Lean-seafood intake decreases urinary markers of mitochondrial lipid and energy metabolism in healthy subjects: Metabolomics results from a randomized crossover intervention study

Scope Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is sparse. We aimed to elucidate diet‐induced metabolic changes through untargeted urinary metabolomics after four weeks of intervention with lean‐...

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Published inMolecular nutrition & food research Vol. 60; no. 7; pp. 1661 - 1672
Main Authors Schmedes, Mette, Aadland, Eli Kristin, Sundekilde, Ulrik Kræmer, Jacques, Hélène, Lavigne, Charles, Graff, Ingvild Eide, Eng, Øyvin, Holthe, Asle, Mellgren, Gunnar, Young, Jette Feveile, Bertram, Hanne Christine, Liaset, Bjørn, Clausen, Morten Rahr
Format Journal Article
LanguageEnglish
Published Germany Blackwell Publishing Ltd 01.07.2016
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Online AccessGet full text
ISSN1613-4125
1613-4133
DOI10.1002/mnfr.201500785

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Abstract Scope Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is sparse. We aimed to elucidate diet‐induced metabolic changes through untargeted urinary metabolomics after four weeks of intervention with lean‐seafood or nonseafood diets. It is shown that lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects. Methods In a randomized controlled trial with crossover design, 20 healthy subjects consumed two balanced diets that varied in main protein sources for 4 weeks. Morning spot urine samples were collected before and after each intervention period. Untargeted metabolomics based on 1H NMR spectroscopy and LC‐MS analyses were applied to characterize the urinary metabolic response to the interventions. Results The lean‐seafood diet period reduced the urinary level of l‐carnitine, 2,6‐dimethylheptanoylcarnitine, and N‐methyl‐2‐pyridone‐5‐carboxamide, relative to the nonseafood period. The dietary analysis revealed that the higher urinary level of trimethylamine‐N‐oxide after the lean‐seafood diet period and guanidinoacetate and 3‐methylhistidine after the nonseafood diet period was related to the endogenous content of these compounds in the diets. Conclusions Our data reveal that 4 weeks of lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects after the lean‐seafood intake. The scope of the present study is to elucidate the diet‐induced metabolic changes in healthy subjects through untargeted urinary metabolomics after four weeks of intervention with lean‐seafood or nonseafood as the main protein sources. It is shown that lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects.
AbstractList SCOPE: Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is sparse. We aimed to elucidate diet‐induced metabolic changes through untargeted urinary metabolomics after four weeks of intervention with lean‐seafood or nonseafood diets. It is shown that lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects. METHODS: In a randomized controlled trial with crossover design, 20 healthy subjects consumed two balanced diets that varied in main protein sources for 4 weeks. Morning spot urine samples were collected before and after each intervention period. Untargeted metabolomics based on ¹H NMR spectroscopy and LC‐MS analyses were applied to characterize the urinary metabolic response to the interventions. RESULTS: The lean‐seafood diet period reduced the urinary level of l‐carnitine, 2,6‐dimethylheptanoylcarnitine, and N‐methyl‐2‐pyridone‐5‐carboxamide, relative to the nonseafood period. The dietary analysis revealed that the higher urinary level of trimethylamine‐N‐oxide after the lean‐seafood diet period and guanidinoacetate and 3‐methylhistidine after the nonseafood diet period was related to the endogenous content of these compounds in the diets. CONCLUSIONS: Our data reveal that 4 weeks of lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects after the lean‐seafood intake.
Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is sparse. We aimed to elucidate diet-induced metabolic changes through untargeted urinary metabolomics after four weeks of intervention with lean-seafood or nonseafood diets. It is shown that lean-seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects. In a randomized controlled trial with crossover design, 20 healthy subjects consumed two balanced diets that varied in main protein sources for 4 weeks. Morning spot urine samples were collected before and after each intervention period. Untargeted metabolomics based on (1) H NMR spectroscopy and LC-MS analyses were applied to characterize the urinary metabolic response to the interventions. The lean-seafood diet period reduced the urinary level of l-carnitine, 2,6-dimethylheptanoylcarnitine, and N-methyl-2-pyridone-5-carboxamide, relative to the nonseafood period. The dietary analysis revealed that the higher urinary level of trimethylamine-N-oxide after the lean-seafood diet period and guanidinoacetate and 3-methylhistidine after the nonseafood diet period was related to the endogenous content of these compounds in the diets. Our data reveal that 4 weeks of lean-seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects after the lean-seafood intake.
