An iTRAQ proteomic study reveals an association between diet-induced enhanced fatty acid metabolism and the development of glucose intolerance in prediabetic mice

Journal of Proteome Research

Volumn 12, Issue 3, 2013, Pages 1120-1133

  Ho, Jennifer H ^a,b   Lee, Oscar K ^c   Fu, Yun Ju ^b   Shih, Hung Ta ^d   Tseng, Chien Yu ^c   Chung, Cheng Chih ^b   Han, Chia Li ^e   Chen, Yu Ju ^e  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^e INSTITUTE OF CHEMISTRY   (Taiwan)

Author keywords

fatty acid metabolism; glucose intolerance; high fat diet; insulin resistance; iTRAQ

Indexed keywords

CARNITINE PALMITOYLTRANSFERASE I; FAT DROPLET; GLUCOSE TRANSPORTER 2; GLUCOSE TRANSPORTER 4; INSULIN RECEPTOR SUBSTRATE 1; LONG CHAIN FATTY ACID; MEMBRANE PROTEIN; TYROSINE;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; FATTY ACID METABOLISM; FATTY ACID TRANSPORT; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOGEN STORAGE DISEASE; IMPAIRED GLUCOSE TOLERANCE; IN VIVO STUDY; INSULIN RESISTANCE; LIPID DIET; LIPID STORAGE; LIVER; LIVER CELL; MALE; MITOCHONDRION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ASSAY; SKELETAL MUSCLE; UPREGULATION;

EID: 84874636831     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300662j     Document Type: Article

References (58)

