Dominant components of the Thoroughbred metabolome characterised by 1H-nuclear magnetic resonance spectroscopy: A metabolite atlas of common biofluids

Equine Veterinary Journal

Volumn 47, Issue 6, 2015, Pages 721-730

  Escalona, E E ^a   Leng, J ^b   Dona, A C ^a   Merrifield, C A ^a   Holmes, E ^a   Proudman, C J ^c,d   Swann, J R ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Biofluids; Horse; Metabolites; Metabolomics; Metabonomics; Nuclear magnetic resonance

Indexed keywords

ANIMAL; BLOOD; BODY FLUID; CHEMISTRY; FECES; HORSE; METABOLISM; METABOLOME; METABOLOMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES; URINE;

ANIMALS; BODY FLUIDS; FECES; HORSES; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; METABOLOMICS; URINE;

EID: 84944516851     PISSN: 04251644     EISSN: 20423306     Source Type: Journal    
DOI: 10.1111/evj.12333     Document Type: Article

References (56)

1. 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.
2. 1H NMR-based metabolomics reveals specific metabolic pathway disturbances in diabetic rats. Anal. Biochem. 383, 76-84.
3. Poli, D., Carbognani, P., Corradi, M., Goldoni, M., Acampa, O., Balbi, B., Bianchi, L., Rusca, M. and Mutti, A. (2005) Exhaled volatile organic compounds in patients with non-small cell lung cancer: cross sectional and nested short-term follow-up study. Respir. Res. 6, 71.
4. Gowda, G.A., Zhang, S., Gu, H., Asiago, V., Shanaiah, N. and Raftery, D. (2008) Metabolomics-based methods for early disease diagnostics. Expert Rev. Mol. Diagn. 8, 617-633.
5. 1H NMR based metabonomics approach to progression of coronary atherosclerosis in a rabbit model. Process Biochem. 46, 2240-2247.
6. Hooper, L.V., Bry, L., Falk, P.G. and Gordon, J.I. (1998) Host-microbial symbiosis in the mammalian intestine: exploring an internal ecosystem. Bioessays 20, 336-343.
7. Saric, J., Wang, Y., Li, J., Coen, M., Utzinger, J., Marchesi, J.R., Keiser, J., Veselkov, K., Lindon, J.C., Nicholson, J.K. and Holmes, E. (2008) Species variation in the fecal metabolome gives insight into differential gastrointestinal function. J. Proteome Res. 7, 352-360.
8. Merrifield, C.A., Lewis, M., Claus, S.P., Beckonert, O.P., Dumas, M.-E., Duncker, S., Kochhar, S., Rezzi, S., Lindon, J.C., Bailey, M., Holmes, E. and Nicholson, J. (2011) A metabolic system-wide characterisation of the pig: a model for human physiology. Mol. Biosyst. 7, 2577-2588.
9. He, Q., Ren, P., Kong, X., Wu, Y., Wu, G., Li, P., Hao, F., Tang, H., Blachier, F. and Yin, Y. (2012) Comparison of serum metabolite compositions between obese and lean growing pigs using an NMR-based metabonomic approach. J. Nutr. Biochem. 23, 133-139.
10. Scarth, J.P., Spencer, H.A., Timbers, S.E., Hudson, S.C. and Hillyer, L.L. (2010) The use of in vitro technologies coupled with high resolution accurate mass LC-MS for studying drug metabolism in equine drug surveillance. Drug Test. Anal. 2, 1-10.
11. Liu, Y., Uboh, C.E., Soma, L.R., Li, X., Guan, F., You, Y. and Chen, J.-W. (2011) Efficient use of retention time for the analysis of 302 drugs in equine plasma by liquid chromatography-MS/MS with scheduled multiple reaction monitoring and instant library searching for doping control. Anal. Chem. 83, 6834-6841.
12. Hodavance, M.S., Ralston, S.L. and Pelczer, I. (2007) Beyond blood sugar: the potential of NMR-based metabonomics for type 2 human diabetes, and the horse as a possible model. Anal. Bioanal. Chem. 387, 533-537.
13. Keller, M.D., Pollitt, C.C. and Marx, U.C. (2011) Nuclear magnetic resonance-based metabonomic study of early time point laminitis in an oligofructose-overload model. Equine Vet. J. 43, 737-743.
14. Ralston, S.L., Pappalardo, L. and Pelczer, I. (2011) Breed and age effects on metabolic profiles of young horses using NMR-based metabonomic analyses of serum. J. Equine Vet. Sci. 31, 304-305.
15. Ralston, S.L., Pelczer, I., Shatynski, C. and Spears, P.F. (2009) NMR-based metabonomic analysis of serum from standardbred yearlings with or without hock osteochondrosis dessicans lesions: preliminary study. J. Equine Vet. Sci. 29, 385-386.
