Therapeutic targeting of GSK3β enhances the Nrf2 antioxidant response and confers hepatic cytoprotection in hepatitis C

Gut

Volumn 64, Issue 1, 2015, Pages 168-179

  Jiang, Yongfang ^a,b   Bao, Hui ^b   Ge, Yan ^b   Tang, Wei ^a   Cheng, Du ^a   Luo, Kaizhong ^a   Gong, Guozhong ^a   Gong, Rujun ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CARBONATE; LITHIUM CHLORIDE; OXYGENASE; OXYGENASE 1; PHOSPHOPROTEIN PHOSPHATASE 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTIOXIDANT; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; NFE2L2 PROTEIN, HUMAN;

ADULT; AGED; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROTECTION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; FEMALE; HEPATITIS C; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER BIOPSY; LIVER CELL; LIVER INJURY; LIVER PROTECTION; MALE; MENTAL DISEASE; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; HEPATITIS C, CHRONIC; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANTIOXIDANTS; CELLS, CULTURED; CYTOPROTECTION; GLYCOGEN SYNTHASE KINASE 3; HEPATITIS C, CHRONIC; HEPATOCYTES; HUMANS; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION;

EID: 84919778896     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2013-306043     Document Type: Article

References (43)

1. Hoofnagle JH Course and outcome of hepatitis C. Hepatology 2002; 36:S21-9.
2. Tanikawa K, Torimura T. Studies on oxidative stress in liver diseases: important future trends in liver research. Med Mol Morphol 2006; 39: 22-7.
3. Clement S, Pascarella S, Negro F. Hepatitis C virus infection: molecular pathways to steatosis, insulin resistance and oxidative stress. Viruses 2009; 1: 126-43.
4. Gong G, Waris G, Tanveer R, et al. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kappa B. Proc Natl Acad Sci USA 2001; 98: 9599-604.
5. de Mochel NS, Seronello S, Wang SH, et al. Hepatocyte NAD(P)H oxidases as an endogenous source of reactive oxygen species during hepatitis C virus infection. Hepatology 2010; 52: 47-59.
6. Santos CX, Tanaka LY, Wosniak J, et al. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal 2009; 11: 2409-27.
7. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 2004; 10: 549-57.
8. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem 1991; 266: 11632-9.
9. Jaiswal AK Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 2004; 36: 1199-207.
10. Chan K, Lu R, Chang JC, et al. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci USA 1996; 93: 13943-8.
11. Alam J, Stewart D, Touchard C, et al. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999; 274: 26071-8.
12. Carvajal-Yepes M, Himmelsbach K, Schaedler S, et al. Hepatitis C virus impairs the induction of cytoprotective Nrf2 target genes by delocalization of small Maf proteins. J Biol Chem 2011; 286: 8941-51.
13. Ivanov AV, Smirnova OA, Ivanova ON, et al. Hepatitis C virus proteins activate NRF2/ARE pathway by distinct ROS-dependent and independent mechanisms in HUH7 cells. PLoS ONE 2011; 6:e24957.
14. Burdette D, Olivarez M, Waris G. Activation of transcription factor Nrf2 by hepatitis C virus induces the cell-survival pathway. J Gen Virol 2010; 91: 681-90.
15. Kurzawski M, Dziedziejko V, Urasinska E, et al. Nuclear factor erythroid 2-like 2 (Nrf2) expression in end-stage liver disease. Environ Toxicol Pharmacol 2012; 34: 87-95.
16. Cohen P, Frame S. The renaissance of GSK3. Nat Rev Mol Cell Biol 2001; 2: 769-76.
17. Jain AK, Jaiswal AK. GSK-3beta acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J Biol Chem 2007; 282: 16502-10.
18. Rada P, Rojo AI, Evrard-Todeschi N, et al. Structural and functional characterization of Nrf2 degradation by the glycogen synthase kinase 3/beta-TrCP axis. Mol Cell Biol 2012; 32: 3486-99.
19. Rada P, Rojo AI, Chowdhry S, et al. SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 2011; 31: 1121-33.
20. Tomobe K, Shinozuka T, Kuroiwa M, et al. Age-related changes of Nrf2 and phosphorylated GSK-3beta in a mouse model of accelerated aging (SAMP8). Arch Gerontol Geriatr 2012; 54:e1-7.
21. Bitar MS, Al-Mulla F. A defect in Nrf2 signaling constitutes a mechanism for cellular stress hypersensitivity in a genetic rat model of type 2 diabetes. Am J Physiol Endocrinol Metab 2011; 301:E1119-29.
