Urinary loss of tricarboxylic acid cycle intermediates as revealed by metabolomics studies: An underlying mechanism to reduce lipid accretion by whey protein ingestion?

Journal of Proteome Research

Volumn 13, Issue 5, 2014, Pages 2560-2570

  Lillefosse, Haldis H ^a,b   Clausen, Morten R ^c   Yde, Christian C ^c   Ditlev, Ditte B ^c   Zhang, Xumin ^c   Du, Zhen Yu ^b,d   Bertram, Hanne C ^c   Madsen, Lise ^a,b   Kristiansen, Karsten ^a   Liaset, Bjørn ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c AARHUS UNIVERSITY   (Denmark)

^d EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

adipose tissue; casein; citric acid cycle; glutaminolysis; Krebs cycle; lipogenesis; metabolomics; obesity; tricarboxylic acid cycle; whey

Indexed keywords

ACONITIC ACID; CASEIN; CITRIC ACID; FAT; FUMARIC ACID; ISOCITRIC ACID; LIPID; MALIC ACID; NITROGEN; SUCCINIC ACID; TRICARBOXYLIC ACID; CARBOXYLIC ACID; MILK PROTEIN; WHEY PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CITRIC ACID CYCLE; CONTROLLED STUDY; DIGESTION; EXPLORATORY RESEARCH; LIPID DIET; LIPID LIVER LEVEL; LIPOGENESIS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLOMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTAKE; PROTON NUCLEAR MAGNETIC RESONANCE; URINARY EXCRETION; WHEY; WHITE ADIPOSE TISSUE; ADIPOSE TISSUE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; LIPID METABOLISM; MALE; METABOLISM; METABOLOME; PROCEDURES; URINE;

ACONITIC ACID; ADIPOSE TISSUE; ANIMALS; CARBOXYLIC ACIDS; CASEINS; CHROMATOGRAPHY, LIQUID; CITRIC ACID; CITRIC ACID CYCLE; DIET, HIGH-FAT; ISOCITRATES; LIPID METABOLISM; MALE; MASS SPECTROMETRY; METABOLOME; METABOLOMICS; MICE, INBRED C57BL; MILK PROTEINS; PROTON MAGNETIC RESONANCE SPECTROSCOPY; SUCCINIC ACID; WHEY PROTEINS;

EID: 84899884472     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500039t     Document Type: Article

References (56)

