Pharmacometabonomic investigation of dynamic metabolic phenotypes associated with variability in response to galactosamine hepatotoxicity

Journal of Proteome Research

Volumn 11, Issue 4, 2012, Pages 2427-2440

  Coen, Muireann ^a   Goldfain Blanc, Françoise ^b   Rolland Valognes, Gaëlle ^c   Walther, Bernard ^b   Robertson, Donald G ^d   Holmes, Elaine ^a   Lindon, John C ^a   Nicholson, Jeremy K ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

^c INSTITUT DE RECHERCHES SERVIER   (France)

^d BRISTOL MYERS SQUIBB   (United States)

Author keywords

galactosamine; inter individual variability; metabonomics; NMR spectroscopy; pharmacometabonomics

Indexed keywords

CYTOKINE; GALACTOSAMINE; N ACETYLGLUCOSAMINE; PYRAZINE; TOXIN; XENOBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL CHEMISTRY; CONTROLLED STUDY; FECES; HEPATITIS; HISTOPATHOLOGY; INTESTINE FLORA; LIVER TOXICITY; MALE; METABOLITE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHENOTYPIC VARIATION; PRIORITY JOURNAL; RAT; TOXICITY;

ANIMALS; CYTOKINES; DRUG-INDUCED LIVER INJURY; FECES; GALACTOSAMINE; LEAST-SQUARES ANALYSIS; LIVER; MALE; METABOLOME; METABOLOMICS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84859594012     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr201161f     Document Type: Article

References (78)

