UPLC-MS-based urine metabolomics reveals indole-3-lactic acid and phenyllactic acid as conserved biomarkers for alcohol-induced liver disease in the Ppara-null mouse model

Journal of Proteome Research

Volumn 10, Issue 9, 2011, Pages 4120-4133

  Manna, Soumen K ^a   Patterson, Andrew D ^a   Yang, Qian ^b   Krausz, Kristopher W ^a   Idle, Jeffrey R ^c   Fornace, Albert J ^b   Gonzalez, Frank J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

alcohol; biomarker; genetic background; liver disease; metabolomics; Ppara null mouse; UPLC ESI QTOF mass spectrometry

Indexed keywords

4 HYDROXYPHENYLACETIC ACID; ACETURIC ACID; ADIPIC ACID; ATROLACTIC ACID; ETHYL BETA GLUCURONIDE; ETHYLSULFATE; GLYCINE DERIVATIVE; INDOLELACTIC ACID; LACTIC ACID DERIVATIVE; PIMELIC ACID; SULFATE; TAURINE; UNCLASSIFIED DRUG; XANTHURENIC ACID;

ALCOHOL CONSUMPTION; ALCOHOL LIVER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HISTOPATHOLOGY; MALE; MASS SPECTROMETRY; METABOLOMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; URINALYSIS; URINARY EXCRETION;

ALCOHOLS; ANALYSIS OF VARIANCE; ANIMALS; BIOLOGICAL MARKERS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; INDOLES; LACTATES; LIVER DISEASES, ALCOHOLIC; MALE; MASS SPECTROMETRY; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MICE; MICE, KNOCKOUT; PHENYLALANINE; PPAR ALPHA; PRINCIPAL COMPONENT ANALYSIS; TAURINE; TRYPTOPHAN;

MUS;

EID: 80052465307     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200310s     Document Type: Article

References (48)

