Untargeted plasma metabolite profiling reveals the broad systemic consequences of xanthine oxidoreductase inactivation in mice

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Chen, Qiuying ^a   Park, Hyeong Cheon ^b   Goligorsky, Michael S ^b   Chander, Praveen ^b   Fischer, Steven M ^c   Gross, Steven S ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

^c AGILENT TECHNOLOGIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; NICOTINAMIDE; PHOSPHOLIPID; PURINE; PYRIMIDINE DERIVATIVE; TRYPTOPHAN; XANTHINE OXIDASE;

ANIMAL CELL; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE MARKER; ENZYME BLOOD LEVEL; ENZYME INACTIVATION; GENE; GENE DELETION; GENOTYPE; HISTOCHEMISTRY; KIDNEY FAILURE; METABOLOMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURINE METABOLISM; UREA CYCLE; XOR GENE;

ANIMALS; CLUSTER ANALYSIS; ENZYME ACTIVATION; GENE DELETION; GENOTYPE; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; XANTHINE DEHYDROGENASE;

EID: 84862497463     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037149     Document Type: Article

References (60)

1. Ganti S, Weiss RH, (2011) Urine metabolomics for kidney cancer detection and biomarker discovery. Urol Oncol 29: 551-557.
2. Zhang GF, Sadhukhan S, Tochtrop GP, Brunengraber H, (2011) Metabolomics, pathway regulation, and pathway discovery. J Biol Chem 286: 23631-23635.
3. Nagrath D, Caneba C, Karedath T, Bellance N, (2011) Metabolomics for mitochondrial and cancer studies. Biochim Biophys Acta 1807: 650-663.
4. Drexler DM, Reily MD, Shipkova PA, (2011) Advances in mass spectrometry applied to pharmaceutical metabolomics. Anal Bioanal Chem 399: 2645-2653.
5. Reaves ML, Rabinowitz JD, (2011) Metabolomics in systems microbiology. Curr Opin Biotechnol 22: 17-25.
6. Mamas M, Dunn WB, Neyses L, Goodacre R, (2011) The role of metabolites and metabolomics in clinically applicable biomarkers of disease. Arch Toxicol 85: 5-17.
7. Fiehn O, editor (2009) Quality control in metabolomics.
8. Issaq HJ, Van QN, Waybright TJ, Muschik GM, Veenstra TD, (2009) Analytical and statistical approaches to metabolomics research. J Sep Sci 32: 2183-2199.
9. Cubbon S, Antonio C, Wilson J, Thomas-Oates J, (2010) Metabolomic applications of HILIC-LC-MS. Mass Spectrom Rev 29: 671-684.
10. Michopoulos F LL, Gika H, Theodoridis G, Wilson I, (2009) UPLC-MS-based analysis of human plasma for metabonomics using solvent precipitation or solid phase extraction. J Proteome Res 8: 2114-2121.
11. Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E, (2009) Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem 81: 6656-6667.
12. Weisenberg SA, Butterfield TR, Fischer SM, Rhee KY, (2009) Suitability of silica hydride stationary phase, aqueous normal phase chromatography for untargeted metabolomic profiling of Enterococcus faecium and Staphylococcus aureus. J Sep Sci 32: 2262-2265.
13. Roux A, Lison D, Junot C, Heilier JF, (2011) Applications of liquid chromatography coupled to mass spectrometry-based metabolomics in clinical chemistry and toxicology: A review. Clin Biochem 44: 119-135.
14. Barbas C, Moraes EP, Villasenor A, (2011) Capillary electrophoresis as a metabolomics tool for non-targeted fingerprinting of biological samples. J Pharm Biomed Anal 55: 823-831.
15. Pesek JJ, Matyska MT, Loo JA, Fischer SM, Sana TR, (2009) Analysis of hydrophilic metabolites in physiological fluids by HPLC-MS using a silica hydride-based stationary phase. J Sep Sci 32: 2200-2208.
16. Sana TR, Roark JC, Li X, Waddell K, Fischer SM, (2008) Molecular formula and METLIN Personal Metabolite Database matching applied to the identification of compounds generated by LC/TOF-MS. J Biomol Tech 19: 258-266.
17. Wei X, Sun W, Shi X, Koo I, Wang B, et al. (2011) MetSign: A Computational Platform for High-Resolution Mass Spectrometry-Based Metabolomics. Anal Chem 83: 7668-7675.
18. Linder N, Butzow R, Lassus H, Lundin M, Lundin J, (2011) Decreased xanthine oxidoreductase (XOR) is associated with a worse prognosis in patients with serous ovarian carcinoma. Gynecol Oncol.