1. Guengerich, F. P. Mechanisms of drug toxicity and relevance to pharmaceutical development Drug Metab. Pharmacokinet. 2011, 26 (1) 3-14
2. Kola, I.; Landis, J. Can the pharmaceutical industry reduce attrition rates? Nat. Rev. Drug Discovery 2004, 3 (8) 711-5
3. Lazarou, J.; Pomeranz, B. H.; Corey, P. N. Incidence of adverse drug reactions in hospitalized patients: a meta-analysis of prospective studies J. Am. Med. Assoc. 1998, 279 (15) 1200-5
4. Decker, K.; Keppler, D. Galactosamine induced liver injury Prog. Liver Dis. 1972, 4, 183-99
5. Decker, K.; Keppler, D. Galactosamine hepatitis: key role of the nucleotide deficiency period in the pathogenesis of cell injury and cell death Rev. Physiol. Biochem. Pharmacol. 1974, 71, 77-106
6. Decker, K.; Keppler, D.; Pausch, J. The regulation of pyrimidine nucleotide level and its role in experimental hepatitis Adv. Enzyme Regul. 1973, 11, 205-30
7. Grun, M.; Liehr, H.; Rasenack, U. Significance of endotoxaemia in experimental "galactosamine-hepatitis" in the rat Acta Hepatogastroenterol. (Stuttgart) 1977, 24 (2) 64-81
8. Kasravi, F. B.; Wang, L.; Wang, X. D.; Molin, G.; Bengmark, S.; Jeppsson, B. Bacterial translocation in acute liver injury induced by D-galactosamine Hepatology 1996, 23 (1) 97-103
9. Liehr, H.; Grun, M.; Seelig, H. P.; Seelig, R.; Reutter, W.; Heine, W. D. On the pathogenesis of galactosamine hepatitis. Indications of extrahepatocellular mechanisms responsible for liver cell death Virchows Arch. B 1978, 26 (4) 331-44
10. Shiratori, Y.; Tanaka, M.; Hai, K.; Kawase, T.; Shirna, S.; Sugimoto, T. Role of endotoxin-responsive macrophages in hepatic injury Hepatology 1990, 11 (2) 183-92
11. Galanos, C.; Freudenberg, M. A.; Reutter, W. Galactosamine-induced sensitization to the lethal effects of endotoxin Proc. Natl. Acad. Sci. U.S.A. 1979, 76 (11) 5939-43
12. Coen, M.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. NMR-based metabolic profiling and metabonomic approaches to problems in molecular toxicology Chem. Res. Toxicol. 2008, 21 (1) 9-27
13. Lindon, J. C.; Holmes, E.; Nicholson, J. K. Metabonomics techniques and applications to pharmaceutical research & development Pharm. Res. 2006, 23 (6) 1075-88
14. Lindon, J. C.; Holmes, E.; Nicholson, J. K. Metabonomics in pharmaceutical R&D FEBS J. 2007, 274 (5) 1140-51
15. Nicholson, J. K.; Holmes, E.; Lindon, J. C.; Wilson, I. D. The challenges of modeling mammalian biocomplexity Nat. Biotechnol. 2004, 22 (10) 1268-74
16. Nicholson, J. K.; Holmes, E.; Wilson, I. D. Gut microorganisms, mammalian metabolism and personalized health care Nat. Rev. Microbiol. 2005, 3 (5) 431-8
17. Nicholson, J. K.; Wilson, I. D.; Lindon, J. C. Pharmacometabonomics as an effector for personalized medicine Pharmacogenomics 2011, 12 (1) 103-11
18. Wilson, I. D. Drugs, bugs, and personalized medicine: pharmacometabonomics enters the ring Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (34) 14187-8
19. Clayton, T. A.; Baker, D.; Lindon, J. C.; Everett, J. R.; Nicholson, J. K. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (34) 14728-33
20. Clayton, T. A.; Lindon, J. C.; Cloarec, O.; Antti, H.; Charuel, C.; Hanton, G.; Provost, J. P.; Le Net, J. L.; Baker, D.; Walley, R. J.; Everett, J. R.; Nicholson, J. K. Pharmaco-metabonomic phenotyping and personalized drug treatment Nature 2006, 440 (7087) 1073-7
21. Winnike, J. H.; Li, Z.; Wright, F. A.; Macdonald, J. M.; OConnell, T. M.; Watkins, P. B. Use of pharmaco-metabonomics for early prediction of acetaminophen-induced hepatotoxicity in humans Clin. Pharmacol. Ther. 2010, 88 (1) 45-51
22. Li, H.; Ni, Y.; Su, M.; Qiu, Y.; Zhou, M.; Qiu, M.; Zhao, A.; Zhao, L.; Jia, W. Pharmacometabonomic phenotyping reveals different responses to xenobiotic intervention in rats J. Proteome Res. 2007, 6 (4) 1364-70
