Microbial-mammalian cometabolites dominate the age-associated urinary metabolic phenotype in Taiwanese and American populations

Journal of Proteome Research

Volumn 12, Issue 7, 2013, Pages 3166-3180

  Swann, Jonathan R ^a   Spagou, Konstantina ^b   Lewis, Matthew ^b   Nicholson, Jeremy K ^b   Glei, Dana A ^c   Seeman, Teresa E ^d   Coe, Christopher L ^e   Goldman, Noreen ^f   Ryff, Carol D ^e   Weinstein, Maxine ^c   Holmes, Elaine ^b  

^a UNIVERSITY OF READING   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c GEORGETOWN UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

^f PRINCETON UNIVERSITY   (United States)

Author keywords

4 cresyl sulfate; age; metabolic profiling; NMR spectroscopy; phenylacetylglutamine; sex

Indexed keywords

4 CRESYL SULFATE; GLUTAMINE DERIVATIVE; PHENYLACETYLGLUTAMINE; SULFUR DERIVATIVE; UNCLASSIFIED DRUG;

ADULT; AGED; AGING; ARTICLE; FEMALE; HUMAN; MALE; MAMMAL; MASS SPECTROMETRY; METABOLITE; MICROORGANISM; PHENOTYPE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; TAIWAN; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; UNITED STATES; URIC ACID URINE LEVEL; URINARY METABOLITE;

AGED; AGING; CRESOLS; GLUTAMINE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOME; MIDDLE AGED; SEX CHARACTERISTICS; SULFURIC ACID ESTERS; TAIWAN; UNITED STATES;

MAMMALIA;

EID: 84879913776     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4000152     Document Type: Article

References (63)

