Excessive caloric intake acutely causes oxidative stress, GLUT4 carbonylation, and insulin resistance in healthy men

Science Translational Medicine

Volumn 7, Issue 304, 2015, Pages

  Boden, Guenther ^a   Homko, Carol ^a   Barrero, Carlos A ^b   Stein, T Peter ^c   Chen, Xinhua ^c   Cheung, Peter ^a   Fecchio, Chiara ^b   Koller, Sarah ^a   Merali, Salim ^b  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF PHARMACY   (United States)

^c UMDNJ School of Osteopathic Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 4; GLUTATHIONE PEROXIDASE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 8; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; SLC2A4 PROTEIN, HUMAN;

ADIPOSE TISSUE; ADULT; ARTICLE; CALORIC INTAKE; CARBOHYDRATE INTAKE; ENDOPLASMIC RETICULUM STRESS; EXCESS CALORIC INTAKE; FAT INTAKE; FEMALE; GLUCOSE TRANSPORT; HUMAN; HUMAN EXPERIMENT; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID PEROXIDATION; MALE; NITROSYLATION; NORMAL HUMAN; OBESITY; OVERNUTRITION; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN FUNCTION; PROTEIN INTAKE; PROTEIN PROCESSING; RESTING ENERGY EXPENDITURE; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT GAIN; CLINICAL TRIAL; HEALTH; METABOLISM; MIDDLE AGED; MOLECULAR MODEL; OXIDATION REDUCTION REACTION; PATHOLOGY;

ADIPOSE TISSUE; ENERGY INTAKE; GLUCOSE TRANSPORTER TYPE 4; HEALTH; HUMANS; INSULIN RESISTANCE; MALE; MIDDLE AGED; MODELS, MOLECULAR; OVERNUTRITION; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; REACTIVE OXYGEN SPECIES;

EID: 84941248927     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aac4765     Document Type: Article

References (44)

