NQO2 is a reactive oxygen species generating off-target for acetaminophen

Molecular Pharmaceutics

Volumn 11, Issue 12, 2014, Pages 4395-4404

  Miettinen, Teemu P ^a   Björklund, Mikael ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

acetaminophen; CETSA; drug target; NQO2; paracetamol; quinone reductase 2; superoxide

Indexed keywords

CYTOPLASM PROTEIN; PARACETAMOL; QUINONE REDUCTASE 2; REACTIVE OXYGEN METABOLITE; RECOMBINANT ENZYME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SUPEROXIDE; UNCLASSIFIED DRUG; NRH - QUINONE OXIDOREDUCTASE2;

ARTICLE; CONTROLLED STUDY; DRUG PROTEIN BINDING; DRUG TARGETING; ENZYME ACTIVE SITE; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; KIDNEY; LIVER; NEPHROTOXICITY; PROTEIN EXPRESSION; TOXIC HEPATITIS; CHEMISTRY; DRUG EFFECTS; METABOLISM;

ACETAMINOPHEN; HELA CELLS; HUMANS; IN VITRO TECHNIQUES; KIDNEY; LIVER; QUINONE REDUCTASES; REACTIVE OXYGEN SPECIES;

EID: 84914127194     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp5004866     Document Type: Article

References (44)

