Systems level metabolic phenotype of methotrexate administration in the context of non-alcoholic steatohepatitis in the rat

Toxicological Sciences

Volumn 142, Issue 1, 2014, Pages 105-116

  Kyriakides, Michael ^a   Hardwick, Rhiannon N ^b   Jin, Zhaosheng ^a   Goedken, Michael J ^c   Holmes, Elaine ^a   Cherrington, Nathan J ^b   Coen, Muireann ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ARIZONA   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Liver toxicity; Metabonomics; Methionine choline deficient diet; Methotrexate; Non alcoholic steatohepatitis; Nuclear magnetic resonance spectroscopy

Indexed keywords

ACETIC ACID; CHOLINE; CITRIC ACID; FOLIC ACID; FORMIC ACID; FORMIMINOGLUTAMIC ACID; FUMARIC ACID; GLUCOSE; GLUTATHIONE; GLYCINE; GLYCOGEN; GUANIDINOACETIC ACID; INOSINE; LACTIC ACID; LIPID; MALTOSE; MANNOSE; METHIONINE; METHOTREXATE; METHYLAMINE; NICOTINAMIDE; NUCLEIC ACID BASE; NUCLEOSIDE; PHENYLALANINE; PHOSPHORYLCHOLINE; TAURINE; TRIMETHYLAMINE; TYROSINE; URIDINE; UROCANIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG LIVER LEVEL; DRUG URINE LEVEL; FOLATE METABOLISM; HEPATITIS; HISTOPATHOLOGY; LIPID STORAGE; LIVER FIBROSIS; LIVER HYPERPLASIA; LIVER NECROSIS; LIVER TOXICITY; MALE; NONALCOHOLIC FATTY LIVER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUTRITIONAL DEFICIENCY; OXIDATIVE STRESS; PHENOTYPIC VARIATION; RAT; ANIMAL; COMPLICATION; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; ENERGY METABOLISM; LIVER; METABOLISM; METABOLOMICS; PATHOLOGY; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION; URINE;

ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-INDUCED LIVER INJURY; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; ENERGY METABOLISM; FOLIC ACID; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOMICS; METHOTREXATE; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATIVE STRESS; RATS, SPRAGUE-DAWLEY; TISSUE DISTRIBUTION;

EID: 84937580277     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu160     Document Type: Article

References (42)

