Characterizing blood metabolomics profiles associated with self-reported food intakes in female twins

PLoS ONE

Volumn 11, Issue 6, 2016, Pages

  Pallister, Tess ^a   Jennings, Amy ^b   Mohney, Robert P ^c   Yarand, Darioush ^a   Mangino, Massimo ^a   Cassidy, Aedin ^b   MacGregor, Alexander ^b   Spector, Tim D ^a   Menni, Cristina ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c METABOLON INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; HYDROCINNAMIC ACID; HYDROXYPROLINE; INDOLEPROPIONIC ACID; THIONEINE; THREITOL; COFFEE; PHENOL; TEA;

ADULT; ARTICLE; BLOOD ANALYSIS; BLOOD SAMPLING; FEMALE; FOOD INTAKE; FRUIT; HUMAN; METABOLITE; METABOLOMICS; MUSHROOM; NUTRITIONAL ASSESSMENT; RED MEAT; SELF REPORT; TWIN DISCORDANCE; TWINS; BLOOD; BODY MASS; COFFEE; COHORT ANALYSIS; DIET; EATING; FEEDING BEHAVIOR; METABOLOME; MONOZYGOTIC TWINS; QUALITY CONTROL; QUESTIONNAIRE; SEA FOOD; STATISTICAL MODEL; TEA; UNITED KINGDOM; VEGETABLE;

ADULT; BIOMARKERS; BLOOD CHEMICAL ANALYSIS; BODY MASS INDEX; COFFEE; COHORT STUDIES; DIET; EATING; FEEDING BEHAVIOR; FEMALE; HUMANS; LINEAR MODELS; METABOLOME; PHENOL; QUALITY CONTROL; RED MEAT; SEAFOOD; SELF REPORT; SURVEYS AND QUESTIONNAIRES; TEA; TWINS, MONOZYGOTIC; UNITED KINGDOM; VEGETABLES;

EID: 84977263277     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158568     Document Type: Article

References (76)

1. Guertin KA, Moore SC, Sampson JN, Huang WY, Xiao Q, Stolzenberg-Solomon RZ, et al. (2014) Metabolomics in nutritional epidemiology: identifying metabolites associated with diet and quantifying their potential to uncover diet-disease relations in populations. Am J Clin Nutr 100: 208-217. doi: 10.3945/ajcn.113.078758 PMID: 24740205
2. Zheng Y, Yu B, Alexander D, Steffen LM, Nettleton JA, Boerwinkle E (2014) Metabolomic patterns and alcohol consumption in African Americans in the Atherosclerosis Risk in Communities Study. Am J Clin Nutr 99: 1470-1478. doi: 10.3945/ajcn.113.074070 PMID: 24760976
3. O'Sullivan A, Gibney MJ, Brennan L (2011) Dietary intake patterns are reflected in metabolomic profiles: potential role in dietary assessment studies. Am J Clin Nutr 93: 314-321. doi: 10.3945/ajcn.110.000950 PMID: 21177801
4. Altmaier E, Kastenmuller G, Romisch-Margl W, Thorand B, Weinberger KM, Illig T, et al. (2011) Questionnaire-based self-reported nutrition habits associate with serum metabolism as revealed by quantitative targeted metabolomics. Eur J Epidemiol 26: 145-156. doi: 10.1007/s10654-010-9524-7 PMID: 21116839
5. Floegel A, von Ruesten A, Drogan D, Schulze MB, Prehn C, Adamski J, et al. (2013) Variation of serum metabolites related to habitual diet: a targeted metabolomic approach in EPIC-Potsdam. Eur J Clin Nutr 67: 1100-1108. doi: 10.1038/ejcn.2013.147 PMID: 23942179
6. Shin SY, Fauman EB, Petersen AK, Krumsiek J, Santos R, Huang J, et al. (2014) An atlas of genetic influences on human blood metabolites. 46: 543-550.