23. Backshall, A.; Sharma, R.; Clarke, S. J.; Keun, H. C. Pharmacometabonomic profiling as a predictor of toxicity in patients with inoperable colorectal cancer treated with capecitabine Clin. Cancer Res. 2011, 17 (9) 3019-28
24. Stebbing, J.; Sharma, A.; North, B.; Athersuch, T. J.; Zebrowski, A.; Pchejetski, D.; Coombes, R. C.; Nicholson, J. K.; Keun, H. C. A metabolic phenotyping approach to understanding relationships between metabolic syndrome and breast tumour responses to chemotherapy. Ann. Oncol. 2011, E-pub ahead of print; DOI: 10.1093/annonc/mdr347.
25. Ebbels, T. M.; Keun, H. C.; Beckonert, O. P.; Bollard, M. E.; Lindon, J. C.; Holmes, E.; Nicholson, J. K. Prediction and classification of drug toxicity using probabilistic modeling of temporal metabolic data: the consortium on metabonomic toxicology screening approach J. Proteome Res. 2007, 6 (11) 4407-22
26. Lindon, J. C.; Keun, H. C.; Ebbels, T. M.; Pearce, J. M.; Holmes, E.; Nicholson, J. K. The Consortium for Metabonomic Toxicology (COMET): aims, activities and achievements Pharmacogenomics 2005, 6 (7) 691-9
27. Lindon, J. C.; Nicholson, J. K.; Holmes, E.; Antti, H.; Bollard, M. E.; Keun, H.; Beckonert, O.; Ebbels, T. M.; Reily, M. D.; Robertson, D.; Stevens, G. J.; Luke, P.; Breau, A. P.; Cantor, G. H.; Bible, R. H.; Niederhauser, U.; Senn, H.; Schlotterbeck, G.; Sidelmann, U. G.; Laursen, S. M.; Tymiak, A.; Car, B. D.; Lehman-McKeeman, L.; Colet, J. M.; Loukaci, A.; Thomas, C. Contemporary issues in toxicology the role of metabonomics in toxicology and its evaluation by the COMET project Toxicol. Appl. Pharmacol. 2003, 187 (3) 137-46
28. Coen, M. A metabonomic approach for mechanistic exploration of pre-clinical toxicology Toxicology 2010, 278 (3) 326-40
29. Coen, M.; Hong, Y. S.; Clayton, T. A.; Rohde, C. M.; Pearce, J. T.; Reily, M. D.; Robertson, D. G.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. The mechanism of galactosamine toxicity revisited; a metabonomic study J. Proteome Res. 2007, 6 (7) 2711-9
30. Coen, M.; Want, E. J.; Clayton, T. A.; Rhode, C. M.; Hong, Y. S.; Keun, H. C.; Cantor, G. H.; Metz, A. L.; Robertson, D. G.; Reily, M. D.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Mechanistic aspects and novel biomarkers of responder and non-responder phenotypes in galactosamine-induced hepatitis J. Proteome Res. 2009, 8 (11) 5175-87
31. Shipkova, P.; Vassallo, J. D.; Aranibar, N.; Hnatyshyn, S.; Zhang, H.; Clayton, T. A.; Cantor, G. H.; Sanders, M.; Coen, M.; Lindon, J. C.; Holmes, E.; Nicholson, J. K.; Lehman-McKeeman, L. Urinary metabolites of 2-bromoethanamine identified by stable isotope labelling: evidence for carbamoylation and glutathione conjugation Xenobiotica 2011, 41 (2) 144-54
32. Spagou, K.; Wilson, I. D.; Masson, P.; Theodoridis, G.; Raikos, N.; Coen, M.; Holmes, E.; Lindon, J. C.; Plumb, R. S.; Nicholson, J. K.; Want, E. J. HILIC-UPLC-MS for exploratory urinary metabolic profiling in toxicological studies Anal. Chem. 2011, 83 (1) 382-90
33. Want, E. J.; Coen, M.; Masson, P.; Keun, H. C.; Pearce, J. T.; Reily, M. D.; Robertson, D. G.; Rohde, C. M.; Holmes, E.; Lindon, J. C.; Plumb, R. S.; Nicholson, J. K. Ultra performance liquid chromatography-mass spectrometry profiling of bile acid metabolites in biofluids: application to experimental toxicology studies Anal. Chem. 2010, 82 (12) 5282-9
34. Beckwith-Hall, B., PhD Thesis, University of London, 1998.
35. Clayton, T. A., PhD Thesis, University of London, 2001.
36. So, P. W., PhD Thesis, University of London, 1996.
37. Beckwith-Hall, B. M.; Nicholson, J. K.; Nicholls, A. W.; Foxall, P. J.; Lindon, J. C.; Connor, S. C.; Abdi, M.; Connelly, J.; Holmes, E. Nuclear magnetic resonance spectroscopic and principal components analysis investigations into biochemical effects of three model hepatotoxins Chem. Res. Toxicol. 1998, 11 (4) 260-72
