Hypoxia potentiates transforming growth factor-β expression of hepatocyte during the cirrhotic condition in rat liver

Liver International

Volumn 24, Issue 6, 2004, Pages 658-668

  Jeong, Won Il ^a   Do, Sun Hee ^a   Yun, Hae Sun ^a   Song, Byoung Joon ^b   Kim, Seong Jin ^c   Kwak, Wie Jong ^d   Yoo, Sung Eun ^e   Park, Ho Yong ^f   Jeong, Kyu Shik ^a  

^a Kyungpook National University   (South Korea)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d SK Chemicals   (South Korea)

^e Korea Research Institute of Chemical Technology   (South Korea)

^f Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Cirrhosis; Hypoxia; Liver; Myofibroblast; Smad protein; Transforming growth factor beta

Indexed keywords

8 AZAGUANINE; CARBON TETRACHLORIDE; COLLAGEN; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; FIBROGENESIS; HYPOTHESIS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIVER CELL; LIVER CIRRHOSIS; LIVER FIBROSIS; MACROPHAGE; MALE; MYOFIBROBLAST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANOXIA; CARBON TETRACHLORIDE; CELLS, CULTURED; COLLAGEN; DNA-BINDING PROTEINS; HEPATOCYTES; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIVER CIRRHOSIS, EXPERIMENTAL; MALE; PROBABILITY; RATS; RATS, WISTAR; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REFERENCE VALUES; RNA, MESSENGER; SENSITIVITY AND SPECIFICITY; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANS-ACTIVATORS;

EID: 11144332398     PISSN: 14783223     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2004.0961.x     Document Type: Article

References (41)