1. Finucane, M. M.; Stevens, G. A.; Cowan, M. J.; Danaei, G.; Lin, J. K.; Paciorek, C. J.; Singh, G. M.; Gutierrez, H. R.; Lu, Y.; Bahalim, A. N.; Farzadfar, F.; Riley, L. M.; Ezzati, M. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9·1 million participants Lancet 2011, 377 (9765) 557-567
2. Mirmiran, P.; Esmaillzadeh, A.; Azizi, F. Dairy consumption and body mass index: an inverse relationship Int. J. Obes. 2005, 29 (1) 115-121
3. Marques-Vidal, P.; Goncalves, A.; Dias, C. M. Milk intake is inversely related to obesity in men and in young women: data from the Portuguese Health Interview Survey 1998-1999 Int. J. Obes. 2006, 30 (1) 88-93
4. Abargouei, A. S.; Janghorbani, M.; Salehi-Marzijarani, M.; Esmaillzadeh, A. Effect of dairy consumption on weight and body composition in adults: a systematic review and meta-analysis of randomized controlled clinical trials Int. J. Obes. 2012, 36 (12) 1485-1493
5. Chen, M.; Pan, A.; Malik, V. S.; Hu, F. B. Effects of dairy intake on body weight and fat: a meta-analysis of randomized controlled trials Am. J. Clin. Nutr. 2012, 96 (4) 735-747
6. Dougkas, A.; Reynolds, C. K.; Givens, I. D.; Elwood, P. C.; Minihane, A. M. Associations between dairy consumption and body weight: a review of the evidence and underlying mechanisms Nutr. Res. Rev. 2011, 24 (1) 72-95
7. Takahira, M.; Noda, K.; Fukushima, M.; Zhang, B.; Mitsutake, R.; Uehara, Y.; Ogawa, M.; Kakuma, T.; Saku, K. Randomized, Double-Blind, Controlled, Comparative Trial of Formula Food Containing Soy Protein vs. Milk Protein in Visceral Fat Obesity-FLAVO Study Circ. J. 2011, 75 (9) 2235-2243
8. Acheson, K. J.; Blondel-Lubrano, A.; Oguey-Araymon, S.; Beaumont, M.; Emady-Azar, S.; Ammon-Zufferey, C.; Monnard, I.; Pinaud, S.; Nielsen-Moennoz, C.; Bovetto, L. Protein choices targeting thermogenesis and metabolism Am. J. Clin. Nutr. 2011, 93 (3) 525-534
9. Baer, D. J.; Stote, K. S.; Paul, D. R.; Harris, G. K.; Rumpler, W. V.; Clevidence, B. A. Whey Protein but Not Soy Protein Supplementation Alters Body Weight and Composition in Free-Living Overweight and Obese Adults J. Nutr. 2011, 141 (8) 1489-1494
10. Shi, J.; Tauriainen, E.; Martonen, E.; Finckenberg, P.; Ahlroos-Lehmus, A.; Tuomainen, A.; Pilvi, T. K.; Korpela, R.; Mervaala, E. M. Whey protein isolate protects against diet-induced obesity and fatty liver formation Int. Dairy J. 2011, 21 (8) 513-522
11. McAllan, L.; Keane, D.; Schellekens, H.; Roche, H. M.; Korpela, R.; Cryan, J. F.; Nilaweera, K. N. Whey protein isolate counteracts the effects of a high-fat diet on energy intake and hypothalamic and adipose tissue expression of energy balance-related genes Br. J. Nutr. 2013, 110, 2114-2126
12. Tranberg, B.; Hellgren, L. I.; Lykkesfeldt, J.; Sejrsen, K.; Jeamet, A.; Rune, I.; Ellekilde, M.; Nielsen, D. S.; Hansen, A. K. Whey Protein Reduces Early Life Weight Gain in Mice Fed a High-Fat Diet PLoS One 2013, 8 (8) e71439
13. Tastesen, H. S.; Keenan, A. H.; Madsen, L.; Kristiansen, K.; Liaset, B. Scallop protein with endogenous high taurine and glycine content prevents high-fat, high-sucrose-induced obesity and improves plasma lipid profile in male C57BL/6J mice Amino Acids 2014, 1-13 10.1007/s00726-014-1715-1
14. Lillefosse, H. H.; Tastesen, H. S.; Du, Z.-Y.; Ditlev, D. B.; Thorsen, F. A.; Madsen, L.; Kristiansen, K.; Liaset, B. Hydrolyzed Casein Reduces Diet-Induced Obesity in Male C57BL/6J Mice J. Nutr. 2013, 143 (9) 1367-1375