1. Lewis, G. F.; Carpentier, A.; Adeli, K.; Giacca, A. Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes Endocr. Rev. 2002, 23, 201-229
2. WHO Expert Committee on Diabetes Mellitus: Second report W. H. O. Tech. Rep. Ser. 1980, 646, 1-80
3. Gavin, J. R.; Alberti, K. G. M. M.; Davidson, M. B.; DeFronzo, R. A.; Drash, A.; Gabbe, S. G.; Genuth, S.; Harris, M. I.; Kahn, R.; Keen, H.; Knowler, W. C.; Lebovitz, H.; Maclaren, N. K.; Palmer, J. P.; Raskin, P.; Rizza, R. A.; Stern, M. P. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus Diabetes Care 1997, 20, 1183-1197
4. Kannel, W. B.; McGee, D. L. Diabetes and cardiovascular disease. The Framingham study JAMA 1979, 241, 2035-2038
5. Kuller, L. H.; Velentgas, P.; Barzilay, J.; Beauchamp, N. J.; O'Leary, D. H.; Savage, P. J. Diabetes mellitus: Subclinical cardiovascular disease and risk of incident cardiovascular disease and all-cause mortality Arterioscler. Thromb. Vasc. Biol. 2000, 20, 823-829
6. DECODE Study Group, the European Diabetes Epidemiology Group. Glucose tolerance and cardiovascular mortality: Comparison of fasting and 2-h diagnostic criteria. Arch. Intern. Med. 2001, 161, 397-405.
7. Harris, M. I.; Flegal, K. M.; Cowie, C. C.; Eberhardt, M. S.; Goldstein, D. E.; Little, R. R.; Wiedmeyer, H. M.; Byrd-Holt, D. D. Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in U.S. adults. The Third National Health and Nutrition Examination Survey, 1988-1994 Diabetes Care 1998, 21, 518-524
8. Gabir, M. M.; Hanson, R. L.; Dabelea, D.; Imperatore, G.; Roumain, J.; Bennett, P. H.; Knowler, W. C. Plasma glucose and prediction of microvascular disease and mortality: Evaluation of 1997 American Diabetes Association and 1999 World Health Organization criteria for diagnosis of diabetes Diabetes Care 2000, 23, 1113-1118
9. Boden, G. Fatty acid-induced inflammation and insulin resistance in skeletal muscle and liver Curr. Diabetes Rep. 2006, 6, 177-181
10. Hotamisligil, G. S.; Shargill, N. S.; Spiegelman, B. M. Adipose expression of tumor necrosis factor-alpha: Direct role in obesity-linked insulin resistance Science 1993, 259, 87-91
11. Izawa, Y.; Yoshizumi, M.; Fujita, Y.; Ali, N.; Kanematsu, Y.; Ishizawa, K.; Tsuchiya, K.; Obata, T.; Ebina, Y.; Tomita, S.; Tamaki, T. ERK1/2 activation by angiotensin II inhibits insulin-induced glucose uptake in vascular smooth muscle cells Exp. Cell Res. 2005, 308, 291-299
12. Ueno, M.; Carvalheira, J. B.; Tambascia, R. C.; Bezerra, R. M.; Amaral, M. E.; Carneiro, E. M.; Folli, F.; Franchini, K. G.; Saad, M. J. Regulation of insulin signalling by hyperinsulinaemia: Role of IRS-1/2 serine phosphorylation and the mTOR/p70 S6K pathway Diabetologia 2005, 48, 506-518
13. Lichtenstein, A. H.; Schwab, U. S. Relationship of dietary fat to glucose metabolism Atherosclerosis 2000, 150, 227-243
14. Lopez, S.; Bermudez, B.; Ortega, A.; Varela, L. M.; Pacheco, Y. M.; Villar, J.; Abia, R.; Muriana, F. J. Effects of meals rich in either monounsaturated or saturated fat on lipid concentrations and on insulin secretion and action in subjects with high fasting triglyceride concentrations Am. J. Clin. Nutr. 2011, 93, 494-499
15. Frayn, K. N. Fat as a fuel: Emerging understanding of the adipose tissue-skeletal muscle axis Acta Physiol. 2010, 199, 509-518
16. Yamauchi, T.; Tobe, K.; Tamemoto, H.; Ueki, K.; Kaburagi, Y.; Yamamoto-Honda, R.; Takahashi, Y.; Yoshizawa, F.; Aizawa, S.; Akanuma, Y.; Sonenberg, N.; Yazaki, Y.; Kadowaki, T. Insulin signalling and insulin actions in the muscles and livers of insulin-resistant, insulin receptor substrate 1-deficient mice Mol. Cell. Biol. 1996, 16, 3074-3084
17. Draznin, B. Molecular mechanisms of insulin resistance: Serine phosphorylation of insulin receptor substrate-1 and increased expression of p85alpha: The two sides of a coin Diabetes 2006, 55, 2392-2397
18. Hotamisligil, G. S.; Peraldi, P.; Budavari, A.; Ellis, R.; White, M. F.; Spiegelman, B. M. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance Science 1996, 271, 665-668
19. Moors, C. C.; van der Zijl, N. J.; Diamant, M.; Blaak, E. E.; Goossens, G. H. Impaired insulin sensitivity is accompanied by disturbances in skeletal muscle fatty acid handling in subjects with impaired glucose metabolism Int. J. Obes. 2012, 36, 709-717
