Hepatocyte nicotinamide adenine dinucleotide phosphate reduced oxidase 4 regulates stress signaling, fibrosis, and insulin sensitivity during development of steatohepatitis in mice

Gastroenterology

Volumn 149, Issue 2, 2015, Pages 468-480.e10

  Bettaieb, Ahmed ^a   Jiang, Joy X ^b   Sasaki, Yu ^b   Chao, Tzu I ^b   Kiss, Zsofia ^b   Chen, Xiangling ^b   Tian, Jijing ^b   Katsuyama, Masato ^c   Yabe Nishimura, Chihiro ^c   Xi, Yannan ^a   Szyndralewiez, Cedric ^d   Schröder, Kathrin ^e   Shah, Ajay ^f   Brandes, Ralph P ^e   Haj, Fawaz G ^a   Török, Natalie J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^d GENKYOTEX SA   (Switzerland)

^e GOETHE UNIVERSITY   (Germany)

^f KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Inflammation; Mouse Model; Obesity; Stress Signaling

Indexed keywords

AMINO ACID; CORN SYRUP; GKT 137831; MITOGEN ACTIVATED PROTEIN KINASE; OXIDOREDUCTASE INHIBITOR; PHOSPHATASE; PROTEIN KINASE R; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; UNCLASSIFIED DRUG; 2 (2 CHLOROPHENYL) 4 [3 (DIMETHYLAMINO)PHENYL] 5 METHYL 1H PYRAZOLO[4,3 C]PYRIDINE 3,6(2H,5H) DIONE; BIOLOGICAL MARKER; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NOX4 PROTEIN, HUMAN; PHOSPHOPROTEIN PHOSPHATASE 1; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR STRESS SIGNAL; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME PHOSPHORYLATION; FAST FOOD; FATTY LIVER; GENE DELETION; HEPATITIS; HUMAN; HUMAN TISSUE; HYPERINSULINEMIA; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INSULIN SENSITIVITY; LIPID PEROXIDATION; LIVER; LIVER BIOPSY; LIVER CELL; LIVER FIBROSIS; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; VITAMIN DEFICIENCY; ANIMAL; BIOPSY; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DIET; DISEASE MODEL; DRUG EFFECTS; GENETICS; INSULIN RESISTANCE; KNOCKOUT MOUSE; LIVER CIRRHOSIS; METABOLISM; OBESITY; PATHOLOGY; PHYSIOLOGICAL STRESS; PROCEDURES;

ANIMALS; BIOMARKERS; BIOPSY; DIET; DISEASE MODELS, ANIMAL; FATTY LIVER; HEPATOCYTES; HUMANS; INSULIN RESISTANCE; LIPID PEROXIDATION; LIVER; LIVER CIRRHOSIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADP; NADPH OXIDASE; OBESITY; OXIDATIVE STRESS; PROTEIN PHOSPHATASE 1; PYRAZOLES; PYRIDINES; STRESS, PHYSIOLOGICAL;

EID: 84938093088     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2015.04.009     Document Type: Article

References (55)