1. Piper, M. D.; Selman, C.; McElwee, J. J.; Partridge, L. Separating cause from effect: how does insulin/IGF signalling control lifespan in worms, flies and mice? J. Intern. Med. 2008, 263 (2) 179-91
2. Wijeyesekera, A.; Selman, C.; Barton, R. H.; Holmes, E.; Nicholson, J. K.; Withers, D. J. Metabotyping of long-lived mice using (1)H NMR spectroscopy J. Proteome Res. 2012, 11 (4) 2224-35
3. Robert, L.; Labat-Robert, J.; Robert, A. M. Genetic, epigenetic and posttranslational mechanisms of aging Biogerontology 2010, 11 (4) 387-99
4. Walston, J.; Hadley, E. C.; Ferrucci, L.; Guralnik, J. M.; Newman, A. B.; Studenski, S. A.; Ershler, W. B.; Harris, T.; Fried, L. P. Research agenda for frailty in older adults: toward a better understanding of physiology and etiology: summary from the American Geriatrics Society/National Institute on Aging Research Conference on Frailty in Older Adults J. Am. Geriatr. Soc. 2006, 54 (6) 991-1001
5. Coe, C. L.; Love, G. D.; Karasawa, M.; Kawakami, N.; Kitayama, S.; Markus, H. R.; Tracy, R. P.; Ryff, C. D. Population differences in proinflammatory biology: Japanese have healthier profiles than Americans Brain Behav. Immun. 2011, 25 (3) 494-502
6. Muangpaisan, W.; Mathews, A.; Hori, H.; Seidel, D. A systematic review of the worldwide prevalence and incidence of Parkinson's disease J. Med. Assoc. Thai. 2011, 94 (6) 749-55
7. van den Bussche, H.; Koller, D.; Kolonko, T.; Hansen, H.; Wegscheider, K.; Glaeske, G.; von Leitner, E. C.; Schafer, I.; Schon, G. Which chronic diseases and disease combinations are specific to multimorbidity in the elderly? Results of a claims data based cross-sectional study in Germany BMC Public Health 2011, 11, 101
8. Regitz-Zagrosek, V.; Lehmkuhl, E.; Weickert, M. O. Gender differences in the metabolic syndrome and their role for cardiovascular disease Clin. Res. Cardiol. 2006, 95 (3) 136-47
9. 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
10. 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 (12) 6647-54
11. 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 (11) 1181-9
12. Mishur, R. J.; Rea, S. L. Applications of mass spectrometry to metabolomics and metabonomics: detection of biomarkers of aging and of age-related diseases Mass Spectrom. Rev. 2012, 31 (1) 70-95
13. Houtkooper, R. H.; Argmann, C.; Houten, S. M.; Canto, C.; Jeninga, E. H.; Andreux, P. A.; Thomas, C.; Doenlen, R.; Schoonjans, K.; Auwerx, J. The metabolic footprint of aging in mice Sci. Rep. 2011, 1, 134
14. Okuda, Y.; Kawai, K.; Yamashita, K. Age-related change in ketone body metabolism: diminished glucagon effect on ketogenesis in adult rats Endocrinology 1987, 120 (5) 2152-7
15. Takiyama, N.; Matsumoto, K. Age-and sex-related differences of serum carnitine in a Japanese population J. Am. Coll. Nutr. 1998, 17 (1) 71-4
16. Goldman, N.; Lin, I. F.; Weinstein, M.; Lin, Y. H. Evaluating the quality of self-reports of hypertension and diabetes J. Clin. Epidemiol. 2003, 56 (2) 148-54
17. Marmot, M. G.; Fuhrer, R.; Ettner, S. L.; Marks, N. F.; Bumpass, L. L.; Ryff, C. D. Contribution of psychosocial factors to socioeconomic differences in health Milbank Q. 1998, 76 (3) 403-48
18. 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 (11) 2692-703
19. Veselkov, K. A.; Lindon, J. C.; Ebbels, T. M.; Crockford, D.; Volynkin, V. V.; Holmes, E.; Davies, D. B.; Nicholson, J. K. Recursive segment-wise peak alignment of biological (1)h NMR spectra for improved metabolic biomarker recovery Anal. Chem. 2009, 81 (1) 56-66
20. Chadeau-Hyam, M.; Ebbels, T. M.; 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 (9) 4620-7
21. 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 (6) 1005-18