7. Kettunen J, Tukiainen T, Sarin AP, Ortega-Alonso A, Tikkanen E, Lyytikainen LP, et al. (2012) Genome-wide association study identifies multiple loci influencing human serum metabolite levels. Nat Genet 44: 269-276. doi: 10.1038/ng.1073 PMID: 22286219
8. Qi Q, Durst R, Schwarzfuchs D, Leitersdorf E, Shpitzen S, Li Y, et al. (2015) CETP genotype and changes in lipid levels in response to weight-loss diet intervention in the POUNDS LOST and DIRECT randomized trials. J Lipid Res 56: 713-721. doi: 10.1194/jlr.P055715 PMID: 25548261
9. Xu M, Ng SS, Bray GA, Ryan DH, Sacks FM, Ning G, et al. (2015) Dietary Fat Intake Modifies the Effect of a Common Variant in the LIPC Gene on Changes in Serum Lipid Concentrations during a Long-Term Weight-Loss Intervention Trial. J Nutr 145: 1289-1294. doi: 10.3945/jn.115.212514 PMID: 25926410
10. Wichmann HE, Gieger C, Illig T (2005) KORA-gen - resource for population genetics, controls and a broad spectrum of disease phenotypes. Gesundheitswesen 67 Suppl 1: S26-30. PMID: 16032514
11. Shin SY, Fauman EB, Petersen AK, Krumsiek J, Santos R, Huang J, et al. (2014) An atlas of genetic influences on human blood metabolites. Nat Genet 46: 543-550. doi: 10.1038/ng.2982 PMID: 24816252
12. Sampson JN, Boca SM, Shu XO, Stolzenberg-Solomon RZ, Matthews CE, Hsing AW, et al. (2013) Metabolomics in epidemiology: sources of variability in metabolite measurements and implications. Cancer Epidemiol Biomarkers Prev 22: 631-640. doi: 10.1158/1055-9965.EPI-12-1109 PMID: 23396963
13. Menni C, Kastenmuller G, Petersen AK, Bell JT, Psatha M, Tsai PC, et al. (2013) Metabolomic markers reveal novel pathways of ageing and early development in human populations. Int J Epidemiol 42: 1111-1119. doi: 10.1093/ije/dyt094 PMID: 23838602
14. Menni C, Zhai G, Macgregor A, Prehn C, Romisch-Margl W, Suhre K, et al. (2013) Targeted metabolomics profiles are strongly correlated with nutritional patterns in women. Metabolomics 9: 506-514. PMID: 23543136
15. Moayyeri A, Hammond CJ, Hart DJ, Spector TD (2013) The UK Adult Twin Registry (TwinsUK Resource). Twin Res Hum Genet 16: 144-149. doi: 10.1017/thg.2012.89 PMID: 23088889
16. Bingham SA, Welch AA, McTaggart A, Mulligan AA, Runswick SA, Luben R, et al. (2001) Nutritional methods in the European Prospective Investigation of Cancer in Norfolk. Public Health Nutr 4: 847-858. PMID: 11415493
17. Teucher B, Skinner J, Skidmore PM, Cassidy A, Fairweather-Tait SJ, Hooper L, et al. (2007) Dietary patterns and heritability of food choice in a UK female twin cohort. Twin Res Hum Genet 10: 734-748. PMID: 17903115
18. Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124: 17-27. PMID: 3521261
19. Menni C, Fauman E, Erte I, Perry JR, Kastenmuller G, Shin SY, et al. (2013) Biomarkers for type 2 diabetes and impaired fasting glucose using a nontargeted metabolomics approach. Diabetes 62: 4270-4276. doi: 10.2337/db13-0570 PMID: 23884885
20. Illig T, Gieger C, Zhai G, Romisch-Margl W, Wang-Sattler R, Prehn C, et al. (2010) A genome-wide perspective of genetic variation in human metabolism. Nat Genet 42: 137-141. doi: 10.1038/ng.507 PMID: 20037589
21. Römisch-Margl W, Prehn C, Bogumil R, Röhring C, Suhre K, Adamski J (2012) Procedure for tissue sample preparation and metabolite extraction for high-throughput targeted metabolomics. Metabolomics 8: 133-142.