Scope Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is sparse. We aimed to elucidate diet‐induced metabolic changes through untargeted urinary metabolomics after four weeks of intervention with lean‐seafood or nonseafood diets. It is shown that lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects. Methods In a randomized controlled trial with crossover design, 20 healthy subjects consumed two balanced diets that varied in main protein sources for 4 weeks. Morning spot urine samples were collected before and after each intervention period. Untargeted metabolomics based on 1H NMR spectroscopy and LC‐MS analyses were applied to characterize the urinary metabolic response to the interventions. Results The lean‐seafood diet period reduced the urinary level of l‐carnitine, 2,6‐dimethylheptanoylcarnitine, and N‐methyl‐2‐pyridone‐5‐carboxamide, relative to the nonseafood period. The dietary analysis revealed that the higher urinary level of trimethylamine‐N‐oxide after the lean‐seafood diet period and guanidinoacetate and 3‐methylhistidine after the nonseafood diet period was related to the endogenous content of these compounds in the diets. Conclusions Our data reveal that 4 weeks of lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects after the lean‐seafood intake. The scope of the present study is to elucidate the diet‐induced metabolic changes in healthy subjects through untargeted urinary metabolomics after four weeks of intervention with lean‐seafood or nonseafood as the main protein sources. It is shown that lean‐seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects.
Scope Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is sparse. We aimed to elucidate diet-induced metabolic changes through untargeted urinary metabolomics after four weeks of intervention with lean-seafood or nonseafood diets. It is shown that lean-seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects. Methods In a randomized controlled trial with crossover design, 20 healthy subjects consumed two balanced diets that varied in main protein sources for 4 weeks. Morning spot urine samples were collected before and after each intervention period. Untargeted metabolomics based on super(1)H NMR spectroscopy and LC-MS analyses were applied to characterize the urinary metabolic response to the interventions. Results The lean-seafood diet period reduced the urinary level of l-carnitine, 2,6-dimethylheptanoylcarnitine, and N-methyl-2-pyridone-5-carboxamide, relative to the nonseafood period. The dietary analysis revealed that the higher urinary level of trimethylamine-N-oxide after the lean-seafood diet period and guanidinoacetate and 3-methylhistidine after the nonseafood diet period was related to the endogenous content of these compounds in the diets. Conclusions Our data reveal that 4 weeks of lean-seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects after the lean-seafood intake. The scope of the present study is to elucidate the diet-induced metabolic changes in healthy subjects through untargeted urinary metabolomics after four weeks of intervention with lean-seafood or nonseafood as the main protein sources. It is shown that lean-seafood intake reduces urinary excretion of metabolites involved in mitochondrial lipid and energy metabolism possibly facilitating a higher lipid catabolism in healthy subjects.
