Sustained activation of Rac1 in hepatic stellate cells promotes liver injury and fibrosis in mice

Hepatology

Volumn 44, Issue 5, 2006, Pages 1267-1277

  Choi, Steve S ^a   Sicklick, Jason K ^a,b   Ma, Qi ^a   Yang, Liu ^a   Huang, Jiawen ^a   Qi, Yi ^a   Chen, Wei ^a   Li, Yin Xiong ^a   Goldschmidt Clermont, Pascal J ^a   Diehl, Anna Mae ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CARBON TETRACHLORIDE; COLLAGEN; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL CULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIVER CELL; LIVER FIBROSIS; LIVER INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STELLATE CELL; TRANSGENE; UPREGULATION;

ACTINS; ANIMALS; CARBON TETRACHLORIDE; CELLS, CULTURED; COLLAGEN; CYTOCHROME P-450 CYP2E1; HEPATOCYTES; IMMUNOHISTOCHEMISTRY; LIVER; LIVER CIRRHOSIS; LIVER DISEASES; MICE; MICE, TRANSGENIC; NADPH OXIDASE; NEUROPEPTIDES; RAC GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 33751003841     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.21375     Document Type: Article

References (56)

1. Albanis E, Friedman SL. Hepatic fibrosis. Pathogenesis and principles of therapy. Clin Liver Dis 2001;5:315-334, v-vi.
2. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005;115:209-218.
3. Fallowfield JA, Iredale JP. Targeted treatments for cirrhosis. Expert Opin Ther Targets 2004;8:423-435.
4. Parola M, Robino G. Oxidative stress-related molecules and liver fibrosis. J Hepatol 2001;35:297-306.
5. Friedman SL. Liver fibrosis - from bench to bedside. J Hepatol 2003; 38(Suppl 1):S38-S53.
6. Mato JM, Camara J, Fernandez de Paz J, Caballería L, Coll S, Caballero A, et al. S-adenosylmethionine in alcoholic cirrhosis: a randomized, placebo-controlled, double-blind, multicenter clinical trial. J Hepatol 1999;30:1081-1089.
7. Zhong Z, Froh M, Wheeler MD, Smutney O, Lehmann TG, Thurman RG. Viral gene delivery of superoxide dismutase attenuates experimental cholestasis-induced liver fibrosis in the rat. Gene Ther 2002;9:183-191.
8. Bataller R, Schwabe RF, Choi YH, Yang L, Paik YH, Lindquist J, et al. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 2003;112:1383-1394.
9. Adachi T, Togashi H, Suzuki A, Kasai S, Ito J, Sugahara K, et al. NAD(P)H oxidase plays a crucial role in PDGF-induced proliferation of hepatic stellate cells. HEPATOLOGY 2005;41:1272-1281.
10. Hassanain H, Goldschmidt-Clermont P. Rac, superoxide, and signal transduction. In: Sen G, editor. Antioxidant and Redox Regulation of Genes. San Diego, CA: Academic Press, 2000:47-79.
11. Hassanain HH, Irshaid F, Wisel S, Sheridan J, Michler RE, Goldschmidt-Clermont PJ. Smooth muscle cell expression of a constitutive active form of human Rac 1 accelerates cutaneous wound repair. Surgery 2005;137:92-101.
12. 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.
13. Lopes N, Gregg D, Vasudevan S, Hassanain H, Goldschmidt-Clermont P, Kovacic H. Thrombospondin 2 regulates cell proliferation induced by Rac1 redox-dependent signaling. Mol Cell Biol 2003;23:5401-5408.
14. Kovacic HN, Irani K, Goldschmidt-Clermont PJ. Redox regulation of human Racl stability by the proteasome in human aortic endothelial cells. J Biol Chem 2001;276:45856-45861.
15. Sicklick JK, Li Y-X, Choi SS, Qi Y, Chen W, Bustamante M, et al. Role for Hedgehog signaling in hepatic stellate cell activation and viability. Lab Invest 2005;85:1368-1380.
16. Nieto N, Dominguez-Rosales JA, Fontana L, Salazar A, Armendariz-Borunda J, Greenwel P, et al. Rat hepatic stellate cells contribute to the acute-phase response with increased expression of alpha1(I) and alpha1(IV) collagens, tissue inhibitor of metalloproteinase-1, and matrix-metalloproteinase-2 messenger RNAs. HEPATOLOGY 2001;33:597-607.