22. Jeter CB, Hergenroeder GW, Ward NH 3rd, Moore AN, Dash PK (2013) Human mild traumatic brain injury decreases circulating branched-chain amino acids and their metabolite levels. J Neurotrauma 30: 671-679. doi: 10.1089/neu.2012.2491 PMID: 23560894
23. Lindtner C, Scherer T, Zielinski E, Filatova N, Fasshauer M, Tonks NK, et al. (2013) Binge drinking induces whole-body insulin resistance by impairing hypothalamic insulin action. Sci Transl Med 5: 170ra114.
24. Barawkar DA, Bandyopadhyay A, Deshpande A, Koul S, Kandalkar S, Patil P, et al. (2012) Discovery of pyrazole carboxylic acids as potent inhibitors of rat long chain L-2-hydroxy acid oxidase. Bioorg Med Chem Lett 22: 4341-4347. doi: 10.1016/j.bmcl.2012.05.020 PMID: 22658862
25. Trysberg E, Hoglund K, Svenungsson E, Blennow K, Tarkowski A (2004) Decreased levels of soluble amyloid beta-protein precursor and beta-amyloid protein in cerebrospinal fluid of patients with systemic lupus erythematosus. Arthritis Res Ther 6: R129-136. PMID: 15059276
26. Jin M, Selkoe DJ (2015) Systematic analysis of time-dependent neural effects of soluble amyloid beta oligomers in culture and in vivo: Prevention by scyllo-inositol. Neurobiol Dis 82: 152-163. doi: 10.1016/j.nbd.2015.05.020 PMID: 26054438
27. Maiti S, Chen G (2015) Ethanol up-regulates phenol sulfotransferase (SULT1A1) and hydroxysteroid sulfotransferase (SULT2A1) in rat liver and intestine. Arch Physiol Biochem 121: 68-74. doi: 10.3109/13813455.2014.992440 PMID: 25720860
28. Goncalves I, Edsfeldt A, Ko NY, Grufman H, Berg K, Bjorkbacka H, et al. (2012) Evidence supporting a key role of Lp-PLA2-generated lysophosphatidylcholine in human atherosclerotic plaque inflammation. Arterioscler Thromb Vasc Biol 32: 1505-1512. doi: 10.1161/ATVBAHA.112.249854 PMID: 22499993
29. Zheng Y, Yu B, Alexander D, Steffen LM, Boerwinkle E (2014) Human metabolome associates with dietary intake habits among African Americans in the atherosclerosis risk in communities study. Am J Epidemiol 179: 1424-1433. doi: 10.1093/aje/kwu073 PMID: 24801555
30. Yang Q, Yin RX, Cao XL, Wu DF, Chen WX, Zhou YJ (2015) Association of two polymorphisms in the FADS1/FADS2 gene cluster and the risk of coronary artery disease and ischemic stroke. Int J Clin Exp Pathol 8: 7318-7331. PMID: 26261632
31. Smith CE, Follis JL, Nettleton JA, Foy M, Wu JH, Ma Y, et al. (2015) Dietary fatty acids modulate associations between genetic variants and circulating fatty acids in plasma and erythrocyte membranes: Meta-analysis of nine studies in the CHARGE consortium. Mol Nutr Food Res 59: 1373-1383. doi: 10.1002/mnfr.201400734 PMID: 25626431
32. Ohara H, Matsumoto H, Ito K, Iwai K, Sato K (2007) Comparison of quantity and structures of hydroxyproline-containing peptides in human blood after oral ingestion of gelatin hydrolysates from different sources. J Agric Food Chem 55: 1532-1535. PMID: 17253720
