Metabolome-wide association study identifies multiple biomarkers that discriminate north and south Chinese populations at differing risks of cardiovascular disease: INTERMAP study

Journal of Proteome Research

Volumn 9, Issue 12, 2010, Pages 6647-6654

  Yap, Ivan K S ^a   Brown, Ian J ^a   Chan, Queenie ^a   Wijeyesekera, Anisha ^a   Garcia Perez, Isabel ^a   Bictash, Magda ^a   Loo, Ruey Leng ^a   Chadeau Hyam, Marc ^a   Ebbels, Timothy ^a   Iorio, Maria De ^a   Maibaum, Elaine ^a   Zhao, Liancheng ^b   Kesteloot, Hugo ^c   Daviglus, Martha L ^d   Stamler, Jeremiah ^d   Nicholson, Jeremy K ^a,e   Elliott, Paul ^a,e   Holmes, Elaine ^a,e  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b FUWAI HOSPITAL   (China)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^d NORTHWESTERN UNIVERSITY   (United States)

^e Imperial College London   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYISOBUTYRATE; 4 CRESYL SULFATE; ACONITIC ACID; ALANINE; BIOLOGICAL MARKER; CREATINE; DIMETHYLGLYCINE; GLYCOPROTEIN; HEPTANOIC ACID DERIVATIVE; HIPPURIC ACID; INOSITOL; ISOLEUCINE; LACTIC ACID; LEUCINE; METHYLGUANIDINE; N ACETYLNEURAMINIC ACID; PHENYLACETYLGLUTAMINE; PROLINEBETAINE; SUCCINIC ACID; TAMM HORSFALL GLYCOPROTEIN; TRACE ELEMENT; UNCLASSIFIED DRUG; VALERIC ACID; VALINE;

ARTICLE; BLOOD PRESSURE; CARDIOVASCULAR RISK; CHINESE; DIET; FALSE POSITIVE RESULT; FEMALE; HUMAN; MACRONUTRIENT; MALE; METABOLITE; METABOLOME; MICROBIAL METABOLISM; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; URINALYSIS;

ADULT; AMINO ACIDS, BRANCHED-CHAIN; ASIAN CONTINENTAL ANCESTRY GROUP; BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; CHINA; CREATINE; DISCRIMINANT ANALYSIS; FEMALE; GEOGRAPHY; HUMANS; LEAST-SQUARES ANALYSIS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOMICS; MIDDLE AGED; N-ACETYLNEURAMINIC ACID; RISK ASSESSMENT; RISK FACTORS; SUCCINIC ACID; UROMODULIN;

MAMMALIA;

EID: 78649859765     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100798r     Document Type: Article

References (52)

