Reversibility of hepatic fibrosis: From the first report of collagenase in the liver to the possibility of gene therapy for recovery

Keio Journal of Medicine

Volumn 50, Issue 2, 2001, Pages 58-65

  Okazaki, Isao ^a,b   Watanabe, Tetsu ^b   Hozawa, Shigenari ^a   Niioka, Maki ^a   Arai, Masao ^c   Maruyama, Katsuya ^d  

^a Department of Community Health ^*  (Japan)

^b TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Hiratsuka City Hospital   (Japan)

^d KURIHAMA NATIONAL HOSPITAL   (Japan)

Author keywords

Collagenase; Liver cirrhosis; Matrix metalloproteinase (MMP), MMP 13; Recovery from liver fibrosis

Indexed keywords

COLLAGENASE; MATRIX METALLOPROTEINASE; MESSENGER RNA; TISSUE INHIBITOR OF METALLOPROTEINASE;

ANIMAL; EXPERIMENTAL LIVER CIRRHOSIS; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE THERAPY; GENETICS; HUMAN; IN SITU HYBRIDIZATION; LIVER CIRRHOSIS; METABOLISM; RAT; REVIEW;

ANIMALS; COLLAGENASES; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE THERAPY; HUMANS; IN SITU HYBRIDIZATION; LIVER CIRRHOSIS; LIVER CIRRHOSIS, EXPERIMENTAL; MATRIX METALLOPROTEINASES; RATS; RNA, MESSENGER; TISSUE INHIBITOR OF METALLOPROTEINASES;

EID: 0035375995     PISSN: 00229717     EISSN: None     Source Type: Journal    
DOI: 10.2302/kjm.50.58     Document Type: Review

References (74)