38. Garrod, S.; Bollard, M. E.; Nicholls, A. W.; Connor, S. C.; Connelly, J.; Nicholson, J. K.; Holmes, E. Integrated metabonomic analysis of the multiorgan effects of hydrazine toxicity in the rat Chem. Res. Toxicol. 2005, 18 (2) 115-22
39. Waters, N. J.; Holmes, E.; Williams, A.; Waterfield, C. J.; Farrant, R. D.; Nicholson, J. K. NMR and pattern recognition studies on the time-related metabolic effects of alpha-naphthylisothiocyanate on liver, urine, and plasma in the rat: an integrative metabonomic approach Chem. Res. Toxicol. 2001, 14 (10) 1401-12
40. Waters, N. J.; Waterfield, C. J.; Farrant, R. D.; Holmes, E.; Nicholson, J. K. Integrated metabonomic analysis of bromobenzene-induced hepatotoxicity: novel induction of 5-oxoprolinosis J. Proteome Res. 2006, 5 (6) 1448-59
41. Yap, I. K.; Clayton, T. A.; Tang, H.; Everett, J. R.; Hanton, G.; Provost, J. P.; Le Net, J. L.; Charuel, C.; Lindon, J. C.; Nicholson, J. K. An integrated metabonomic approach to describe temporal metabolic disregulation induced in the rat by the model hepatotoxin allyl formate J. Proteome Res. 2006, 5 (10) 2675-84
42. Beckonert, O.; Keun, H. C.; Ebbels, T. M.; Bundy, J.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts Nat. Protoc. 2007, 2 (11) 2692-703
43. 1H NMR metabonomics Anal. Chem. 2006, 78 (13) 4281-90
44. 1H NMR spectroscopic metabonomic studies Anal. Chem. 2005a, 77 (2) 517-26
45. Trygg, J.; Holmes, E.; Lundstedt, T. Chemometrics in metabonomics J. Proteome Res. 2007, 6 (2) 469-79
46. Trygg, J.; Wold, S. O2-PLS, a two-block (X-Y) latent variable regression (LVR) method with an integral OSC filter J. Chemom. 2003, 17, 53-64
47. Keppler, D.; Lesch, R.; Reutter, W.; Decker, K. Experimental hepatitis induced by D-galactosamine Exp. Mol. Pathol. 1968, 9 (2) 279-90
48. Reutter, W.; Reynolds, R. Inhibition of induction of tyrosine aminotransferase following administration of D-galactosamine Hoppe-Seyler's Z. Physiol. Chem. 1972, 353 (10) 1561
49. Reynolds, R. D.; Reutter, W. Inhibition of induction of rat liver tyrosine aminotransferase by D-galactosamine J. Biol. Chem. 1973, 248 (5) 1562-7
50. Koff, R. S.; Fitts, J. J.; Sabesin, S. M.; Zimmerman, H. J. D-galactosamine hepatotoxicity. II. Mechanism of fatty liver production Proc. Soc. Exp. Biol. Med. 1971, 138 (1) 89-92
51. Medline, A.; Schaffner, F.; Popper, H. Ultrastructural features in galactosamine-induced hepatitis Exp. Mol. Pathol. 1970, 12 (2) 201-11
52. McMillan, J. M.; McMillan, D. C. S-adenosylmethionine but not glutathione protects against galactosamine-induced cytotoxicity in rat hepatocyte cultures Toxicology 2006, 222 (3) 175-84
53. Hamer, H. M.; Jonkers, D.; Venema, K.; Vanhoutvin, S.; Troost, F. J.; Brummer, R. J. Review article: the role of butyrate on colonic function Aliment. Pharmacol. Ther. 2008, 27 (2) 104-19
54. Scharlau, D.; Borowicki, A.; Habermann, N.; Hofmann, T.; Klenow, S.; Miene, C.; Munjal, U.; Stein, K.; Glei, M. Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre Mutat. Res. 2009, 682 (1) 39-53
55. Levine, M. On the significance of the Voges-Proskauer reaction J. Bacteriol. 1916, 1 (2) 153-64
56. Xiao, Z.; Xu, P. Acetoin metabolism in bacteria Crit. Rev. Microbiol. 2007, 33 (2) 127-40
57. Brinkkotter, A.; Kloss, H.; Alpert, C.; Lengeler, J. W. Pathways for the utilization of N-acetyl-galactosamine and galactosamine in Escherichia coli Mol. Microbiol. 2000, 37 (1) 125-35
58. Brinkkotter, A.; Shakeri-Garakani, A.; Lengeler, J. W. Two class II D-tagatose-bisphosphate aldolases from enteric bacteria Arch. Microbiol. 2002, 177 (5) 410-9
59. Shakeri-Garakani, A.; Brinkkotter, A.; Schmid, K.; Turgut, S.; Lengeler, J. W. The genes and enzymes for the catabolism of galactitol, D-tagatose, and related carbohydrates in Klebsiella oxytoca M5a1 and other enteric bacteria display convergent evolution Mol. Genet. Genomics 2004, 271 (6) 717-28