1. Beckonert, O., Keun, H. C., Ebbels, T. M., Bundy, J., Holmes, E., Lindon, J. C. and Nicholson, J. K. (2007). Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat. Protoc. 2, 2692-2703.
2. Brunt, E. M. (2004). Nonalcoholic steatohepatitis. Semin. Liver Dis. 24, 3-20.
3. Burke, P. A., Stack, J. A., Wagner, D., Lewis, D. W., Jenkins, R. L. and Forse, R. A. (1997). L-[1-(13)C] Phenylalanine oxidation as a measure of hepatocyte functional capacity in end-stage liver disease. Am. J. Surg. 173, 270-273; discussion 273-274.
4. Burkhardt, J. E., Pandher, K., Solter, P. F., Troth, S. P., Boyce, R.W., Zabka, T. S. and Ennulat, D. (2011). Recommendations for the evaluation of pathology data in nonclinical safety biomarker qualification studies. Toxicol. Pathol. 39, 1129-1137.
5. Cloarec, O., Dumas, M. E., Craig, A., Barton, R. H., Trygg, J., Hudson, J., Blancher, C., Gauguier, D., Lindon, J. C., Holmes, E., et al. (2005). Statistical total correlation spectroscopy: An exploratory approach for latent biomarker identification from metabolic 1H NMR data sets. Anal. Chem. 77, 1282-1289.
6. Connor, S. C.,Wu,W., Sweatman, B. C., Manini, J., Haselden, J. N., Crowther, D. J. and Waterfield, C. J. (2004). Effects of feeding and body weight loss on the 1H-NMR-based urine metabolic profiles of male Wistar Han rats: Implications for biomarker discovery. Biomarkers 9, 156-179.
7. Coomes, E., Chan, E. S. and Reiss, A. B. (2011). Methotrexate in atherogenesis and cholesterol metabolism. Cholesterol 2011, 1-8.
8. Day, C. P. and James, O. F. (1998). Steatohepatitis: A tale of two "hits"? Gastroenterology 114, 842-845.
9. Dieterle, F., Ross, A., Schlotterbeck, G. and Senn, H. (2006). Probabilistic quotient normalization as robust method to account for dilution of complex biologicalmixtures. Application in 1H NMR metabonomics. Anal. Chem. 78, 4281-4290.
10. Farber, S., Pinkel, D., Sears, E. M. and Toch, R. (1956). Advances in chemotherapy of cancer in man. Adv. Cancer Res. 4, 1-71.
11. Fisher, C. D., Lickteig, A. J., Augustine, L. M., Ranger-Moore, J., Jackson, J. P., Ferguson, S. S. and Cherrington,N. J. (2009). Hepatic cytochrome P450 enzyme alterations in humans with progressive stages of nonalcoholic fatty liver disease. Drug Metab. Dispos. 37, 2087-2094.
12. Fonville, J. M., Richards, S. E., Barton, R.H., Boulange, C. L., Ebbels, T. M. D., Nicholson, J. K., Holmes, E. and Dumas, M.-E. (2010). The evolution of partial least squares models and related chemometric approaches in metabonomics and metabolic phenotyping. J. Chemometrics 24, 636-649.
13. Fowler, B. (2001). The folate cycle and disease in humans. Kidney Int. Suppl. 78, S221-S229.
14. Genestier, L., Paillot, R., Quemeneur, L., Izeradjene, K. and Revillard, J. P. (2000). Mechanisms of action of methotrexate. Immunopharmacology 47, 247-257.
15. Hardwick, R. N., Fisher, C. D., Canet, M. J., Scheffer, G. L. and Cherrington, N. J. (2011). Variations in ATP-binding cassette transporter regulation during the progression of human nonalcoholic fatty liver disease. Drug Metab. Dispos. 39, 2395-2402.
16. Hilton, M. A., Bertolone, S. and Patel, C. C. (1989). Daily profiles of plasma phenylalanine and tyrosine in patients with osteogenic sarcoma during treatment with high-dose methotrexate-citrovorum rescue. Med. Pediatr. Oncol. 17, 265-270.
17. Kalhan, S. C., Edmison, J., Marczewski, S., Dasarathy, S., Gruca, L. L., Bennett, C., Duenas, C. and Lopez, R. (2011). Methionine and protein metabolism in non-alcoholic steatohepatitis: Evidence for lower rate of transmethylation of methionine. Clin. Sci. 121, 179-189.
18. Lake, A. D., Novak, P., Fisher, C. D., Jackson, J. P., Hardwick, R. N., Billheimer, D. D., Klimecki,W. T. and Cherrington, N. J. (2011). Analysis of global and absorption, distribution, metabolism, and elimination gene expression in the progressive stages of human nonalcoholic fatty liver disease. Drug Metab. Dispos. 39, 1954-1960.
19. Langman, G., Hall, P. M. and Todd, G. (2001). Role of non-alcoholic steatohepatitis in methotrexate-induced liver injury. J. Gastroenterol. Hepatol. 16, 1395-1401.
20. Larter, C. Z. and Yeh, M. M. (2008). Animal models of NASH: Getting both pathology and metabolic context right. J. Gastroenterol. Hepatol. 23, 1635-1648.
21. Lazarou, J., Pomeranz, B. H. and Corey, P. N. (1998). Incidence of adverse drug reactions in hospitalized patients: A metaanalysis of prospective studies. JAMA 279, 1200-1205.
