Monitoring the response of the human urinary metabolome to brief maximal exercise by a combination of RP-UPLC-MS and 1H NMR spectroscopy

Journal of Proteome Research

Volumn 14, Issue 11, 2015, Pages 4610-4622

  Pechlivanis, Alexandros ^a,b   Papaioannou, Konstantinos G ^b   Tsalis, George ^b   Saraslanidis, Ploutarchos ^b   Mougios, Vassilis ^b   Theodoridis, Georgios A ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

metabonomics; NMR spectroscopy; physical exercise; sprint running; UPLC MS; urinary metabolite fingerprinting

Indexed keywords

2 HYDROXYISOBUTYRIC ACID; 2 HYDROXYISOVALERATE; 2 OXOISOCAPROIC ACID; 2 OXOISOVALERIC ACID; 3 HYDROXY 2 METHYLPROPIONIC ACID; 3 HYDROXYBUTYRIC ACID; 3 METHYL 2 OXOVALERATE; 4 AMINOHIPPURIC ACID; ACETIC ACID; ALANINE; BIOLOGICAL MARKER; CITRIC ACID; CREATININE; FORMIC ACID; GLYCINE; HIPPURIC ACID; HYDROXYBUTYRIC ACID; HYPOXANTHINE; INOSINE; ISOLEUCINE; LACTIC ACID; PYRUVIC ACID; SUCCINIC ACID; TRIMETHYLAMINE; TRIMETHYLAMINE OXIDE; TYROSINE; UNCLASSIFIED DRUG; URATE; VALINE; AMINO ACID; CARBOXYLIC ACID;

ADULT; ARTICLE; EXERCISE; HUMAN; MALE; METABOLISM; METABOLITE; METABOLOME; NORMAL HUMAN; PHOTOMETRY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; URINALYSIS; URINE BIOCHEMISTRY; ADOLESCENT; ANALYSIS OF VARIANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; REVERSED PHASE LIQUID CHROMATOGRAPHY; RUNNING; URINE; YOUNG ADULT;

ADOLESCENT; AMINO ACIDS; ANALYSIS OF VARIANCE; CARBOXYLIC ACIDS; CHROMATOGRAPHY, REVERSE-PHASE; CREATININE; EXERCISE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOME; RUNNING; YOUNG ADULT;

EID: 84946893477     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00470     Document Type: Article

References (48)