60. Keppler, D. O.; Rudigier, J. F.; Bischoff, E.; Decker, K. F. The trapping of uridine phosphates by D-galactosamine, D-glucosamine, and 2-deoxy-D-galactose. A study on the mechanism of galactosamine hepatitis Eur. J. Biochem. 1970, 17 (2) 246-53
61. Rolando, N.; Wade, J.; Davalos, M.; Wendon, J.; Philpott-Howard, J.; Williams, R. The systemic inflammatory response syndrome in acute liver failure Hepatology 2000, 32 (4 Pt 1) 734-9
62. Adawi, D.; Ahrne, S.; Molin, G. Effects of different probiotic strains of Lactobacillus and Bifidobacterium on bacterial translocation and liver injury in an acute liver injury model Int. J. Food Microbiol. 2001, 70 (3) 213-20
63. Adawi, D.; Kasravi, F. B.; Molin, G.; Jeppsson, B. Effect of Lactobacillus supplementation with and without arginine on liver damage and bacterial translocation in an acute liver injury model in the rat Hepatology 1997, 25 (3) 642-7
64. Kasravi, F. B.; Adawi, D.; Molin, G.; Bengmark, S.; Jeppsson, B. Effect of oral supplementation of lactobacilli on bacterial translocation in acute liver injury induced by D-galactosamine J Hepatol 1997, 26 (2) 417-24
65. Osman, N.; Adawi, D.; Ahrne, S.; Jeppsson, B.; Molin, G. Endotoxin- and D-galactosamine-induced liver injury improved by the administration of Lactobacillus, Bifidobacterium and blueberry Dig. Liver Dis. 2007, 39 (9) 849-56
66. Shiratori, Y.; Kawase, T.; Shiina, S.; Okano, K.; Sugimoto, T.; Teraoka, H.; Matano, S.; Matsumoto, K.; Kamii, K. Modulation of hepatotoxicity by macrophages in the liver Hepatology 1988, 8 (4) 815-21
67. Wells, C. L.; Maddaus, M. A.; Simmons, R. L. Role of the macrophage in the translocation of intestinal bacteria Arch. Surg. 1987, 122 (1) 48-53
68. Shiratori, Y.; Hikiba, Y.; Mawet, E.; Niwa, Y.; Matsumura, M.; Kato, N.; Shiina, S.; Tada, M.; Komatsu, Y.; Kawabe, T. Modulation of KC/gro protein (interleukin-8 related protein in rodents) release from hepatocytes by biologically active mediators Biochem. Biophys. Res. Commun. 1994, 203 (3) 1398-403
69. Mera, S.; Tatulescu, D.; Cismaru, C.; Bondor, C.; Slavcovici, A.; Zanc, V.; Carstina, D.; Oltean, M. Multiplex cytokine profiling in patients with sepsis APMIS 2011, 119 (2) 155-63
70. Li, L. J.; Wu, Z. W.; Xiao, D. S.; Sheng, J. F. Changes of gut flora and endotoxin in rats with D-galactosamine-induced acute liver failure World J. Gastroenterol. 2004, 10 (14) 2087-90
71. Saric, J.; Li, J. V.; Swann, J. R.; Utzinger, J.; Calvert, G.; Nicholson, J. K.; Dirnhofer, S.; Dallman, M. J.; Bictash, M.; Holmes, E. Integrated cytokine and metabolic analysis of pathological responses to parasite exposure in rodents J. Proteome Res. 2008, 9 (5) 2255-64
72. Bell, J. D.; Brown, J. C.; Nicholson, J. K.; Sadler, P. J. Assignment of resonances for 'acute-phase' glycoproteins in high resolution proton NMR spectra of human blood plasma FEBS Lett. 1987, 215 (2) 311-5
73. 1H n.m.r. studies of vertebrate blood and plasma Biochem. J. 1983, 211 (3) 605-15
74. Libert, C.; Brouckaert, P.; Fiers, W. Protection by alpha 1-acid glycoprotein against tumor necrosis factor-induced lethality J. Exp. Med. 1994, 180 (4) 1571-5
75. Al Mardini, H.; al Jumaili, B.; Record, C. O.; Burke, D. Effect of protein and lactulose on the production of gamma-aminobutyric acid by faecal Escherichia coli Gut 1991, 32 (9) 1007-10
76. Jones, E. A.; Schafer, D. F.; Ferenci, P.; Pappas, S. C. The GABA hypothesis of the pathogenesis of hepatic encephalopathy: current status Yale J. Biol. Med. 1984, 57 (3) 301-16
77. Schafer, D. F.; Jones, E. A. Hepatic encephalopathy and the gamma-aminobutyric-acid neurotransmitter system Lancet 1982, 1 (8262) 18-20
78. Li, J. V.; Ashrafian, H.; Bueter, M.; Kinross, J.; Sands, C.; le Roux, C. W.; Bloom, S. R.; Darzi, A.; Athanasiou, T.; Marchesi, J. R.; Nicholson, J. K.; Holmes, E. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk Gut 2011, 60 (9) 1214-23