Mechanisms of spontaneous resolution of rat liver fibrosis: Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors

Journal of Clinical Investigation

Volumn 102, Issue 3, 1998, Pages 538-549

  Iredale, J P ^a,b   Benyon, R C ^a   Pickering, J ^a   McCullen, M ^a   Northrop, M ^a   Pawley, S ^a   Hovell, C ^a   Arthur, M J P ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

Author keywords

Apoptosis; Collagenase; Hepatic stellate cells; Liver fibrosis; TIMP

Indexed keywords

METALLOPROTEINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; HISTOPATHOLOGY; LIVER FIBROSIS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REMISSION; STELLATE CELL;

EID: 0032146551     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1018     Document Type: Article

References (38)

1. Friedman, S.L. 1993. The cellular basis of hepatic fibrosis: mechanisms and treatment strategies. N. Engl. J. Med. 328:1828-1835.
2. Rojkind, M., and M.A. Dunn. 1979. Hepatic fibrosis. Gastroenterology. 76:849-863.
3. Hunt, J. 1992. Long-term follow-up of patients with hepatitis B treated with interferon. Interferons Cytokines. 20:6-9.
4. Abdel-Aziz, G., G. Lebeau, P.Y. Rescan, B. Clement, M. Rissel, Y. Deugnier, J.P. Campion, and A. Guillouzo. 1990. Reversibility of hepatic fibrosis in experimentally induced cholestasis in rat. Am. J. Pathol. 137:1333-1342.
5. Vaux, D.L., and A. Strasser. 1996. The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA. 93:2239-2244.
6. Evan, G.I., L. Brown, M. Whyte, and E. Harrington, 1995. Apoptosis and the cell cycle. Curr. Opin. Cell Biol. 7:825-834.
7. Patel, T., and G.J. Gores. 1995. Apoptosis and hepatobiliary disease. Hepatology. 21:1725-1741.
8. Fraser, A., and G. Evan. 1996. A license to kill. Cell. 85:781-784.
9. Freije, J.M.P., I. Diezitza, M. Balbin, L.M. Sanchez, R. Blasco, J. Tolivia, and C. Lopezotin. 1994. Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J. Biol. Chem. 269:16766-16773.
10. Benyon, R.C., J.P. Iredale, S. Goddard, P.J. Winwood, and M.J.P. Arthur. 1996. Expression of tissue inhibitor of metalloproteinases-1 and -2 is increased in fibrotic human liver. Gastroenterology. 110:821-831.
11. Iredale, J.P., P.J. Winwood, C.A. Kawser, and M.J.P. Arthur. 1993. Lipocyte proliferation in the C. parvum model of macrophage-induced liver injury is associated with expression of 72-kD type IV collagenase/gelatinase. In Cells of the Hepatic Sinusoid, Vol. 4. D.L. Knook and E. Wisse, editors. Kupffer Cell Foundation, Leiden. 105-108.
12. Herbst, H., O. Heinrichs, D. Schuppan, S. Milani, and H. Stein. 1991. Temporal and spatial patterns of transin/stromelysin RNA expression following toxic injury in rat liver. Virchows Arch. B Cell Pathol. 60:295-300.
13. Arthur, M.J.P. 1994. Matrix degradation in the liver. In Fat-Storing Cells and Liver Fibrosis. C. Surrenti, A. Casini, S. Milani, and M. Pinzani, editors. Kluwer Academic Publishers, Dordrecht, Germany. 110-127.
14. Li, J.J., C.I. Kim, M.A. Leo, K.M. Mak, M. Rojkind, and C.S. Lieber. 1992. Polyunsaturated lecithin prevents acetaldehyde-mediated hepatic collagen accumulation by stimulating collagenase activity in cultured lipocytes. Hepatology. 15:373-381.
15. Iredale, J.P., R.C. Benyon, M.J.P. Arthur, W.F. Ferris, R. Alcolado, P.J. Winwood, N. Clark, and G. Murphy. 1996. Tissue inhibitor of metalloproteinase-1 messenger RNA expression is enhanced relative to interstitial collagenase messenger RNA in experimental liver injury and fibrosis. Hepatology. 24:176-184.
16. Okazaki, I., and K. Maruyama. 1974. Collagenase activity in experimental hepatic fibrosis. Nature. 252:49-50.
17. Perez-Tamayo, R., I. Montfort, and E. Gonzalez. 1987. Collagenolytic activity in experimental cirrhosis of the liver. Exp. Mol. Pathol. 47:300-308.