1. Mandayam, S.; Jamal, M. M.; Morgan, T. R. Epidemiology of alcoholic liver disease Semin. Liver Dis. 2004, 24 (3) 217-32 (Pubitemid 39167681)
2. Shibuya, A.; Yoshida, A. Genotypes of alcohol-metabolizing enzymes in Japanese with alcohol liver diseases: a strong association of the usual Caucasian-type aldehyde dehydrogenase gene (ALDH1(2)) with the disease Am. J. Hum. Genet. 1988, 43 (5) 744-8 (Pubitemid 18269256)
3. Pirmohamed, M.; Kitteringham, N. R.; Quest, L. J.; Allott, R. L.; Green, V. J.; Gilmore, I. T.; Park, B. K. Genetic polymorphism of cytochrome P4502E1 and risk of alcoholic liver disease in Caucasians Pharmacogenetics 1995, 5 (6) 351-7 (Pubitemid 26010114)
4. Tanaka, F.; Shiratori, Y.; Yokosuka, O.; Imazeki, F.; Tsukada, Y.; Omata, M. High incidence of ADH2*1/ALDH2*1 genes among Japanese alcohol dependents and patients with alcoholic liver disease Hepatology 1996, 23 (2) 234-9 (Pubitemid 26045938)
5. Zintzaras, E.; Stefanidis, I.; Santos, M.; Vidal, F. Do alcohol-metabolizing enzyme gene polymorphisms increase the risk of alcoholism and alcoholic liver disease? Hepatology 2006, 43 (2) 352-61
6. Sherva, R.; Rice, J. P.; Neuman, R. J.; Rochberg, N.; Saccone, N. L.; Bierut, L. J. Associations and interactions between SNPs in the alcohol metabolizing genes and alcoholism phenotypes in European Americans Alcohol.: Clin. Exp. Res. 2009, 33 (5) 848-57
7. Auguet, T.; Vidal, F.; Broch, M.; Olona, M.; Aguilar, C.; Morancho, B.; Lopez-Dupla, M.; Quer, J. C.; Sirvent, J. J.; Richart, C. Polymorphisms in the interleukin-10 gene promoter and the risk of alcoholism and alcoholic liver disease in Caucasian Spaniard men Alcohol 2010, 44 (3) 211-6
8. Linneberg, A.; Gonzalez-Quintela, A.; Vidal, C.; Jorgensen, T.; Fenger, M.; Hansen, T.; Pedersen, O.; Husemoen, L. L. Genetic determinants of both ethanol and acetaldehyde metabolism influence alcohol hypersensitivity and drinking behaviour among Scandinavians Clin. Exp. Allergy 2010, 40 (1) 123-30
9. O'Shea, R. S.; Dasarathy, S.; McCullough, A. J. Alcoholic liver disease Am. J. Gastroenterol. 2010, 105 (1) 14-32
10. Chen, A. C.; Manz, N.; Tang, Y.; Rangaswamy, M.; Almasy, L.; Kuperman, S.; Nurnberger, J., Jr.; O'Connor, S. J.; Edenberg, H. J.; Schuckit, M. A.; Tischfield, J.; Foroud, T.; Bierut, L. J.; Rohrbaugh, J.; Rice, J. P.; Goate, A.; Hesselbrock, V.; Porjesz, B. Single-nucleotide polymorphisms in corticotropin releasing hormone receptor 1 gene (CRHR1) are associated with quantitative trait of event-related potential and alcohol dependence Alcohol.: Clin. Exp. Res. 2010, 34 (6) 988-96
11. Hoyert, D. L.; Heron, M. P.; Murphy, S. L.; Kung, H. C. Deaths: final data for 2003 Natl. Vital Stat. Rep. 2006, 54 (13) 1-120
12. Welte, J.; Barnes, G.; Wieczorek, W.; Tidwell, M. C.; Parker, J. Alcohol and gambling pathology among U.S. adults: prevalence, demographic patterns and comorbidity J. Stud. Alcohol 2001, 62 (5) 706-12 (Pubitemid 33021410)
13. Grove, J.; Brown, A. S.; Daly, A. K.; Bassendine, M. F.; James, O. F.; Day, C. P. The RsaI polymorphism of CYP2E1 and susceptibility to alcoholic liver disease in Caucasians: effect on age of presentation and dependence on alcohol dehydrogenase genotype Pharmacogenetics 1998, 8 (4) 335-42 (Pubitemid 28372327)
14. Wong, N. A.; Rae, F.; Bathgate, A.; Smith, C. A.; Harrison, D. J. Polymorphisms of the gene for microsomal epoxide hydrolase and susceptibility to alcoholic liver disease and hepatocellular carcinoma in a Caucasian population Toxicol. Lett. 2000, 115 (1) 17-22 (Pubitemid 30417451)