1. Lopez, A. D.; Mathers, C. D.; Ezzati, M.; Jamison, D. T.; Murray, C. J. L. Global Burden of Disease and Risk Factors; Oxford University Press: New York, 2006.
2. Zhou, B.; Zhang, H.; Wu, Y.; Li, Y.; Yang, J.; Zhao, L.; X., Z. Ecological analysis of the association between incidence and risk factors of coronary heart disease and stroke in Chinese populations CVD Prev. 1998, 1, 207-16
3. Liu, M.; Wu, B.; Wang, W. Z.; Lee, L. M.; Zhang, S. H.; Kong, L. Z. Stroke in China: epidemiology, prevention, and management strategies Lancet Neurol. 2007, 6 (5) 456-64
4. Lawes, C. M.; Vander Hoorn, S.; Law, M. R.; Elliott, P.; MacMahon, S.; Rodgers, A. Blood pressure and the global burden of disease 2000. Part II: estimates of attributable burden J. Hypertens. 2006, 24 (3) 423-30
5. Lewington, S.; Whitlock, G.; Clarke, R.; Sherliker, P.; Emberson, J.; Halsey, J.; Qizilbash, N.; Peto, R.; Collins, R. Blood cholesterol and vascular mortality by age, sex, and blood pressure: a meta-analysis of individual data from 61 prospective studies with 55,000 vascular deaths Lancet 2007, 370 (9602) 1829-39
6. Teo, K. K.; Ounpuu, S.; Hawken, S.; Pandey, M. R.; Valentin, V.; Hunt, D.; Diaz, R.; Rashed, W.; Freeman, R.; Jiang, L.; Zhang, X.; Yusuf, S. Tobacco use and risk of myocardial infarction in 52 countries in the INTERHEART study: a case-control study Lancet 2006, 368 (9536) 647-58
7. Zhao, L.; Stamler, J.; Yan, L. L.; Zhou, B.; Wu, Y.; Liu, K.; Daviglus, M. L.; Dennis, B. H.; Elliott, P.; Ueshima, H.; Yang, J.; Zhu, L.; Guo, D. Blood pressure differences between northern and southern Chinese: role of dietary factors: the International Study on Macronutrients and Blood Pressure Hypertension 2004, 43 (6) 1332-7
8. Holmes, E.; Loo, R. L.; Stamler, J.; Bictash, M.; Yap, I. K.; Chan, Q.; Ebbels, T.; De Iorio, M.; Brown, I. J.; Veselkov, K. A.; Daviglus, M. L.; Kesteloot, H.; Ueshima, H.; Zhao, L.; Nicholson, J. K.; Elliott, P. Human metabolic phenotype diversity and its association with diet and blood pressure Nature 2008, 453 (7193) 396-400
9. Stamler, J.; Elliott, P.; Dennis, B.; Dyer, A. R.; Kesteloot, H.; Liu, K.; Ueshima, H.; Zhou, B. F. INTERMAP: background, aims, design, methods, and descriptive statistics (nondietary) J. Hum. Hypertens. 2003, 17 (9) 591-608
10. Smith, L. M.; Maher, A. D.; Want, E. J.; Elliott, P.; Stamler, J.; Hawkes, G. E.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Large-scale human metabolic phenotyping and molecular epidemiological studies via 1H NMR spectroscopy of urine: investigation of borate preservation Anal. Chem. 2009, 81 (12) 4847-56
11. Dennis, B.; Stamler, J.; Buzzard, M.; Conway, R.; Elliott, P.; Moag-Stahlberg, A.; Okayama, A.; Okuda, N.; Robertson, C.; Robinson, F.; Schakel, S.; Stevens, M.; Van Heel, N.; Zhao, L.; Zhou, B. F. INTERMAP: the dietary data - process and quality control J. Hum. Hypertens. 2003, 17 (9) 609-22
12. Dieterle, F.; Ross, A.; Schlotterbeck, G.; Senn, H. Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics Anal. Chem. 2006, 78 (13) 4281-90
13. Hotelling, H. The generalization of Student's ratio Ann. Math. Stat. 1931, 2, 360-78
14. Trygg, J.; Wold, S. O2-PLS, a two-block (X-Y) latent variable regression (LVR) method with an integral OSC filter J. Chemometr. 2003, 17 (1) 53-64
15. Cloarec, O.; Dumas, M. E.; Trygg, J.; Craig, A.; Barton, R. H.; Lindon, J. C.; Nicholson, J. K.; Holmes, E. Evaluation of the orthogonal projection on latent structure model limitations caused by chemical shift variability and improved visualization of biomarker changes in 1H NMR spectroscopic metabonomic studies Anal. Chem. 2005, 77 (2) 517-26
16. Chadeau-Hyam, M.; Ebbels, T. M. D.; Brown, I. J.; Chan, Q.; Stamler, J.; Huang, C. C.; Daviglus, M. L.; Ueshima, H.; Zhao, L.; Holmes, E.; Nicholson, J. K.; Elliott, P.; De Iorio, M. Metabolic profiling and the metabolome-wide association study: significance level for biomarker identification J. Proteome Res. 2010, 9, 4620-7