18. Maruyama, K., L. Feinman, Z. Fainsilber, M. Nakano, I. Okazaki, and C.S. Lieber. 1982. Mammalian collagenase increases in early alcoholic liver disease and decreases with cirrhosis. Life Sci. 30:1379-1384.
19. Iredale, J.P., G. Murphy, R.M. Hembry, S.L. Friedman, and M.J.P. Arthur. 1992. Human hepatic lipocytes synthesize tissue inhibitor of metalloproteinases-1 (TIMP-1): implications for regulation of matrix degradation in liver. J. Clin. Invest. 90:282-287.
20. Hovell, C.J., R.C. Benyon, S.J. Pawley, J.P. Iredale, and M.J.P. Arthur. 1997. Membrane-type matrix metalloproteinase (MTMMP) is upregulated in liver fibrosis. J. Hepatol. 26:133.
21. Iredale, J.P., S. Goddard, G. Murphy, R.C. Benyon, and M.J.P. Arthur. 1995. Tissue inhibitor of metalloproteinase-1 and interstitial collagenase expression in autoimmune chronic active hepatitis and activated human hepatic lipocytes. Clin. Sci. 89:75-81.
22. Murawaki, Y., H. Yamamoto, H. Kawasaki, and H. Shima. 1993. Serum tissue inhibitor of metalloproteinases in patients with chronic liver disease and with hepatocellular carcinoma. Clin. Chim. Acta. 218:47-58.
23. Muzzillo, D.A., M. Imoto, Y. Fukuda, Y. Koyama, S. Saga, Y. Nagai, and T. Hayakawa. 1993. Clinical evaluation of serum tissue inhibitor of metalloproteinases-1 levels in patients with liver diseases. J. Gastroenterol. Hepatol. 8: 437-441.
24. Murawaki, Y., H. Kawasaki, and H. Burkhardt. 1994. Serum collagenase activity in chronic liver diseases. Pathol. Res. Pract. 190:929-933.
25. Rockey, D.C., J.K. Boyles, G. Gabbiani, and S.L. Friedman. 1992. Rat hepatic lipocytes express smooth muscle actin upon activation in vivo and in culture. J. Submicrosc. Cytol. Pathol. 24:193-203.
26. Baker, A.J., A. Mooney, J. Hughes, D. Lombardi, R.J. Johnson, and J. Savill. 1994. Mesangial cell apoptosis: the major mechanism for resolution of glomerular hypercellularity in experimental mesangial proliferative nephritis. J. Clin. Invest. 94:2105-2116.
27. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson. 1992. Identification of programmed cell death via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
28. Arthur, M.J.P., S.L. Friedman, F.J. Roll, and D.M. Bissell. 1989. Lipocytes from normal rat liver release a neutral metalloproteinase that degrades basement membrane (type IV) collagen. J. Clin. Invest. 84:1076-1085.
29. Bergman, I., and R. Loxley. 1963. Two improved and simplified methods for the spectrophotometric determination of hydroxyproline. Anal. Chem. 35:1961-1965.
30. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
31. Burt, A.D. 1993. Cellular and molecular aspects of hepatic fibrosis. J. Pathol. 170:105-114.
32. De Bleser, P.J., T. Niki, T. Xu, V. Rogiers, and A. Geerts. 1997. Localization and cellular sources of activins in normal and fibrotic rat liver. Hepatology. 26:905-912.
33. Saile, B., T. Knittel, N. Matthes, P. Schott, and G. Ramadori. 1997. CD95/CD95L-mediated apoptosis of the hepatic stellate cell. Am. J. Pathol. 151:1265-1272.
34. Fanidi, A., E.A. Harrington, and G.I. Evan. 1992. Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature. 359:554-556.
35. Evan, G.I., A.H. Wyllie, C.S. Gilbert, T.D. Littlewood, H. Land, M. Brooks, C.M. Waters, L.Z. Penn, and D.C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 69:119-128.
36. Carter, E.A., M.J. McCarron, E. Alpert, and K.J. Isselbacher. 1982. Lysyl oxidase and collagenase in experimental acute and chronic liver injury. Gastroenterology. 82:526-534.
37. Murawaki, Y., S. Yamada, M. Koda, and C. Hirayama. 1990. Collagenase and collagenolytic cathepsin in normal and fibrotic rat liver. J. Biochem. 108:241-244.
38. Montfort, I., R. Perez-Tamayo, A.M. Alvizouri, and E. Tello. 1990. Collagenase of hepatocytes and sinusoidal liver cells in the reversibility of experimental cirrhosis of the liver. Virchows Arch. B Cell Pathol. 59:281-289.