19. Kim AW, Batus M, Myint R, Fidler MJ, Basu S, et al. (2011) Prognostic value of xanthine oxidoreductase expression in patients with non-small cell lung cancer. Lung Cancer 71: 186-190.
20. Gibbings S, Elkins ND, Fitzgerald H, Tiao J, Weyman ME, et al. (2011) Xanthine oxidoreductase promotes the inflammatory state of mononuclear phagocytes through effects on chemokine expression, peroxisome proliferator-activated receptor-{gamma} sumoylation, and HIF-1{alpha}. J Biol Chem 286: 961-975.
21. Fini MA, Monks J, Farabaugh SM, Wright RM, (2011) Contribution of xanthine oxidoreductase to mammary epithelial and breast cancer cell differentiation in part modulates inhibitor of differentiation-1. Mol Cancer Res 9: 1242-1254.
22. Battelli MG, Ravaioli M, Musiani S, Scicchitano V, Grazi GL, et al. (2011) Increased serum level of xanthine oxidoreductase in liver transplanted patients. J Biol Regul Homeost Agents 25: 77-84.
23. Agarwal A, Banerjee A, Banerjee UC, (2011) Xanthine oxidoreductase: a journey from purine metabolism to cardiovascular excitation-contraction coupling. Crit Rev Biotechnol 31: 264-280.
24. Huang L, Borniquel S, Lundberg JO, (2010) Enhanced xanthine oxidoreductase expression and tissue nitrate reduction in germ free mice. Nitric Oxide 22: 191-195.
25. Meneshian A, Bulkley GB, (2002) The physiology of endothelial xanthine oxidase: from urate catabolism to reperfusion injury to inflammatory signal transduction. Microcirculation 9: 161-175.
26. Ohtsubo T, Rovira, II, Starost MF, Liu C, Finkel T, (2004) Xanthine oxidoreductase is an endogenous regulator of cyclooxygenase-2. Circ Res 95: 1118-1124.
27. Ohtsubo T, Matsumura K, Sakagami K, Fujii K, Tsuruya K, et al. (2009) Xanthine oxidoreductase depletion induces renal interstitial fibrosis through aberrant lipid and purine accumulation in renal tubules. Hypertension 54: 868-876.
28. Sanders SA, Massey V, (1999) The thermodynamics of xanthine oxidoreductase catalysis. Antioxid Redox Signal 1: 371-379.
29. Harrison R, (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic Biol Med 33: 774-797.
30. Martelin E, Lapatto R, Raivio KO, (2002) Regulation of xanthine oxidoreductase by intracellular iron. Am J Physiol Cell Physiol 283: C1722-1728.
31. McManaman JL, Bain DL, (2002) Structural and conformational analysis of the oxidase to dehydrogenase conversion of xanthine oxidoreductase. J Biol Chem 277: 21261-21268.
32. Nishino T, Amaya Y, Kawamoto S, Kashima Y, Okamoto K, (2002) Purification and characterization of multiple forms of rat liver xanthine oxidoreductase expressed in baculovirus-insect cell system. J Biochem 132: 597-606.
33. Cheung KJ, Tzameli I, Pissios P, Rovira I, Gavrilova O, et al. (2007) Xanthine oxidoreductase is a regulator of adipogenesis and PPARgamma activity. Cell Metab 5: 115-128.
34. Webb AJ, Milsom AB, Rathod KS, Chu WL, Qureshi S, et al. (2008) Mechanisms underlying erythrocyte and endothelial nitrite reduction to nitric oxide in hypoxia: role for xanthine oxidoreductase and endothelial nitric oxide synthase. Circ Res 103: 957-964.
35. Gierasch LM, Gershenson A, (2009) Post-reductionist protein science, or putting Humpty Dumpty back together again. Nat Chem Biol 5: 774-777.
36. Joel D. Kopple SGM, (2004) Uremic toxicity and its effects on metabolism and body function, in Kopple and Massry's nutritional management of renal disease. in Kopple and Massry's nutritional management of renal disease.
37. Zhang Z, Blake DR, Stevens CR, Kanczler JM, Winyard PG, et al. (1998) A reappraisal of xanthine dehydrogenase and oxidase in hypoxic reperfusion injury: the role of NADH as an electron donor. Free Radic Res 28: 151-164.
38. Zhang R, Pinson A, Samuni A, (1998) Both hydroxylamine and nitroxide protect cardiomyocytes from oxidative stress. Free Radic Biol Med 24: 66-75.
39. Kamleh MA, Hobani Y, Dow JA, Watson DG, (2008) Metabolomic profiling of Drosophila using liquid chromatography Fourier transform mass spectrometry. FEBS Lett 582: 2916-2922.