1. Friedman S L. Seminars in medicine of the Beth Israel Hospital, Boston. The cellular basis of hepatic fibrosis. Mechanisms and treatment strategies. N Engl J Med 1993; 328: 1828-35.
2. Tao L H, Enzan H, Hayashi Y, Miyazaki E, Saibara T, Hiroi M, et al. Appearance of denuded hepatic stellate cells and their subsequent myofibroblast-like transformation during the early stage of biliary fibrosis in the rat. Med Electron Microsc 2000; 33: 217-30.
3. Dooley S, Delvoux B, Streckert M, Bonzel L, Stopa M, Ten Dijke P, et al. Transforming growth factor beta signal transduction in hepatic stellate cells via Smad2/3 phosphorylation, a pathway that is abrogated during in vitro progression to myofibroblasts. TGFbeta signal transduction during transdifferentiation of hepatic stellate cells. FEBS Lett 2001; 502: 4-10.
4. Gao C, Gressner G, Zoremba M, Gressner A M. Transforming growth factor beta (TGF-beta) expression in isolated and cultured rat hepatocytes. J Cell Physiol 1996; 167: 394-405.
5. Friedman S L. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J Biol Chem 2000; 275: 2247-50.
6. Gressner A M. The cell biology of liver fibrogenesis - an imbalance of proliferation, growth arrest and apoptosis of myofibroblasts. Cell Tissue Res 1998; 292: 447-52.
7. Blobe G C, Schiemann W P, Lodish H F. Role of transforming growth factor beta in human disease. N Engl J Med 2000; 342: 1350-8.
8. Heldin C H, Miyazono K, Ten Dijke P. TGF-beta signaling from cell membrane to nucleus through SMAD proteins. Nature 1997; 390: 465-71.
9. Massague J. TGF-beta signal transduction. Annu Rev Biochem 1998; 67: 753-91.
10. Whitman M. Smads and early developmental signaling by the TGF-beta superfamily. Genes Dev 1998; 12: 2445-62.
11. Corpechot C, Barbu V, Wendum D, Kinnman N, Rey C, Poupon R, et al. Hypoxia-induced VEGF and collagen I expressions are associated with angiogenesis and fibrogenesis in experimental cirrhosis. Hepatology 2002; 35: 1010-21.
12. Corpechot C, Barbu V, Wendum D, Chignard N, Housset C, Poupon R, et al. Hepatocyte growth factor and c-Met inhibition by hepatic cell hypoxia: a potential mechanism for liver regeneration failure in experimental cirrhosis. Am J Pathol 2002; 160: 613-20.
13. Rosmorduc O, Wendum D, Corpechot C, Galy B, Sebbagh N, Raleigh J, et al. Hepatocellular hypoxia-induced vascular endothelial growth factor expression and angiogenesis in experimental biliary cirrhosis. Am J Pathol 1999; 155: 1065-73.
14. Zhang H, Akman H O, Smith E L, Zhao J, Murphy-Ullrich J E, Batuman O A. Cellular response to hypoxia involves signaling via Smad proteins. Blood 2003; 101: 2253-60.
15. Akman H O, Zhang H, Siddiqui M A, Solomon W, Smith E L, Batuman O A. Response to hypoxia involves transforming growth factor-beta2 and Smad proteins in human endothelial cells. Blood 2001; 98: 3324-31.
16. Jeong W I, Lee C S, Park S J, Chung J Y, Jeong K S. Kinetics of macrophages, myofibroblasts and mast cells in carbon tetrachloride-induced rat liver cirrhosis. Anticancer Res 2002; 22: 869-77.
17. Annoni G, Weiner F R, Zern M A. Increased transforming growth factor-beta 1 gene expression in human liver disease. J Hepatol 1992; 14: 259-64.
18. Bachem M G, Meyer D, Melchior R, Sell K M, Gressner A M. 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.
19. De Bleser P J, Niki T, Rogiers V, Geerts A. Transforming growth factor-beta gene expression in normal and fibrotic rat liver. J Hepatol 1997; 26: 886-93.
20. Nakatsukasa H, Nagy P, Evarts R P, Hsia C C, Marsden E, Thorgeirsson S S. Cellular distribution of transforming growth factor-beta 1 and procollagen types I, III, and IV transcripts in carbon tetrachloride-induced rat liver fibrosis. J Clin Invest 1990; 85: 1833-43.
21. Arteel G E, Thurman R G, Raleigh J A. Reductive metabolism of the hypoxia marker pimonidazole is regulated by oxygen tension independent of the pyridine nucleotide redox state. Eur J Biochem 1998; 253: 743-50.
22. Arteel G E, Iimuro Y, Yin M, Raleigh J A, Thurman R G. Chronic enteral ethanol treatment causes hypoxia in rat liver tissue in vivo. Hepatology 1997; 25: 920-26.
23. Raleigh J A, Chou S C, Tables L, Suchindran S, Varia M A, Horsman M R. Relationship of hypoxia to metallothionein expression in murine tumors. Int J Radiat Oncol Biol Phys 1998; 42: 727-30.
24. Dennler S, Itoh S, Vivien D, Ten Dijke P, Huet S, Gauthier J M. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998; 17: 3091-100.
25. Bradford M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-54.
26. Date M, Matsuzaki K, Matsushita M, Tahashi Y, Furukawa F, Inoue K. Modulation of transforming growth factor beta function in hepatocytes and hepatic stellate cells in rat liver injury. Gut 2000; 46: 719-24.
27. Tahashi Y, Matsuzaki K, Date M, Yoshida K, Furukawa F, Sugano Y, et al. Differential regulation of TGF-beta signal in hepatic stellate cells between acute and chronic rat liver injury. Hepatology 2002; 35: 49-61.
28. Roberts A B, Flanders K C, Kondaiah P, Thompson N L, Van Obberghen-Schilling E, Wakefield L, et al. Transforming growth factor beta: biochemistry and roles in embryogenesis, tissue repair and remodeling, and carcinogenesis. Recent Prog Horm Res 1988; 44: 157-97.
29. Jirtle R L, Carr B I, Scott C D. Modulation of insulin-like growth factor-II/mannose 6-phosphate receptors and transforming growth factor-beta 1 during liver regeneration. J Biol Chem 1991; 266: 22444-50.
30. Klempt N D, Sirimanne E, Gunn A J, Klempt M, Singh K, Williams C, et al. Hypoxia-ischemia induces transforming growth factor beta 1 mRNA in the infant rat brain. Brain Res Mol Brain Res 1992; 13: 93-101.
31. Falanga V, Martin T A, Takagi H, Kirsner R S, Helfman T, Pardes J, et al. Low oxygen tension increases mRNA levels of alpha 1 (I) procollagen in human dermal fibroblasts. J Cell Physiol 1993; 157: 408-12.
32. Patel B, Khaliq A, Jarvis-Evans J, McLeod D, Mackness M, Boulton M. Oxygen regulation of TGF-beta 1 mRNA in human hepatoma (Hep G2) cells. Biochem Mol Biol Int 1994; 34: 639-44.
33. Campra J L, Reynolds T B. The hepatic circulation. In: Arias IM, Jakoby WB, Popper H, Schachter D, Shafritz DA, eds. The Liver: Biology and Pathobiology. New York: Raven, 1982; 911-30.
34. Ichikawa T, Zhang Y Q, Kogure K, Hasegawa Y, Takagi H, Mori M, et al. Transforming growth factor beta and activin tonically inhibit DNA synthesis in the rat liver. Hepatology 2001; 34: 918-25.
35. Nakamura T, Sakata R, Ueno T, Sata M, Ueno H. Inhibition of transforming growth factor beta prevents progression of liver fibrosis and enhances hepatocyte regeneration in dimethylnitrosamine-treated rats. Hepatology 2000; 32: 247-55.
36. Qi Z, Atsuchi N, Ooshima A, Takeshita A, Ueno H. Blockade of type beta transforming growth factor signaling prevents liver fibrosis and dysfunction in the rat. Proc Natl Acad Sci USA 1999; 96: 2345-9.
37. Ueno H, Sakamoto T, Nakamura T, Qi Z, Astuchi N, Takeshita A, et al. A soluble transforming growth factor beta receptor expressed in muscle prevents liver fibrogenesis and dysfunction in rats. Hum Gene Ther 2000; 11: 33-42.
38. Harvey P J, Gready J E, Yin Z, Le Couteur D G, Mclean A J. Acute oxygen supplementation restores markers of hepatocyte energy status and hypoxia in cirrhotic rats. J Pharmacol Exp Ther 2000; 293: 641-5.
39. Froomes P R, Morgan D J, Smallwood R A, Angus P W. Comparative effects of oxygen supplementation on theophylline and acetaminophen clearance in human cirrhosis. Gastroenterology 1999; 116: 915-20.
40. Hickey P L, Angus P W, Mclean A J, Morgan D J. Oxygen supplementation restores theophylline clearance to normal in cirrhotic rats. Gastroenterology 1995; 108: 1504-9.
41. Harvey P J, Lecouteur D, Mclean A J. Hepatic oxygen supplementation as therapy in cirrhotic liver disease. Gastroenterology 1999; 117: 1025-6.