33. Delanghe J, De Slypere JP, De Buyzere M, Robbrecht J, Wieme R, Vermeulen A (1989) Normal reference values for creatine, creatinine, and carnitine are lower in vegetarians. Clin Chem 35: 1802-1803. PMID: 2758659
34. Gall WE, Beebe K, Lawton KA, Adam KP, Mitchell MW, Nakhle PJ, et al. (2010) alpha-hydroxybutyrate is an early biomarker of insulin resistance and glucose intolerance in a nondiabetic population. PLoS One 5: e10883. doi: 10.1371/journal.pone.0010883 PMID: 20526369
35. Kalhan SC, Guo L, Edmison J, Dasarathy S, McCullough AJ, Hanson RW, et al. (2011) Plasma metabolomic profile in nonalcoholic fatty liver disease. Metabolism 60: 404-413. doi: 10.1016/j.metabol.2010.03.006 PMID: 20423748
36. Alexander D, Lombardi R, Rodriguez G, Mitchell MM, Marian AJ (2011) Metabolomic distinction and insights into the pathogenesis of human primary dilated cardiomyopathy. Eur J Clin Invest 41: 527-538. doi: 10.1111/j.1365-2362.2010.02441.x PMID: 21155767
37. Rodriguez-Suarez E, Mato JM, Elortza F (2012) Proteomics analysis of human nonalcoholic fatty liver. Methods Mol Biol 909: 241-258. doi: 10.1007/978-1-61779-959-4-16 PMID: 22903720
38. Franceschini N, Haack K, Almasy L, Laston S, Lee ET, Best LG, et al. (2014) Generalization of associations of kidney-related genetic loci to American Indians. Clin J Am Soc Nephrol 9: 150-158. doi: 10.2215/CJN.02300213 PMID: 24311711
39. Liu CT, Garnaas MK, Tin A, Kottgen A, Franceschini N, Peralta CA, et al. (2011) Genetic association for renal traits among participants of African ancestry reveals new loci for renal function. PLoS Genet 7: e1002264. doi: 10.1371/journal.pgen.1002264 PMID: 21931561
40. Abdullah MM, Cyr A, Lepine MC, Labonte ME, Couture P, Jones PJ, et al. (2015) Recommended dairy product intake modulates circulating fatty acid profile in healthy adults: a multi-centre cross-over study. Br J Nutr 113: 435-444. doi: 10.1017/S0007114514003894 PMID: 25609231
41. Yamagishi K, Nettleton JA, Folsom AR (2008) Plasma fatty acid composition and incident heart failure in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) Study. Am Heart J 156: 965-974. doi: 10.1016/j.ahj.2008.06.017 PMID: 19061714
42. Sun H, Liu D (2015) Hydrodynamic delivery of interleukin 15 gene promotes resistance to high fat diet-induced obesity, fatty liver and improves glucose homeostasis. Gene Ther 22: 341-347. doi: 10.1038/gt.2014.114 PMID: 25503694
43. Bondia-Pons I, Barri T, Hanhineva K, Juntunen K, Dragsted LO, Mykkanen H, et al. (2013) UPLC-QTOF/MS metabolic profiling unveils urinary changes in humans after a whole grain rye versus refined wheat bread intervention. Mol Nutr Food Res 57: 412-422. doi: 10.1002/mnfr.201200571 PMID: 23307617
44. Jensen BM, Adhikari KB, Schnoor HJ, Juel-Berg N, Fomsgaard IS, Poulsen LK (2015) Quantitative analysis of absorption, metabolism, and excretion of benzoxazinoids in humans after the consumption of high- and low-benzoxazinoid diets with similar contents of cereal dietary fibres: a crossover study. Eur J Nutr.
