Glutathione metabolism modeling: A mechanism for liver drug-robustness and a new biomarker strategy

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 10, 2013, Pages 4943-4959

  Geenen, Suzanne ^a,b   Du Preez, Franco B ^a,c   Snoep, Jacky L ^a,c,d   Foster, Alison J ^b   Sarda, Sunil ^b   Kenna, J Gerry ^b   Wilson, Ian D ^b,f   Westerhoff, Hans V ^a,d,e  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

^c STELLENBOSCH UNIVERSITY   (South Africa)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Acetaminophen toxicity; Adaptation; Biomarker; Gene expression metabolism hybrid model; Glutathione metabolism

Indexed keywords

BIOLOGICAL MARKER; CYTOCHROME P450 2E1; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; METHIONINE; OPHTHALMIC ACID; PARACETAMOL; PEPTIDES AND PROTEINS; PYROGLUTAMIC ACID; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ADAPTATION; ARTICLE; CELL PROTECTION; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; DETOXIFICATION; DRUG CYTOTOXICITY; DRUG EXPOSURE; ENZYME ACTIVITY; ENZYME INDUCTION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER METABOLISM; LIVER TOXICITY; MATHEMATICAL MODEL; METABOLITE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEIN SYNTHESIS;

ACETAMINOPHEN TOXICITY; ADAPTATION; BIOMARKER; GENE EXPRESSION-METABOLISM HYBRID MODEL; GLUTATHIONE METABOLISM;

ACETAMINOPHEN; BIOLOGICAL MARKERS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CULTURE MEDIA; GLUTATHIONE; HUMANS; LIVER; MODELS, BIOLOGICAL; TANDEM MASS SPECTROMETRY;

EID: 84878746693     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.04.014     Document Type: Article

References (57)

