AICAR induces Nrf2 activation by an AMPK-independent mechanism in hepatocarcinoma cells

Biochemical Pharmacology

Volumn 91, Issue 2, 2014, Pages 168-180

  Sid, Brice ^a   Glorieux, Christophe ^a   Valenzuela, Manuel ^a,d   Rommelaere, Guillaume ^b   Najimi, Mustapha ^a   Dejeans, Nicolas ^a,e   Renard, Patricia ^b   Verrax, Julien ^a   Calderon, Pedro Buc ^a,c  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b University of Namur   (Belgium)

^c UNIVERSIDAD ARTURO PRAT   (Chile)

^d UNIVERSITY OF CHILE   (Chile)

^e UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

AICAR; AMPK; Hepatocarcinoma cells; Nrf2; Redox homeostasis

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; 6,7 DIHYDRO 4 HYDROXY 3 (2' HYDROXY 1,1' BIPHENYL 4 YL) 6 OXOTHIENO[2,3 B]PYRIDINE 5 CARBONITRILE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; TRANSCRIPTION FACTOR NRF2; NUCLEAR PROTEIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; HOMEOSTASIS; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; METABOLISM; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; RESEARCH; BINDING ASSAY; CARCINOMA CELL; CONTROLLED STUDY; DNA BINDING; GENETIC TRANSFECTION; HEPG2 CELL LINE; HUMAN CELL CULTURE; IMMUNOBLOTTING; IN VITRO STUDY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

AICAR; AMPK; HEPATOCARCINOMA CELLS; NRF2; REDOX HOMEOSTASIS;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER NEOPLASMS; NF-E2-RELATED FACTOR 2; PHOSPHORYLATION; PYRONES; RIBONUCLEOSIDES; THIOPHENES;

EID: 84906791632     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.07.010     Document Type: Article

References (59)