16. Pappalardo, L., Pelczer, I. and Ralston, S.L. (2013) Metabolic differences between draft-cross and mustang horses detected by metabonomic analyses. J. Equine Vet. Sci. 33, 1044-1049.
17. Dumas, M.E., Maibaum, E.C., Teague, C., Ueshima, H., Zhou, B.F., Lindon, J.C., Nicholson, J.K., Stamler, J., Elliott, P., Chan, Q. and Holmes, E. (2006) Assessment of analytical reproducibility of H-1 NMR spectroscopy based metabonomics for large-scale epidemiological research: the INTERMAP study. Anal. Chem. 78, 2199-2208.
18. Beckonert, O., Keun, H.C., Ebbels, T.M.D., Bundy, J.G., 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.
19. Wright, B., Greatbanks, D., Taberner, J. and Wilson, I.D. (1995) Comparison of three methods for water suppression in biofluid NMR: advantages of NOESYPRESAT. Pharm. Pharmacol. Commun. 1, 197-199.
20. Pearce, J.T.M., Athersuch, T.J., Ebbels, T.M.D., Lindon, J.C., Nicholson, J.K. and Keun, H.C. (2008) Robust algorithms for automated chemical shift calibration of 1D H-1 NMR spectra of blood serum. Anal. Chem. 80, 7158-7162.
21. Dieterle, F., Ross, A., Schlotterbeck, G. and Senn, H. (2006) Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in H-1 NMR metabonomics. Anal. Chem. 78, 4281-4290.
22. Trygg, J., Holmes, E. and Lundstedt, T. (2007) Chemometrics in metabonomics. J. Proteome Res. 6, 469-479.
23. Craig, A., Cloareo, O., Holmes, E., Nicholson, J.K. and Lindon, J.C. (2006) Scaling and normalization effects in NMR spectroscopic metabonomic data sets. Anal. Chem. 78, 2262-2267.
24. Fan, T.W.M. (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog. Nucl. Magn. Reson. Spectrosc. 28, 161-219.
25. Nicholson, J.K. and Wilson, I.D. (1989) High resolution proton magnetic resonance spectroscopy of biological fluids. Prog. Nucl. Magn. Reson. Spectrosc. 21, 449-501.
26. Bollard, M.E., Keun, H.C., Beckonert, O., Ebbels, T.M.D., Antti, H., Nicholls, A.W., Shockcor, J.P., Cantor, G.H., Stevens, G., Lindon, J.C., Holmes, E. and Nicholson, J. (2005) Comparative metabonomics of differential hydrazine toxicity in the rat and mouse. Toxicol. Appl. Pharmacol. 204, 135-151.
27. Cloarec, O., Dumas, M.E., Craig, A., Barton, R.H., Trygg, J., Hudson, J., Blancher, C., Gauguier, D., Lindon, J.C., Holmes, E. and Nicholson, J. (2005) Statistical total correlation spectroscopy: an exploratory approach for latent biomarker identification from metabolic H-1 NMR data sets. Anal. Chem. 77, 1282-1289.
28. Kirwan, G.M., Coffey, V.G., Niere, J.O., Hawley, J.A. and Adams, M.J. (2009) Spectroscopic correlation analysis of NMR-based metabonomics in exercise science. Anal. Chim. Acta 652, 173-179.
29. 13C NMR spectroscopy of human blood plasma. Anal. Chem. 67, 793-811.
30. 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. 15, 1647-1659.
31. Le Gall, G., Noor, S.O., Ridgway, K., Scovell, L., Jamieson, C., Johnson, I.T., Colquhoun, I.J., Kemsley, E.K. and Narbad, A. (2011) Metabolomics of fecal extracts detects altered metabolic activity of gut microbiota in ulcerative colitis and irritable bowel syndrome. J. Proteome Res. 10, 4208-4218.
32. Ametaj, B.N., Zebeli, Q., Saleem, F., Psychogios, N., Lewis, M.J., Dunn, S.M., Xia, J.G. and Wishart, D.S. (2010) Metabolomics reveals unhealthy alterations in rumen metabolism with increased proportion of cereal grain in the diet of dairy cows. Metabolomics 6, 583-594.
33. Nyberg, N.T., Nielsen, M.O. and Jaroszewski, J.W. (2010) Metabolic trajectories based on H-1 NMR spectra of urines from sheep exposed to nutritional challenges during prenatal and early postnatal life. Metabolomics 6, 489-496.
34. Li, J., Wijffels, G., Yu, Y., Nielsen, L.K., Niemeyer, D.O., Fisher, A.D., Ferguson, D.M. and Schirra, H.J. (2011) Altered fatty acid metabolism in long duration road transport: an NMR-based metabonomics study in sheep. J. Proteome Res. 10, 1073-1087.