45. Bene J, Komlosi K, Gasztonyi B, Juhasz M, Tulassay Z, Melegh B (2005) Plasma carnitine ester profile in adult celiac disease patients maintained on long-term gluten free diet. World J Gastroenterol 11: 6671-6675. PMID: 16425363
46. Smith EA, Macfarlane GT (1996) Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J Appl Bacteriol 81: 288-302. PMID: 8810056
47. Karbownik M, Reiter RJ, Garcia JJ, Cabrera J, Burkhardt S, Osuna C, et al. (2001) Indole-3-propionic acid, a melatonin-related molecule, protects hepatic microsomal membranes from iron-induced oxidative damage: relevance to cancer reduction. J Cell Biochem 81: 507-513. PMID: 11255233
48. van Dorsten FA, Peters S, Gross G, Gomez-Roldan V, Klinkenberg M, de Vos RC, et al. (2012) Gut microbial metabolism of polyphenols from black tea and red wine/grape juice is source-specific and colon-region dependent. J Agric Food Chem 60: 11331-11342. doi: 10.1021/jf303165w PMID: 23072624
49. Anson NM, Selinheimo E, Havenaar R, Aura AM, Mattila I, Lehtinen P, et al. (2009) Bioprocessing of wheat bran improves in vitro bioaccessibility and colonic metabolism of phenolic compounds. J Agric Food Chem 57: 6148-6155. doi: 10.1021/jf900492h PMID: 19537710
50. Ou K, Sarnoski P, Schneider KR, Song K, Khoo C, Gu L (2014) Microbial catabolism of procyanidins by human gut microbiota. Mol Nutr Food Res 58: 2196-2205. doi: 10.1002/mnfr.201400243 PMID: 25045165
51. Lustgarten MS, Price LL, Chale A, Phillips EM, Fielding RA (2014) Branched chain amino acids are associated with muscle mass in functionally limited older adults. J Gerontol A Biol Sci Med Sci 69: 717-724. doi: 10.1093/gerona/glt152 PMID: 24085401
52. Kasuya F, Igarashi K, Fukui M (1996) Participation of a medium chain acyl-CoA synthetase in glycine conjugation of the benzoic acid derivatives with the electron-donating groups. Biochem Pharmacol 51: 805-809. PMID: 8602876
53. Lindner I, Rubin D, Helwig U, Nitz I, Hampe J, Schreiber S, et al. (2006) The L513S polymorphism in medium-chain acyl-CoA synthetase 2 (MACS2) is associated with risk factors of the metabolic syndrome in a Caucasian study population. Mol Nutr Food Res 50: 270-274. PMID: 16521160
54. Deiana M, Rosa A, Casu V, Piga R, Assunta Dessi M, Aruoma OI (2004) L-ergothioneine modulates oxidative damage in the kidney and liver of rats in vivo: studies upon the profile of polyunsaturated fatty acids. Clin Nutr 23: 183-193. PMID: 15030958
55. Ey J, Schomig E, Taubert D (2007) Dietary sources and antioxidant effects of ergothioneine. J Agric Food Chem 55: 6466-6474. PMID: 17616140
56. Li RW, Yang C, Sit AS, Kwan YW, Lee SM, Hoi MP, et al. (2014) Uptake and protective effects of ergothioneine in human endothelial cells. J Pharmacol Exp Ther 350: 691-700. doi: 10.1124/jpet.114.214049 PMID: 25022513
57. Guertin KA, Moore SC, Sampson JN, Huang WY, Xiao Q, Stolzenberg-Solomon RZ, et al. (2014) Metabolomics in nutritional epidemiology: identifying metabolites associated with diet and quantifying their potential to uncover diet-disease relations in populations. Am J Clin Nutr 100: 208-217. doi: 10.3945/ajcn.113.078758 PMID: 24740205
58. Ling Y, van Herpt TT, van Hoek M, Dehghan A, Hofman A, Uitterlinden AG, et al. (2014) A genetic variant in SLC6A20 is associated with Type 2 diabetes in white-European and Chinese populations. Diabet Med 31: 1350-1356. doi: 10.1111/dme.12528 PMID: 24958070
59. Wittenbecher C, Muhlenbruch K, Kroger J, Jacobs S, Kuxhaus O, Floegel A, et al. (2015) Amino acids, lipid metabolites, and ferritin as potential mediators linking red meat consumption to type 2 diabetes. Am J Clin Nutr 101: 1241-1250. doi: 10.3945/ajcn.114.099150 PMID: 25948672
60. Floegel A, Stefan N, Yu Z, Muhlenbruch K, Drogan D, Joost HG, et al. (2013) Identification of serum metabolites associated with risk of type 2 diabetes using a targeted metabolomic approach. Diabetes 62: 639-648. doi: 10.2337/db12-0495 PMID: 23043162
61. Butler MA, Lang NP, Young JF, Caporaso NE, Vineis P, Hayes RB, et al. (1992) Determination of CYP1A2 and NAT2 phenotypes in human populations by analysis of caffeine urinary metabolites. Pharmacogenetics 2: 116-127. PMID: 1306111
62. Kiyohara C, Washio M, Horiuchi T, Asami T, Ide S, Atsumi T, et al. (2014) Modifying effect of N-acetyltransferase 2 genotype on the association between systemic lupus erythematosus and consumption of alcohol and caffeine-rich beverages. Arthritis Care Res (Hoboken) 66: 1048-1056.