1. J.R. Mitchell, D.J. Jollow, W.Z. Potter, D.C. Davis, J.R. Gillette, and B.B. Brodie Acetaminophen-induced hepatic necrosis. I. Role of drug metabolism J. Pharmacol. Exp. Ther. 187 1973 185 194
2. A. Meister Glutathione metabolism and its selective modification J. Biol. Chem. 263 1988 17205 17208 (Pubitemid 19029311)
3. B. Ketterer, B. Coles, and D.J. Meyer The role of glutathione in detoxification Environ. Heal. Perspect. 49 1983 59 69
4. T. Nguyen, P. Nioi, and C.B. Pickett The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress J. Biol. Chem. 284 2009 13291 13295
5. J. Hinson, D. Roberts, and L. James Mechanisms of acetaminophen-induced liver necrosis Handb. Exp. Pharmacol. 196 2010 369 405
6. B.K. Park, A. Boobis, S. Clarke, C.E.P. Goldring, D. Jones, J.G. Kenna, C. Lambert, H.G. Laverty, D.J. Naisbitt, S. Nelson, D.A. Nicoll-Griffith, R.S. Obach, P. Routledge, D.A. Smith, D.J. Tweedie, N. Vermeulen, D.P. Williams, I.D. Wilson, and T.A. Baillie Managing the challenge of chemically reactive metabolites in drug development Nat. Rev. Drug Discov. 10 2011 292 306
7. S.C. Lu Regulation of glutathione synthesis Mol. Aspects Med. 30 2009 42 59
8. V.A. da Silva, and A.E.M. McLean Effect of two different types of malnutrition on the rate of elimination of ethanol in rats Biochem. Pharmacol. 37 1988 4235 4238
9. A.E.M. McLean, and P.A. Day The effect of diet on the toxicity of paracetamol and the safety of paracetamol-methionine mixtures Biochem. Pharmacol. 24 1975 37 42
10. F. Ghauri, A. McLean, D. Beales, I. Wilson, and J. Nicholson Induction of 5-oxoprolinuria in the rat following chronic feeding with N-acetyl 4-aminophenol (paracetamol) Biochem. Pharmacol. 46 5 Sep 1 1993 953 957 (Pubitemid 23272778)
11. A.E.M. McLean, G.R. Armstrong, and D. Beales Effect of d- or l-methionine and cysteine on the growth inhibitory effects of feeding 1% paracetamol to rats Biochem. Pharmacol. 38 1989 347 352 (Pubitemid 19033348)
12. A. Wild, and R. Mulcahy Regulation of gamma-glutamylcysteine synthetase subunit gene expression: insights into transcriptional control of antioxidant defenses Free Radic. Res. 32 2000 281 301 (Pubitemid 30167475)
13. K. Chan, X.-D. Han, and Y.W. Kan An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen Proc. Natl. Acad. Sci. U. S. A. 98 2001 4611 4616 (Pubitemid 32295024)
14. N.R. Kitteringham, H. Powell, Y.N. Clement, C.C. Dodd, J.N. Tettey, M. Pirmohamed, D.A. Smith, L.I. McLellan, and B.K. Park Hepatocellular response to chemical stress in CD-1 mice: induction of early genes and γ- glutamylcysteine synthetase Hepatology 32 2000 321 333 (Pubitemid 30614665)
15. L.A. McConnachie, I. Mohar, F.N. Hudson, C.B. Ware, W.C. Ladiges, C. Fernandez, S. Chatterton-Kirchmeier, C.C. White, R.H. Pierce, and T.J. Kavanagh Glutamate cysteine ligase modifier subunit deficiency and gender as determinants of acetaminophen-induced hepatotoxicity in mice Toxicol. Sci. 99 2007 628 636 (Pubitemid 351753076)
16. T.P. Dalton, M.Z. Dieter, Y. Yang, H.G. Shertzer, and D.W. Nebert Knockout of the mouse glutamate cysteine ligase catalytic subunit (Gclc) gene: embryonic lethal when homozygous, and proposed model for moderate glutathione deficiency when heterozygous Biochem. Biophys. Res. Commun. 279 2000 324 329 (Pubitemid 32016716)
17. S.-i. Nakamura, S. Sugiyama, D. Fujioka, K.-i. Kawabata, H. Ogawa, and K. Kugiyama Polymorphism in glutamate-cysteine ligase modifier subunit gene is associated with impairment of nitric oxide-mediated coronary vasomotor function Circulation 108 2003 1425 1427 (Pubitemid 37176445)
18. E. Ristoff, C. Augustson, J. Geissler, T. de Rijk, K. Carlsson, J.-L. Luo, K. Andersson, R.S. Weening, R. van Zwieten, A. Larsson, and D. Roos A missense mutation in the heavy subunit of γ-glutamylcysteine synthetase gene causes hemolytic anemia Blood 95 2000 2193 2196
19. A.C. Walsh, J.A. Feulner, and A. Reilly Evidence for functionally significant polymorphism of human glutamate cysteine ligase catalytic subunit: association with glutathione levels and drug resistance in the National Cancer Institute tumor cell line panel Toxicol. Sci. 61 2001 218 223 (Pubitemid 32499389)