1. Moynihan, R. FDA fails to reduce accessibility of paracetamol despite 450 deaths a year BMJ 2002, 325 (7366) 678
2. Graham, G. G.; Davies, M. J.; Day, R. O.; Mohamudally, A.; Scott, K. F. The modern pharmacology of paracetamol: therapeutic actions, mechanism of action, metabolism, toxicity and recent pharmacological findings Inflammopharmacology 2013, 21 (3) 201-32
3. Andersson, D. A.; Gentry, C.; Alenmyr, L.; Killander, D.; Lewis, S. E.; Andersson, A.; Bucher, B.; Galzi, J. L.; Sterner, O.; Bevan, S.; Hogestatt, E. D.; Zygmunt, P. M. TRPA1 mediates spinal antinociception induced by acetaminophen and the cannabinoid Delta(9)-tetrahydrocannabiorcol Nat. Commun. 2011, 2, 551
4. McGill, M. R.; Jaeschke, H. Metabolism and disposition of acetaminophen: recent advances in relation to hepatotoxicity and diagnosis Pharm. Res. 2013, 30 (9) 2174-87
5. Bessems, J. G.; Vermeulen, N. P. Paracetamol (acetaminophen)-induced toxicity: molecular and biochemical mechanisms, analogues and protective approaches Crit. Rev. Toxicol. 2001, 31 (1) 55-138
6. James, L. P.; Mayeux, P. R.; Hinson, J. A. Acetaminophen-induced hepatotoxicity Drug Metab. Dispos. 2003, 31 (12) 1499-506
7. Knight, T. R.; Kurtz, A.; Bajt, M. L.; Hinson, J. A.; Jaeschke, H. Vascular and hepatocellular peroxynitrite formation during acetaminophen toxicity: role of mitochondrial oxidant stress Toxicol. Sci. 2001, 62 (2) 212-20
8. Dahlin, D. C.; Miwa, G. T.; Lu, A. Y.; Nelson, S. D. N-acetyl-p-benzoquinone imine: a cytochrome P-450-mediated oxidation product of acetaminophen Proc. Natl. Acad. Sci. U.S.A. 1984, 81 (5) 1327-31
9. James, L. P.; McCullough, S. S.; Knight, T. R.; Jaeschke, H.; Hinson, J. A. Acetaminophen toxicity in mice lacking NADPH oxidase activity: role of peroxynitrite formation and mitochondrial oxidant stress Free Radical Res. 2003, 37 (12) 1289-97
10. Bajt, M. L.; Knight, T. R.; Lemasters, J. J.; Jaeschke, H. Acetaminophen-induced oxidant stress and cell injury in cultured mouse hepatocytes: protection by N-acetyl cysteine Toxicol. Sci. 2004, 80 (2) 343-9
11. Moore, M.; Thor, H.; Moore, G.; Nelson, S.; Moldeus, P.; Orrenius, S. The Toxicity of Acetaminophen and N-Acetyl-Para-Benzoquinone Imine in Isolated Hepatocytes Is Associated with Thiol Depletion and Increased Cytosolic Ca-2+ J. Biol. Chem. 1985, 260 (24) 3035-3040
12. Cover, C.; Mansouri, A.; Knight, T. R.; Bajt, M. L.; Lemasters, J. J.; Pessayre, D.; Jaeschke, H. Peroxynitrite-induced mitochondrial and endonuclease-mediated nuclear DNA damage in acetaminophen hepatotoxicity J. Pharmacol. Exp. Ther. 2005, 315 (2) 879-87
13. Tirmenstein, M. A.; Nelson, S. D. Subcellular binding and effects on calcium homeostasis produced by acetaminophen and a nonhepatotoxic regioisomer, 3′-hydroxyacetanilide, in mouse liver J. Biol. Chem. 1989, 264 (17) 9814-9
14. Cheung, C.; Yu, A. M.; Ward, J. M.; Krausz, K. W.; Akiyama, T. E.; Feigenbaum, L.; Gonzalez, F. J. The cyp2e1-humanized transgenic mouse: role of cyp2e1 in acetaminophen hepatotoxicity Drug Metab. Dispos. 2005, 33 (3) 449-57
15. Cohen, S. D.; Khairallah, E. A. Selective protein arylation and acetaminophen-induced hepatotoxicity Drug Metab. Rev. 1997, 29 (1-2) 59-77
16. Kheradpezhouh, E.; Ma, L.; Morphett, A.; Barritt, G. J.; Rychkov, G. Y. TRPM2 channels mediate acetaminophen-induced liver damage Proc. Natl. Acad. Sci. U.S.A. 2014, 111 (8) 3176-81
17. Laukkanen, M. O.; Leppanen, P.; Turunen, P.; Tuomisto, T.; Naarala, J.; Yla-Herttuala, S. EC-SOD gene therapy reduces paracetamol-induced liver damage in mice J. Gene Med. 2001, 3 (4) 321-5
18. Jaeschke, H.; Bajt, M. L. Intracellular signaling mechanisms of acetaminophen-induced liver cell death Toxicol. Sci. 2006, 89 (1) 31-41
19. Shuhendler, A. J.; Pu, K.; Cui, L.; Uetrecht, J. P.; Rao, J. Real-time imaging of oxidative and nitrosative stress in the liver of live animals for drug-toxicity testing Nat. Biotechnol. 2014, 32, 373-80
20. Niesen, F. H.; Berglund, H.; Vedadi, M. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability Nat. Protoc. 2007, 2 (9) 2212-21
21. Miettinen, T. P.; Pessa, H. K.; Caldez, M. J.; Fuhrer, T.; Diril, M. K.; Sauer, U.; Kaldis, P.; Bjorklund, M. Identification of transcriptional and metabolic programs related to Mammalian cell size Curr. Biol. 2014, 24 (6) 598-608
22. Martinez Molina, D.; Jafari, R.; Ignatushchenko, M.; Seki, T.; Larsson, E. A.; Dan, C.; Sreekumar, L.; Cao, Y.; Nordlund, P. Monitoring drug target engagement in cells and tissues using the cellular thermal shift assay Science 2013, 341 (6141) 84-7