63. Westerterp KR, Goris AH (2002) Validity of the assessment of dietary intake: problems of misreporting. Curr Opin Clin Nutr Metab Care 5: 489-493. PMID: 12172471
64. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al. (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155: 1451-1463. doi: 10.1016/j.cell.2013.11.024 PMID: 24315484
65. Johnson IT, Gee JM, Price K, Curl C, Fenwick GR (1986) Influence of saponins on gut permeability and active nutrient transport in vitro. J Nutr 116: 2270-2277. PMID: 3794833
66. Knudsen D, Jutfelt F, Sundh H, Sundell K, Koppe W, Frokiaer H (2008) Dietary soya saponins increase gut permeability and play a key role in the onset of soyabean-induced enteritis in Atlantic salmon (Salmo salar L.). Br J Nutr 100: 120-129. doi: 10.1017/S0007114507886338 PMID: 18167174
67. Rodriguez A, Costa-Bauza A, Saez-Torres C, Rodrigo D, Grases F (2015) HPLC method for urinary theobromine determination: Effect of consumption of cocoa products on theobromine urinary excretion in children. Clin Biochem.
68. Suzuki T, Takahashi E (1975) Biosynthesis of caffeine by tea-leaf extracts. Enzymic formation of theobromine from 7-methylxanthine and of caffeine from theobromine. Biochem J 146: 87-96. PMID: 238504
69. Safranow K, Machoy Z (2005) Simultaneous determination of 16 purine derivatives in urinary calculi by gradient reversed-phase high-performance liquid chromatography with UV detection. J Chromatogr B Analyt Technol Biomed Life Sci 819: 229-235. PMID: 15833286
70. Suhre K, Shin SY, Petersen AK, Mohney RP, Meredith D, Wagele B, et al. (2011) Human metabolic individuality in biomedical and pharmaceutical research. Nature 477: 54-60. doi: 10.1038/nature10354 PMID: 21886157
71. Lee YH, Song GG (2012) Pathway analysis of genome-wide association studies on uric acid concentrations. Hum Immunol 73: 805-810. doi: 10.1016/j.humimm.2012.05.004 PMID: 22609445
72. Nakayama A, Matsuo H, Shimizu T, Ogata H, Takada Y, Nakashima H, et al. (2013) Common missense variant of monocarboxylate transporter 9 (MCT9/SLC16A9) gene is associated with renal overload gout, but not with all gout susceptibility. Hum Cell 26: 133-136. doi: 10.1007/s13577-013-0073-8 PMID: 23990105
73. Ballatori N, Fang F, Christian WV, Li N, Hammond CL (2008) Ostalpha-Ostbeta is required for bile acid and conjugated steroid disposition in the intestine, kidney, and liver. Am J Physiol Gastrointest Liver Physiol 295: G179-g186. doi: 10.1152/ajpgi.90319.2008 PMID: 18497332
74. Charlton KE, Tapsell LC, Batterham MJ, O'Shea J, Thorne R, Beck E, et al. (2012) Effect of 6 weeks' consumption of beta-glucan-rich oat products on cholesterol levels in mildly hypercholesterolaemic overweight adults. Br J Nutr 107: 1037-1047. doi: 10.1017/S0007114511003850 PMID: 21810288
75. Wolever TM, Tosh SM, Gibbs AL, Brand-Miller J, Duncan AM, Hart V, et al. (2010) Physicochemical properties of oat beta-glucan influence its ability to reduce serum LDL cholesterol in humans: a randomized clinical trial. Am J Clin Nutr 92: 723-732. doi: 10.3945/ajcn.2010.29174 PMID: 20660224
76. Yousri NA, Kastenmuller G, Gieger C, Shin SY, Erte I, Menni C, et al. (2014) Long term conservation of human metabolic phenotypes and link to heritability. Metabolomics 10: 1005-1017. PMID: 25177233