NF-κB/RelA and Nrf2 cooperate to maintain hepatocyte integrity and to prevent development of hepatocellular adenoma

Journal of Hepatology

Volumn 64, Issue 1, 2016, Pages 94-102

  Köhler, Ulrike A ^a   Böhm, Friederike ^b   Rolfs, Frank ^a   Egger, Michèle ^b   Hornemann, Thorsten ^c   Pasparakis, Manolis ^d   Weber, Achim ^b   Werner, Sabine ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Hepatocellular adenoma; Inflammation; Liver fibrosis; NF B; Nrf2

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CD3 ANTIGEN; CYTOKERATIN ANTIBODY; DEHYDROGENASE QUINONE 1 PROTEIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE TRANSFERASE A2; LY6G PROTEIN; PROTEIN; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NFE2L2 PROTEIN, MOUSE; RELA PROTEIN, MOUSE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOTTING; CELL PROTECTION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GENOTYPE; HEPATITIS; HEPATOCELLULAR ADENOMA; HISTOPATHOLOGY; HOMEOSTASIS; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; LIVER ADENOMA; LIVER CELL; LIVER FIBROSIS; LIVER HOMEOSTASIS; MOUSE; NONHUMAN; OXYBLOT ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ADENOMA; ANIMAL; HUMAN; LIVER NEOPLASMS; METABOLISM; PHYSIOLOGY;

ADENOMA; ANIMALS; FEMALE; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; MICE; NF-E2-RELATED FACTOR 2; NF-KAPPA B; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTOR RELA;

EID: 84953297386     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2015.08.033     Document Type: Article

References (42)