17. Geerts A, Greenwel P, Cunningham M, De Bleser P, Rogiers V, Wisse E, et al. Identification of connective tissue gene transcripts in freshly isolated parenchymal, endothelial, Kupffer and fat-storing cells by northern hybridization analysis. J Hepatol 1993;19:148-158.
18. Xu L, Hui AY, Albanis E, Arthur MJ, O'Byrne SM, Blaner WS, et al. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut 2005;54:142-151.
19. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A 2004;101:7618-7623.
20. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 1994;74:1141-1148.
21. Jalil JE, Perez A, Ocaranza MP, Bargetto J, Galaz A, Lavandero S. Increased aortic NADPH oxidase activity in rats with genetically high angiotensin-converting enzyme levels. Hypertension 2005;46:1362-1367.
22. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
23. Ren XD, Kiosses WB, Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBOJ 1999;18:578-585.
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-408.
25. Yata Y, Gotwals P, Koteliansky V, Rockey DC. Dose-dependent inhibition of hepatic fibrosis in mice by a TGF-beta soluble receptor: implications for antifibrotic therapy. HEPATOLOGY 2002;35:1022-1030.
26. Lopez-De Leon A, Rojkind M. A simple micromethod for collagen and total protein determination in formalin-fixed paraffin-embedded sections. J Histochem Cytochem 1985;33:737-743.
27. Foster DN, Min B, Foster LK, Stoflet ES, Sun S, Getz MJ, et al. Positive and negative cis-acting regulatory elements mediate expression of the mouse vascular smooth muscle alpha-actin gene. J Biol Chem 1992;267:11995-12003.
28. Min BH, Foster DN, Strauch AR. The 5′-flanking region of the mouse vascular smooth muscle alpha-actin gene contains evolutionarily conserved sequence motifs within a functional promoter. J Biol Chem 1990;265:16667-16675.
29. 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.
30. She H, Xiong S, Hazra S, Tsukamoto H. Adipogenic transcriptional regulation of hepatic stellate cells. J Biol Chem 2005;280:4959-4967.
31. Niki T, Pekny M, Hellemans K, Bleser PD, Berg KV, Vaeyens F, et al. Class VI intermediate filament protein nestin is induced during activation of rat hepatic stellate cells. HEPATOLOGY 1999;29:520-527.
32. Knittel T, Aurisch S, Neubauer K, Eichhorst S, Ramadori G. Cell-type-specific expression of neural cell adhesion molecule (N-CAM) in Ito cells of rat liver. Up-regulation during in vitro activation and in hepatic tissue repair. Am J Pathol 1996;149:449-462.
33. Zhang LP, Takahara T, Yata Y, Furui K, Jin B, Kawada N, et al. Increased expression of plasminogen activator and plasminogen activator inhibitor during liver fibrogenesis of rats: role of stellate cells. J Hepatol 1999;31:703-711.
34. Sundaresan M, Yu ZX, Ferrans VJ, Sulciner DJ, Gutkind JS, Irani K, et al. Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem J 1996;318:379-382.
35. Goldschmidt-Clermont PJ, Moldovan L. Stress, superoxide, and signal transduction. Gene Expr 1999;7:255-260.
36. Gregg D, Rauscher FM, Goldschmidt-Clermont PJ. Rac regulates cardiovascular superoxide through diverse molecular interactions: more than a binary GTP switch. Am J Physiol Cell Physiol 2003;285:C723-C734.
37. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993;362:801-809.
38. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, et al. Cell migration: integrating signals from front to back. Science 2003;302:1704-1709.