17. Holmes, E.; Loo, R. L.; Cloarec, O.; Coen, M.; Tang, H.; Maibaum, E.; Bruce, S.; Chan, Q.; Elliott, P.; Stamler, J.; Wilson, I. D.; Lindon, J. C.; Nicholson, J. K. Detection of urinary drug metabolite (xenometabolome) signatures in molecular epidemiology studies via statistical total correlation (NMR) spectroscopy Anal. Chem. 2007, 79 (7) 2629-40
18. 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 (5) 1282-9
19. Diaz, E.; Ferrandez, A.; Prieto, M. A.; Garcia, J. L. Biodegradation of aromatic compounds by Escherichia coli Microbiol. Mol. Biol. Rev. 2001, 65 (4) 523-69 and table of contents
20. Nicholson, J. K.; Holmes, E.; Wilson, I. D. Gut microorganisms, mammalian metabolism and personalized health care Nat. Rev. Microbiol. 2005, 3 (5) 431-8
21. Schwab, A. J.; Tao, L.; Yoshimura, T.; Simard, A.; Barker, F.; Pang, K. S. Hepatic uptake and metabolism of benzoate: a multiple indicator dilution, perfused rat liver study Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 280 (6) G1124-36
22. Yap, I. K.; Li, J. V.; Saric, J.; Martin, F. P.; Davies, H.; Wang, Y.; Wilson, I. D.; Nicholson, J. K.; Utzinger, J.; Marchesi, J. R.; Holmes, E. Metabonomic and microbiological analysis of the dynamic effect of vancomycin-induced gut microbiota modification in the mouse J. Proteome Res. 2008, 7 (9) 3718-28
23. Yap, I. K.; Angley, M.; Veselkov, K. A.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Urinary Metabolic Phenotyping Differentiates Children with Autism from Their Unaffected Siblings and Age-Matched Controls J. Proteome Res. 2010, 9 (6) 2996-3004
24. Selmer, T.; Andrei, P. I. p-Hydroxyphenylacetate decarboxylase from Clostridium difficile. A novel glycyl radical enzyme catalysing the formation of p-cresol Eur. J. Biochem. 2001, 268 (5) 1363-72
25. Backhed, F.; Ding, H.; Wang, T.; Hooper, L. V.; Koh, G. Y.; Nagy, A.; Semenkovich, C. F.; Gordon, J. I. The gut microbiota as an environmental factor that regulates fat storage Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (44) 15718-23
26. Backhed, F.; Manchester, J. K.; Semenkovich, C. F.; Gordon, J. I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (3) 979-84
27. Ley, R. E.; Turnbaugh, P. J.; Klein, S.; Gordon, J. I. Microbial ecology: human gut microbes associated with obesity Nature 2006, 444 (7122) 1022-3
28. Turnbaugh, P. J.; Ley, R. E.; Mahowald, M. A.; Magrini, V.; Mardis, E. R.; Gordon, J. I. An obesity-associated gut microbiome with increased capacity for energy harvest Nature 2006, 444 (7122) 1027-31
29. Elliott, P.; Stamler, J.; Nichols, R.; Dyer, A. R.; Stamler, R.; Kesteloot, H.; Marmot, M. Intersalt revisited: further analyses of 24 h sodium excretion and blood pressure within and across populations. Intersalt Cooperative Research Group BMJ 1996, 312 (7041) 1249-53
30. Pischon, T.; Boeing, H.; Hoffmann, K.; Bergmann, M.; Schulze, M. B.; Overvad, K.; van der Schouw, Y. T.; Spencer, E.; Moons, K. G.; Tjonneland, A.; Halkjaer, J.; Jensen, M. K.; Stegger, J.; Clavel-Chapelon, F.; Boutron-Ruault, M. C.; Chajes, V.; Linseisen, J.; Kaaks, R.; Trichopoulou, A.; Trichopoulos, D.; Bamia, C.; Sieri, S.; Palli, D.; Tumino, R.; Vineis, P.; Panico, S.; Peeters, P. H.; May, A. M.; Bueno-de-Mesquita, H. B.; van Duijnhoven, F. J.; Hallmans, G.; Weinehall, L.; Manjer, J.; Hedblad, B.; Lund, E.; Agudo, A.; Arriola, L.; Barricarte, A.; Navarro, C.; Martinez, C.; Quiros, J. R.; Key, T.; Bingham, S.; Khaw, K. T.; Boffetta, P.; Jenab, M.; Ferrari, P.; Riboli, E. General and abdominal adiposity and risk of death in Europe N. Engl. J. Med. 2008, 359 (20) 2105-20
31. Li, M.; Wang, B.; Zhang, M.; Rantalainen, M.; Wang, S.; Zhou, H.; Zhang, Y.; Shen, J.; Pang, X.; Wei, H.; Chen, Y.; Lu, H.; Zuo, J.; Su, M.; Qiu, Y.; Jia, W.; Xiao, C.; Smith, L. M.; Yang, S.; Holmes, E.; Tang, H.; Zhao, G.; Nicholson, J. K.; Li, L.; Zhao, L. Symbiotic gut microbes modulate human metabolic phenotypes Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (6) 2117-22
32. Zuppi, C.; Messana, I.; Forni, F.; Ferrari, F.; Rossi, C.; Giardina, B. Influence of feeding on metabolite excretion evidenced by urine 1H NMR spectral profiles: a comparison between subjects living in Rome and subjects living at arctic latitudes (Svaldbard) Clin. Chim. Acta 1998, 278 (1) 75-9