Author Aadland, Eli Kristin
Clausen, Morten Rahr
Schmedes, Mette
Bertram, Hanne Christine
Liaset, Bjørn
Lavigne, Charles
Graff, Ingvild Eide
Jacques, Hélène
Holthe, Asle
Mellgren, Gunnar
Eng, Øyvin
Sundekilde, Ulrik Kræmer
Young, Jette Feveile
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  surname: Schmedes
  fullname: Schmedes, Mette
  organization: Department of Food Science, Aarhus University, Aarslev, Denmark
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  givenname: Eli Kristin
  surname: Aadland
  fullname: Aadland, Eli Kristin
  organization: National Institute of Nutrition and Seafood Research, Bergen, Norway
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  givenname: Ulrik Kræmer
  surname: Sundekilde
  fullname: Sundekilde, Ulrik Kræmer
  organization: Department of Food Science, Aarhus University, Aarslev, Denmark
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  givenname: Hélène
  surname: Jacques
  fullname: Jacques, Hélène
  organization: School of Nutrition, Laval Université, Québec, Canada
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  givenname: Charles
  surname: Lavigne
  fullname: Lavigne, Charles
  organization: National Institute of Nutrition and Seafood Research, Bergen, Norway
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  givenname: Ingvild Eide
  surname: Graff
  fullname: Graff, Ingvild Eide
  organization: National Institute of Nutrition and Seafood Research, Bergen, Norway
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  surname: Eng
  fullname: Eng, Øyvin
  organization: Hormone Laboratory, Haukeland University Hospital, Bergen, Norway
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  surname: Holthe
  fullname: Holthe, Asle
  organization: Bergen University College, Faculty of Education, Bergen, Norway
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  givenname: Gunnar
  surname: Mellgren
  fullname: Mellgren, Gunnar
  organization: Department of Clinical Science, University of Bergen, Bergen, Norway
– sequence: 10
  givenname: Jette Feveile
  surname: Young
  fullname: Young, Jette Feveile
  organization: Department of Food Science, Aarhus University, Foulum, Denmark
– sequence: 11
  givenname: Hanne Christine
  surname: Bertram
  fullname: Bertram, Hanne Christine
  organization: Department of Food Science, Aarhus University, Aarslev, Denmark
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  surname: Liaset
  fullname: Liaset, Bjørn
  organization: National Institute of Nutrition and Seafood Research, Bergen, Norway
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  givenname: Morten Rahr
  surname: Clausen
  fullname: Clausen, Morten Rahr
  email: mortenr.clausen@food.au.dk
  organization: Department of Food Science, Aarhus University, Aarslev, Denmark
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Keywords Urine
Biomarkers
Dietary protein
Lipid metabolism
Metabolism
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Seibel, B. A., Walsh, P. J., Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage. J. Exp. Biol. 2002, 205, 297-306.
Wang, Z., Tang, W. H., Buffa, J. A., Fu, X. et al., Prognostic value of choline and betaine depends on intestinal microbiota-generated metabolite trimethylamine-N-oxide. Eur. Heart J. 2014, 35, 904-910.
Kris-Etherton, P. M., Harris, W. S., Appel, L. J., Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 2002, 106, 2747-2757.
Roberts, L. D., Koulman, A., Griffin, J. L., Towards metabolic biomarkers of insulin resistance and type 2 diabetes: progress from the metabolome. Lancet Diabetes Endocrinol. 2014, 2, 65-75.
Parra, D., Bandarra, N. M., Kiely, M., Thorsdottir, I. et al., Impact of fish intake on oxidative stress when included into a moderate energy-restricted program to treat obesity. Eur. J. Nutr. 2007, 46, 460-467.
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Bondia-Pons, I., Barri, T., Hanhineva, K., Juntunen, K. et al., UPLC-QTOF/MS metabolic profiling unveils urinary changes in humans after a whole grain rye versus refined wheat bread intervention. Mol. Nutr. Food Res. 2013, 57, 412-422.
Haverberg, L. N., Omstedt, P. T., Munro, H. N., Young, V. R., Nτ-Methylhistidine content of mixed proteins in various rat tissues. Biochim. Biophys. Acta 1975, 405, 67-71.
Ho, J. E., Larson, M. G., Vasan, R. S., Ghorbani, A. et al., Metabolite profiles during oral glucose challenge. Diabetes 2013, 62, 2689-2698.
Tomasi, G., Savorani, F., Engelsen, S. B., icoshift: an effective tool for the alignment of chromatographic data. J. Chromatogr. A 2011, 1218, 7832-7840.
Suhre, K., Metabolic profiling in diabetes. J. Endocrinol. 2014, 221, R75-R85.
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Cantó, C., Menzies, K. J., Auwerx, J., NAD+ metabolism and the control of energy homeostasis: a balancing act between mitochondria and the nucleus. Cell Metab. 2015, 22, 31-53.