1. Cameron GR, Karunaratne WAE: Carbon tetrachloride cirrhosis in relation to liver regeneration. J Path Bact 1936; 42: 1-21
2. Quinn PS, Higginson J: Reversible and irreversible changes in experimental cirrhosis. Am J Pathol 1965; 47: 353-369
3. Morrione TG, Levine J: Collagenolytic activity and collagen resorption in experimental cirrhosis. Arch Pathol 1967; 84: 59-63
4. Hutterer F, Rubin E, Popper H: Mechanism of collagen resorption in reversible hepatic fibrosis. Exp Mol Pathol 1964; 86: 215-223
5. Takada A, Porta EA, Hartroft WS: The recovery of experimental dietary cirrhosis. Am J Pathol 1967; 51: 929-957, 959-976
6. Jacques WE, McAdams AI: Reversible biliary cirrhosis in rat after partial ligation of common bile duct. AMA Arch Path 1957; 63: 149-153
7. Okazaki I, Oda M, Maruyama K, Funatsu K, Matsuzaki S, Kamegaya K, Tsuchiya M: Mechanism of collagen resorption in experimental hepatic fibrosis with special reference to the activity of lysosomal enzymes. Biochem Exp Biol 1974; 11: 15-28
8. Rubin E, Hutterer F: Hepatic fibrosis: studies in the formation and resorption. In: Wagner BM, Smith DE, eds, The Connective Tissue, Baltimore, Williams and Wilkins, 1967; 142-160
9. Perez-Tamayo R: Some aspects of connective tissue of the liver. In: Popper H, Schaffner F, eds, Progress in Liver Diseases 2, New York, Grune & Stratton, 1965; 192-210
10. Rojkind M, Dunn MA: Hepatic fibrosis. Gastroenterology 1979; 76: 849-863
11. Maruyama K, Okazaki I, Kashiwazaki K, Oda M, Ishii H, Tsuchiya M: A case of subacute hepatitis with reversible liver fibrosis. Gastroenterol Jpn 1981; 16: 611-615
12. Arai M, Niioka M, Maruyama K, Wada N, Fujimoto N, Nomiyama T, Tanaka S, Okazaki I: Changes in serum levels of metalloproteinases and their inhibitors by treatment of chronic hepatitis C with interferon. Dig Dis Sci 1996; 41: 995-1000
13. Gross J, Lapiere CM: Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci 1962; 48: 1014-1022
14. Harris ED, Krane SM: Collagenases. N Engl J Med 1974; 291: 557-563
15. Okazaki I, Maruyama K: Mammalian collagenase in the process of hepatic fibrosis. J UOEH 1980; 2: 401-424
16. Okazaki I, Maruyama K: Collagenase activity in experimental hepatic fibrosis. Nature 1974; 252: 49-50
17. Maruyama K, Feinman L, Okazaki I, Lieber CS: Direct measurement of neutral collagenase activity in homogenates from baboon and human liver. Biochim Biophys Acta 1981; 658: 124-131
18. Maruyama K, Feinman L, Fainsilber Z, Nakano M, Okazaki I, Lieber CS: Mammalian collagenase increases in early alcoholic liver disease and decreases with cirrhosis. Life Sci 1982; 30: 1379-1384
19. Okazaki I, Feinman L, Lieber C: Hepatic mammalian collagenase: development of an assay and demonstration of increased activity after ethanol consumption. Gastroenterology 1977; 73: 1236
20. Okazaki I, Feinman L, Fainsilber Z, Nakano M, Lieber CS: Development of an assay for hepatic mammalian collagenase and study of the effect of ethanol on enzyme activity. In: Lieber CS, ed, Biological Approach to Alcoholism, New York, Rockville, 1983; 392-398
21. Okazaki I, Maruyama K, Ono A, Kobayashi T, Suzuki H: Reversibility of hepatic fibrosis in toxic liver injury. J UOEH 1982; 4(Suppl): 169-181
22. Maruyama K, Okazaki I, Kashiwazaki K, Funatsu K, Oda M, Kamegaya K, Tsuchiya M: Different appearance of collagenase and lysosomal enzymes in recovery of experimental hepatic fibrosis. Biochem Exp Biol 1978; 14: 191-201
23. Carter EA, McCarron MJ, Alpert E, Isselbacher KJ: Lysyl oxidase and collagenase in experimental acute and chronic liver injury. Gastroenterology 1982; 82: 526-34
24. Montfort I, Perez-Tamayo R, Alvizouri AM, Tello E: Collagenase of hepatocytes and sinusoidal liver cells in the reversibility of experimental cirrhosis of the liver. Virchows Arch B Cell Pathol Incl Mol Pathol 1990; 59: 281-289
25. Lindblad WJ, Fuller GC: Hepatic collagenase activity during carbon tetrachloride induced fibrosis. Fundam Appl Toxicol 1983; 3: 34-40
26. Nagase H, Barret AJ, Woessner JF: Nomenclature and glossary of the matrix metalloproteinases. Matrix (Suppl) 1992; 1: 421-424
27. Seiki M: Membrane-type matrix metalloproteinases. Connective Tissue 1998; 30: 313-319 (in Japanese)
28. Iredale JP, Benyon RC, Arthur MJ, Ferris WF, Alcolado R, Winwood PJ, Clark N, Murphy G: Tissue inhibitor of metalloproteinase-1 messenger RNA expression is enhanced relative to interstitial collagenase messenger RNA in experimental liver injury and fibrosis. Hepatology 1996; 24: 176-184
29. Iredale JP, Murphy G, Hembry RM, Friedman SL, Arthur MJ: Human hepatic lipocytes synthesize tissue inhibitor of metalloproteinases-1. Implications for regulation of matrix degradation in liver. J Clin Invest 1992; 90: 282-287