20. D. Larrey, and G.P. Pageaux Genetic predisposition to drug-induced hepatotoxicity J. Hepatol. 26 Supplement 2 1997 12 21
21. M.W. Russo, and P.B. Watkins Genetic basis for susceptibility to drug induced liver injury L. N.D. Kaplowitz, Drug-Induced Liver Disease 2007 Informa Healthcare New York 207 222
22. A.K. Groen, R. Van der Meer, H.V. Westerhoff, R.J.A. Wanders, T.P.M. Akerboom, and J.M. Tager Control of Metabolic Fluxes, Metabolic Compartmentation H. Siess, 257 1982 Academic Press New York 9 37
23. J.H. Winnike, Z. Li, F.A. Wright, J.M. Macdonald, T.M. O'Connell, and P.B. Watkins Use of pharmaco-metabonomics for early prediction of acetaminophen-induced hepatotoxicity in humans Clin. Pharmacol. Ther. 88 2010 45 51
24. H.V. Westerhoff, and D.B. Kell The methodologies of systems biology F.C. Boogerd, F.J. Bruggeman, J.-H.S. Hofmeyr, H.V. Westerhoff, Systems Biology - Philosophical Foundations 2007 Elsevier Amsterdam 23 70
25. K. Macé, F. Aguilar, J.S. Wang, P. Vautravers, M. Gómez-Lechón, F.J. Gonzalez, J. Groopman, C.C. Harris, and A.M. Pfeifer Aflatoxin B1-induced DNA adduct formation and p53 mutations in CYP450-expressing human liver cell lines Carcinogenesis 18 1997 1291 1297 (Pubitemid 28134700)
26. S. Geenen, C. Guallar-Hoyas, F. Michopoulos, J.G. Kenna, K.L. Kolaja, H.V. Westerhoff, P. Thomas, and I.D. Wilson HPLC-MS/MS methods for the quantitative analysis of 5-oxoproline (pyroglutamate) in rat plasma and hepatic cell line culture medium J. Pharm. Biomed. Anal. 56 2011 655 663
27. J.W. Benbow, J. Aubrecht, M.J. Banker, D. Nettleton, and M.D. Aleo Predicting safety toleration of pharmaceutical chemical leads: cytotoxicity correlations to exploratory toxicity studies Toxicol. Lett. 197 2010 175 182
28. R.A. Thompson, E.M. Isin, Y. Li, L. Weidolf, K. Page, I. Wilson, S. Swallow, B. Middleton, S. Stahl, A.J. Foster, H. Dolgos, R. Weaver, and J.G. Kenna In vitro approach to assess the potential for risk of idiosyncratic adverse reactions caused by candidate drugs Chem. Res. Toxicol. 25 2012 1616 1632
29. I. Antolino-Lobo, J. Meulenbelt, J. Molendijk, S.M. Nijmeijer, P. Scherpenisse, M. van den Berg, and M.B.M. van Duursen Induction of glutathione synthesis and conjugation by 3,4-methylenedioxymethamphetamine (MDMA) and 3,4-dihydroxymethamphetamine (HHMA) in human and rat liver cells, including the protective role of some antioxidants Toxicology 289 2011 175 184
30. M.E. Gegg, J.B. Clark, and S.J.R. Heales Determination of glutamate-cysteine ligase ([gamma]-glutamylcysteine synthetase) activity by high-performance liquid chromatography and electrochemical detection Anal. Biochem. 304 2002 26 32 (Pubitemid 34492839)
31. J.R. Mitchell, D.J. Jollow, W.Z. Potter, J.R. Gillette, and B.B. Brodie Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione J. Pharmacol. Exp. Ther. 187 1973 211 217
32. T. Marshall, and K.M. Williams Drug interference in the Bradford and 2,2′-bicinchoninic acid protein assays Anal. Biochem. 198 1991 352 354
33. P.L. Else, M.D. Brand, N. Turner, and A.J. Hulbert Respiration rate of hepatocytes varies with body mass in birds J. Exp. Biol. 207 2004 2305 2311 (Pubitemid 38893568)
34. M.E. Tischler, P. Hecht, and J.R. Williamson Determination of mitochondrial/cytosolic metabolite gradients in isolated rat liver cells by cell disruption Arch. Biochem. Biophys. 181 1977 278 292 (Pubitemid 8115477)
35. R.J. Ellis Macromolecular crowding: obvious but underappreciated Trends Biochem. Sci. 26 2001 597 604 (Pubitemid 32925190)
36. S. Geenen, F.B. du Preez, M. Reed, H. Frederik Nijhout, J. Gerry Kenna, I.D. Wilson, H.V. Westerhoff, and J.L. Snoep A mathematical modelling approach to assessing the reliability of biomarkers of glutathione metabolism Eur. J. Pharm. Sci. 46 2012 233 243
37. M. Inoue, K. Okajima, and Y. Morino Metabolic coordination of liver and kidney in mercapturic acid biosynthesis in vivo Hepatology 2 1982 311S 316S
38. S. Hoops, S. Sahle, R. Gauges, C. Lee, J. Pahle, N. Simus, M. Singhal, L. Xu, P. Mendes, and U. Kummer COPASI - a COmplex PAthway SImulator Bioinformatics 22 2006 3067 3074 (Pubitemid 44884083)