22. Kay HY, Kim YW, Ryu da H, et al. Nrf2-mediated liver protection by sauchinone, an antioxidant lignan, from acetaminophen toxicity through the PKCdelta-GSK3beta pathway. Br J Pharmacol 2011; 163: 1653-65.
23. Espada S, Rojo AI, Salinas M, et al. The muscarinic M1 receptor activates Nrf2 through a signaling cascade that involves protein kinase C and inhibition of GSK-3beta: connecting neurotransmission with neuroprotection. J Neurochem 2009; 110: 1107-19.
24. Correa F, Mallard C, Nilsson M, et al. Activated microglia decrease histone acetylation and Nrf2-inducible anti-oxidant defence in astrocytes: restoring effects of inhibitors of HDACs, p38 MAPK and GSK3beta. Neurobiol Dis 2011; 44: 142-51.
25. Rojo AI, Rada P, Egea J, et al. Functional interference between glycogen synthase kinase-3 beta and the transcription factor Nrf2 in protection against kainate-induced hippocampal cell death. Mol Cell Neurosci 2008; 39: 125-32.
26. Muller-Oerlinghausen B, Berghofer A, Ahrens B. The antisuicidal and mortality-reducing effect of lithium prophylaxis: consequences for guidelines in clinical psychiatry. Can J Psychiatry 2003; 48: 433-9.
27. Moradpour D, Evans MJ, Gosert R, et al. Insertion of green fluorescent protein into nonstructural protein 5A allows direct visualization of functional hepatitis C virus replication complexes. J Virol 2004; 78: 7400-9.
28. Kato T, Date T, Miyamoto M, et al. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 2003; 125: 1808-17.
29. Kato T, Furusaka A, Miyamoto M, et al. Sequence analysis of hepatitis C virus isolated from a fulminant hepatitis patient. J Med Virol 2001; 64: 334-9.
30. Rojo AI, Sagarra MR, Cuadrado A. GSK-3beta down-regulates the transcription factor Nrf2 after oxidant damage: relevance to exposure of neuronal cells to oxidative stress. J Neurochem 2008; 105: 192-202.
31. Gong R, Ge Y, Chen S, et al. Glycogen synthase kinase 3beta: a novel marker and modulator of inflammatory injury in chronic renal allograft disease. Am J Transplant 2008; 8: 1852-63.
32. Salazar M, Rojo AI, Velasco D, et al. Glycogen synthase kinase-3beta inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2. J Biol Chem 2006; 281: 14841-51.
33. Niture SK, Jain AK, Shelton PM, et al. Src subfamily kinases regulate nuclear export and degradation of transcription factor Nrf2 to switch off Nrf2-mediated antioxidant activation of cytoprotective gene expression. J Biol Chem 2011; 286: 28821-32.
34. Di Bona D, Cippitelli M, Fionda C, et al. Oxidative stress inhibits IFN-alpha-induced antiviral gene expression by blocking the JAK-STAT pathway. J Hepatol 2006; 45: 271-9.
35. Nishina S, Hino K, Korenaga M, et al. Hepatitis C virus-induced reactive oxygen species raise hepatic iron level in mice by reducing hepcidin transcription. Gastroenterology 2008; 134: 226-38.
36. Street A, Macdonald A, McCormick C, et al. Hepatitis C virus NS5A-mediated activation of phosphoinositide 3-kinase results in stabilization of cellular beta-catenin and stimulation of beta-catenin-responsive transcription. J Virol 2005; 79: 5006-16.
37. Michaeloudes C, Sukkar MB, Khorasani NM, et al. TGF-beta regulates Nox4, MnSOD and catalase expression, and IL-6 release in airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2011; 300:L295-304.
38. Gruppuso PA, Mikumo R, Brautigan DL, et al. Growth arrest induced by transforming growth factor beta 1 is accompanied by protein phosphatase activation in human keratinocytes. J Biol Chem 1991; 266: 3444-8.
39. King TD, Gandy JC, Bijur GN. The protein phosphatase-1/inhibitor-2 complex differentially regulates GSK3 dephosphorylation and increases sarcoplasmic/endoplasmic reticulum calcium ATPase 2 levels. Exp Cell Res 2006; 312: 3693-700.
40. Xu J, Culman J, Blume A, et al. Chronic treatment with a low dose of lithium protects the brain against ischemic injury by reducing apoptotic death. Stroke 2003; 34: 1287-92.
41. Petrini M, Azzara A. Lithium in the treatment of neutropenia. Curr Opin Hematol 2012; 19: 52-7.
42. Nieper HA The clinical applications of lithium orotate. A two years study. Agressologie 1973; 14: 407-11.
43. Sartori HE Lithium orotate in the treatment of alcoholism and related conditions. Alcohol 1986; 3: 97-100.