15. Liaset, B.; Julshamn, K.; Espe, M. Chemical composition and theoretical nutritional evaluation of the produced fractions from enzymic hydrolysis of salmon frames with Protamex (TM) Proc. Biochem. 2003, 38 (12) 1747-1759
16. Bas, S.; Giacobino, J. P. Peroxisomal and Mitochondrial Palmitoyl Coenzyme-a Beta-Oxidation Activities in Rat White Adipose-Tissue and Their Regulation in Hypothyroidism Arch. Biochem. Biophys. 1983, 222 (2) 416-423
17. Du, Z. Y.; Araujo, P.; Stubhaug, I.; Froyland, L. Unbound DHA causes a high blank value in beta-oxidation assay: a concern for in vitro studies Eur. J. Lipid Sci. Technol. 2010, 112 (3) 333-342
18. Wishart, D. S.; Tzur, D.; Knox, C.; Eisner, R.; Guo, A. C.; Young, N.; Cheng, D.; Jewell, K.; Arndt, D.; Sawhney, S.; Fung, C.; Nikolai, L.; Lewis, M.; Coutouly, M. A.; Forsythe, I.; Tang, P.; Shrivastava, S.; Jeroncic, K.; Stothard, P.; Amegbey, G.; Block, D.; Hau, D. D.; Wagner, J.; Miniaci, J.; Clements, M.; Gebremedhin, M.; Guo, N.; Zhang, Y.; Duggan, G. E.; MacInnis, G. D.; Weljie, A. M.; Dowlatabadi, R.; Bamforth, F.; Clive, D.; Greiner, R.; Li, L.; Marrie, T.; Sykes, B. D.; Vogel, H. J.; Querengesser, L. HMDB: the human metabolome database Nucleic Acids Res. 2007, 35, D521-D526
19. Savorani, F.; Tomasi, G.; Engelsen, S. B. icoshift: A versatile tool for the rapid alignment of 1D NMR spectra J. Magn. Reson. 2010, 202 (2) 190-202
20. Zhang, X. M.; Clausen, M. R.; Zhao, X. L.; Zheng, H.; Bertram, H. C. Enhancing the Power of Liquid Chromatography-Mass Spectrometry-Based Urine Metabolomics in Negative Ion Mode by Optimization of the Additive Anal. Chem. 2012, 84 (18) 7785-7792
21. Pluskal, T.; Castillo, S.; Villar-Briones, A.; Oresic, M. MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data BMC Bioinf. 2010, 11, 395
22. Smith, C. A.; O'Maille, G.; Want, E. J.; Qin, C.; Trauger, S. A.; Brandon, T. R.; Custodio, D. E.; Abagyan, R.; Siuzdak, G. METLIN-A metabolite mass spectral database Ther. Drug Monit. 2005, 27 (6) 747-751
23. Xia, J. G.; Psychogios, N.; Young, N.; Wishart, D. S. MetaboAnalyst: a web server for metabolomic data analysis and interpretation Nucleic Acids Res. 2009, 37, W652-W660
24. Considine, R. V.; Sinha, M. K.; Heiman, M. L.; Kriauciunas, A.; Stephens, T. W.; Nyce, M. R.; Ohannesian, J. P.; Marco, C. C.; McKee, L. J.; Bauer, T. L.; Caro, J. F. Serum immunoreactive leptin concentrations in normal-weight and obese humans New Engl. J. Med. 1996, 334 (5) 292-295
25. Maffei, M.; Halaas, J.; Ravussin, E.; Pratley, R. E.; Lee, G. H.; Zhang, Y.; Fei, H.; Kim, S.; Lallone, R.; Ranganathan, S.; Kern, P. A.; Friedman, J. M. Leptin Levels in Human and Rodent-Measurement of Plasma Leptin and Ob Rna in Obese and Weight-Reduced Subjects Nat. Med. 1995, 1 (11) 1155-1161
26. Madsen, L.; Pedersen, L. M.; Liaset, B.; Ma, T.; Petersen, R. K.; van den Berg, S.; Pan, J.; Muller-Decker, K.; Dulsner, E. D.; Kleemann, R.; Kooistra, T.; Doskeland, S. O.; Kristiansen, K. cAMP-dependent signaling regulates the adipogenic effect of n-6 polyunsaturated fatty acids J. Biol. Chem. 2008, 283 (11) 7196-7205
27. Ma, T.; Liaset, B.; Hao, Q.; Petersen, R. K.; Fjære, E.; Ngo, H. T.; Lillefosse, H. H.; Ringholm, S.; Sonne, S. B.; Treebak, J. T.; Pilegaard, H.; Frøyland, L.; Kristiansen, K.; Madsen, L. Sucrose Counteracts the Anti-Inflammatory Effect of Fish Oil in Adipose Tissue and Increases Obesity Development in Mice PLoS One 2011, 6 (6) e21647