39. S.M. Aitken, and J.F. Kirsch Kinetics of the yeast cystathionine β-synthase forward and reverse reactions: continuous assays and the equilibrium constant for the reaction Biochemistry 42 2003 571 578 (Pubitemid 36105777)
40. Q. Sun, R. Collins, S. Huang, L. Holmberg-Schiavone, G.S. Anand, C.-H. Tan, S. van-den-Berg, L.-W. Deng, P.K. Moore, T. Karlberg, and J. Sivaraman Structural basis for the inhibition mechanism of human cystathionine gamma-lyase, an enzyme responsible for the production of H2S J. Biol. Chem. 284 2009 3076 3085
41. M.C. Reed, R. Thomas, J. Pavisic, S. James, C.M. Ulrich, and H.F. Nijhout A mathematical model of glutathione metabolism Theor. Biol. Med. Model. 5 2008 1 16
42. K. Luersen, S. Muller, A. Hussein, E. Liebau, and R.D. Walter The y-glutamylcysteine synthetase of Onchocerca volvulus Mol. Biochem. Parasitol. 111 2000 243 251
43. M. Romero-Gomez, R. Ramos-Guerrero, L. Grande, L.C. de TerÃn, R. Corpas, I. Camacho, and J.D. Bautista Intestinal glutaminase activity is increased in liver cirrhosis and correlates with minimal hepatic encephalopathy J. Hepatol. 41 2004 49 54 (Pubitemid 39005152)
44. S.C. Hartman Glutaminases and gamma-glutamyltransferases P.D. Boyer, The Enzymes 3rd ed. 1971
45. M. Michalik, J. Nelson, and M. Erecińska Glutamate production in islets of Langerhans: properties of phosphate-activated glutaminase Metabolism 41 1992 1319 1326 (Pubitemid 23001569)
46. H. Lodish, A. Berk, P. Matsudaira, C.A. Kaiser, M. Krieger, M.P. Scott, S.L. Zipursky, and J. Darnell Molecular Cell Biology 2004 WH Freeman and Company, New York New York
47. C.C. White, H. Viernes, C.M. Krejsa, D. Botta, and T.J. Kavanagh Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity Anal. Biochem. 318 2003 175 180 (Pubitemid 36694107)
48. M.R. McGill, H.-M. Yan, A. Ramachandran, G.J. Murray, D.E. Rollins, and H. Jaeschke HepaRG cells: a human model to study mechanisms of acetaminophen hepatotoxicity Hepatology 53 2011 974 982
49. M.H. Creer, B.W. Lau, J.D. Jones, and K.M. Chan Pyroglutamic acidemia in an adult patient Clin. Chem. 35 1989 684 686 (Pubitemid 19111098)
50. N.J. Waters, C.J. Waterfield, R.D. Farrant, E. Holmes, and J.K. Nicholson Integrated metabonomic analysis of bromobenzene-induced hepatotoxicity: novel induction of 5-oxoprolinosis J. Proteome Res. 5 2006 1448 1459 (Pubitemid 43865813)
51. T. Soga, R. Baran, M. Suematsu, Y. Ueno, S. Ikeda, T. Sakurakawa, Y. Kakazu, T. Ishikawa, M. Robert, T. Nishioka, and M. Tomita Differential metabolomics reveals ophthalmic acid as an oxidative stress biomarker indicating hepatic glutathione consumption J. Biol. Chem. 281 2006 16768 16776
52. J.L. Snoep, C.C. van der Weijden, H.W. Andersen, H.V. Westerhoff, and P.R. Jensen DNA supercoiling in Escherichia coli is under tight and subtle homeostatic control, involving gene-expression and metabolic regulation of both topoisomerase I and DNA gyrase Eur. J. Biochem. 269 2002 1662 1669 (Pubitemid 34304465)
53. P. Daran-Lapujade, S. Rossell, W.M. van Gulik, M.A.H. Luttik, M.J.L. de Groot, M. Slijper, A.J.R. Heck, J.-M. Daran, J.H. de Winde, H.V. Westerhoff, J.T. Pronk, and B.M. Bakker The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels Proc. Natl. Acad. Sci. 104 2007 15753 15758 (Pubitemid 350035372)
54. H. Westerhoff, A. Kolodkin, R. Conradie, S. Wilkinson, F. Bruggeman, K. Krab, J. van Schuppen, H. Hardin, B. Bakker, M. Moné, K.N. Rybakova, M. Eijken, H. van Leeuwen, and J. Snoep Systems biology towards life in silico: mathematics of the control of living cells J. Math. Biol. 58 2009 7 34
55. B.G. Olivier, and J.L. Snoep Web-based kinetic modelling using JWS Online Bioinformatics 20 2004 2143 2144 (Pubitemid 39236569)
56. P.B. Watkins, N. Kaplowitz, J.T. Slattery, C.R. Colonese, S.V. Colucci, P.W. Stewart, and S.C. Harris Aminotransferase elevations in healthy adults receiving 4 grams of acetaminophen daily: a randomized controlled trial JAMA 296 2006 87 93
57. H. Lehrach, R. Subrak, P. Boyle, M. Pasterk, K. Zatloukal, H. Muller, T. Hubbard, A. Brand, M. Girolami, D. Jameson, F.J. Bruggeman, and H.V. Westerhoff ITFoM - the IT future of medicine Procedia Comput. Sci. 7 2011 26 29