1. G. M. Reaven, Role of insulin resistance in human disease. Diabetes 37, 1595-1607 (1988).
2. G. Boden, Obesity, insulin resistance and free fatty acids. Curr. Opin. Endocrinol. Diabetes Obes. 18, 139-143 (2011).
3. P. Dandona, A. Aljada, A. Bandyopadhyay, Inflammation: The link between insulin resistance, obesity and diabetes. Trends Immunol. 25, 4-7 (2004).
4. S. E. Shoelson, L. Herrero, A. Naaz, Obesity, inflammation, and insulin resistance. Gastroenterology 132, 2169-2180 (2007).
5. S. Schenk, M. Saberi, J. M. Olefsky, Insulin sensitivity: Modulation by nutrients and inflammation. J. Clin. Invest. 118, 2992-3002 (2008).
6. U. Ozcan, Q. Cao, E. Yilmaz, A. H. Lee, N. N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Görgün, L. H. Glimcher, G. S. Hotamisligil, Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461 (2004).
7. N. K. Sharma, S. K. Das, A. K. Mondal, O. G. Hackney, W. S. Chu, P. A. Kern, N. Rasouli, H. J. Spencer, A. Yao-Borengasser, S. C. Elbein, Endoplasmic reticulum stress markers are associated with obesity in nondiabetic subjects. J. Clin. Endocrinol. Metab. 93, 4532-4541 (2008).
8. G. Boden, X. Duan, C. Homko, E. J. Molina, W. Song, O. Perez, P. Cheung, S. Merali, Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 57, 2438-2444 (2008).
9. J. L. Evans, I. D. Goldfine, B. A. Maddux, G. M. Grodsky, Oxidative stress and stress-activated signaling pathways: A unifying hypothesis of type 2 diabetes. Endocr. Rev. 23, 599-622 (2002).
10. J. F. Keaney Jr., M. G. Larson, R. S. Vasan, P. W. Wilson, I. Lipinska, D. Corey, J. M. Massaro, P. Sutherland, J. A. Vita, E. J. Benjamin, Framingham Study, Obesity and systemic oxidative stress: Clinical correlates of oxidative stress in the Framingham Study. Arterioscler. Thromb. Vasc. Biol. 23, 434-439 (2003).
11. J. Styskal, H. Van Remmen, A. Richardson, A. B. Salmon, Oxidative stress and diabetes: What can we learn about insulin resistance from antioxidant mutant mouse models? Free Radic. Biol. Med. 52, 46-58 (2012).
12. P. Jiao, J. Ma, B. Feng, H. Zhang, J. Alan-Diehl, Y. Eugene-Chin, W. Yan, H. Xu, FFA-induced adipocyte inflammation and insulin resistance: Involvement of ER stress and IKKb pathways. Obesity 19, 483-491 (2011).
13. G. S. Hotamisligil, Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917 (2010).
14. L. J. Roberts II, G. L. Milne, Isoprostanes. J. Lipid Res. 50, S219-S223 (2009).
15. S. Furukawa, T. Fujita, M. Shimabukuro, M. Iwaki, Y. Yamada, Y. Nakajima, O. Nakayama, M. Makishima, M. Matsuda, I. Shimomura, Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114, 1752-1761 (2004).
16. D. Samocha-Bonet, L. V. Campbell, T. A. Mori, K. D. Croft, J. R. Greenfield, N. Turner, L. K. Heilbronn, Overfeeding reduces insulin sensitivity and increases oxidative stress, without altering markers of mitochondrial content and function in humans. PLOS One 7, e36320 (2012).
17. R. J. Schaur, Basic aspects of the biochemical reactivity of 4-hydroxynonenal. Mol. Aspects Med. 24, 149-159 (2003).
18. M. Kastle, T. Grune, Protein oxidative modification in the aging organism and the role of the ubiquitin proteasomal system. Curr. Pharm. Des. 17, 4007-4022 (2011).
19. D. L. Johannsen, Y. Tchoukalova, C. S. Tam, J. D. Covington, W. Xie, J.-M. Schwarz, S. Bajpeyi, E. Ravussin, Effect of 8 weeks of overfeeding on ectopic fat deposition and insulin sensitivity: Testing the "adipose tissue expandability" hypothesis. Diabetes Care 37, 2789-2797 (2014).
20. N. Houstis, E. D. Rosen, E. S. Lander, Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440, 944-948 (2006).
21. K. L. Hoehn, A. B. Salmon, C. Hohnen-Behrens, N. Turner, A. J. Hoy, G. J. Maghzal, R. Stocker, H. Van Remmen, E. W. Kraegen, G. J. Cooney, A. R. Richardson, D. E. James, Insulin resistance is a cellular antioxidant defense mechanism. Proc. Natl. Acad. Sci. U. S. A. 106, 17787-17792 (2009).
22. E. J. Anderson, M. E. Lustig, K. E. Boyle, T. L. Woodlief, D. A. Kane, C. T. Lin, J. W. Price III, L. Kang, P. S. Rabinovitch, H. H. Szeto, J. A. Houmard, R. N. Cortright, D. H. Wasserman, P. D. Neufer, Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J. Clin. Invest. 119, 573-581 (2009).