28. Hao, Q.; Lillefosse, H. H.; Fjaere, E.; Myrmel, L. S.; Midtbo, L. K.; Jarlsby, R. H.; Ma, T.; Jia, B. B.; Petersen, R. K.; Sonne, S. B.; Chwalibog, A.; Froyland, L.; Liaset, B.; Kristiansen, K.; Madsen, L. High-glycemic index carbohydrates abrogate the antiobesity effect of fish oil in mice Am. J. Physiol.: Endocrinol. Metab. 2012, 302 (9) E1097-E1112
29. Liaset, B.; Madsen, L.; Hao, Q.; Criales, G.; Mellgren, G.; Marschall, H.-U.; Hallenborg, P.; Espe, M.; Frøyland, L.; Kristiansen, K. Fish protein hydrolysate elevates plasma bile acids and reduces visceral adipose tissue mass in rats Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2009, 1791 (4) 254-262
30. Liaset, B.; Hao, Q.; Jørgensen, H.; Hallenborg, P.; Du, Z.-Y.; Ma, T.; Marschall, H.-U.; Kruhöffer, M.; Li, R.; Li, Q.; Yde, C. C.; Criales, G.; Bertram, H. C.; Mellgren, G.; Øfjord, E. S.; Lock, E.-J.; Espe, M.; Frøyland, L.; Madsen, L.; Kristiansen, K. Nutritional Regulation of Bile Acid Metabolism Is Associated with Improved Pathological Characteristics of the Metabolic Syndrome J. Biol. Chem. 2011, 286 (32) 28382-28395
31. Fabbrini, E.; Magkos, F.; Mohammed, B. S.; Pietka, T.; Abumrad, N. A.; Patterson, B. W.; Okunade, A.; Klein, S. Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity Proc. Natl. Acad. Sci. 2009, 106 (36) 15430-15435
32. Takamura, T.; Misu, H.; Matsuzawa-Nagata, N.; Sakurai, M.; Ota, T.; Shimizu, A.; Kurita, S.; Takeshita, Y.; Ando, H.; Honda, M.; Kaneko, S. Obesity Upregulates Genes Involved in Oxidative Phosphorylation in Livers of Diabetic Patients Obesity 2008, 16 (12) 2601-2609
33. Deng, W.-J.; Nie, S.; Dai, J.; Wu, J.-R.; Zeng, R. Proteome, Phosphoproteome, and Hydroxyproteome of Liver Mitochondria in Diabetic Rats at Early Pathogenic Stages Mol. Cell. Proteomics 2010, 9 (1) 100-116
34. Guo, Y.; Darshi, M.; Ma, Y.; Perkins, G. A.; Shen, Z.; Haushalter, K. J.; Saito, R.; Chen, A.; Lee, Y. S.; Patel, H. H.; Briggs, S. P.; Ellisman, M. H.; Olefsky, J. M.; Taylor, S. S. Quantitative Proteomic and Functional Analysis of Liver Mitochondria from High Fat Diet Diabetic Mice Mol. Cell. Proteomics 2013, 10.1074/mcp.M113.027441
35. Fabbrini, E.; Sullivan, S.; Klein, S. Obesity and nonalcoholic fatty liver disease: Biochemical, metabolic, and clinical implications Hepatology 2010, 51 (2) 679-689
36. Bertram, H. C.; Knudsen, K. E. B.; Serena, A.; Malmendal, A.; Nielsen, N. C.; Frette, X. C.; Andersen, H. J. NMR-based metabonomic studies reveal changes in the biochemical profile of plasma and urine from pigs fed high-fibre rye bread Br. J. Nutr. 2006, 95 (5) 955-962
37. Bertram, H. C.; Hoppe, C.; Petersen, B. O.; Duus, J. O.; Molgaard, C.; Michaelsen, K. F. An NMR-based metabonomic investigation on effects of milk and meat protein diets given to 8-year-old boys Br. J. Nutr. 2007, 97 (4) 758-763
38. Legido-Quigley, C.; Stella, C.; Perez-Jimenez, F.; Lopez-Miranda, J.; Ordovas, J.; Powell, J.; Van-Der-Ouderaa, F.; Ware, L.; Lindon, J. C.; Nicholson, J. K.; Holmes, E. Liquid chromatography-mass spectrometry methods for urinary biomarker detection in metabonomic studies with application to nutritional studies Biomed. Chromatogr. 2010, 24 (7) 737-743