39. Brown MR, Miller FJ Jr, Li WG, Ellingson AN, Mozena JD, Chatterjee P, et al. Overexpression of human catalase inhibits proliferation and promotes apoptosis in vascular smooth muscle cells. Circ Res 1999;85:524-533.
40. Tsai JC, Jain M, Hsieh CM, Lee WS, Yoshizumi M, Patterson C, et al. Induction of apoptosis by pyrrolidinedithiocarbamate and N-acetylcysteine in vascular smooth muscle cells. J Biol Chem 1996;271:3667-3670.
41. Kong G, Lee S, Kim KS. Inhibition of rac1 reduces PDGF-induced reactive oxygen species and proliferation in vascular smooth muscle cells. J Korean Med Sci 2001;16:712-718.
42. Iredale JP, Benyon RC, Pickering J, McCullen M, Northrop M, Pawley S, et al. Mechanisms 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.
43. Schnabl B, Choi YH, Olsen JC, Hagedorn CH, Brenner DA. Immortal activated human hepatic stellate cells generated by ectopic telomerase expression. Lab Invest 2002;82:323-333.
44. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995;270:296-299.
45. Doanes AM, Irani K, Goldschmidt-Clermont PJ, Finkel T. A requirement for rac1 in the PDGF-stimulated migration of fibroblasts and vascular smooth cells. Biochem Mol Biol Int 1998;45:279-287.
46. Pinzani M, Milani S, Grappone C, Weber FL Jr, Gentilini P, Abboud HE. Expression of platelet-derived growth factor in a model of acute liver injury. HEPATOLOGY 1994;19:701-707.
47. Lee JS, Kang Decker N, Chatterjee S, Yao J, Friedman S, Shah V. Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts. Am J Pathol 2005;166:1861-1870.
48. Wong L, Yamasaki G, Johnson RJ, Friedman SL. Induction of beta-platelet-derived growth factor receptor in rat hepatic lipocytes during cellular activation in vivo and in culture. J Clin Invest 1994;94:1563-1569.
49. Campbell JS, Hughes SD, Gilbertson DG, Palmer TE, Holdren MS, Haran AC, et al. Platelet-derived growth factor C induces liver fibrosis, steatosis, and hepatocellular carcinoma. Proc Natl Acad Sci U S A 2005;102:3389-3394.
50. Bradford BU, Kono H, Isayama F, Kosyk O, Wheeler MD, Akiyama TE, et al. Cytochrome P450 CYP2E1, but not nicotinamide adenine dinucleotide phosphate oxidase, is required for ethanol-induced oxidative DNA damage in rodent liver. HEPATOLOGY 2005;41:336-344.
51. Schmitt-Graff A, Kruger S, Bochard F, Gabbiani G, Denk H. Modulation of alpha smooth muscle actin and desmin expression in perisinusoidal cells of normal and diseased human livers. Am J Pathol 1991;138:1233-1242.
52. Rockey DC, Friedman SL. Cytoskeleton of liver perisinusoidal cells (lipocytes) in normal and pathological conditions. Cell Motil Cytoskeleton 1992;22:227-234.
53. Kim KY, Choi I, Kim SS. Progression of hepatic stellate cell activation is associated with the level of oxidative stress rather than cytokines during CC14-induced fibrogenesis. Mol Cells 2000;10:289-300.
54. McGuire TF, Corey SJ, Sebti SM. Lovastatin inhibits platelet-derived growth factor (PDGF) stimulation of phosphatidylinositol 3-kinase activity as well as association of p85 subunit to tyrosine-phosphorylated PDGF receptor. J Biol Chem 1993;268:22227-22230.
55. Kohno M, Shinomiya K, Abe S, Noma T, Kondo I, Oshita A, et al. Inhibition of migration and proliferation of rat vascular smooth muscle cells by a new HMG-CoA reductase inhibitor, pitavastatin. Hypertens Res 2002;25:279-285.
56. Zeng L, Xu H, Chew TL, Chisholm R, Sadeghi MM, Kanwar YS, et al. Simvastatin modulates angiotensin II signaling pathway by preventing Rac1-mediated upregulation of p27. J Am Soc Nephrol 2004;15:1711-1720.