15. Teli, M. R.; Day, C. P.; Burt, A. D.; Bennett, M. K.; James, O. F. Determinants of progression to cirrhosis or fibrosis in pure alcoholic fatty liver Lancet 1995, 346 (8981) 987-90
16. Schutte, K.; Bornschein, J.; Malfertheiner, P. Hepatocellular carcinoma - epidemiological trends and risk factors Dig. Dis. 2009, 27 (2) 80-92
17. Sherman, M. Hepatocellular carcinoma: New and emerging risks Dig. Liver Dis. 2010, 42 (Suppl 3) S215-22
18. Levitsky, J.; Mailliard, M. E. Diagnosis and therapy of alcoholic liver disease Semin. Liver Dis. 2004, 24 (3) 233-47 (Pubitemid 39167682)
19. Sharpe, P. C. Biochemical detection and monitoring of alcohol abuse and abstinence Ann. Clin. Biochem. 2001, 38 (Pt 6) 652-64 (Pubitemid 33702271)
20. Cadranel, J. F.; Rufat, P.; Degos, F. Practices of liver biopsy in France: results of a prospective nationwide survey. For the Group of Epidemiology of the French Association for the Study of the Liver (AFEF) Hepatology 2000, 32 (3) 477-81
21. Martin, P. G.; Guillou, H.; Lasserre, F.; Dejean, S.; Lan, A.; Pascussi, J. M.; Sancristobal, M.; Legrand, P.; Besse, P.; Pineau, T. Novel aspects of PPARalpha-mediated regulation of lipid and xenobiotic metabolism revealed through a nutrigenomic study Hepatology 2007, 45 (3) 767-77 (Pubitemid 46450628)
22. Rakhshandehroo, M.; Sanderson, L. M.; Matilainen, M.; Stienstra, R.; Carlberg, C.; de Groot, P. J.; Muller, M.; Kersten, S. Comprehensive analysis of PPARalpha-dependent regulation of hepatic lipid metabolism by expression profiling PPAR Res. 2007, 2007, 26839
23. Nakajima, T.; Kamijo, Y.; Tanaka, N.; Sugiyama, E.; Tanaka, E.; Kiyosawa, K.; Fukushima, Y.; Peters, J. M.; Gonzalez, F. J.; Aoyama, T. Peroxisome proliferator-activated receptor alpha protects against alcohol-induced liver damage Hepatology 2004, 40 (4) 972-80 (Pubitemid 39288131)
24. Manna, S. K.; Patterson, A. D.; Yang, Q.; Krausz, K. W.; Li, H.; Idle, J. R.; Fornace, A. J., Jr.; Gonzalez, F. J. Identification of noninvasive biomarkers for alcohol-induced liver disease using urinary metabolomics and the Ppara-null mouse J. Proteome Res. 2010, 9 (8) 4176-88
25. Loftus, N.; Barnes, A.; Ashton, S.; Michopoulos, F.; Theodoridis, G.; Wilson, I.; Ji, C.; Kaplowitz, N. Metabonomic investigation of liver profiles of nonpolar metabolites obtained from alcohol-dosed rats and mice using high mass accuracy MSn analysis J. Proteome Res. 2011, 10 (2) 705-13
26. Bradford, B. U.; O'Connell, T. M.; Han, J.; Kosyk, O.; Shymonyak, S.; Ross, P. K.; Winnike, J.; Kono, H.; Rusyn, I. Metabolomic profiling of a modified alcohol liquid diet model for liver injury in the mouse uncovers new markers of disease Toxicol. Appl. Pharmacol. 2008, 232 (2) 236-43
27. Fernando, H.; Kondraganti, S.; Bhopale, K. K.; Volk, D. E.; Neerathilingam, M.; Kaphalia, B. S.; Luxon, B. A.; Boor, P. J.; Shakeel Ansari, G. A. (1)H and (3)(1)P NMR lipidome of ethanol-induced fatty liver Alcohol.: Clin. Exp. Res. 2010, 34 (11) 1937-47
28. Nguyen, P. V.; Abel, T.; Kandel, E. R.; Bourtchouladze, R. Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice Learn. Mem. 2000, 7 (3) 170-9 (Pubitemid 30407782)
29. Syn, W. K.; Yang, L.; Chiang, D. J.; Qian, Y.; Jung, Y.; Karaca, G.; Choi, S. S.; Witek, R. P.; Omenetti, A.; Pereira, T. A.; Diehl, A. M. Genetic differences in oxidative stress and inflammatory responses to diet-induced obesity do not alter liver fibrosis in mice Liver Int. 2009, 29 (8) 1262-72
30. Liu, J.; Corton, C.; Dix, D. J.; Liu, Y.; Waalkes, M. P.; Klaassen, C. D. Genetic background but not metallothionein phenotype dictates sensitivity to cadmium-induced testicular injury in mice Toxicol. Appl. Pharmacol. 2001, 176 (1) 1-9 (Pubitemid 32977285)