1. B.N. Bohinc, and A.M. Diehl Mechanisms of disease progression in NASH: new paradigms Clin Liver Dis 16 2012 549 565
2. H.C. Masuoka, and N. Chalasani Nonalcoholic fatty liver disease: an emerging threat to obese and diabetic individuals Ann N Y Acad Sci 1281 2013 106 122
3. A.E. Feldstein, and S.M. Bailey Emerging role of redox dysregulation in alcoholic and nonalcoholic fatty liver disease Antioxid Redox Signal 15 2011 421 424
4. K. Bedard, and K.H. Krause The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology Physiol Rev 87 2007 245 313
5. S. Altenhofer, P.W. Kleikers, K.A. Radermacher, and et al. The NOX toolbox: validating the role of NADPH oxidases in physiology and disease Cell Mol Life Sci 69 2012 2327 2343
6. M. Zhang, A. Perino, A. Ghigo, and et al. NADPH oxidases in heart failure: poachers or gamekeepers? Antioxid Redox Signal 18 2013 1024 1041
7. Y. Gorin, and K. Block Nox as a target for diabetic complications Clin Sci (Lond) 125 2013 361 382
8. Y. Gorin, and K. Block Nox4 and diabetic nephropathy: with a friend like this, who needs enemies? Free Radic Biol Med 61C 2013 130 142
9. N.S. de Mochel, S. Seronello, S.H. Wang, and et al. Hepatocyte NAD(P)H oxidases as an endogenous source of reactive oxygen species during hepatitis C virus infection Hepatology 52 2010 47 59
10. J.X. Jiang, X. Chen, N. Serizawa, and et al. Liver fibrosis and hepatocyte apoptosis are attenuated by GKT137831, a novel NOX4/NOX1 inhibitor in vivo Free Radic Biol Med 53 2012 289 296
11. P. Sancho, J. Mainez, E. Crosas-Molist, and et al. NADPH oxidase NOX4 mediates stellate cell activation and hepatocyte cell death during liver fibrosis development PLoS One 7 2012 e45285
12. Y.H. Paik, K. Iwaisako, E. Seki, and et al. The nicotinamide adenine dinucleotide phosphate oxidase (NOX) homologues NOX1 and NOX2/gp91(phox) mediate hepatic fibrosis in mice Hepatology 53 2011 1730 1741
13. H. Nishitoh CHOP is a multifunctional transcription factor in the ER stress response J Biochem 151 2012 217 219
14. C. Brenner, L. Galluzzi, O. Kepp, and et al. Decoding cell death signals in liver inflammation J Hepatol 59 2013 583 594
15. H. Malhi, and R.J. Kaufman Endoplasmic reticulum stress in liver disease J Hepatol 54 2011 795 809
16. B.R. Williams PKR; a sentinel kinase for cellular stress Oncogene 18 1999 6112 6120
17. G. Li, C. Scull, L. Ozcan, and et al. NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis J Cell Biol 191 2010 1113 1125
18. A. Higa, and E. Chevet Redox signaling loops in the unfolded protein response Cell Signal 24 2012 1548 1555
19. M.A. Carvalho-Filho, B.M. Carvalho, A.G. Oliveira, and et al. Double-stranded RNA-activated protein kinase is a key modulator of insulin sensitivity in physiological conditions and in obesity in mice Endocrinology 153 2012 5261 5274
20. T. Nakamura, A. Arduini, B. Baccaro, and et al. Small-molecule inhibitors of PKR improve glucose homeostasis in obese diabetic mice Diabetes 63 2014 526 534
21. N. Anilkumar, R. Weber, M. Zhang, and et al. Nox4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation Arterioscler Thromb Vasc Biol 28 2008 1347 1354
22. V. Medici, M.R. Ali, S. Seo, and et al. Increased soluble leptin receptor levels in morbidly obese patients with insulin resistance and nonalcoholic fatty liver disease Obesity (Silver Spring) 18 2010 2268 2273
23. J.D. Lambeth NOX enzymes and the biology of reactive oxygen Nat Rev Immunol 4 2004 181 189
24. M. Charlton, A. Krishnan, K. Viker, and et al. Fast food diet mouse: novel small animal model of NASH with ballooning, progressive fibrosis, and high physiological fidelity to the human condition Am J Physiol Gastrointest Liver Physiol 301 2011 G825 G834
25. K. Miura, Y. Kodama, S. Inokuchi, and et al. Toll-like receptor 9 promotes steatohepatitis by induction of interleukin-1beta in mice Gastroenterology 139 2010 323 334 e7
26. Y. Kodama, T. Kisseleva, K. Iwaisako, and et al. c-Jun N-terminal kinase-1 from hematopoietic cells mediates progression from hepatic steatosis to steatohepatitis and fibrosis in mice Gastroenterology 137 2009 1467 1477 e5
27. S.H. Ibrahim, R. Kohli, and G.J. Gores Mechanisms of lipotoxicity in NAFLD and clinical implications J Pediatr Gastroenterol Nutr 53 2011 131 140
28. S.H. Ibrahim, G.J. Gores, P. Hirsova, and et al. Mixed lineage kinase 3 deficient mice are protected against the high fat high carbohydrate diet-induced steatohepatitis Liver Int 34 2014 427 437
29. T. Aoyama, Y.H. Paik, S. Watanabe, and et al. Nicotinamide adenine dinucleotide phosphate oxidase in experimental liver fibrosis: GKT137831 as a novel potential therapeutic agent Hepatology 56 2012 2316 2327