1. R.F. Schwabe, and D.A. Brenner Mechanisms of liver injury. I. TNF-alpha-induced liver injury: role of IKK, JNK, and ROS pathways Am J Physiol Gastrointest Liver Physiol 290 2006 G583 G589
2. T. Luedde, N. Beraza, V. Kotsikoris, G. van Loo, A. Nenci, R. De Vos, and et al. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma Cancer Cell 11 2007 119 132
3. J. Choi, N.L. Corder, B. Koduru, and Y. Wang Oxidative stress and hepatic Nox proteins in chronic hepatitis C and hepatocellular carcinoma Free Radic Biol Med 72 2014 267 284
4. G.P. Sykiotis, and D. Bohmann Stress-activated Cap'n'Collar transcription factors in aging and human disease Sci Signal 3 2010 re3
5. S.M. Shin, J.H. Yang, and S.H. Ki Role of the Nrf2-ARE pathway in liver diseases Oxid Med Cell Longev 2013 2013 763257
6. L.M. Aleksunes, and J.E. Manautou Emerging role of Nrf2 in protecting against hepatic and gastrointestinal disease Toxicol Pathol 35 2007 459 473
7. T.A. Beyer, W. Xu, D. Teupser, U. auf dem Keller, P. Bugnon, E. Hildt, and et al. Impaired liver regeneration in Nrf2 knockout mice. Role of ROS-mediated insulin/IGF-1 resistance EMBO J 27 2008 212 223
8. N. Wakabayashi, S. Shin, S.L. Slocum, E.S. Agoston, J. Wakabayashi, M.-K. Kwak, and et al. Regulation of Notch1 signaling by Nrf2: implications for tissue regeneration Sci Signal 3 2010 ra52
9. W. Xu, C. Hellerbrand, U. Köhler, P. Bugnon, Y. Kan, S. Werner, and et al. The Nrf2 transcription factor protects from toxin-induced liver injury and fibrosis Lab Invest 88 2008 1068 1078
10. R. Schreck, P. Rieber, and P.A. Baeuerle Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and hiv-1 EMBO J 10 1991 2247 2258
11. M.L. Chaisson, J.T. Brooling, W. Ladiges, S. Tsai, and N. Fausto Hepatocyte-specific inhibition of NF-kappaB leads to apoptosis after TNF treatment, but not after partial hepatectomy J Clin Invest 110 2002 193 202
12. Y. Iimuro, T. Nishiura, C. Hellerbrand, K.E. Behrns, R. Schoonhoven, J.W. Grisham, and et al. NFkappaB prevents apoptosis and liver dysfunction during liver regeneration J Clin Invest 101 1998 802 811
13. T. Luedde, J. Heinrichsdorff, R. de Lorenzi, R. de Vos, T. Roskams, and M. Pasparakis IKK1 and IKK2 cooperate to maintain bile duct integrity in the liver PNAS 105 2008 9733 9738
14. S.G. Pereira, and F. Oakley Nuclear factor-kappaB1: regulation and function Int J Biochem Cell Biol 40 2008 1425 1430
15. F. Geisler, H. Algül, S. Paxian, and R.M. Schmid Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to tnf-induced apoptosis in vivo and in vitro Gastroenterology 132 2007 2489 2503
16. Y.-S. Keum, Y.-H. Han, C. Liew, J.-H. Kim, C. Xu, X. Yuan, and et al. Induction of heme oxygenase-1 (HO-1) and NAD[P]H: Quinone oxidoreductase 1 (NQO1) by a phenolic antioxidant, butylated hydroxyanisole (BHA) and its metabolite, tert-butylhydroquinone (tBHQ) in primary-cultured human and rat hepatocytes Pharm Res 23 2006 2586 2594
17. X. Yuan, C. Xu, Z. Pan, Y.-S. Keum, J.-H. Kim, G. Shen, and et al. Butylated hydroxyanisole regulates are-mediated gene expression via Nrf2 coupled with Erk and Jnk signaling pathway in HepG2 cells Mol Carcinog 45 2006 841 850
18. K. Chan, R. Lu, J.C. Chang, and Y.W. Kan Nrf2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development Proc Natl Acad Sci U S A 93 1996 13943 13948
19. P. Chomczynski, and N. Sacchi Single-step method of RNAa isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal Biochem 162 1987 156 159
20. H. Koegel, L. von Tobel, M. Schäfer, S. Albert, E. Kremmer, C. Mauch, and et al. Loss of serum response factor in keratinocytes results in hyperproliferative skin disease in mice J Clin Invest 119 2009 899 910
21. K. Hensley Detection of protein carbonyls by means of biotin hydrazide-streptavidin affinity methods Methods Mol Biol 536 2009 457 462
22. P. Bioulac-Sage, C. Balabaud, and J. Zucman-Rossi Focal nodular hyperplasia, hepatocellular adenomas: past, present, future Gastroenterol Clin Biol 34 2010 355 358
23. P. Bioulac-Sage, G. Cubel, C. Balabaud, and J. Zucman-Rossi Revisiting the pathology of resected benign hepatocellular nodules using new immunohistochemical markers Semin Liver Dis 31 2011 91 103
24. W.-S. Jeong, I.-W. Kim, and R. Hu Kong A-NT. Modulatory properties of various natural chemopreventive agents on the activation of NF-kappaB signaling pathway Pharm Res 21 2004 661 670
25. K. Reyes-Gordillo, J. Segovia, M. Shibayama, P. Vergara, M.G. Moreno, and P. Muriel Curcumin protects against acute liver damage in the rat by inhibiting NF-kappaB, proinflammatory cytokines production and oxidative stress Biochim Biophys Acta 1770 2007 989 996
26. C. Xu, G. Shen, C. Chen, C. Gélinas, and A.-N. Kong Suppression of NF-kappaB and NF-kappaB-regulated gene expression by sulforaphane and PEITC through ikappabalpha, IKK pathway in human prostate cancer PC-3 cells Oncogene 24 2005 4486 4495
27. W. Li, T.O. Khor, C. Xu, G. Shen, W.-S. Jeong, S. Yu, and et al. Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis Biochem Pharmacol 76 2008 1485 1489
28. S.D. Catz, and J.L. Johnson Transcriptional regulation of Bcl-2 by nuclear factor kappa B and its significance in prostate cancer Oncogene 20 2001 7342 7351
29. S. Kreuz, D. Siegmund, P. Scheurich, and H. Wajant NF-kappaB inducers upregulate cFlip, a cycloheximide-sensitive inhibitor of death receptor signaling Mol Cell Biol 21 2001 3964 3973
30. H.H. Lee, H. Dadgostar, Q. Cheng, J. Shu, and G. Cheng NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/a1 is required for CD40 survival signaling in B lymphocytes Proc Natl Acad Sci U S A 96 1999 9136 9141
31. C. Stehlik, R. de Martin, B.R. Binder, and J. Lipp Cytokine induced expression of porcine inhibitor of apoptosis protein (IAP) family member is regulated by NF-kappa B Biochem Biophys Res Commun 243 1998 827 832
32. C. Stehlik, R. de Martin, I. Kumabashiri, J.A. Schmid, B.R. Binder, and J. Lipp Nuclear factor (NF)-kappaB-regulated X-chromosome-linked IAP gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis J Exp Med 188 1998 211 216
33. M. You, P.T. Ku, R. Hrdlicková, and H.R. Bose Ch-IAP1, a member of the inhibitor-of-apoptosis protein family, is a mediator of the antiapoptotic activity of the v-rel oncoprotein Mol Cell Biol 17 1997 7328 7341
34. N. Morito, K. Yoh, K. Itoh, A. Hirayama, A. Koyama, M. Yamamoto, and et al. Nrf2 regulates the sensitivity of death receptor signals by affecting intracellular glutathione levels Oncogene 22 2003 9275 9281
35. H. Bühler, M. Pirovino, A. Akobiantz, J. Altorfer, M. Weitzel, E. Maranta, and et al. Regression of liver cell adenoma. A follow-up study of three consecutive patients after discontinuation of oral contraceptive use Gastroenterology 82 1982 775 782
36. P. Bioulac-Sage, J.F. Blanc, S. Rebouissou, C. Balabaud, and J. Zucman-Rossi Genotype phenotype classification of hepatocellular adenoma World J Gastroenterol 13 2007 2649 2654
37. P. Bioulac-Sage, H. Laumonier, C. Laurent, J. Zucman-Rossi, and C. Balabaud Hepatocellular adenoma: what is new in 2008 Hepatol Int 2 2008 316 321
38. S. Rebouissou, M. Amessou, G. Couchy, K. Poussin, S. Imbeaud, C. Pilati, and et al. Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumors Nature 457 2009 200 204
39. M.M. Spannbauer, and C. Trautwein Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumors Hepatology 49 2009 1387 1389
40. C. Pilati, E. Letouzé, J.C. Nault, S. Imbeaud, A. Boulai, J. Calderaro, and et al. Genomic profiling of hepatocellular adenomas reveals recurrent FRK-activating mutations and the mechanisms of malignant transformation Cancer Cell 25 2014 428 441
41. E. Schutyser, S. Struyf, and J. Van Damme The cc chemokine CC0L20 and its receptor CCR6 Cytokine Growth Factor Rev 14 2003 409 426
42. J. Zucman-Rossi, E. Jeannot, J.T.V. Nhieu, J.-Y. Scoazec, C. Guettier, S. Rebouissou, and et al. Genotype-phenotype correlation in hepatocellular adenoma: new classification and relationship with HCC Hepatology 43 2006 515 524