DC, Maher JJ, Jarnagin WR, Gabbiani G, Friedman SL Inhibition of rat hepatic lipocyte activation in culture by interferon-gamma. Hepatology 1992; 16:776-784
67. Davis BH, Kramer RT, Davidson NO Retinoic acid modulates rat Ito cell proliferation, collagen, and transforming growth factor β production. J Clin Invest 1990; 86:2062-2070
68. Ferns GAA, Raines EW, Sprugel KH, Motani AS, Reidy MA, Ross R Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 1991; 253:1129-1132
69. Border WA, Noble NA, Yamamoto T, Natural inhibitor of transforming growth factor-β protects against scarring in experimental kidney disease. Nature 1992; 360:361-364
70. Liver selective fibrosuppression: a new approach in therapy of liver fibrosis. J Hepatol 1991; 13: Suppl 3-Suppl 3
71. Li J, Kim CI, Leo MA, Mak KM, Rojkind M, Lieber CS Polyunsaturated lecithin prevents acetaldehyde-mediated hepatic collagen accumulation by stimulating collagenase activity in cultured lipocytes. Hepatology 1992; 15:373-381
72. Friedman SL “Cuts both ways”: collagenases, lipocyte activation and polyunsaturated lecithin. Hepatology 1992; 15:549-551
73. Buck J, Derguini F, Levi E, Nakanishi K, Hammerling U Intracellular signaling by 14-hydroxy-4,14-retro-retinol. Science 1991; 254:1654-1656
74. Hultcrantz R, Bissell DM, Roll FJ Iron mediates production of a neutrophil chemoattractant in rat hepatocytes metabolizing ethanol. J Clin Invest 1991; 87:45-49