30. R.F. Schwabe, H. Uchinami, T. Qian, and et al. Differential requirement for c-Jun NH2-terminal kinase in TNFalpha- and Fas-mediated apoptosis in hepatocytes FASEB J 18 2004 720 722
31. P. Peidis, A.I. Papadakis, H. Muaddi, and et al. Doxorubicin bypasses the cytoprotective effects of eIF2alpha phosphorylation and promotes PKR-mediated cell death Cell Death Differ 18 2011 145 154
32. B.R. Williams Signal integration via PKR Sci STKE 2001 2001 re2
33. G. Bai, T.D. Hock, N. Logsdon, and et al. A far-upstream AP-1/Smad binding box regulates human NOX4 promoter activation by transforming growth factor-beta Gene 540 2014 62 67
34. N.V. Jammi, and P.A. Beal Phosphorylation of the RNA-dependent protein kinase regulates its RNA-binding activity Nucleic Acids Res 29 2001 3020 3029
35. I. Ben Mosbah, I. Alfany-Fernandez, C. Martel, and et al. Endoplasmic reticulum stress inhibition protects steatotic and non-steatotic livers in partial hepatectomy under ischemia-reperfusion Cell Death Dis 1 2010 e52
36. S.S. Cao, and R.J. Kaufman Targeting endoplasmic reticulum stress in metabolic disease Expert Opin Ther Targets 17 2013 437 448
37. Y. Sumida, E. Niki, Y. Naito, and et al. Involvement of free radicals and oxidative stress in NAFLD/NASH Free Radic Res 47 2013 869 880
38. S.K. Mantena, A.L. King, K.K. Andringa, and et al. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol- and obesity-induced fatty liver diseases Free Radic Biol Med 44 2008 1259 1272
39. J.X. Jiang, S. Venugopal, N. Serizawa, and et al. Reduced nicotinamide adenine dinucleotide phosphate oxidase 2 plays a key role in stellate cell activation and liver fibrogenesis in vivo Gastroenterology 139 2010 1375 1384
40. J.X. Jiang, X. Chen, H. Fukada, and et al. Advanced glycation endproducts induce fibrogenic activity in nonalcoholic steatohepatitis by modulating TNF-alpha-converting enzyme activity in mice Hepatology 58 2013 1339 1348
41. J.X. Jiang, K. Mikami, S. Venugopal, and et al. Apoptotic body engulfment by hepatic stellate cells promotes their survival by the JAK/STAT and Akt/NF-kappaB-dependent pathways J Hepatol 51 2009 139 148
42. I. Carmona-Cuenca, C. Roncero, P. Sancho, and et al. Upregulation of the NADPH oxidase NOX4 by TGF-beta in hepatocytes is required for its pro-apoptotic activity J Hepatol 49 2008 965 976
43. J. Jou, S.S. Choi, and A.M. Diehl Mechanisms of disease progression in nonalcoholic fatty liver disease Semin Liver Dis 28 2008 370 379
44. W.K. Syn, S.S. Choi, and A.M. Diehl Apoptosis and cytokines in non-alcoholic steatohepatitis Clin Liver Dis 13 2009 565 580
45. M.E. Guicciardi, and G.J. Gores Apoptosis as a mechanism for liver disease progression Semin Liver Dis 30 2010 402 410
46. J.A. Marchal, G.J. Lopez, M. Peran, and et al. The impact of PKR activation: from neurodegeneration to cancer FASEB J 28 2014 1965 1974
47. H. Wang, X. Xu, J. Fassett, and et al. Double-stranded RNA-dependent protein kinase deficiency protects the heart from systolic overload-induced congestive heart failure Circulation 129 2014 1397 1406
48. C. Tronel, G. Page, S. Bodard, and et al. The specific PKR inhibitor C16 prevents apoptosis and IL-1beta production in an acute excitotoxic rat model with a neuroinflammatory component Neurochem Int 64 2014 73 83
49. B. Lu, T. Nakamura, K. Inouye, and et al. Novel role of PKR in inflammasome activation and HMGB1 release Nature 488 2012 670 674
50. F.G. Haj, J.M. Zabolotny, Y.B. Kim, and et al. Liver-specific protein-tyrosine phosphatase 1B (PTP1B) re-expression alters glucose homeostasis of PTP1B-/-mice J Biol Chem 280 2005 15038 15046
51. K. Mahadev, H. Motoshima, X. Wu, and et al. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction Mol Cell Biol 24 2004 1844 1854
52. T. Tiganis PTP1B and TCPTP - nonredundant phosphatases in insulin signaling and glucose homeostasis FEBS J 280 2013 445 458
53. M. Subichin, J. Clanton, M. Makuszewski, and et al. Liver disease in the morbidly obese: a review of 1000 consecutive patients undergoing weight loss surgery Surg Obes Relat Dis 11 2015 137 141
54. P. Sukumar, H. Viswambharan, H. Imrie, and et al. Nox2 NADPH oxidase has a critical role in insulin resistance-related endothelial cell dysfunction Diabetes 62 2013 2130 2134
55. C. Langhi, and A. Baldan CIDEC/FSP27 is regulated by peroxisome proliferator-activated receptor alpha and plays a critical role in fasting- and diet-induced hepatosteatosis Hepatology 61 2015 1227 1238