40. Yamaoka K, Imajoh-Ohmi S, Fukuda H, Akita Y, Kurosawa K, et al. (2006) Identification of phosphoproteins associated with maintenance of transformed state in temperature-sensitive Rous sarcoma-virus infected cells by proteomic analysis. Biochem Biophys Res Commun 345: 1240-1246.
41. Igarashi K, Ueda S, Yoshida K, Kashiwagi K, (2006) Polyamines in renal failure. Amino Acids 31: 477-483.
42. Barreto FC, Barreto DV, Liabeuf S, Meert N, Glorieux G, et al. (2009) Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin J Am Soc Nephrol 4: 1551-1558.
43. Pawlak D, Tankiewicz A, Matys T, Buczko W, (2003) Peripheral distribution of kynurenine metabolites and activity of kynurenine pathway enzymes in renal failure. J Physiol Pharmacol 54: 175-189.
44. Tankiewicz A, Pawlak D, Topczewska-Bruns J, Buczko W, (2003) Kidney and liver kynurenine pathway enzymes in chronic renal failure. Adv Exp Med Biol 527: 409-414.
45. Schefold JC, Zeden JP, Fotopoulou C, von Haehling S, Pschowski R, et al. (2009) Increased indoleamine 2,3-dioxygenase (IDO) activity and elevated serum levels of tryptophan catabolites in patients with chronic kidney disease: a possible link between chronic inflammation and uraemic symptoms. Nephrol Dial Transplant 24: 1901-1908.
46. Swendseid ME, Wang M, Schutz I, Kopple JD, (1978) Metabolism of urea cycle intermediates in chronic renal failure. Am J Clin Nutr 31: 1581-1586.
47. Biasioli S, Feriani M, Bigi L, Dell'Aquila R, Bragantini L, et al. (1987) Tricarboxylic acid cycle intermediates in chronic renal failure. Nephrol Dial Transplant 2: 313-315.
48. Spector T, Hall WW, Krenitsky TA, (1986) Human and bovine xanthine oxidases. Inhibition studies with oxipurinol. Biochem Pharmacol 35: 3109-3114.
49. Noman A, Ang DS, Ogston S, Lang CC, Struthers AD, (2010) Effect of high-dose allopurinol on exercise in patients with chronic stable angina: a randomised, placebo controlled crossover trial. Lancet 375: 2161-2167.
50. Dawson J, Quinn TJ, Harrow C, Lees KR, Walters MR, (2009) The effect of allopurinol on the cerebral vasculature of patients with subcortical stroke; a randomized trial. Br J Clin Pharmacol 68: 662-668.
51. George J, Carr E, Davies J, Belch JJ, Struthers A, (2006) High-dose allopurinol improves endothelial function by profoundly reducing vascular oxidative stress and not by lowering uric acid. Circulation 114: 2508-2516.
52. Goicoechea M, de Vinuesa SG, Verdalles U, Ruiz-Caro C, Ampuero J, et al. (2010) Effect of allopurinol in chronic kidney disease progression and cardiovascular risk. Clin J Am Soc Nephrol 5: 1388-1393.
53. Kosugi T, Nakayama T, Heinig M, Zhang L, Yuzawa Y, et al. (2009) Effect of lowering uric acid on renal disease in the type 2 diabetic db/db mice. Am J Physiol Renal Physiol 297: F481-488.
54. Tanaka T, Doi K, Maeda-Mamiya R, Negishi K, Portilla D, et al. (2009) Urinary L-type fatty acid-binding protein can reflect renal tubulointerstitial injury. Am J Pathol 174: 1203-1211.
55. Stamp LK, O'Donnell JL, Zhang M, James J, Frampton C, et al. (2010) Using allopurinol above the dose based on creatinine clearance is effective and safe in chronic gout, including in those with renal impairment. Arthritis Rheum.
56. George J, Struthers A, (2009) The role of urate and xanthine oxidase in vascular oxidative stress: future directions. Ther Clin Risk Manag 5: 799-803.
57. Chohan S, Becker MA, (2009) Update on emerging urate-lowering therapies. Curr Opin Rheumatol 21: 143-149.
58. Dewan AK, Quinonez RA, (2010) Allopurinol-induced DRESS syndrome in an adolescent patient. Pediatr Dermatol 27: 270-273.
59. Govani SM, Higgins PD, (2010) Combination of thiopurines and allopurinol: adverse events and clinical benefit in IBD. J Crohns Colitis 4: 444-449.
60. Sana TR, Waddell K, Fischer SM, (2008) A sample extraction and chromatographic strategy for increasing LC/MS detection coverage of the erythrocyte metabolome. J Chromatogr B Analyt Technol Biomed Life Sci 871: 314-321.