22. 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 (15) 5864-72
23. Zhang, A. Q.; Mitchell, S. C.; Smith, R. L. Dimethylamine in human urine Clin. Chim. Acta 1995, 233 (1-2) 81-8
24. 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 (7341) 57-63
25. Saude, E. J.; Adamko, D.; Rowe, B. H.; Marrie, T.; Sykes, B. D. Variation of metabolites in normal human urine Metabolomics 2007, 3, 439-51
26. Hehemann, J. H.; Correc, G.; Barbeyron, T.; Helbert, W.; Czjzek, M.; Michel, G. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota Nature 2010, 464 (7290) 908-12
27. Davies, K. M.; Heaney, R. P.; Rafferty, K. Decline in muscle mass with age in women: a longitudinal study using an indirect measure Metabolism 2002, 51 (7) 935-9
28. Kochhar, S.; Jacobs, D. M.; Ramadan, Z.; Berruex, F.; Fuerholz, A.; Fay, L. B. Probing gender-specific metabolism differences in humans by nuclear magnetic resonance-based metabonomics Anal. Biochem. 2006, 352 (2) 274-81
29. Slupsky, C. M.; Rankin, K. N.; Wagner, J.; Fu, H.; Chang, D.; Weljie, A. M.; Saude, E. J.; Lix, B.; Adamko, D. J.; Shah, S.; Greiner, R.; Sykes, B. D.; Marrie, T. J. Investigations of the effects of gender, diurnal variation, and age in human urinary metabolomic profiles Anal. Chem. 2007, 79 (18) 6995-7004
30. Psihogios, N. G.; Gazi, I. F.; Elisaf, M. S.; Seferiadis, K. I.; Bairaktari, E. T. Gender-related and age-related urinalysis of healthy subjects by NMR-based metabonomics NMR Biomed 2008, 21 (3) 195-207
31. Stanley, E. G.; Bailey, N. J.; Bollard, M. E.; Haselden, J. N.; Waterfield, C. J.; Holmes, E.; Nicholson, J. K. Sexual dimorphism in urinary metabolite profiles of Han Wistar rats revealed by nuclear-magnetic-resonance- based metabonomics Anal. Biochem. 2005, 343 (2) 195-202
32. Yasuda, M.; Tsunoda, S.; Nagasawa, H. Comparison of urinary component levels in 4 strains of mice with different physiological characteristics In Vivo 1997, 11 (2) 109-13
33. Hammar, M. L.; Berg, G. E.; Larsson, L.; Tiselius, H. G.; Varenhorst, E. Endocrine changes and urinary citrate excretion Scand J Urol Nephrol 1987, 21 (1) 51-3
34. Welshman, S. G.; McGeown, M. G. Urinary citrate excretion in stone-formers and normal controls Br J Urol 1976, 48 (1) 7-11
35. Laidlaw, S. A.; Shultz, T. D.; Cecchino, J. T.; Kopple, J. D. Plasma and urine taurine levels in vegans Am. J. Clin. Nutr. 1988, 47 (4) 660-3
36. Carmel, R.; Green, R.; Jacobsen, D. W.; Rasmussen, K.; Florea, M.; Azen, C. Serum cobalamin, homocysteine, and methylmalonic acid concentrations in a multiethnic elderly population: ethnic and sex differences in cobalamin and metabolite abnormalities Am. J. Clin. Nutr. 1999, 70 (5) 904-10
37. Clarke, R.; Refsum, H.; Birks, J.; Evans, J. G.; Johnston, C.; Sherliker, P.; Ueland, P. M.; Schneede, J.; McPartlin, J.; Nexo, E.; Scott, J. M. Screening for vitamin B-12 and folate deficiency in older persons Am. J. Clin. Nutr. 2003, 77 (5) 1241-7
38. Hurley, B. F. Age, gender, and muscular strength J. Gerontol. A: Biol. Sci. Med. Sci. 1995, 50, 41-4
39. Wang, Y.; Lawler, D.; Larson, B.; Ramadan, Z.; Kochhar, S.; Holmes, E.; Nicholson, J. K. Metabonomic investigations of aging and caloric restriction in a life-long dog study J. Proteome Res. 2007, 6 (5) 1846-54
40. Perrone, R. D.; Madias, N. E.; Levey, A. S. Serum creatinine as an index of renal function: new insights into old concepts Clin. Chem. 1992, 38 (10) 1933-53
41. Wolfe, R. R. The underappreciated role of muscle in health and disease Am. J. Clin. Nutr. 2006, 84 (3) 475-82
42. Cannon, J. G. Intrinsic and extrinsic factors in muscle aging Ann. N.Y. Acad. Sci. 1998, 854, 72-7