23. C.-W. Kim, B.-T. Kim, K.-H. Park, K.-M. Kim, D.-J. Lee, S.-W. Yang, N.-S. Joo, Effects of shortterm chromium supplementation on insulin sensitivity and body composition in overweight children: Randomized, double-blind, placebo-controlled study. J. Nutr. Biochem. 22, 1030-1034 (2011).
24. D. Nguyen, J. W. Hsu, F. Jahoor, R. V. Sekhar, Effect of increasing glutathione with cysteine and glycine supplementation on mitochondrial fuel oxidation, insulin sensitivity, and body composition in older HIV-infected patients. J. Clin. Endocrinol. Metab. 99, 169-177 (2014).
25. Y. Rhee, A. Brunt, Flaxseed supplementation improved insulin resistance in obese glucose intolerant people: A randomized crossover design. Nutr. J. 10, 44 (2011).
26. Z. Asemi, M. Samimi, Z. Tabassi, H. Shakeri, A. Esmaillzadeh, Vitamin D supplementation affects serum high-sensitivity C-reactive protein, insulin resistance, and biomarkers of oxidative stress in pregnant women. J. Nutr. 143, 1432-1438 (2013).
27. F. Fang, Z. Kang, C. Wong, Vitamin E tocotrienols improve insulin sensitivity through activating peroxisome proliferator-activated receptors. Mol. Nutr. Food Res. 54, 345-352 (2010).
28. X. Ge, Q. Yu, W. Qi, X. Shi, Q. Zhai, Chronic insulin treatment causes insulin resistance in 3T3-L1 adipocytes through oxidative stress. Free Radic. Res. 42, 582-591 (2008).
29. A. Bloch-Damti, N. Bashan, Proposed mechanisms for the induction of insulin resistance by oxidative stress. Antioxid. Redox Signal. 7, 1553-1567 (2005).
30. A. Rudich, A. Tirosh, R. Potashnik, R. Hemi, H. Kanety, N. Bashan, Prolonged oxidative stress impairs insulin-induced GLUT4 translocation in 3T3-L1 adipocytes. Diabetes 47, 1562-1569 (1998).
31. T. L. Archuleta, A. M. Lemieux, V. Saengsirisuwan, M. K. Teachey, K. A. Lindborg, J. S. Kim, E. J. Henriksen, Oxidant stress-induced loss of IRS-1 and IRS-2 proteins in rat skeletal muscle: Role of p38 MAPK. Free Radic. Biol. Med. 47, 1486-1493 (2009).
32. J. Hirosumi, G. Tuncman, L. Chang, C. Z. Görgün, K. T. Uysal, K. Maeda, M. Karin, G. S. Hotamisligil, A central role for JNK in obesity and insulin resistance. Nature 420, 333-336 (2002).
33. B. I. Frohnert, D. A. Bernlohr, Protein carbonylation, mitochondrial dysfunction, and insulin resistance. Adv. Nutr. 4, 157-163 (2013).
34. D. Demozay, J. C. Mas, S. Rocchi, E. Van Obberghen, FALDH reverses the deleterious action of oxidative stress induced by lipid peroxidation product 4-hydroxynonenal on insulin signaling in 3T3-L1 adipocytes. Diabetes 57, 1216-1226 (2008).
35. O. E. Owen, V. E. Trapp, G. A. Reichard Jr., M. A. Mozzoli, R. Smith, G. Boden, Effects of therapy on the nature and quantity of fuels oxidized during diabetic ketoacidosis. Diabetes 29, 365-372 (1980).
36. L. Tappy, O. E. Owen, G. Boden, Effect of hyperinsulinemia on urea pool size and substrate oxidation rates. Diabetes 37, 1212-1216 (1988).
37. C. H. Best, N. B. Taylor, in The Physiological Basis of Medical Practice, N. B. Taylor, Ed. (William and Wilkins, Baltimore, 1961), p. 756.
38. H. C. Lukaski, Methods for the assessment of human body composition: Traditional and new. Am. J. Clin. Nutr. 46, 537-556 (1987).
39. A. K. Saenger, T. J. Laha, M. J. Edenfield, S. M. Sadrzadeh, Quantification of urinary 8-iso-PGF2a using liquid chromatography-tandem mass spectrometry and association with elevated troponin levels. Clin. Biochem. 40, 1297-1304 (2007).
40. G. Boden, S. Merali, Chapter four-Measurement of the increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Methods Enzymol. 489, 67-82 (2011).
41. X. Duan, S. G. Kelsen, S. Merali, Proteomic analysis of oxidative stress-responsive proteins in human pneumocytes: Insight into the regulation of DJ-1 expression. J. Proteome Res. 7, 4955-4961 (2008).
42. C. A. Barrero, O. Perez-Leal, M. Aksoy, C. Moncada, R. Ji, Y. Lopez, K. Mallilankaraman, M. Madesh, G. J. Criner, S. G. Kelsen, S. Merali, Histone 3. 3 participates in a self-sustaining cascade of apoptosis that contributes to the progression of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 188, 673-683 (2013).
43. L. Bordoli, F. Kiefer, K. Arnold, P. Benkert, J. Battey, T. Schwede, Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4, 1-13 (2009).
44. F. Kiefer, K. Arnold, M. Kunzli, L. Bordoli, T. Schwede, The SWISS-MODEL Repository and associated resources. Nucleic Acids Res. 37, D387-D392 (2009).