30. Roeb E, Purucker E, Breuer B, Nguyen H, Heinrich PC, Rose-John S, Matern S: TIMP expression in toxic and cholestatic liver injury in rat. J Hepatol 1997; 27: 535-544
31. Herbst H, Wege T, Milani S, Pellegrini G, Orzechowski HD, Bechstein WO, Neuhaus P, Gressner AM, Schuppan D: Tissue inhibitor of metalloproteinase-1 and -2 RNA expression in rat and human liver fibrosis. Am J Pathol 1997; 150: 1647-1659
32. Freije JM, Diez-Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, Lopez-Otin C: Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 1994; 269: 16766-16773
33. Knauper V, Lopez-Otin C, Smith B, Knight G, Murphy G: Biochemical characterization of human collagenase-3. J Biol Chem 1996; 271: 1544-1550
34. Friedman SL: Seminars in medicine of the Beth Israel Hospital, Boston. The cellular basis of hepatic fibrosis. Mechanisms and treatment strategies. N Eng J Med 1993; 328: 1828-1835
35. Arthur MJ: Role of Ito cells in the degradation of matrix in liver. J Gastroenterol Hepatol 1995; 10 (Suppl): 557-562
36. Friedman SL: Molecular mechanisms of hepatic fibrosis and principles of therapy. J Gastroenterol 1997; 32: 424-430
37. Rojkind M: Role of metalloproteinases in liver fibrosis. Alcoholism. Clin Exp Res 1999; 23: 934-939
38. Okazaki I, Watanabe T, Hozawa S, Maruyama K: Molecular Pathology of Liver Fibrosis. In: Progress in Hepatology. In: Yamanaka M, Toda G, Tanaka T, eds, Liver Cirrhosis, Amsterdam, Excerpta Medica, 1998; 23-33
39. Okazaki I, Watanabe T, Hozawa S, Niioka M, Arai M, Maruyama K: Hepatic Fibrolysis and hepatic sinusoidal cells. In: Tanikawa K, Ueno T, eds, Liver Diseases and Hepatic Sinusoidal Cells, Tokyo, Springer Verlag, 1999; 242-251
40. Okazaki I, Watanabe T, Hozawa S, Arai M, Maruyama K: Molecular mechanism of the reversibility of hepatic fibrosis: with special reference to the role of matrix metalloproteinases. J Gastroenterol Hepatol 2000; 15(Suppl): D26-D32
41. Arthur MJ: Fibrogenesis II. Metalloproteinases and their inhibitors in liver fibrosis. Am J Physiol Gastrointest Liver Physiol 2000; 279: G245-G249
42. Arthur MJ, 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
43. Arthur MJ, Stanley A, Iredale JP, Rafferty JA, Hembry RM, Friedman SL: Secretion of 72 kDa type IV collagenase/gelatinase by cultured human lipocytes. Analysis of gene expression, protein synthesis and proteinase activity. Biochem J 1992; 287: 701-707
44. Aimes RT, Quigley JP: Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments. J Biol Chem 1995; 270: 5872-5876
45. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y: Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 1997; 272: 2446-2451
46. Okazaki I, Maruyama K, Kashiwazaki K, Ebihara Y, Shigeta Y, Ishii H, Tsuchiya M: Type-specific collagen-degrading enzyme activity in alcoholic liver disease. In: Kamada T, Kuriyama K, Suwaki H, eds, Biomedical Aspects of Alcohol and Alcoholism, Tokyo, Gendaikikakushitsu Publishers, 1988; 329-339
47. Maruyama K, Okazaki I, Kashiwazaki K, Sonoda I, Ishii H, Tsuchiya M, Shibata T, Inayama S: Biosynthesis of Type IV collagenase by hepatic sinusoidal cells in rats. Acta Hep Jap, 1987; 28: 973-974
48. Maruyama K, Okazaki I, Takagi T, Ishii H: Formation and degradation of basement membrane collagen. Alcohol and Alcoholism 1991; 26(Suppl 1): 309-374
49. Iredale JP, Goddard S, Murphy G, Benyon RC, Arthur MJ: Tissue inhibitor of metalloproteinase-I and interstitial collagenase expression in autoimmune chronic active hepatitis and activated human hepatic lipocytes. Clin Sci 1995; 89: 75-81
50. Iredale JP, Benyon RC, Pickering J, McCullen M, Northrop M, Pawley S, Hovell C, Arthur MJ: Mechanism of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J Clin Invest 1998; 102: 538-549
51. Takahara T, Furui K, Funaki J, Nakayama Y, Itoh H, Miyabayashi C, Sato H, Seiki M, Ooshima A, Watanabe A: Increased expression of matrix metalloproteinase-II in experimental liver fibrosis in rats. Hepatology 1995; 21: 787-795
52. Takahara T, Furui K, Yata Y, Jin B, Zhang LP, Nambu S, Sato H, Seiki M, Watanabe A: Dual expression of matrix metalloproteinase-2 and membrane-type 1-matrix metalloproteinase in fibrotic human livers. Hepatology 1997; 26: 1521-1529
53. Watanabe T, Niioka M, Hozawa S, Kameyama K, Hayashi T, Arai M, Ishikawa A, Maruyama K, Okazaki I: Gene expression of interstitial collagenase in both progressive and recovery phase of rat liver fibrosis induced by carbon tetrachloride. J Hepatol 2000; 33: 224-235