1. Nicholson, J. K.; Lindon, J. C.; Holmes, E. 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data Xenobiotica 1999, 29, 1181-9 10.1080/004982599238047
2. Ramautar, R.; Berger, R.; van der Greef, J.; Hankemeier, T. Human metabolomics: strategies to understand biology Curr. Opin. Chem. Biol. 2013, 17, 841-846 10.1016/j.cbpa.2013.06.015
3. Revilla, S.; Suñol, C.; García-Mesa, Y.; Giménez-Llort, L.; Sanfeliu, C.; Cristòfol, R. Physical exercise improves synaptic dysfunction and recovers the loss of survival factors in 3xTg-AD mouse brain Neuropharmacology 2014, 81, 55-63 10.1016/j.neuropharm.2014.01.037
4. Vina, J.; Sanchis-Gomar, F.; Martinez-Bello, V.; Gomez-Cabrera, M. C. Exercise acts as a drug; the pharmacological benefits of exercise Br. J. Pharmacol. 2012, 167, 1-12 10.1111/j.1476-5381.2012.01970.x
5. Powers, S. K.; Nelson, W. B.; Hudson, M. B. Exercise-induced oxidative stress in humans: Cause and consequences Free Radical Biol. Med. 2011, 51, 942-950 10.1016/j.freeradbiomed.2010.12.009
6. Cook, M. D.; Martin, S. A.; Williams, C.; Whitlock, K.; Wallig, M. A.; Pence, B. D.; Woods, J. A. Forced treadmill exercise training exacerbates inflammation and causes mortality while voluntary wheel training is protective in a mouse model of colitis Brain, Behav., Immun. 2013, 33, 46-56 10.1016/j.bbi.2013.05.005
7. Lewis, G. D.; Farrell, L.; Wood, M. J.; Martinovic, M.; Arany, Z.; Rowe, G. C.; Souza, A.; Cheng, S.; McCabe, E. L.; Yang, E.; Shi, X.; Deo, R.; Roth, F. P.; Asnani, A.; Rhee, E. P.; Systrom, D. M.; Semigran, M. J.; Vasan, R. S.; Carr, S. A.; Wang, T. J.; Sabatine, M. S.; Clish, C. B.; Gerszten, R. E. Metabolic signatures of exercise in human plasma Sci. Transl. Med. 2010, 2, 33ra37 10.1126/scitranslmed.3001006
8. Lee, D. C.; Sui, X.; Artero, E. G.; Lee, I. M.; Church, T. S.; McAuley, P. A.; Stanford, F. C.; Kohl, H. W., 3rd; Blair, S. N. Long-term effects of changes in cardiorespiratory fitness and body mass index on all-cause and cardiovascular disease mortality in men: the Aerobics Center Longitudinal Study Circulation 2011, 124, 2483-90 10.1161/CIRCULATIONAHA.111.038422
9. Dumas, M. E.; Maibaum, E. C.; Teague, C.; Ueshima, H.; Zhou, B.; Lindon, J. C.; Nicholson, J. K.; Stamler, J.; Elliott, P.; Chan, Q.; Holmes, E. Assessment of analytical reproducibility of 1H NMR spectroscopy based metabonomics for large-scale epidemiological research: the INTERMAP Study Anal. Chem. 2006, 78, 2199-208 10.1021/ac0517085
10. Theodoridis, G. A.; Gika, H. G.; Want, E. J.; Wilson, I. D. Liquid chromatography-mass spectrometry based global metabolite profiling: A review Anal. Chim. Acta 2012, 711, 7-16 10.1016/j.aca.2011.09.042
11. Tsugawa, H.; Tsujimoto, Y.; Sugitate, K.; Sakui, N.; Nishiumi, S.; Bamba, T.; Fukusaki, E. Highly sensitive and selective analysis of widely targeted metabolomics using gas chromatography/triple-quadrupole mass spectrometry J. Biosci. Bioeng. 2014, 117, 122-128 10.1016/j.jbiosc.2013.06.009
12. Zhang, H.; Fu, P.; Ke, B.; Wang, S.; Li, M.; Han, L.; Peng, C.; Zhang, W.; Liu, R. Metabolomic analysis of biochemical changes in the plasma and urine of collagen-induced arthritis in rats after treatment with Huang-Lian-Jie-Du-Tang J. Ethnopharmacol. 2014, 154, 55-64 10.1016/j.jep.2014.03.007
13. Jain, M.; Nilsson, R.; Sharma, S.; Madhusudhan, N.; Kitami, T.; Souza, A. L.; Kafri, R.; Kirschner, M. W.; Clish, C. B.; Mootha, V. K. Metabolite profiling identifies a key role for glycine in rapid cancer cell proliferation Science 2012, 336, 1040-4 10.1126/science.1218595
14. Pechlivanis, A.; Kostidis, S.; Saraslanidis, P.; Petridou, A.; Tsalis, G.; Mougios, V.; Gika, H. G.; Mikros, E.; Theodoridis, G. A. 1)H NMR-based metabonomic investigation of the effect of two different exercise sessions on the metabolic fingerprint of human urine J. Proteome Res. 2010, 9, 6405-16 10.1021/pr100684t
