Impaired mitochondrial fatty acid oxidation and insulin resistance in aging: Novel protective role of glutathione

Aging Cell

Volumn 12, Issue 3, 2013, Pages 415-425

  Nguyen, Dan ^a   Samson, Susan L ^a   Reddy, Vasumathi T ^a   Gonzalez, Erica V ^a   Sekhar, Rajagopal V ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Aging; Fuel oxidation; Glutathione; Insulin resistance; Mitochondria

Indexed keywords

ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; CARBON 13; CARNITINE PALMITOYLTRANSFERASE I; CD36 ANTIGEN; CYSTEINE; GLUCOSE; GLUCOSE TRANSPORTER 4; GLUTATHIONE; GLYCINE; INSULIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TRANSCRIPTION FACTOR NRF2; VERY LOW DENSITY LIPOPROTEIN;

AGING; ANIMAL EXPERIMENT; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; BODY COMPOSITION; BODY FAT; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET SUPPLEMENTATION; FAT CONTENT; FATTY ACID OXIDATION; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIVER; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLEUS MUSCLE; TRIACYLGLYCEROL BLOOD LEVEL; UREA NITROGEN BLOOD LEVEL;

AGING; ANIMALS; ANTIOXIDANTS; BODY COMPOSITION; CHOLESTEROL, LDL; CHOLESTEROL, VLDL; CYSTEINE; FATTY ACIDS; GLUCOSE; GLUTATHIONE; GLYCINE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; PALMITATES;

MUS;

EID: 84877825603     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12073     Document Type: Article

References (45)