20. Greenberg, A. S.; Coleman, R. A.; Kraemer, F. B.; McManaman, J. L.; Obin, M. S.; Puri, V.; Yan, Q. W.; Miyoshi, H.; Mashek, D. G. The role of lipid droplets in metabolic disease in rodents and humans J. Clin. Invest. 2011, 121, 2102-2110
21. Sinha, R.; Dufour, S.; Petersen, K. F.; LeBon, V.; Enoksson, S.; Ma, Y. Z.; Savoye, M.; Rothman, D. L.; Shulman, G. I.; Caprio, S. Assessment of skeletal muscle triglyceride content by (1)H nuclear magnetic resonance spectroscopy in lean and obese adolescents: Relationships to insulin sensitivity, total body fat, and central adiposity Diabetes 2002, 51, 1022-1027
22. Schmid, G. M.; Converset, V.; Walter, N.; Sennitt, M. V.; Leung, K. Y.; Byers, H.; Ward, M.; Hochstrasser, D. F.; Cawthorne, M. A.; Sanchez, J. C. Effect of high-fat diet on the expression of proteins in muscle, adipose tissues, and liver of C57BL/6 mice Proteomics 2004, 4, 2270-2282
23. 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, 100-116
24. Lu, H.; Yang, Y.; Allister, E. M.; Wijesekara, N.; Wheeler, M. B. The identification of potential factors associated with the development of type 2 diabetes: A quantitative proteomics approach Mol. Cell. Proteomics 2008, 7, 1434-1451
25. Adachi, J.; Kumar, C.; Zhang, Y.; Mann, M. In-depth analysis of the adipocyte proteome by mass spectrometry and bioinformatics Mol. Cell. Proteomics 2007, 6, 1257-1273
26. Katz, A.; Nambi, S. S.; Mather, K.; Baron, A. D.; Follmann, D. A.; Sullivan, G.; Quon, M. J. Quantitative insulin sensitivity check index: A simple, accurate method for assessing insulin sensitivity in humans J. Clin. Endocrinol. Metab. 2000, 85, 2402-2410
27. Kersey, P. J.; Duarte, J.; Williams, A.; Karavidopoulou, Y.; Birney, E.; Apweiler, R. The International Protein Index: An integrated database for proteomics experiments Proteomics 2004, 4, 1985-1988
28. Lin, W. T.; Hung, W. N.; Yian, Y. H.; Wu, K. P.; Han, C. L.; Chen, Y. R.; Chen, Y. J.; Sung, T. Y.; Hsu, W. L. Multi-Q: A fully automated tool for multiplexed protein quantitation J. Proteome Res. 2006, 5, 2328-2338
29. Han, C. L.; Chien, C. W.; Chen, W. C.; Chen, Y. R.; Wu, C. P.; Li, H.; Chen, Y. J. A multiplexed quantitative strategy for membrane proteomics: Opportunities for mining therapeutic targets for autosomal dominant polycystic kidney disease Mol. Cell. Proteomics 2008, 7, 1983-1997
30. Bonnefont, J. P.; Djouadi, F.; Prip-Buus, C.; Gobin, S.; Munnich, A.; Bastin, J. Carnitine palmitoyltransferases 1 and 2: Biochemical, molecular and medical aspects Mol. Aspects Med. 2004, 25, 495-520
31. Elbein, S. C.; Hoffman, M. D.; Matsutani, A.; Permutt, M. A. Linkage analysis of GLUT1 (HepG2) and GLUT2 (liver/islet) genes in familial NIDDM Diabetes 1992, 41, 1660-1667
32. James, D. E.; Brown, R.; Navarro, J.; Pilch, P. F. Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein Nature 1988, 333, 183-185
33. Michel, P. E.; Reymond, F.; Arnaud, I. L.; Josserand, J.; Girault, H. H.; Rossier, J. S. Protein fractionation in a multicompartment device using Off-Gel isoelectric focusing Electrophoresis 2003, 24, 3-11
34. Heller, M.; Michel, P. E.; Morier, P.; Crettaz, D.; Wenz, C.; Tissot, J. D.; Reymond, F.; Rossier, J. S. Two-stage Off-Gel isoelectric focusing: Protein followed by peptide fractionation and application to proteome analysis of human plasma Electrophoresis 2005, 26, 1174-1188
35. Horth, P.; Miller, C. A.; Preckel, T.; Wenz, C. Efficient fractionation and improved protein identification by peptide OFFGEL electrophoresis Mol. Cell. Proteomics 2006, 5, 1968-1974
36. Cargile, B. J.; Bundy, J. L.; Freeman, T. W.; Stephenson, J. L., Jr. Gel based isoelectric focusing of peptides and the utility of isoelectric point in protein identification J. Proteome Res. 2004, 3, 112-119
37. Elschenbroich, S.; Ignatchenko, V.; Sharma, P.; Schmitt-Ulms, G.; Gramolini, A. O.; Kislinger, T. Peptide separations by on-line MudPIT compared to isoelectric focusing in an off-gel format: Application to a membrane-enriched fraction from C2C12 mouse skeletal muscle cells J. Proteome Res. 2009, 8, 4860-4869
38. Kuhn, J. F.; Hoerth, P.; Hoehn, S. T.; Preckel, T.; Tomer, K. B. Proteomics study of anthrax lethal toxin-treated murine macrophages Electrophoresis 2006, 27, 1584-1597
39. Waller, L. N.; Shores, K.; Knapp, D. R. Shotgun proteomic analysis of cerebrospinal fluid using off-gel electrophoresis as the first-dimension separation J. Proteome Res. 2008, 7, 4577-4584