23. Winger, J. A.; Hantschel, O.; Superti-Furga, G.; Kuriyan, J. The structure of the leukemia drug imatinib bound to human quinone reductase 2 (NQO2) BMC Struct. Biol. 2009, 9, 7
24. Fu, Y.; Buryanovskyy, L.; Zhang, Z. Quinone reductase 2 is a catechol quinone reductase J. Biol. Chem. 2008, 283 (35) 23829-35
25. Celli, C. M.; Tran, N.; Knox, R.; Jaiswal, A. K. NRH:quinone oxidoreductase 2 (NQO2) catalyzes metabolic activation of quinones and anti-tumor drugs Biochem. Pharmacol. 2006, 72 (3) 366-76
26. Vella, F.; Ferry, G.; Delagrange, P.; Boutin, J. A. NRH:quinone reductase 2: an enzyme of surprises and mysteries Biochem. Pharmacol. 2005, 71 (1-2) 1-12
27. Bantscheff, M.; Eberhard, D.; Abraham, Y.; Bastuck, S.; Boesche, M.; Hobson, S.; Mathieson, T.; Perrin, J.; Raida, M.; Rau, C.; Reader, V.; Sweetman, G.; Bauer, A.; Bouwmeester, T.; Hopf, C.; Kruse, U.; Neubauer, G.; Ramsden, N.; Rick, J.; Kuster, B.; Drewes, G. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors Nat. Biotechnol. 2007, 25 (9) 1035-44
28. Buryanovskyy, L.; Fu, Y.; Boyd, M.; Ma, Y.; Hsieh, T. C.; Wu, J. M.; Zhang, Z. Crystal structure of quinone reductase 2 in complex with resveratrol Biochemistry 2004, 43 (36) 11417-26
29. Antoine, M.; Marcheteau, E.; Delagrange, P.; Ferry, G.; Boutin, J. A. Characterization of cofactors, substrates and inhibitor binding to flavoenzyme quinone reductase 2 by automated supramolecular nano-electrospray ionization mass spectrometry Int. J. Mass Spectrom. 2012, 312, 87-96
30. Knox, R. J.; Jenkins, T. C.; Hobbs, S. M.; Chen, S.; Melton, R. G.; Burke, P. J. Bioactivation of 5-(aziridin-1-yl)-2,4-dinitrobenzamide (CB 1954) by human NAD(P)H quinone oxidoreductase 2: a novel co-substrate-mediated antitumor prodrug therapy Cancer Res. 2000, 60 (15) 4179-86
31. Reybier, K.; Perio, P.; Ferry, G.; Bouajila, J.; Delagrange, P.; Boutin, J. A.; Nepveu, F. Insights into the redox cycle of human quinone reductase 2 Free Radical Res. 2011, 45 (10) 1184-95
32. Nosjean, O.; Ferro, M.; Coge, F.; Beauverger, P.; Henlin, J. M.; Lefoulon, F.; Fauchere, J. L.; Delagrange, P.; Canet, E.; Boutin, J. A. Identification of the melatonin-binding site MT3 as the quinone reductase 2 J. Biol. Chem. 2000, 275 (40) 31311-7
33. Graves, P. R.; Kwiek, J. J.; Fadden, P.; Ray, R.; Hardeman, K.; Coley, A. M.; Foley, M.; Haystead, T. A. Discovery of novel targets of quinoline drugs in the human purine binding proteome Mol. Pharmacol. 2002, 62 (6) 1364-72
34. Forman, H. J.; Fridovich, I. On the stability of bovine superoxide dismutase. The effects of metals J. Biol. Chem. 1973, 248 (8) 2645-9
35. Manyike, P. T.; Kharasch, E. D.; Kalhorn, T. F.; Slattery, J. T. Contribution of CYP2E1 and CYP3A to acetaminophen reactive metabolite formation Clin. Pharmacol. Ther. 2000, 67 (3) 275-82
36. Liao, S.; Williams-Ashman, H. G. Enzymatic Oxidation of Some Non-Phosphorylated Derivatives of Dihydronicotinamide Biochem. Biophys. Res. Commun. 1961, 4 (3) 208-13
37. Tripathy, D.; Grammas, P. Acetaminophen protects brain endothelial cells against oxidative stress Microvasc. Res. 2009, 77 (3) 289-96
38. Long, D. J., 2nd; Iskander, K.; Gaikwad, A.; Arin, M.; Roop, D. R.; Knox, R.; Barrios, R.; Jaiswal, A. K. Disruption of dihydronicotinamide riboside:quinone oxidoreductase 2 (NQO2) leads to myeloid hyperplasia of bone marrow and decreased sensitivity to menadione toxicity J. Biol. Chem. 2002, 277 (48) 46131-9
39. Chung, C. W.; Dean, A. W.; Woolven, J. M.; Bamborough, P. Fragment-based discovery of bromodomain inhibitors part 1: inhibitor binding modes and implications for lead discovery J. Med. Chem. 2012, 55 (2) 576-86
40. Shah, A. D.; Wood, D. M.; Dargan, P. I. Understanding lactic acidosis in paracetamol (acetaminophen) poisoning Br. J. Clin. Pharmacol. 2011, 71 (1) 20-8
41. Lister, C. F.; McLean, A. E. Inhibition of DNA synthesis by paracetamol in different tissues of the rat in vivo Toxicology 1997, 116 (1-3) 49-57
42. Ahn, K. S.; Gong, X.; Sethi, G.; Chaturvedi, M. M.; Jaiswal, A. K.; Aggarwal, B. B. Deficiency of NRH:quinone oxidoreductase 2 differentially regulates TNF signaling in keratinocytes: up-regulation of apoptosis correlates with down-regulation of cell survival kinases Cancer Res. 2007, 67 (20) 10004-11
43. Sener, G.; Toklu, H. Z.; Sehirli, A. O.; Velioglu-Ogunc, A.; Cetinel, S.; Gedik, N. Protective effects of resveratrol against acetaminophen-induced toxicity in mice Hepatol. Res. 2006, 35 (1) 62-8
44. Janbaz, K. H.; Saeed, S. A.; Gilani, A. H. Studies on the protective effects of caffeic acid and quercetin on chemical-induced hepatotoxicity in rodents Phytomedicine 2004, 11 (5) 424-30