1. Abumrad N, Harmon C, Ibrahimi A (1998) Membrane transport of long-chain fatty acids: evidence for a facilitated process. J. Lipid Res. 39, 2309-2318.
2. Bevilacqua S, Bonadonna R, Buzzigoli G, Boni C, Ciociaro D, Maccari F, Giorico MA, Ferrannini E (1987) Acute elevation of free fatty acid levels leads to hepatic insulin resistance in obese subjects. Metabolism 36, 502-506.
3. Bianchi G, Bertaccini G, Marchesini G, Conte C, Chianese R, Zoli M (2010) Non-alcoholic fatty liver disease and aging: prevalence and associated factors. 45th annual meeting of the European Association for the Study of the Liver (EASL) Poster Presentation: Session Title: Category 8c. Alcoholic drug induced and fatty liver disease: c. NASH/NAFLD - Clinical.
4. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
5. Bloch-Damti A, Bashan N (2005) Proposed mechanisms for the induction of insulin resistance by oxidative stress. Antioxid. Redox Signal. 7, 1553-1567.
6. Boden G (1997) Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes 46, 3-10.
7. Bruce R, Godsland I, Walton C, Crook D, Wynn V (1994) Associations between insulin sensitivity, and free fatty acid and triacylglycerol metabolism independent of uncomplicated obesity. Metabolism 43, 1275-1281.
8. Calles Escandon J, Arciero PJ, Gardner AW, Bauman C, Poehlman ET (1995) Basal fat oxidation decreases with aging in women. J. Appl. Physiol. 78, 266-271.
9. Chen Y, Miller ML, Shen D, Shertzer HG, Stringer KF, Wang B, Schneider SN, Nebert DW, Dalton TP (2007) Hepatocyte-specific Gclc deletion leads to rapid onset of steatosis with mitochondrial injury and liver failure. Hepatology 45, 1118-1128.
10. Corpeleijn E, Saris WH, Blaak EE (2009) Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle. Obes. Rev. 10, 178-193.
11. Cree MG, Newcomer BR, Katsanos CS, Sheffield-Moore M, Chinkes D, Aarsland A, Urban R, Wolfe RR (2004) Intramuscular and liver triacylglycerols are increased in the elderly. J. Clin. Endocrinol. Metab. 89, 3864-3871.
12. Dokken BB, Saengsirisuwan V, Kim JS, Teachey MK, Henriksen EJ (2008) Oxidative stress- induced insulin resistance in rat skeletal muscle: role of glycogen synthase kinase-3. Am. J. Physiol. Endocrinol. Metab. 294, E615-E621.
13. Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, Pearce SF, Silverstein RL (1999) A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J. Biol. Chem. 274, 19055-19062.
14. Findeisen HM, Gizard F, Zhao Y, Qing H, Jones KL, Cohn D, Heywood EB, Bruemmer D (2011) Glutathione depletion prevents diet-induced obesity and enhances insulin sensitivity. Obesity (Silver Spring) 19, 2429-2432.
15. Flegal KM, Carroll MD, Ogden CL, Curtin LR (2010) Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303, 235-241.
16. Frayn KN (1983) Calculation of substrate oxidation rates in vivo from gaseous exchange. J. Appl. Physiol. 55, 628-634.
17. Ghosh S, Pulinilkunnil T, Yuen G, Kewalramani G, An D, Qi D, Abrahani A, Rodrigues B (2005) Cardiomyocyte apoptosis induced by short-term diabetes requires mitochondrial GSH repletion. Am. J. Physiol. Heart Circ. Physiol. 289, H768-H776.
18. Goldstein BJ, Mahadev K, Wu X, Zhu L, Motoshima H (2005) Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxid. Redox Signal. 7, 1021-1031.
19. Harris MI, Flegal KM, Cowie CC, Eberhardt MS, Goldstein DE, Little RR, Wiedmeyer HM, Byrd-Holt DD (1998) 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 21, 518-524.
20. Iwakami S, Misu H, Takeda T, Sugimori M, Matsugo S, Kaneko S, Takamura T (2011) Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in H4IIEC hepatocytes. PLoS ONE 6, e27401.
21. Johannsen DL, Ravussin E (2010) Obesity in the elderly: is faulty metabolism to blame? Aging Health 6, 159-167.
22. Johannsen DL, Conley KE, Bajpeyi S, Punyanitya M, Gallagher D, Zhang Z, Covington J, Smith SR, Ravussin E (2012) Ectopic lipid accumulation and reduced glucose tolerance in elderly adults are accompanied by altered skeletal muscle mitochondrial activity. J. Clin. Endocrinol. Metab. 97, 242-250.
23. Karnieli E, Armoni M (2008) Transcriptional regulation of the insulin-responsive glucose transporter GLUT4 gene: from physiology to pathology. Am. J. Physiol. Endocrinol. Metab. 295, E38-E45. Epub 2008 May 20.