43. Vukovich, M. D.; Stubbs, N. B.; Bohlken, R. M. Body composition in 70-year-old adults responds to dietary beta-hydroxy-beta-methylbutyrate similarly to that of young adults J. Nutr. 2001, 131 (7) 2049-52
44. Zhang, F.; Jia, Z.; Gao, P.; Kong, H.; Li, X.; Lu, X.; Wu, Y.; Xu, G. Metabonomics study of urine and plasma in depression and excess fatigue rats by ultra fast liquid chromatography coupled with ion trap-time of flight mass spectrometry Mol. Biosyst. 2010, 6 (5) 852-61
45. Willets, J. M.; Lunec, J.; Williams, A. C.; Griffiths, H. R. Neurotoxicity of nicotinamide derivatives: their role in the aetiology of Parkinson's disease Biochem. Soc. Trans. 1993, 21 (3) 299S
46. Williams, A.; Sturman, S.; Steventon, G.; Waring, R. Metabolic biomarkers of Parkinson's disease Acta Neurol. Scand. Suppl. 1991, 136, 19-23
47. Fukushima, T.; Kaetsu, A.; Lim, H.; Moriyama, M. Possible role of 1-methylnicotinamide in the pathogenesis of Parkinson's disease Exp. Toxicol. Pathol. 2002, 53 (6) 469-73
48. Kaiser, L. G.; Schuff, N.; Cashdollar, N.; Weiner, M. W. Scyllo-inositol in normal aging human brain: 1H magnetic resonance spectroscopy study at 4 T NMR Biomed. 2005, 18 (1) 51-5
49. Dean, M.; Raats, M. M.; Grunert, K. G.; Lumbers, M. Factors influencing eating a varied diet in old age Public Health Nutr. 2009, 12 (12) 2421-7
50. Wald, A. Constipation in elderly patients. Pathogenesis and management Drugs Aging 1993, 3 (3) 220-31
51. Cho, S.; Lau, S. W.; Tandon, V.; Kumi, K.; Pfuma, E.; Abernethy, D. R. Geriatric drug evaluation: where are we now and where should we be in the future? Arch. Intern. Med. 2011, 171 (10) 937-40
52. Triantafyllou, K.; Vlachogiannakos, J.; Ladas, S. D. Gastrointestinal and liver side effects of drugs in elderly patients Best Pract. Res. Clin. Gastroenterol. 2010, 24 (2) 203-15
53. Ramakrishna, B. S.; Gee, D.; Weiss, A.; Pannall, P.; Roberts-Thomson, I. C.; Roediger, W. E. Estimation of phenolic conjugation by colonic mucosa J. Clin. Pathol. 1989, 42 (6) 620-3
54. Ramakrishna, B. S.; Roberts-Thomson, I. C.; Pannall, P. R.; Roediger, W. E. Impaired sulphation of phenol by the colonic mucosa in quiescent and active ulcerative colitis Gut 1991, 32 (1) 46-9
55. Hebuterne, X. Gut changes attributed to ageing: effects on intestinal microflora Curr. Opin. Clin. Nutr. Metab. Care 2003, 6 (1) 49-54
56. Mariat, D.; Firmesse, O.; Levenez, F.; Guimaraes, V.; Sokol, H.; Dore, J.; Corthier, G.; Furet, J. P. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age BMC Microbiol. 2009, 9, 123
57. Partridge, L.; Thornton, J.; Bates, G. The new science of ageing Philos. Trans. R. Soc. Lond., B: Biol. Sci. 2011, 366 (1561) 6-8
58. Hopkins, M. J.; Sharp, R.; Macfarlane, G. T. Variation in human intestinal microbiota with age Dig. Liver Dis. 2002, 34 (Suppl 2) S12-8
59. He, F.; Ouwehand, A. C.; Isolauri, E.; Hosoda, M.; Benno, Y.; Salminen, S. Differences in composition and mucosal adhesion of bifidobacteria isolated from healthy adults and healthy seniors Curr. Microbiol. 2001, 43 (5) 351-4
60. Tiihonen, K.; Ouwehand, A. C.; Rautonen, N. Human intestinal microbiota and healthy ageing Ageing Res. Rev. 2010, 9 (2) 107-16
61. O'Sullivan, O.; Coakley, M.; Lakshminarayanan, B.; Claesson, M. J.; Stanton, C.; O'Toole, P. W.; Ross, R. P. Correlation of rRNA gene amplicon pyrosequencing and bacterial culture for microbial compositional analysis of faecal samples from elderly Irish subjects J. Appl. Microbiol. 2011, 111 (2) 467-73
62. Elsden, S. R.; Hilton, M. G.; Waller, J. M. The end products of the metabolism of aromatic amino acids by Clostridia Arch. Microbiol. 1976, 107 (3) 283-8
63. Bell, J. D.; Sadler, P. J.; Morris, V. C.; Levander, O. A. Effect of aging and diet on proton NMR spectra of rat urine Magn. Reson. Med. 1991, 17 (2) 414-22