15. Pechlivanis, A.; Kostidis, S.; Saraslanidis, P.; Petridou, A.; Tsalis, G.; Veselkov, K.; Mikros, E.; Mougios, V.; Theodoridis, G. A. 1H NMR study on the short- and long-term impact of two training programs of sprint running on the metabolic fingerprint of human serum J. Proteome Res. 2013, 12, 470-80 10.1021/pr300846x
16. Want, E. J.; Wilson, I. D.; Gika, H.; Theodoridis, G.; Plumb, R. S.; Shockcor, J.; Holmes, E.; Nicholson, J. K. Global metabolic profiling procedures for urine using UPLC-MS Nat. Protoc. 2010, 5, 1005-18 10.1038/nprot.2010.50
17. 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, 2692-703 10.1038/nprot.2007.376
18. Plumb, R. S.; Johnson, K. A.; Rainville, P.; Smith, B. W.; Wilson, I. D.; Castro-Perez, J. M.; Nicholson, J. K. UPLC/MSE; a new approach for generating molecular fragment information for biomarker structure elucidation Rapid Commun. Mass Spectrom. 2006, 20, 1989-1994 10.1002/rcm.2550
19. Smith, C. A.; Want, E. J.; O'Maille, G.; Abagyan, R.; Siuzdak, G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification Anal. Chem. 2006, 78, 779-87 10.1021/ac051437y
20. Tautenhahn, R.; Bottcher, C.; Neumann, S. Highly sensitive feature detection for high resolution LC/MS BMC Bioinf. 2008, 9, 504 10.1186/1471-2105-9-504
21. Veselkov, K. A.; Vingara, L. K.; Masson, P.; Robinette, S. L.; Want, E.; Li, J. V.; Barton, R. H.; Boursier-Neyret, C.; Walther, B.; Ebbels, T. M.; Pelczer, I.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Optimized preprocessing of ultra-performance liquid chromatography/mass spectrometry urinary metabolic profiles for improved information recovery Anal. Chem. 2011, 83, 5864-72 10.1021/ac201065j
22. Field, A. Discovering Statistics Using SPSS; Sage: London, 2009.
23. Holmes, E.; Foxall, P. J.; Nicholson, J. K.; Neild, G. H.; Brown, S. M.; Beddell, C. R.; Sweatman, B. C.; Rahr, E.; Lindon, J. C.; Spraul, M. et al. Automatic data reduction and pattern recognition methods for analysis of 1H nuclear magnetic resonance spectra of human urine from normal and pathological states Anal. Biochem. 1994, 220, 284-96 10.1006/abio.1994.1339
24. Holmes, E.; Foxall, P. J.; Spraul, M.; Farrant, R. D.; Nicholson, J. K.; Lindon, J. C. 750 MHz 1H NMR spectroscopy characterisation of the complex metabolic pattern of urine from patients with inborn errors of metabolism: 2-hydroxyglutaric aciduria and maple syrup urine disease J. Pharm. Biomed. Anal. 1997, 15, 1647-1659 10.1016/S0731-7085(97)00066-6
25. Cloarec, O.; Dumas, M. E.; Craig, A.; Barton, R. H.; Trygg, J.; Hudson, J.; Blancher, C.; Gauguier, D.; Lindon, J. C.; Holmes, E.; Nicholson, J. Statistical total correlation spectroscopy: an exploratory approach for latent biomarker identification from metabolic 1H NMR data sets Anal. Chem. 2005, 77, 1282-9 10.1021/ac048630x
26. Gastin, P. B. Energy system interaction and relative contribution during maximal exercise Sports Med. 2001, 31, 725-41 10.2165/00007256-200131100-00003
27. Groussard, C.; Machefer, G.; Rannou, F.; Faure, H.; Zouhal, H.; Sergent, O.; Chevanne, M.; Cillard, J.; Gratas-Delamarche, A. Physical fitness and plasma non-enzymatic antioxidant status at rest and after a wingate test Can. J. Appl. Physiol. 2003, 28, 79-92 10.1139/h03-007
28. Kabasakalis, A.; Tsalis, G.; Zafrana, E.; Loupos, D.; Mougios, V. Effects of endurance and high-intensity swimming exercise on the redox status of adolescent male and female swimmers J. Sports Sci. 2014, 32, 747-56 10.1080/02640414.2013.850595
29. Glantzounis, G. K.; Tsimoyiannis, E. C.; Kappas, A. M.; Galaris, D. A. Uric acid and oxidative stress Curr. Pharm. Des. 2005, 11, 4145-51 10.2174/138161205774913255
30. Berg, J. M.; Tymoczko, J. L.; Stryer, L. Biochemistry, 5 th ed.; W. H. Freeman: New York, 2002.
31. Nicholson, J. K.; Timbrell, J. A.; Sadler, P. J. Proton NMR spectra of urine as indicators of renal damage. Mercury-induced nephrotoxicity in rats Mol. Pharmacol. 1985, 27, 644-51
32. Bairaktari, E.; Seferiadis, K.; Liamis, G.; Psihogios, N.; Tsolas, O.; Elisaf, M. Rhabdomyolysis-related renal tubular damage studied by proton nuclear magnetic resonance spectroscopy of urine Clin. Chem. 2002, 48, 1106-9