24. Kelley DE, Mandarino LJ (2000) Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 49, 677-683.
25. Kelley DE, Simoneau JA (1994) Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J. Clin. Invest. 94, 2349-2356.
26. Lang CA, Naryshkin S, Schneider DL, Mills BJ, Lindeman RD (1992) Low blood glutathione levels in healthy aging adults. J. Lab. Clin. Med. 120, 720-725.
27. Levadoux E, Morio B, Montaurier C, Puissant V, Boirie Y, Fellmann N, Picard B, Rousset P, Beaufrere B, Ritz P (2001) Reduced whole-body fat oxidation in women and in the elderly. Int. J. Obes. Relat. Metab. Disord. 25, 39-44.
28. Mastrocola R, Restivo F, Vercellinatto I, Danni O, Brignardello E, Aragno M, Boccuzzi G (2005) Oxidative and nitrosative stress in brain mitochondria of diabetic rats. J. Endocrinol. 187, 37-44.
29. McClung JP, Roneker CA, Mu W (2004) Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidase. Proc. Natl Acad. Sci. USA 101, 8852-8857.
30. 13C-NMR study. J. Exp. Biol. 203, 995-1001.
31. Moinova HR, Mulcahy RT (1999) Up-regulation of the human gamma-glutamylcysteine synthetase regulatory subunit gene involves binding of Nrf-2 to an electrophile responsive element. Biochem. Biophys. Res. Commun. 261, 661-668.
32. Mouzannar R, McCafferty J, Benedetto G, Richardson C (2011) Transcriptional and phospho-proteomic screens reveal stem cell activation of insulin resistance and transformation pathways following a single minimally toxic episode of ROS. Int. J. Genomics Proteomics. 2, 34-49.
33. Nguyen D, Sekhar RV (2012) Lack of evidence to support a beneficial role for glutathione depletion on body weight or glucose tolerance. Obesity (Silver Spring) 20, 1756.
34. Noale M, Maggi S, Marzari C, Limongi F, Gallina P, Bianchi D, Crepaldi G, ILSA Working Group (2006) Components of the metabolic syndrome and incidence of diabetes in elderly Italians: the Italian Longitudinal Study on Aging. Atherosclerosis, 187, 385-392.
35. Noale M, Maggi S, Zanoni S, Limongi F, Zambon S, Crepaldi G, ILSA working group (2012) The metabolic syndrome, incidence of diabetes and mortality among the elderly: the Italian Longitudinal Study of Ageing. Diabetes Metab. 38, 135-141.
36. Pi J, Bai Y, Zhang Q, Wong V, Floering LM, Daniel K, Reece JM, Deeney JT, Andersen ME, Corkey BE, Collins S (2007) Reactive oxygen species as a signal in glucose-stimulated insulin secretion. Diabetes 56, 1783-1791.
37. Rising R, Tatarrani PA, Snitker S, Ravussin E (1996) Decreased ratio of fat to carbohydrate oxidation with increasing age in Pima Indians. J. Am. Coll. Nutr. 15, 309-312.
38. Samiec PS, Drews-Botsch C, Flagg EW, Kurtz JC, Sternberg P Jr, Reed RL, Jones DP. (1998) Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic. Biol. Med. 24, 699-704.
39. Samson SL, Sathyanarayana P, Jogi M, Gonzalez EV, Gutierrez A, Krishnamurthy R, Muthupillai R, Chan L, Bajaj M (2011) Exenatide decreases hepatic fibroblast growth factor 21 resistance in non-alcoholic fatty liver disease in a mouse model of obesity and in a randomised controlled trial. Diabetologia 54, 3093-3100.
40. Sekhar RV, Patel SG, Guthikonda AP, Reid M, Balasubramanyam A, Taffet GE, Jahoor F (2011) Deficient synthesis of glutathione underlies oxidative stress in aging and can be corrected by dietary cysteine and glycine supplementation. Am. J. Clin. Nut. 94, 847-853.
41. Solomon TP, Marchetti CM, Krishnan RK, Gonzalez F, Kirwan JP (2008) Effects of aging on basal fat oxidation in obese humans. Metabolism 57, 1141-1147.
42. Toth MJ, Arciero P, Gardner AW, Calles-Escandon J, Poehlman ET (1996) Rates of free fatty acid appearance and fat oxidation in healthy younger and older men. J. Appl. Physiol. 80, 506-511.
43. Weyer C, Snitker S, Rising R, Bogardus C, Ravussin E (1999) Determinants of Energy expenditure and fuel utilization in man: effects of body composition, age, sex, ethnicity and glucose tolerance in 916 subjects. Int. J. Obes. Relat. Metab. Discor. 23, 715-722.
44. Wild AC, Moinova HR, Mulcahy RT (1999) Regulation of gamma-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 274, 33627-33636.
45. Zurlo F, Lillioja S, Esposito-Del Puente A, Nyomba BL, Raz I, Saad MF, Swinburn BA, Knowler WC, Bogardus C, Ravussin E (1990) Low ratio of fat to carbohydrate oxidation as predictor of weight gain: study of 24-h RQ. Am. J. Physiol. 259, E650-E657.