1. D.M. Parkin, F. Bray, J. Ferlay, and P. Pisani Global cancer statistics, 2002 CA Cancer J Clin 55 2 2005 74 108 (Pubitemid 40372904)
2. H.B. El-Serag, and K.L. Rudolph Hepatocellular carcinoma: epidemiology and molecular carcinogenesis Gastroenterology 132 7 2007 2557 2576 (Pubitemid 46890874)
3. A.P. Venook, C. Papandreou, J. Furuse, and L.L. de Guevara The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective Oncologist 15 Suppl. 4 2010 5 13
4. E. Mormone, J. George, and N. Nieto Molecular pathogenesis of hepatic fibrosis and current therapeutic approaches Chem Biol Interact 193 3 2011 225 231
5. P. Muriel Role of free radicals in liver diseases Hepatol Int 3 4 2009 526 536
6. B. Sid, J. Verrax, and P.B. Calderon Role of oxidative stress in the pathogenesis of alcohol-induced liver disease Free Radic Res 47 11 2013 894 904
7. H.L. Ha, H.J. Shin, M.A. Feitelson, and D.Y. Yu Oxidative stress and antioxidants in hepatic pathogenesis World J Gastroenterol 16 48 2010 6035 6043
8. J. Choi, and J.H. Ou Mechanisms of liver injury. III. Oxidative stress in the pathogenesis of hepatitis C virus Am J Physiol Gastrointest Liver Physiol 290 5 2006 G847 G851
9. J1 Nair, P. Srivatanakul, C. Haas, A. Jedpiyawongse, T. Khuhaprema, and H.K. Seitz et al. High urinary excretion of lipid peroxidation-derived DNA damage in patients with cancer-prone liver diseases Mutat Res 683 1-2 2010 23 28
10. C.D. Klaassen, and S.A. Reisman Nrf2 the rescue: effects of the antioxidative/electrophilic response on the liver Toxicol Appl Pharmacol 244 1 2010 57 65
11. K.I. Tong, Y. Katoh, H. Kusunoki, K. Itoh, T. Tanaka, and M. Yamamoto Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model Mol Cell Biol 26 8 2006 2887 2900
12. S.B. Cullinan, J.D. Gordan, J. Jin, J.W. Harper, and J.A. Diehl The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase Mol Cell Biol 24 19 2004 8477 8486 (Pubitemid 39245070)
13. K. Taguchi, H. Motohashi, and M. Yamamoto Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution Genes Cells 16 2 2011 123 140
14. H. Motohashi, F. Katsuoka, J.D. Engel, and M. Yamamoto Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway Proc Natl Acad Sci U S A 101 17 2004 6379 6384 (Pubitemid 38585982)
15. K.T. Turpaev Keap1-Nrf2 signaling pathway: mechanisms of regulation and role in protection of cells against toxicity caused by xenobiotics and electrophiles Biochemistry (Mosc) 78 2 2013 111 126
16. W.O. Osburn, and T.W. Kensler Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults Mutat Res 659 1-2 2008 31 39
17. M.H. Zou, S.S. Kirkpatrick, B.J. Davis, J.S. Nelson, W.G. Wiles 4th, and U. Schlattner et al. Activation of the AMP-activated protein kinase by the anti-diabetic drug metformin in vivo. Role of mitochondrial reactive nitrogen species J Biol Chem 279 42 2004 43940 43951 (Pubitemid 39390702)
18. H.C. Choi, P. Song, Z. Xie, Y. Wu, J. Xu, and M. Zhang et al. Reactive nitrogen species is required for the activation of the AMP-activated protein kinase by statin in vivo J Biol Chem 283 29 2008 20186 20197
19. B. Sid, J. Verrax, and P.B. Calderon Role of AMPK activation in oxidative cell damage: implications for alcohol-induced liver disease Biochem Pharmacol 86 2 2013 200 209
20. D.G. Hardie, and D. Carling The AMP-activated protein kinase - fuel gauge of the mammalian cell? Eur J Biochem 246 2 1997 259 273 (Pubitemid 27232500)
21. D. Carling, F.V. Mayer, M.J. Sanders, and S.J. Gamblin AMP-activated protein kinase: nature's energy sensor Nat Chem Biol 7 8 2011 512 518
22. M.F. Vincent, F. Bontemps, and G. Van den Berghe Substrate cycling between 5-amino-4-imidazolecarboxamide riboside and its monophosphate in isolated rat hepatocytes Biochem Pharmacol 52 7 1996 999 1006 (Pubitemid 26338259)
23. A. Woods, S.R. Johnstone, K. Dickerson, F.C. Leiper, L.G. Fryer, and D. Neumann et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade Curr Biol 13 22 2003 2004 2008 (Pubitemid 37425212)
24. R.L. Hurley, K.A. Anderson, J.M. Franzone, B.E. Kemp, A.R. Means, and L.A. Witters The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases J Biol Chem 280 32 2005 29060 29066 (Pubitemid 41161355)
25. X.M. Liu, K.J. Peyton, A.R. Shebib, H. Wang, R.J. Korthuis, and W. Durante Activation of AMPK stimulates heme oxygenase-1 gene expression and human endothelial cell survival Am J Physiol Heart Circ Physiol 300 1 2011 H84 H93
26. B. Onken, and M. Driscoll Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans Health span via AMPK, LKB1, and SKN-1 PLoS One 5 1 2010 e8758
27. J.E. Sullivan, K.J. Brocklehurst, A.E. Marley, F. Carey, D. Carling, and R.K. Beri Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase FEBS Lett 353 1 1994 33 36 (Pubitemid 24312538)
28. J.M. Corton, J.G. Gillespie, S.A. Hawley, and D.G. Hardie 5-Aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem 229 2 1995 558 565
29. B. Cool, B. Zinker, W. Chiou, L. Kifle, N. Cao, and M. Perham et al. Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome Cell Metab 3 6 2006 403 416 (Pubitemid 43811782)
30. D. Wu, and A.I. Cederbaum Development and properties of HepG2 cells that constitutively express CYP2E1 Methods Mol Biol 447 2008 137 150
31. F. Tietze Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues Anal Biochem 27 3 1969 502 522
32. O.W. Griffith Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine Anal Biochem 106 1 1980 207 212 (Pubitemid 11246585)
33. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1 1951 265 275
34. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
35. Y. Chen, A. Takeshita, K. Ozaki, S. Kitano, and S. Hanazawa Transcriptional regulation by transforming growth factor beta of the expression of retinoic acid and retinoid X receptor genes in osteoblastic cells is mediated through AP-1 J Biol Chem 271 49 1996 31602 31606 (Pubitemid 26408621)
36. P. Renard, I. Ernest, A. Houbion, M. Art, H. Le Calvez, and M. Raes et al. Development of a sensitive multi-well colorimetric assay for active NFkappaB Nucleic Acids Res 29 4 2001 E21
37. S. Toffoli, A. Roegiers, O. Feron, M. Van Steenbrugge, N. Ninane, and M. Raes et al. Intermittent hypoxia is an angiogenic inducer for endothelial cells: role of HIF-1 Angiogenesis 12 1 2009 47 67
38. L. Mattart, D. Calay, D. Simon, L. Roebroek, L. Caesens-Koenig, and M. Van Steenbrugge et al. The peroxynitrite donor 3-morpholinosydnonimine activates Nrf2 and the UPR leading to a cytoprotective response in endothelial cells Cell Signal 24 1 2012 199 213
39. T. Satoh, S.R. McKercher, and S.A. Lipton Reprint of: Nrf2/ARE-mediated antioxidant actions of pro-electrophilic drugs Free Radic Biol Med 66 2014 45 57
40. B. Sid, L. Miranda, D. Vertommen, B. Viollet, and M.H. Rider Stimulation of human and mouse erythrocyte Na(+)-K(+)-2Cl(-) cotransport by osmotic shrinkage does not involve AMP-activated protein kinase, but is associated with STE20/SPS1-related proline/alanine-rich kinase activation J Physiol 588 Pt 13 2010 2315 2328
41. L. Miranda, S. Carpentier, A. Platek, N. Hussain, M.A. Gueuning, and D. Vertommen et al. AMP-activated protein kinase induces actin cytoskeleton reorganization in epithelial cells Biochem Biophys Res Commun 396 3 2010 656 661
42. S.C. Lo, X. Li, M.T. Henzl, L.J. Beamer, and M. Hannink Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling EMBO J 25 15 2006 3605 3617 (Pubitemid 44264871)
43. Z. Sun, Z. Huang, and D.D. Zhang Phosphorylation of Nrf2 at multiple sites by MAP kinases has a limited contribution in modulating the Nrf2-dependent antioxidant response PLoS One 4 8 2009 e6588
44. L. Baird, and A.T. Dinkova-Kostova The cytoprotective role of the Keap1-Nrf2 pathway Arch Toxicol 85 4 2011 241 272
45. J.T. Lanner, D.K. Georgiou, A. Dagnino-Acosta, A. Ainbinder, Q. Cheng, and A.D. Joshi et al. AICAR prevents heat-induced sudden death in RyR1 mutant mice independent of AMPK activation Nat Med 18 2 2012 244 251
46. B. Guigas, N. Taleux, M. Foretz, D. Detaille, F. Andreelli, and B. Viollet et al. AMP-activated protein kinase-independent inhibition of hepatic mitochondrial oxidative phosphorylation by AICA riboside Biochem J 404 3 2007 499 507 (Pubitemid 46953924)
47. R.L. Jacobs, S. Lingrell, J.R. Dyck, and D.E. Vance Inhibition of hepatic phosphatidylcholine synthesis by 5-aminoimidazole-4-carboxamide-1-beta-4- ribofuranoside is independent of AMP-activated protein kinase activation J Biol Chem 282 7 2007 4516 4523 (Pubitemid 47100967)
48. D. Meley, C. Bauvy, J.H. Houben-Weerts, P.F. Dubbelhuis, M.T. Helmond, and P. Codogno et al. AMP-activated protein kinase and the regulation of autophagic proteolysis J Biol Chem 281 46 2006 34870 34879 (Pubitemid 46036526)
49. B. Guigas, K. Sakamoto, N. Taleux, S.M. Reyna, N. Musi, and B. Viollet et al. Beyond AICA riboside: in search of new specific AMP-activated protein kinase activators IUBMB Life 61 1 2009 18 26
50. M.F. Vincent, F. Bontemps, and G. Van den Berghe Inhibition of glycolysis by 5-amino-4-imidazolecarboxamide riboside in isolated rat hepatocytes Biochem J 281 Pt 1 1992 267 272
51. J. Shang, and M.A. Lehrman Activation of glycogen phosphorylase with 5-aminoimidazole-4-carboxamide riboside (AICAR). Assessment of glycogen as a precursor of mannosyl residues in glycoconjugates J Biol Chem 279 13 2004 12076 12080 (Pubitemid 38445770)
52. S.L. Longnus, R.B. Wambolt, H.L. Parsons, R.W. Brownsey, and M.F. Allard 5-Aminoimidazole-4-carboxamide 1-beta-D-ribofuranoside (AICAR) stimulates myocardial glycogenolysis by allosteric mechanisms Am J Physiol Regul Integr Comp Physiol 284 4 2003 R936 R944
53. M.F. Vincent, P.J. Marangos, H.E. Gruber, and G. Van den Berghe Inhibition by AICA riboside of gluconeogenesis in isolated rat hepatocytes Diabetes 40 10 1991 1259 1266
54. N.R. Kitteringham, A. Abdullah, J. Walsh, L. Randle, R.E. Jenkins, and R. Sison et al. Proteomic analysis of Nrf2 deficient transgenic mice reveals cellular defence and lipid metabolism as primary Nrf2-dependent pathways in the liver J Proteomics 73 8 2010 1612 1631
55. M.H. Ludtmann, P.R. Angelova, Y. Zhang, A.Y. Abramov, and A.T. Dinkova-Kostova Nrf2 affects the efficiency of mitochondrial fatty acid oxidation Biochem J 457 3 2014 415 424
56. Y. Mitsuishi, K. Taguchi, Y. Kawatani, T. Shibata, T. Nukiwa, and H. Aburatani et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming Cancer Cell 22 1 2012 66 79
57. J.D. Hayes, and A.T. Dinkova-Kostova The Nrf2 regulatory network provides an interface between redox and intermediary metabolism Trends Biochem Sci 39 4 2014 199 218
58. A. Singh, C. Happel, S.K. Manna, G. Acquaah-Mensah, J. Carrerero, and S. Kumar et al. Transcription factor NRF2 regulates miR-1 and miR-206 to drive tumorigenesis J Clin Invest 123 7 2013 2921 2934
59. E. Kansanen, S.M. Kuosmanen, H. Leinonen, and A.L. Levonen The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer Redox Biol 1 1 2013 45 49