The nicotinamide adenine dinucleotide phosphate oxidase (NOX) homologues NOX1 and NOX2/gp91phox mediate hepatic fibrosis in mice

Hepatology

Volumn 53, Issue 5, 2011, Pages 1730-1741

  Paik, Yong Han ^a,b   Iwaisako, Keiko ^a   Seki, Ekihiro ^a   Inokuchi, Sayaka ^a   Schnabl, Bernd ^a   Österreicher, Christoph H ^a   Kisseleva, Tatiana ^a   Brenner, David A ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; CARBON TETRACHLORIDE; COLLAGEN; COLLAGEN ALPHA1; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BILE DUCT LIGATION; BONE MARROW; CLINICAL ASSESSMENT; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; INJECTION; KUPFFER CELL; LIVER FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STELLATE CELL;

ANIMALS; BILE DUCTS; CARBON TETRACHLORIDE; HEPATIC STELLATE CELLS; LIGATION; LIVER; LIVER CIRRHOSIS; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; REACTIVE OXYGEN SPECIES;

EID: 79955091590     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24281     Document Type: Article

References (38)

1. Bubici C, Papa S, Dean K, Franzoso G. Mutual cross-talk between reactive oxygen species and nuclear factor-kappa B: molecular basis and biological significance. Oncogene 2006; 25: 6731-6748.
2. Parola M, Robino G. Oxidative stress-related molecules and liver fibrosis. J Hepatol 2001; 35: 297-306.
3. 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.
4. Lee KS, Buck M, Houglum K, Chojkier M. Activation of hepatic stellate cells by TGF alpha and collagen type I is mediated by oxidative stress through c-myb expression. J Clin Invest 1995; 96: 2461-2468.
5. Nieto N, Greenwel P, Friedman SL, Zhang F, Dannenberg AJ, Cederbaum AI. Ethanol and arachidonic acid increase alpha 2(I) collagen expression in rat hepatic stellate cells overexpressing cytochrome P450 2E1. Role of H2O2 and cyclooxygenase-2. J Biol Chem 2000; 275: 20136-20145.
6. Maher JJ, Tzagarakis C, Gimenez A. Malondialdehyde stimulates collagen production by hepatic lipocytes only upon activation in primary culture. Alcohol Alcohol 1994; 29: 605-610.
7. De Bleser PJ, Xu G, Rombouts K, Rogiers V, Geerts A. Glutathione levels discriminate between oxidative stress and transforming growth factor-beta signaling in activated rat hepatic stellate cells. J Biol Chem 1999; 274: 33881-33887.
8. Babior BM, Lambeth JD, Nauseef W. The neutrophil NADPH oxidase. Arch Biochem Biophys 2002; 397: 342-344.
9. Leto TL, Morand S, Hurt D, Ueyama T. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid Redox Signal 2009; 11: 2607-2619.
10. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007; 87: 245-313.
11. Banfi B, Clark RA, Steger K, Krause KH. Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J Biol Chem 2003; 278: 3510-3513.
12. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, et al. Cell transformation by the superoxide-generating oxidase Mox1. Nature 1999; 401: 79-82.
13. 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.
14. De Minicis S, Seki E, Oesterreicher C, Schnabl B, Schwabe RF, Brenner DA. Reduced nicotinamide adenine dinucleotide phosphate oxidase mediates fibrotic and inflammatory effects of leptin on hepatic stellate cells. HEPATOLOGY 2008; 48: 2016-2026.
15. Marden JJ, Harraz MM, Williams AJ, Nelson K, Luo M, Paulson H, et al. Redox modifier genes in amyotrophic lateral sclerosis in mice. J Clin Invest 2007; 117: 2913-2919.
16. Gavazzi G, Banfi B, Deffert C, Fiette L, Schappi M, Herrmann F, et al. Decreased blood pressure in NOX1-deficient mice. FEBS Lett 2006; 580: 497-504.
17. Uchinami H, Seki E, Brenner DA, D'Armiento J. Loss of MMP 13 attenuates murine hepatic injury and fibrosis during cholestasis. HEPATOLOGY 2006; 44: 420-429.