40. Fraterman, S.; Zeiger, U.; Khurana, T. S.; Rubinstein, N. A.; Wilm, M. Combination of peptide OFFGEL fractionation and label-free quantitation facilitated proteomics profiling of extraocular muscle Proteomics 2007, 7, 3404-3416
41. McQuade, L. R.; Schmidt, U.; Pascovici, D.; Stojanov, T.; Baker, M. S. Improved membrane proteomics coverage of human embryonic stem cells by peptide IPG-IEF J. Proteome Res. 2009, 8, 5642-5649
42. Chick, J. M.; Haynes, P. A.; Bjellqvist, B.; Baker, M. S. A combination of immobilised pH gradients improves membrane proteomics J. Proteome Res. 2008, 7, 4974-4981
43. Chick, J. M.; Haynes, P. A.; Molloy, M. P.; Bjellqvist, B.; Baker, M. S.; Len, A. C. Characterization of the rat liver membrane proteome using peptide immobilized pH gradient isoelectric focusing J. Proteome Res. 2008, 7, 1036-1045
44. Lottenberg, A. M.; Afonso Mda, S.; Lavrador, M. S.; Machado, R. M.; Nakandakare, E. R. The role of dietary fatty acids in the pathology of metabolic syndrome J. Nutr. Biochem. 2012, 23, 1027-1040
45. Sondergaard, E.; Gormsen, L. C.; Nellemann, B.; Jensen, M. D.; Nielsen, S. Body composition determines direct FFA storage pattern in overweight women Am. J. Physiol. Endocr. Metab. 2012, 302, E1599-1604
46. Tuomilehto, J.; Lindstrom, J.; Eriksson, J. G.; Valle, T. T.; Hamalainen, H.; Ilanne-Parikka, P.; Keinanen-Kiukaanniemi, S.; Laakso, M.; Louheranta, A.; Rastas, M.; Salminen, V.; Uusitupa, M. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance N. Engl. J. Med. 2001, 344, 1343-1350
47. Marshall, J. A.; Hamman, R. F.; Baxter, J. High-fat, low-carbohydrate diet and the etiology of non-insulin-dependent diabetes mellitus: The San Luis Valley Diabetes Study Am. J. Epidemiol. 1991, 134, 590-603
48. Erkkila, A.; de Mello, V. D.; Riserus, U.; Laaksonen, D. E. Dietary fatty acids and cardiovascular disease: An epidemiological approach Prog. Lipid Res. 2008, 47, 172-187
49. Nguyen, M. T.; Satoh, H.; Favelyukis, S.; Babendure, J. L.; Imamura, T.; Sbodio, J. I.; Zalevsky, J.; Dahiyat, B. I.; Chi, N. W.; Olefsky, J. M. JNK and tumor necrosis factor-alpha mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes J. Biol. Chem. 2005, 280, 35361-35371
50. Montecucco, F.; Steffens, S.; Mach, F. Insulin resistance: A proinflammatory state mediated by lipid-induced signaling dysfunction and involved in atherosclerotic plaque instability Mediators Inflammation 2008, 2008, 767623
51. Solinas, G.; Naugler, W.; Galimi, F.; Lee, M. S.; Karin, M. Saturated fatty acids inhibit induction of insulin gene transcription by JNK-mediated phosphorylation of insulin-receptor substrates Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 16454-16459
52. Holzer, R. G.; Park, E. J.; Li, N.; Tran, H.; Chen, M.; Choi, C.; Solinas, G.; Karin, M. Saturated fatty acids induce c-Src clustering within membrane subdomains, leading to JNK activation Cell 2011, 147, 173-184
53. Schreurs, M.; Kuipers, F.; van der Leij, F. R. Regulatory enzymes of mitochondrial beta-oxidation as targets for treatment of the metabolic syndrome Obes. Rev. 2010, 11, 380-388
54. Ryu, M. H.; Cha, Y. S. The effects of a high-fat or high-sucrose diet on serum lipid profiles, hepatic acyl-CoA synthetase, carnitine palmitoyltransferase-I, and the acetyl-CoA carboxylase mRNA levels in rats J. Biochem. Mol. Biol. 2003, 36, 312-318
55. Karlic, H.; Lohninger, A.; Laschan, C.; Lapin, A.; Bohmer, F.; Huemer, M.; Guthann, E.; Rappold, E.; Pfeilstocker, M. Downregulation of carnitine acyltransferases and organic cation transporter OCTN2 in mononuclear cells in healthy elderly and patients with myelodysplastic syndromes J. Mol. Med. 2003, 81, 435-442
56. Joo, J. I.; Oh, T. S.; Kim, D. H.; Choi, D. K.; Wang, X.; Choi, J. W.; Yun, J. W. Differential expression of adipose tissue proteins between obesity-susceptible and -resistant rats fed a high-fat diet Proteomics 2011, 11, 1429-1448
57. Virtanen, K. A.; Lidell, M. E.; Orava, J.; Heglind, M.; Westergren, R.; Niemi, T.; Taittonen, M.; Laine, J.; Savisto, N. J.; Enerback, S.; Nuutila, P. Functional brown adipose tissue in healthy adults N. Engl. J. Med. 2009, 360, 1518-1525
58. Cypess, A. M.; Lehman, S.; Williams, G.; Tal, I.; Rodman, D.; Goldfine, A. B.; Kuo, F. C.; Palmer, E. L.; Tseng, Y. H.; Doria, A.; Kolodny, G. M.; Kahn, C. R. Identification and importance of brown adipose tissue in adult humans N. Engl. J. Med. 2009, 360, 1509-1517