22. Leclercq, I. A., Farrell, G. C., Field, J., Bell, D. R., Gonzalez, F. J. and Robertson, G. R. (2000). CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J. Clin. Invest. 105, 1067-1075.
23. Merrell, M. D. and Cherrington, N. J. (2011). Drug metabolism alterations in nonalcoholic fatty liver disease. Drug Metab. Rev. 43, 317-334.
24. Naruhashi, K., Nadai, M., Nakao, M., Suzuki, N., Nabeshima, T. and Hasegawa, T. (2000). Changes in absorptive function of rat intestine injured by methotrexate. Clin. Exp. Pharmacol. Physiol. 27, 980-986.
25. Nicholson, J. K., Foxall, P. J., Spraul, M., Farrant, R. D. and Lindon, J. C. (1995). 750 MHz 1H and 1H-13C NMR spectroscopy of human blood plasma. Anal. Chem. 67, 793-811.
26. Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W. and Pettersson, S. (2012). Host-gut microbiota metabolic interactions. Science 336, 1262-1267.
27. Nicholson, J. K., Lindon, J. C. and Holmes, E. (1999). 'Metabonomics': Understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29, 1181-1189.
28. Perez-Carreras, M., Del Hoyo, P.,Martin, M. A., Rubio, J. C., Martin, A., Castellano, G., Colina, F., Arenas, J. and Solis-Herruzo, J. A. (2003). Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 38, 999-1007.
29. Pirmohamed, M., James, S., Meakin, S., Green, C., Scott, A. K., Walley, T. J., Farrar, K., Park, B. K. and Breckenridge, A. M. (2004). Adverse drug reactions as cause of admission to hospital: prospective analysis of 18 820 patients. BMJ 329, 15-19.
30. Puri, P., Wiest, M. M., Cheung, O., Mirshahi, F., Sargeant, C., Min, H. K., Contos, M. J., Sterling, R. K., Fuchs, M., Zhou, H., et al. (2009). The plasma lipidomic signature of nonalcoholic steatohepatitis. Hepatology 50, 1827-1838.
31. Rabinowitz, J. C. and Tabor, H. (1958). The urinary excretion of formic acid and formiminoglutamic acid in folic acid deficiency. J. Biol. Chem. 233, 252-255.
32. Rinella,M. E., Elias, M. S., Smolak, R. R., Fu, T., Borensztajn, J. and Green, R. M. (2008). Mechanisms of hepatic steatosis in mice fed a lipogenic methionine choline-deficient diet. J. Lipid Res. 49, 1068-1076.
33. Rizki, G., Arnaboldi, L., Gabrielli, B., Yan, J., Lee, G. S., Ng, R. K., Turner, S. M., Badger, T. M., Pitas, R. E. and Maher, J. J. (2006). Mice fed a lipogenic methionine-choline-deficient diet develop hypermetabolism coincident with hepatic suppression of SCD-1. J. Lipid Res. 47, 2280-2290.
34. Rosenberg, P., Urwitz, H., Johannesson, A., Ros, A. M., Lindholm, J., Kinnman, N. and Hultcrantz, R. (2007). Psoriasis patients with diabetes type 2 are at high risk of developing liver fibrosis during methotrexate treatment. J. Hepatol. 46, 1111-1118.
35. Szkudelski, T., Okulicz, M., Bialik, I. and Szkudelska, K. (2004). The influence of fasting on liver sulfhydryl groups, glutathione peroxidase and glutathione-S-transferase activities in the rat. J. Physiol. Biochem. 60, 1-6.
36. Tanaka, N., Matsubara, T., Krausz, K. W., Patterson, A. D. and Gonzalez, F. J. (2012). Disruption of phospholipid and bile acid homeostasis in mice with nonalcoholic steatohepatitis. Hepatology 56, 118-129.
37. Wang, Z., Chen, Z., Yang, S., Wang, Y., Yu, L., Zhang, B., Rao, Z., Gao, J. and Tu, S. (2012). (1)H NMR-based metabolomic analysis for identifying serum biomarkers to evaluate methotrexate treatment in patients with early rheumatoid arthritis. Exp. Ther. Med. 4, 165-171.
38. Waters, N. J., Waterfield, C. J., Farrant, R. D., Holmes, E. and Nicholson, J. K. (2005). Metabonomic deconvolution of embedded toxicity: Application to thioacetamide hepato-and nephrotoxicity. Chem. Res. Toxicol. 18, 639-654.
39. West, S. G. (1997). Methotrexate hepatotoxicity. Rheum. Dis. Clin. North Am. 23, 883-915.
40. Widemann, B. C. and Adamson, P. C. (2006). Understanding and managing methotrexate nephrotoxicity. Oncologist 11, 694-703.
41. Williams, C.D., Stengel, J., Asike, M. I., Torres,D. M., Shaw, J., Contreras, M., Landt, C. L. and Harrison, S. A. (2011). Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: A prospective study. Gastroenterology 140, 124-131.
42. Yamamoto, N., Oliveira, M. B., Campello Ade, P., Lopes, L. C. and Kluppel, M. L. (1988). Methotrexate: Studies on the cellular metabolism. I. Effect on mitochondrial oxygen uptake and oxidative phosphorylation. Cell Biochem. Funct. 6, 61-66.