33. McPherson RA, B.-E. J. Basic examination of urine, 22 nd ed.; Elsevier Saunders: Philadelphia PA, 2011.
34. Poortmans, J. R. Exercise and renal function Sports Med. 1984, 1, 125-53 10.2165/00007256-198401020-00003
35. Knowles, S. E.; Jarrett, I. G.; Filsell, O. H.; Ballard, F. J. Production and utilization of acetate in mammals Biochem. J. 1974, 142, 401-11 10.1042/bj1420401
36. Mougios, V. Exercise Biochemistry; Human Kinetics, Champaign IL, 2006.
37. Landaas, S.; Pettersen, J. E. Clinical conditions associated with urinary excretion of 2-hydroxybutyric acid Scand. J. Clin. Lab. Invest. 1975, 35, 259-66 10.3109/00365517509095738
38. Amberg, A.; Rosner, E.; Dekant, W. Biotransformation and kinetics of excretion of methyl-tert-butyl ether in rats and humans Toxicol. Sci. 1999, 51, 1-8 10.1093/toxsci/51.1.1
39. Dai, L.; Peng, C.; Montellier, E.; Lu, Z.; Chen, Y.; Ishii, H.; Debernardi, A.; Buchou, T.; Rousseaux, S.; Jin, F.; Sabari, B. R.; Deng, Z.; Allis, C. D.; Ren, B.; Khochbin, S.; Zhao, Y. Lysine 2-hydroxyisobutyrylation is a widely distributed active histone mark Nat. Chem. Biol. 2014, 10, 365-70 10.1038/nchembio.1497
40. Yap, I. K.; Brown, I. J.; Chan, Q.; Wijeyesekera, A.; Garcia-Perez, I.; Bictash, M.; Loo, R. L.; Chadeau-Hyam, M.; Ebbels, T.; De Iorio, M.; Maibaum, E.; Zhao, L.; Kesteloot, H.; Daviglus, M. L.; Stamler, J.; Nicholson, J. K.; Elliott, P.; Holmes, E. Metabolome-wide association study identifies multiple biomarkers that discriminate north and south Chinese populations at differing risks of cardiovascular disease: INTERMAP study J. Proteome Res. 2010, 9, 6647-54 10.1021/pr100798r
41. Wang, Z.; Klipfell, E.; Bennett, B. J.; Koeth, R.; Levison, B. S.; Dugar, B.; Feldstein, A. E.; Britt, E. B.; Fu, X.; Chung, Y. M.; Wu, Y.; Schauer, P.; Smith, J. D.; Allayee, H.; Tang, W. H.; DiDonato, J. A.; Lusis, A. J.; Hazen, S. L. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 2011, 472, 57-63 10.1038/nature09922
42. Tang, W. H.; Wang, Z.; Levison, B. S.; Koeth, R. A.; Britt, E. B.; Fu, X.; Wu, Y.; Hazen, S. L. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk N. Engl. J. Med. 2013, 368, 1575-84 10.1056/NEJMoa1109400
43. Koeth, R. A.; Wang, Z.; Levison, B. S.; Buffa, J. A.; Org, E.; Sheehy, B. T.; Britt, E. B.; Fu, X.; Wu, Y.; Li, L.; Smith, J. D.; DiDonato, J. A.; Chen, J.; Li, H.; Wu, G. D.; Lewis, J. D.; Warrier, M.; Brown, J. M.; Krauss, R. M.; Tang, W. H.; Bushman, F. D.; Lusis, A. J.; Hazen, S. L. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis Nat. Med. 2013, 19, 576-85 10.1038/nm.3145
44. Lamarre, S. G.; Morrow, G.; Macmillan, L.; Brosnan, M. E.; Brosnan, J. T. Formate: an essential metabolite, a biomarker, or more? Clin. Chem. Lab. Med. 2013, 51, 571-8 10.1515/cclm-2012-0552
45. Washburn, S. E.; Caudill, M. A.; Malysheva, O.; MacFarlane, A. J.; Behan, N. A.; Harnett, B.; MacMillan, L.; Pongnopparat, T.; Brosnan, J. T.; Brosnan, M. E. Formate metabolism in the fetal and neonatal sheep Am. J. Physiol.: Endocrinol. Metab. 2015, 308, E921 10.1152/ajpendo.00046.2015
46. Hiatt, W. R.; Regensteiner, J. G.; Wolfel, E. E.; Ruff, L.; Brass, E. P. Carnitine and acylcarnitine metabolism during exercise in humans. Dependence on skeletal muscle metabolic state J. Clin. Invest. 1989, 84, 1167-73 10.1172/JCI114281
47. Nieman, D. C.; Shanely, R. A.; Gillitt, N. D.; Pappan, K. L.; Lila, M. A. Serum metabolic signatures induced by a three-day intensified exercise period persist after 14 h of recovery in runners J. Proteome Res. 2013, 12, 4577-84 10.1021/pr400717j
48. Hansen, J. S.; Zhao, X.; Irmler, M.; Liu, X.; Hoene, M.; Scheler, M.; Li, Y.; Beckers, J.; Hrabe de Angelis, M.; Haring, H. U.; Pedersen, B. K.; Lehmann, R.; Xu, G.; Plomgaard, P.; Weigert, C. Type 2 diabetes alters metabolic and transcriptional signatures of glucose and amino acid metabolism during exercise and recovery Diabetologia 2015, 58, 1845-54 10.1007/s00125-015-3584-x