33. Balasse, E. O.; De Graef, J.; Neef, M. A. Alanine turnover in normal and diabetic dogs Horm. Metab. Res. 1985, 17 (11) 554-8
34. Nicholson, J. K.; O'Flynn, M. P.; Sadler, P. J.; Macleod, A. F.; Juul, S. M.; Sonksen, P. H. Proton-nuclear-magnetic-resonance studies of serum, plasma and urine from fasting normal and diabetic subjects Biochem. J. 1984, 217 (2) 365-75
35. Terentyeva, E. A.; Hayakawa, K.; Tanae, A.; Katsumata, N.; Tanaka, T.; Hibi, I. Urinary biotinidase and alanine excretion in patients with insulin-dependent diabetes mellitus Eur. J. Clin. Chem. Clin. Biochem. 1997, 35 (1) 21-4
36. 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 (6) 644-51
37. Simpson, D. P. Citrate excretion: a window on renal metabolism Am. J. Physiol. 1983, 244 (3) F223-34
38. Wyss, M.; Kaddurah-Daouk, R. Creatine and creatinine metabolism Physiol Rev 2000, 80 (3) 1107-213
39. Stella, C.; Beckwith-Hall, B.; Cloarec, O.; Holmes, E.; Lindon, J. C.; Powell, J.; van der Ouderaa, F.; Bingham, S.; Cross, A. J.; Nicholson, J. K. Susceptibility of human metabolic phenotypes to dietary modulation J. Proteome Res. 2006, 5 (10) 2780-8
40. Candy, D. J. Occurrence and metabolism of scylloinositol in the locust Biochem. J. 1967, 103 (3) 666-71
41. Needham, J. Scyllitol in selachian ontogeny Biochem. J. 1929, 23 (3) 319-23
42. Yancey, P. H.; Rhea, M. D.; Kemp, K. M.; Bailey, D. M. Trimethylamine oxide, betaine and other osmolytes in deep-sea animals: depth trends and effects on enzymes under hydrostatic pressure Cell. Mol. Biol. 2004, 50 (4) 371-6
43. Heinzmann, S. S.; Brown, I. J.; Chan, Q.; Bictash, M.; Dumas, M. E.; Kochhar, S.; Stamler, J.; Holmes, E.; Elliott, P.; Nicholson, J. K. Metabolic profiling strategy for discovery of nutritional biomarkers: proline betaine as a marker of citrus consumption Am. J. Clin. Nutr. 2010, 92
44. Brauer, D.; Teel, M. R. Metabolism of trans -aconitic acid in maize: II. Regulatory properties of two compartmented forms of citrate dehydrase Plant Physiol. 1982, 70 (3) 723-7
45. Altekar, W. W.; Rao, M. R. Microbiological dissimilation of tricarballylate and trans -aconitate J. Bacteriol. 1963, 85, 604-13
46. Huang, Z.; Wu, X.; Stamler, J.; Rao, X.; Tao, S.; Friedewald, W. T.; Liao, Y.; Tsai, R.; Stamler, R.; He, H. et al., A north-south comparison of blood pressure and factors related to blood pressure in the People's Republic of China: a report from the PRC-USA Collaborative Study of Cardiovascular Epidemiology J. Hypertens. 1994, 12 (9) 1103-12
47. Reynolds, K.; Gu, D.; Muntner, P.; Wu, X.; Chen, J.; Huang, G.; Duan, X.; Whelton, P. K.; He, J. Geographic variations in the prevalence, awareness, treatment and control of hypertension in China J. Hypertens. 2003, 21 (7) 1273-81
48. Stamler, J. Dietary salt and blood pressure Ann. N.Y. Acad. Sci. 1993, 676, 122-56
49. Zhou, B.; Zhang, X.; Zhu, A.; Zhao, L.; Zhu, S.; Ruan, L.; Zhu, L.; Liang, S. The relationship of dietary animal protein and electrolytes to blood pressure: a study on three Chinese populations Int. J. Epidemiol. 1994, 23 (4) 716-22
50. Zhou, B. F.; Wu, X. G.; Tao, S. Q.; Yang, J.; Cao, T. X.; Zheng, R. P.; Tian, X. Z.; Lu, C. Q.; Miao, H. Y.; Ye, F. M. et al., Dietary patterns in 10 groups and the relationship with blood pressure. Collaborative Study Group for Cardiovascular Diseases and Their Risk Factors Chin. Med. J. (Engl.) 1989, 102 (4) 257-61
51. Chen, J.; Zheng, H.; Bei, J. X.; Sun, L.; Jia, W. H.; Li, T.; Zhang, F.; Seielstad, M.; Zeng, Y. X.; Zhang, X.; Liu, J. Genetic structure of the Han Chinese population revealed by genome-wide SNP variation Am. J. Hum. Genet. 2009, 85 (6) 775-85
52. Xu, S.; Yin, X.; Li, S.; Jin, W.; Lou, H.; Yang, L.; Gong, X.; Wang, H.; Shen, Y.; Pan, X.; He, Y.; Yang, Y.; Wang, Y.; Fu, W.; An, Y.; Wang, J.; Tan, J.; Qian, J.; Chen, X.; Zhang, X.; Sun, Y.; Wu, B.; Jin, L. Genomic dissection of population substructure of Han Chinese and its implication in association studies Am. J. Hum. Genet. 2009, 85 (6) 762-74