18. Kisseleva T, Uchinami H, Feirt N, Quintana-Bustamante O, Segovia JC, Schwabe RF, et al. Bone marrow-derived fibrocytes participate in pathogenesis of liver fibrosis. J Hepatol 2006; 45: 429-438.
19. Seki E, De Minicis S, Osterreicher CH, Kluwe J, Osawa Y, Brenner DA, et al. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 2007; 13: 1324-1332.
20. Seki E, De Minicis S, Gwak GY, Kluwe J, Inokuchi S, Bursill CA, et al. CCR1 and CCR5 promote hepatic fibrosis in mice. J Clin Invest 2009; 119: 1858-1870.
21. Kodama Y, Kisseleva T, Iwaisako K, Miura K, Taura K, De Minicis S, et al. c-Jun N-terminal kinase-1 from hematopoietic cells mediates progression from hepatic steatosis to steatohepatitis and fibrosis in mice. Gastroenterology 2009; 137: 1467-1477.
22. Paik YH, Kim JK, Lee JI, Kang SH, Kim DY, An SH, et al. Celecoxib induces hepatic stellate cell apoptosis through inhibition of Akt activation and suppresses hepatic fibrosis in rats. Gut 2009; 58: 1517-1527.
23. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351-358.
24. Taura K, De Minicis S, Seki E, Hatano E, Iwaisako K, Osterreicher CH, et al. Hepatic stellate cells secrete angiopoietin 1 that induces angiogenesis in liver fibrosis. Gastroenterology 2008; 135: 1729-1738.
25. Aram G, Potter JJ, Liu X, Wang L, Torbenson MS, Mezey E. Deficiency of nicotinamide adenine dinucleotide phosphate, reduced form oxidase enhances hepatocellular injury but attenuates fibrosis after chronic carbon tetrachloride administration. HEPATOLOGY 2009; 49: 911-919.
26. De Minicis S, Seki E, Paik YH, Osterreicher CH, Kodama Y, Kluwe J, et al. Role and cellular source of nicotinamide adenine dinucleotide phosphate oxidase in hepatic fibrosis. HEPATOLOGY 2010; 52: 1420-1430.
27. Jiang JX, Venugopal S, Serizawa N, Chen X, Scott F, Li Y, et al. Reduced nicotinamide adenine dinucleotide phosphate oxidase 2 plays a key role in stellate cell activation and liver fibrogenesis in vivo. Gastroenterology 2010; 139: 1375-1384.
28. 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.
29. Vinas O, Bataller R, Sancho-Bru P, Gines P, Berenguer C, Enrich C, et al. Human hepatic stellate cells show features of antigen-presenting cells and stimulate lymphocyte proliferation. HEPATOLOGY 2003; 38: 919-929.
30. Zhan SS, Jiang JX, Wu J, Halsted C, Friedman SL, Zern MA, et al. Phagocytosis of apoptotic bodies by hepatic stellate cells induces NADPH oxidase and is associated with liver fibrosis in vivo. HEPATOLOGY 2006; 43: 435-443.
31. Geiszt M, Lekstrom K, Brenner S, Hewitt SM, Dana R, Malech HL, et al. NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J Immunol 2003; 171: 299-306.
32. Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, et al. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest 2001; 108: 1513-1522.
33. Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, et al. Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res 2001; 88: 888-894.
34. Rodrigues CM, Fan G, Wong PY, Kren BT, Steer CJ. Ursodeoxycholic acid may inhibit deoxycholic acid-induced apoptosis by modulating mitochondrial transmembrane potential and reactive oxygen species production. Mol Med 1998; 4: 165-178.
35. Jackson SH, Devadas S, Kwon J, Pinto LA, Williams MS. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol 2004; 5: 818-827.
36. Cadenas E. Biochemistry of oxygen toxicity. Annu Rev Biochem 1989; 58: 79-110.
37. Reth M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol 2002; 3: 1129-1134.
38. Novo E, Marra F, Zamara E, Valfre di Bonzo L, Caligiuri A, Cannito S, et al. Dose dependent and divergent effects of superoxide anion on cell death, proliferation, and migration of activated human hepatic stellate cells. Gut 2006; 55: 90-97.