Gender dimorphism in high-fat-diet-induced insulin resistance in skeletal muscle of aged rats

Cellular Physiology and Biochemistry

Volumn 22, Issue 5-6, 2008, Pages 539-548

  Gómez Pérez, Yolanda ^a,b   Amengual Cladera, Emilia ^a,b   Català Niell, Antoni ^a,b   Thomàs Moyà, Elena ^a,b   Gianotti, Magdalena ^a,b   Proenza, Ana Maria ^a,b   Lladó, Isabel ^a,b  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b Instituto de Salud Carlos III   (Spain)

Author keywords

Adipokine; GLUT4; Obesity; Oxidative damage; Oxidative stress; UCP3

Indexed keywords

ADIPONECTIN; CYTOCHROME C; GLUCOSE TRANSPORTER 4; HYDROGEN PEROXIDE; INSULIN; MANGANESE SUPEROXIDE DISMUTASE; RESISTIN; UNCOUPLING PROTEIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GLUCOSE TOLERANCE TEST; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; MALE; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; SKELETAL MUSCLE;

RATTUS;

EID: 57649231744     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000185538     Document Type: Article

References (56)

1. Stump CS, Henriksen EJ, Wei Y, Sowers JR: The metabolic syndrome: role of skeletal muscle metabolism. Ann Med 2006;38:389-402.
2. Dandona P, Aljada A, Bandyopadhyay A: Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 2004;25:4-7.
3. Milagro FI, Campion J, Martinez JA: Weight gain induced by high-fat feeding involves increased liver oxidative stress. Obesity (Silver Spring) 2006;14:1118-1123.
4. Fridlyand LE, Philipson LH: Reactive species and early manifestation of insulin resistance in type 2 diabetes. Diabetes Obes Metab 2006;8:136-145.
5. Carmiel-Haggai M, Cederbaum AI, Nieto N: A high-fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats. Faseb J 2005;19:136-138.
6. Eriksson JW: Metabolic stress in insulin's target cells leads to ROS accumulation - a hypothetical common pathway causing insulin resistance. FEBS Lett 2007;581:3734-3742.
7. Coatmellec-Taglioni G, Dausse JP, Giudicelli Y, Ribiere C: Sexual dimorphism in cafeteria diet-induced hypertension is associated with gender-related difference in renal leptin receptor down-regulation. J Pharmacol Exp Ther 2003;305:362-367.
8. Llado I, Rodriguez-Cuenca S, Pujol E, Monjo M, Estrany ME, Roca P, Palou A: Gender effects on adrenergic receptor expression and lipolysis in white adipose tissue of rats. Obes Res 2002;10:296-305.
9. Horton TJ, Gayles EC, Prach PA, Koppenhafer TA, Pagliassotti MJ: Female rats do not develop sucrose-induced insulin resistance. Am J Physiol 1997;272:R1571-1576.
10. Colom B, Alcolea MP, Valle A, Oliver J, Roca P, Garcia-Palmer FJ: Skeletal muscle of female rats exhibit higher mitochondrial mass and oxidative-phosphorylative capacities compared to males. Cell Physiol Biochem 2007;19:205-212.
11. Colom B, Oliver J, Roca P, Garcia-Palmer FJ: Caloric restriction and gender modulate cardiac muscle mitochondrial H2O2 production and oxidative damage. Cardiovasc Res 2007;74:456-465.
12. Borras C, Sastre J, Garcia-Sala D, Lloret A, Pallardo FV, Vina J: Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 2003;34:546-552.
13. Justo R, Boada J, Frontera M, Oliver J, Bermudez J, Gianotti M: Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis. Am J Physiol Cell Physiol 2005;289:C372-378.
14. Valle A, Guevara R, Garcia-Palmer FJ, Roca P, Oliver J: Sexual dimorphism in liver mitochondrial oxidative capacity is conserved under caloric restriction conditions. Am J Physiol Cell Physiol 2007;293:C1302-1308.
15. Rodriguez-Cuenca S, Pujol E, Justo R, Frontera M, Oliver J, Gianotti M, Roca P: Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem 2002;277:42958-42963.
16. Justo R, Frontera M, Pujol E, Rodriguez-Cuenca S, Llado I, Garcia-Palmer FJ, Roca P, Gianotti M: Gender-related differences in morphology and thermogenic capacity of brown adipose tissue mitochondrial subpopulations. Life Sci 2005;76:1147-1158.
17. Wolever TM, Jenkins DJ: The use of the glycemic index in predicting the blood glucose response to mixed meals. Am J Clin Nutr 1986;43:167-172.