39. Jung, J. Y.; Kim, I. Y.; Kim, Y. N.; Kim, J. S.; Shin, J. H.; Jang, Z. H.; Lee, H. S.; Hwang, G. S.; Seong, J. K. H-1 NMR-based metabolite profiling of diet-induced obesity in a mouse mode BMB Rep. 2012, 45 (7) 419-424
40. Martin, D. B.; Vagelos, P. R. The Mechanism of Tricarboxylic Acid Cycle Regulation of Fatty Acid Synthesis J. Biol. Chem. 1962, 237 (6) 1787-1792
41. Watson, J. A.; Lowenstein, J. M. Citrate and the Conversion of Carbohydrate into Fat: Fatty Acid Synthesis by a Combination of Cytoplasm and Mitochondria J. Biol. Chem. 1970, 245 (22) 5993-6002
42. Wakil, S. J.; Stoops, J. K.; Joshi, V. C. Fatty Acid Synthesis and its Regulation Annu. Rev. Biochem. 1983, 52 (1) 537-579
43. Warburg, O. Origin of Cancer Cells Science 1956, 123 (3191) 309-314
44. Lunt, S. Y.; Vander Heiden, M. G. Aerobic Glycolysis: Meeting the Metabolic Requirements of Cell Proliferation Annu. Rev. Cell Dev. Biol. 2011, 27 (1) 441-464
45. DeBerardinis, R. J.; Mancuso, A.; Daikhin, E.; Nissim, I.; Yudkoff, M.; Wehrli, S.; Thompson, C. B. Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (49) 19345-19350
46. Durán, R. V.; Oppliger, W.; Robitaille, A. M.; Heiserich, L.; Skendaj, R.; Gottlieb, E.; Hall, M. N. Glutaminolysis Activates Rag-mTORC1 Signaling Mol. Cell 2012, 47 (3) 349-358
47. An, Y.; Xu, W.; Li, H.; Lei, H.; Zhang, L.; Hao, F.; Duan, Y.; Yan, X.; Zhao, Y.; Wu, J.; Wang, Y.; Tang, H. High-Fat Diet Induces Dynamic Metabolic Alterations in Multiple Biological Matrices of Rats J. Proteome Res. 2013, 12 (8) 3755-3768
48. Simpson, D. P. Citrate excretion: a window on renal metabolism Am. J. Physiol.: Renal Physiol 1983, 244 (3) F223-F234
49. HMBD Showing Metabocard for Citramalic acid (HMDB00426). http://www.hmdb.ca/metabolites/HMDB00426.
50. Sunny, N. E.; Parks, E. J.; Browning, J. D.; Burgess, S. C. Excessive Hepatic Mitochondrial TCA Cycle and Gluconeogenesis in Humans with Nonalcoholic Fatty Liver Disease Cell Metab. 2011, 14 (6) 804-810
51. Burgess, S. C.; Leone, T. C.; Wende, A. R.; Croce, M. A.; Chen, Z. J.; Sherry, A. D.; Malloy, C. R.; Finck, B. N. Diminished hepatic gluconeogenesis via defects in tricarboxylic acid cycle flux in peroxisome proliferator- activated receptor gamma coactivator-1 alpha (PGC-1 alpha)-deficient mice J. Biol. Chem. 2006, 281 (28) 19000-19008
52. Satapati, S.; Sunny, N. E.; Kucejova, B.; Fu, X.; He, T. T.; Méndez-Lucas, A.; Shelton, J. M.; Perales, J. C.; Browning, J. D.; Burgess, S. C. Elevated TCA cycle function in the pathology of diet-induced hepatic insulin resistance and fatty liver J. Lipid Res. 2012, 53 (6) 1080-1092
53. Herman, M. A.; Peroni, O. D.; Villoria, J.; Schon, M. R.; Abumrad, N. A.; Bluher, M.; Klein, S.; Kahn, B. B. A novel ChREBP isoform in adipose tissue regulates systemic glucose metabolism Nature 2012, 484 (7394) 333-338
54. Owen, O. E.; Kalhan, S. C.; Hanson, R. W. The Key Role of Anaplerosis and Cataplerosis for Citric Acid Cycle Function J. Biol. Chem. 2002, 277 (34) 30409-30412
55. Singal, S. A.; Hazan, S. J.; Sydenstricker, V. P.; Littlejohn, J. M. The Production of Fatty Livers in Rats on Threonine-Deficient and Lysine-Deficient Diets J. Biol. Chem. 1953, 200 (2) 867-874
56. Noguchi, Y.; Nishikata, N.; Shikata, N.; Kimura, Y.; Aleman, J. O.; Young, J. D.; Koyama, N.; Kelleher, J. K.; Takahashi, M.; Stephanopoulos, G. Ketogenic Essential Amino Acids Modulate Lipid Synthetic Pathways and Prevent Hepatic Steatosis in Mice PLoS One 2010, 5 (8) e12057