35. Bollard, M.E., Stanley, E.G., Lindon, J.C., Nicholson, J.K. and Holmes, E. (2005) NMR-based metabonomic approaches for evaluating physiological influences on biofluid composition. NMR Biomed. 18, 143-162.
36. Argenzio, R.A. (1975) Functions of equine large-intestine and their interrelationship in disease. Cornell Vet. 65, 303-330.
37. Cummings, J.H. and Macfarlane, G.T. (1997) Role of intestinal bacteria in nutrient metabolism. Clin. Nutr. 16, 3-11.
38. Desrousseaux, G., Santos, A.S., Pellikaan, W.F., Van der Poel, A.F.B., Cone, J.W., Guedes, C.M.V., Ferreira, L.M.M. and Rodrigues, M.A.M. (2012) Effect of collection time on the fermentative activity of microbes in equine faeces. Anim. Feed Sci. Technol. 178, 183-189.
39. Van Weyenberg, S., Sales, J. and Janssens, G.P.J. (2006) Passage rate of digesta through the equine gastrointestinal tract: a review. Livestock Sci. 99, 3-12.
40. Hudson, N.P.H. and Merritt, A.M. (2008) Equine gastrointestinal motility research: where we are and where we need to go. Equine Vet. J. 40, 422-428.
41. Bugaut, M. and Bentejac, M. (1993) Biological effects of short-chain fatty acids in nonruminant mammals. Annu. Rev. Nutr. 13, 217-241.
42. Wyss, M. and Kaddurah-Daouk, R. (2000) Creatine and creatinine metabolism. Physiol. Rev. 80, 1107-1213.
43. Baxmann, A.C., Ahmed, M.S., Marques, N.C., Menon, V.B., Pereira, A.B., Kirsztajn, G.M. and Heilberg, I.P. (2008) Influence of muscle mass and physical activity on serum and urinary creatinine and serum cystatin C. Clin. J. Am. Soc. Nephrol. 3, 348-354.
44. Nicholson, J.K., Holmes, E. and Wilson, I.D. (2005) Gut microorganisms, mammalian metabolism and personalized health care. Nat. Rev. Microbiol. 3, 431-438.
45. Lees, H.J., Swann, J.R., Wilson, I.D., Nicholson, J.K. and Holmes, E. (2013) Hippurate: the natural history of a mammalian-microbial cometabolite. J. Proteome Res. 5, 1527-1546.
46. Clayton, T.A., Baker, D., Lindon, J.C., Everett, J.R. and Nicholson, J.K. (2009) Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc. Natl Acad. Sci. U.S.A. 106, 14728-14733.
47. Bennett, B.J., de Aguiar Vallim, T.Q., Wang, Z., Shih, D.M., Meng, Y., Gregory, J., Allayee, H., Lee, R., Graham, M., Crooke, R., Edwards, P.A., Hazen, S.L. and Lusis, A.J. (2013) Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. Cell Metab. 17, 49-60.
48. Waldram, A., Holmes, E., Wang, Y., Rantalainen, M., Wilson, I.D., Tuohy, K.M., McCartney, A.L., Gibson, G.R. and Nicholson, J.K. (2009) Top-down systems biology modeling of host metabotype-microbiome associations in obese rodents. J. Proteome Res. 8, 2361-2375.
49. Peppercorn, M.A. and Goldman, P. (1971) Caffeic acid metabolism by bacteria of the human gastrointestinal tract. J. Bacteriol. 108, 996-1000.
50. 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. and Holmes, E. (2011) Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 60, 1214-1223.
51. Diab, S.S., Rodriguez-Bertos, A. and Uzal, F.A. (2013) Pathology and diagnostic criteria of Clostridium difficile enteric infection in horses. Vet. Pathol. 50, 1028-1036.
52. Diab, S.S., Songer, G. and Uzal, F.A. (2013) Clostridium difficile infection in horses: a review. Vet. Microbiol. 167, 42-49.
53. Costa, M.C., Arroyo, L.G., Allen-Vercoe, E., Stampfli, H.R., Kim, P.T., Sturgeon, A. and Weese, J.S. (2012) Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene. PLoS One 7, e41484.
54. O'Donnell, M.M., Harris, H.M., Jeffery, I.B., Claesson, M.J., Younge, B., O'Toole, P.W. and Ross, R.P. (2013) The core faecal bacterial microbiome of Irish Thoroughbred racehorses. Lett. Appl. Microbiol. 57, 492-501.
55. Bollard, M.E., Holmes, E., Lindon, J.C., Mitchell, S.C., Branstetter, D., Zhang, W. and Nicholson, J.K. (2001) Investigations into biochemical changes due to diurnal variation and estrus cycle in female rats using high-resolution H-1 NMR spectroscopy of urine and pattern recognition. Anal. Biochem. 295, 194-202.
56. Saude, E.J. and Sykes, B.D. (2007) Urine stability for metabolomic studies: effects of preparation and storage. Metabolomics 3, 19-27.