Smith, J. L., Wishnok, J. S., Deen, W. M., Metabolism and excretion of methylamines in rats. Toxicol. Appl. Pharm. 1994, 125, 296-308.
Tang, W. H. W., Hazen, S. L., The contributory role of gut microbiota in cardiovascular disease. J. Clin. Invest. 2014, 124, 4204-4211.
Petersen, K. F., Dufour, S., Savage, D. B., Bilz, S. et al., The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc. Natl. Acad. Sci. USA 2007, 104, 12587-12594.
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Turner, N., Kowalski, G. M., Leslie, S. J., Risis, S. et al., Distinct patterns of tissue-specific lipid accumulation during the induction of insulin resistance in mice by high-fat feeding. Diabetologia 2013, 56, 1638-1648.
Rylander, C., Sandanger, T. M., Engeset, D., Lund, E., Consumption of lean fish reduces the risk of type 2 diabetes mellitus: a prospective population based cohort study of Norwegian Women. PLoS One 2014, 9, e89845.
Garcia-Rodriguez, C. E., Mesa, M. D., Olza, J., Vlachava, M. et al., Does consumption of two portions of salmon per week enhance the antioxidant defense system in pregnant women? Antioxid. Redox. Sign. 2012, 16, 1401-1406.
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Braidy, N., Guillemin, G. J., Mansour, H., Chan-Ling, T. et al., Age related changes in NAD+ metabolism oxidative stress and Sirt1 activity in wistar rats. PLoS One 2011, 6, e19194.
Cross, A. J., Major, J. M., Sinha, R., Urinary biomarkers of meat consumption. Cancer Epidemiol. Biomarkers Prev. 2011, 20, 1107-1111.
Zheng, H., Clausen, M. R., Dalsgaard, T. K., Mortensen, G. et al., Time-saving design of experiment protocol for optimization of LC-MS data processing in metabolomic approaches. Anal. Chem. 2013, 85, 7109-7116.
Shibata, K., Toda, S., Effects of sex hormones on the metabolism of tryptophan to niacin and to serotonin in male rats. Biosci. Biotechnol. Biochem. 1997, 61, 1200-1202.
Bernstein, A. M., Sun, Q., Hu, F. B., Stampfer, M. J. et al., Major dietary protein sources and risk of coronary heart disease in women. Circulation 2010, 122, 876-883.
Zhang, J., Wang, C., Li, L., Man, Q. et al., Dietary inclusion of salmon, herring and pompano as oily fish reduces CVD risk markers in dyslipidaemic middle-aged and elderly Chinese women. Brit. J. Nutr. 2012, 108, 1455-1465.
Vikoren, L. A., Nygard, O. K., Lied, E., Rostrup, E. et al., A randomised study on the effects of fish protein supplement on glucose tolerance, lipids and body composition in overweight adults. Brit. J. Nutr. 2013, 109, 648-657.
Rogatzki, M. J., Ferguson, B. S., Goodwin, M. L., Gladden, L. B., Lactate is always the end product of glycolysis. Front. Neurosci. 2015, 9, 22.
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Snippet Scope Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is...
Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is sparse....
Scope Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is...
SCOPE: Proteins constitute an important part of the human diet, but understanding of the effects of different dietary protein sources on human metabolism is...
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StartPage 1661
SubjectTerms Adolescent
Adult
Aged
Biomarkers
Biomarkers - urine
Carnitine - urine
Cross-Over Studies
Diet
Dietary protein
Dietary Proteins - administration & dosage
Energy Metabolism
excretion
Female
Glycine - analogs & derivatives
Glycine - urine
Healthy Volunteers
Humans
Lipid Metabolism
lipids
Male
Metabolism
metabolites
Metabolomics
Methylamines - urine
Methylhistidines - urine
Middle Aged
mitochondria
Mitochondria - metabolism
nuclear magnetic resonance spectroscopy
protein sources
proteins
Pyridones - urine
randomized clinical trials
Seafood
Urine
Young Adult
Title Lean-seafood intake decreases urinary markers of mitochondrial lipid and energy metabolism in healthy subjects: Metabolomics results from a randomized crossover intervention study
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