54. Milani S, Herbst H, Schuppan D, Grappone C, Pellegrini G, Pinzani M, Casini A, Calabro A, Ciancio G, Stefanini F, et al.: Differential expression of matrix-metalloproteinase-1 and -2 genes in normal and fibrotic human liver. Am J Pathol 1994; 144: 528-537
55. Vyas SK, Leyland H, Gentry J, Arthur MJ: Rat hepatic lipocytes synthesize and secrete transin (stromelysin) in early primary culture. Gastroenterol 1995; 109: 889-898
56. Herbst H, Heinrichs O, Schuppan D, Milani S, Stein H: Temporal and spatial patterns of transin/stromelysin RNA expression following toxic injury in rat liver. Virchows Arch B Cell Pathol Incl Mol Pathol 1991; 60: 295-300
57. Winwood PJ, Schuppan D, Iredale JP, Kawser CA, Docherty AJ, Arthur MJ: Kupffer cell-derived 95-kd type IV collagenase/ gelatinase B: Characterization and expression in cultured cells. Hepatology 1995; 22: 304-315
58. Okazaki I, Brinckerhoff CE, Sinclair JR, Sinclair PR, Bonkowsky HL, Harris ED Jr: Iron increases collagenase production by rabbit synovial fibroblasts. J Lab Clin Med 1981; 97: 396-402
59. Maruyama K, Okazaki I, Kobayashi T, Suzuki H, Kashiwazaki K, Tsuchiya M: Collagenase production by rabbit liver cells in monolayer culture. J Lab Clin Med 1983; 102: 543-550
60. Okazaki I, Maruyama K, Kashiwazaki K, Tsuchiya M: Mechanism of collagenase production by liver cells. In: Hirayama C, Kivirikko KI, eds, Pathobiology of Hepatic Fibrosis, Amsterdam, Elsevir Sience Publishers 1985; 141-149
61. Lee KS, Buck M, Houglum K, Chojkier M: Activation of hepatic stellate cells by TGF-α and collagen type I is mediated by oxidative stress through c-myb expression. J Clin Invest 1995; 96: 2461-2468
62. Rockey DC, Chung JJ: Endothelin antagonism in experimental hepatic fibrosis. Implications for endothelin in the pathogenesis of wound healing. J Clin Invest 1996; 98: 1381-1388
63. Pinzani M, Marra F, Caligiuri A, DeFranco R, Gentilini A, Failli P, Gentilini P: Inhibition by pentoxifylline of extracellular signal-regulated kinase activation by platelet-derived growth factor in hepatic stellate cells. Br J Pharmacol 1996; 119: 1117-24
64. Marra F, Gentilini A, Pinzani M, Choudhury GG, Parola M, Herbst H, Dianzani MU, Laffi G, Abboud HE, Gentilini P: Phosphatidylinositol 3-kinase is required for platelet-derived growth factor's actions on hepatic stellate cells. Gastroenterology 1997; 112: 1297-1306
65. Newberry EP, Willis D, Latifi T, Boudreaux JM, Towler DA: Fibroblast growth factor receptor signaling activates the human interstitial collagenase promoter via the bipartite Ets-AP1 element. Mol Endocrinol 1997; 11: 1129-1144
66. Vincenti MP, White LA, Schroen DJ, Benbow U, Brinckerhoff CE: Regulating expression of the gene for matrix metalloproteinase-1 (collagenase): mechanisms that control enzyme activity, transcription, and mRNA stability. Crit Rev Eukaryot Gene Expr 1996; 6: 391-411
67. Grumbles RM, Shao L, Jeffrey JJ, Howell DS: Regulation of the rat interstitial collagenase promoter by IL-1 beta, c-Jun, and Ras-dependent signaling in growth plate chondrocytes. J Cell Biochem 1997; 67: 92-102
68. Vincenti MP, Coon CI, Brinckerhoff CE: Nuclear factor kappaB/p50 activates an element in the distal matrix metalloproteinase 1 promoter in interleukin-1beta-stimulated synovial fibroblasts. Arthritis Rheum 1998; 41: 1987-1994
69. Poulos JE, Weber JD, Bellezzo JM, Di Bisceglie AM, Britton RS, Bacon BR, Baldassare JJ: Fibronectin and cytokines increase JNK, ERK. AP-1 activity, and transin gene expression in rat hepatic stellate cells. Am J Physiol 1997; 273: G804-G811
70. Elsharkawy AM, Wright MC, Hay RT, Arthur MJ, Hughes T, Bahr MJ, Degitz K, Mann DA: Persistent activation of nuclear factor-kappaB in cultured rat hepatic stellate cells involves the induction of potentially novel Rel-like factors and prolonged changes in the expression of IkappaB family proteins. Hepatology 1999; 30: 761-769
71. Yasuda H, Imai E, Shiota A, Fujise N, Morinaga T, Higashio K: Antifibrogenic effect of a deletion variant of hepatocyte growth factor on liver fibrosis in rats. Hepatology 1996; 24: 636-642
72. Ueki T, Kaneda Y, Tsutsui H, Nakanishi K, Sawa Y, Morishita R, Matsumoto K, Nakamura T, Takahashi H, Okamoto E, Fujimoto J: Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nat Med 1999; 5: 226-230
73. Ozaki I, Zhao G, Mizuta T, Ogawa Y, Hara T, Kajihara S, Hisatomi A: Induction of collagenase (matrix metalloproteinase-1) by hepatocytes growth factor in human Ito cell LI90. Hepatology 1999; 30: 491A
74. Okazaki I, Wada N, Nakano M, Saito A, Takasaki K, Doi M, Kameyama K, Otani Y, Kubochi K, Niioka M, Watanabe T, Maruyama K: Difference in gene expression for matrix metalloproteinase-1 between early and advanced hepatocellular carcinomas. Hepatology 1997; 25: 580-584