31. Pearson, K. On lines and planes of closest fit to systems of points in space Philos. Mag. 1901, 2 (6) 559-572
32. Suhre, K.; Schmitt-Kopplin, P. MassTRIX: mass translator into pathways Nucleic Acids Res. 2008, 36 (Web Server) W481-4
33. Kind, T.; Fiehn, O. Seven Golden Rules for heuristic filtering of molecular formulas obtained by accurate mass spectrometry BMC Bioinform. 2007, 8, 105
34. Cui, Q.; Lewis, I. A.; Hegeman, A. D.; Anderson, M. E.; Li, J.; Schulte, C. F.; Westler, W. M.; Eghbalnia, H. R.; Sussman, M. R.; Markley, J. L. Metabolite identification via the Madison Metabolomics Consortium Database Nat. Biotechnol. 2008, 26 (2) 162-4 (Pubitemid 351225941)
35. Smith, C. A.; O'Maille, G.; Want, E. J.; Qin, C.; Trauger, S. A.; Brandon, T. R.; Custodio, D. E.; Abagyan, R.; Siuzdak, G. METLIN: a metabolite mass spectral database Ther. Drug Monit. 2005, 27 (6) 747-51 (Pubitemid 44391729)
36. Albano, E. Alcohol, oxidative stress and free radical damage Proc. Nutr. Soc. 2006, 65 (3) 278-90 (Pubitemid 46323842)
37. Das, S. K.; Vasudevan, D. M. Alcohol-induced oxidative stress Life Sci. 2007, 81 (3) 177-87 (Pubitemid 46978376)
38. Wikoff, W. R.; Anfora, A. T.; Liu, J.; Schultz, P. G.; Lesley, S. A.; Peters, E. C.; Siuzdak, G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (10) 3698-703
39. Nicholson, J. K.; Wilson, I. D. Opinion: understanding 'global' systems biology: metabonomics and the continuum of metabolism Nat. Rev. Drug Discovery 2003, 2 (8) 668-76 (Pubitemid 37361770)
40. Cariello, N. F.; Romach, E. H.; Colton, H. M.; Ni, H.; Yoon, L.; Falls, J. G.; Casey, W.; Creech, D.; Anderson, S. P.; Benavides, G. R.; Hoivik, D. J.; Brown, R.; Miller, R. T. Gene expression profiling of the PPAR-alpha agonist ciprofibrate in the cynomolgus monkey liver Toxicol. Sci. 2005, 88 (1) 250-64 (Pubitemid 41548767)
41. Shin, M.; Kim, I.; Inoue, Y.; Kimura, S.; Gonzalez, F. J. Regulation of mouse hepatic alpha-amino-beta-carboxymuconate-epsilon-semialdehyde decarboxylase, a key enzyme in the tryptophan-nicotinamide adenine dinucleotide pathway, by hepatocyte nuclear factor 4alpha and peroxisome proliferator- activated receptor alpha Mol. Pharmacol. 2006, 70 (4) 1281-90 (Pubitemid 44435980)
42. Recasens, M.; Benezra, R.; Basset, P.; Mandel, P. Cysteine sulfinate aminotransferase and aspartate aminotransferase isoenzymes of rat brain. Purification, characterization, and further evidence for identity Biochemistry 1980, 19 (20) 4583-9
43. Yagi, T.; Kagamiyama, H.; Motosugi, K.; Nozaki, M.; Soda, K. Crystallization and properties of aspartate aminotransferase from Escherichia coli B FEBS Lett. 1979, 100 (1) 81-4
44. Morland, J. Effect of chronic ethanol treatment on tryptophan oxygenase, tyrosine aminotransferase and general protein metabolism in the intact and perfused rat liver Biochem. Pharmacol. 1974, 23 (1) 21-35
45. Jean, M.; DeMoss, R. D. Indolelactate dehydrogenase from Clostridium sporogenes Can. J. Microbiol. 1968, 14 (4) 429-35
46. Leelayoova, S.; Marbury, D.; Rainey, P. M.; Mackenzie, N. E.; Hall, J. E. In vitro tryptophan catabolism by Leishmania donovani donovani promastigotes J. Protozool. 1992, 39 (2) 350-8
47. Owen, T. G.; Hochachka, P. W. Purification and properties of dolphin muscle aspartate and alanine transaminases and thier possible roles in the energy metabolism of diving mammals Biochem. J. 1974, 143 (3) 541-53
48. Bode, R.; Lippoldt, A.; Birnbaum, D. Purification and properties of D-aromatic lactate dehydrogenase, an enzyme involved in the catabolism of the aromatic amino acids of Candida maltosa Biochem. Physiol. Pflanz. 1986, 181, 189-198