18. Pickavance LC, Wilding JP: Effects of S 15511, a therapeutic metabolite of the insulin-sensitizing agent S 15261, in the Zucker Diabetic Fatty rat. Diabetes Obes Metab 2007;9:114-120.
19. Xu A, Chan KW, Hoo RL, Wang Y, Tan KC, Zhang J, Chen B, Lam MC, Tse C, Cooper GJ, Lam KS: Testosterone selectively reduces the high molecular weight form of adiponectin by inhibiting its secretion from adipocytes. J Biol Chem 2005;280:18073-18080.
20. Rolfe DF, Hulbert AJ, Brand MD: Characteristics of mitochondrial proton leak and control of oxidative phosphorylation in the major oxygen-consuming tissues of the rat. Biochim Biophys Acta 1994;1188:405-416.
21. Lopez-Torres M, Gredilla R, Sanz A, Barja G: Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radic Biol Med 2002;32:882-889.
22. Chrzanowska-Lightowlers ZM, Turnbull DM, Lightowlers RN: A microtiter plate assay for cytochrome c oxidase in permeabilized whole cells. Anal Biochem 1993;214:45-49.
23. Muller FL, Liu Y, Van Remmen H: Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 2004;279:49064-49073.
24. Sanz A, Caro P, Ayala V, Portero-Otin M, Pamplona R, Barja G: Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. Faseb J 2006;20:1064-1073.
25. Slater TF, Sawyer BC: The stimulatory effects of carbon tetrachloride on peroxidative reactions in rat liver fractions in vitro. Inhibitory effects of free-radical scavengers and other agents. Biochem J 1971;123:823-828.
26. Aebi H: Catalase in vitro. Methods Enzymol. 1984;105:121-126.
27. Carlberg I, Mannervik B. Glutathione reductase. Methods Enzymol 1985;113:484-490.
28. 8 Paglia D: Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of laboratory and clinical medicine 1967;70:158-169.
29. Quick K: Rapid microplate assay for superoxide scavenging efficiency. Journal of neurocience methods 2000;97:139-144.
30. Combs TP, Berg AH, Rajala MW, Klebanov S, Iyengar P, Jimenez-Chillaron JC, Patti ME, Klein SL, Weinstein RS, Scherer PE: Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes 2003;52:268-276.
31. Thomas-Moya E, Gianotti M, Proenza AM, Llado I: Paraoxonase 1 response to a high-fat diet: gender differences in the factors involved. Mol Med 2007;13:203-209.
32. Turcotte LP, Swenberger JR, Zavitz Tucker M, Yee AJ: Increased fatty acid uptake and altered fatty acid metabolism in insulin-resistant muscle of obese Zucker rats. Diabetes 2001;50:1389-1396.
33. Hegarty BD, Cooney GJ, Kraegen EW, Furler SM: Increased efficiency of fatty acid uptake contributes to lipid accumulation in skeletal muscle of high fat-fed insulin-resistant rats. Diabetes 2002;51:1477-1484.
34. Hegarty BD, Furler SM, Ye J, Cooney GJ, Kraegen EW: The role of intramuscular lipid in insulin resistance. Acta Physiol Scand 2003;178:373-383.
35. Vina J, Borras C, Gambini J, Sastre J, Pallardo FV: Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds. FEBS Lett 2005;579:2541-2545.
36. Ordonez P, Moreno M, Alonso A, Llaneza P, Diaz F, Gonzalez C: 17beta-Estradiol and/or progesterone protect from insulin resistance in STZ-induced diabetic rats. J Steroid Biochem Mol Biol 2008;111:287-294.
37. Shehata M, Kamel MA: Protective effect of antioxidant adjuvant treatment with hormone replacement therapy against cardiovascular diseases in ovariectomized rats. Endocr Regul 2008;42:69-75.
38. Huang CJ, Fwu ML: Protein insufficiency aggravates the enhanced lipid peroxidation and reduced activities of antioxidative enzymes in rats fed diets high in polyunsaturated fat. J Nutr 1992;122:1182-1189.
39. Garait B, Couturier K, Servais S, Letexier D, Perrin D, Batandier C, Rouanet JL, Sibille B, Rey B, Leverve X, Favier R: Fat intake reverses the beneficial effects of low caloric intake on skeletal muscle mitochondrial H(2)O(2) production. Free Radic Biol Med 2005;39:1249-1261.
40. Pereira B, Rosa LF, Safi DA, Guimaraes AR, Bechara EJ, Curi R: Antioxidant enzyme activities in the lymphoid organs and muscles of rats fed fatty acids-rich diets subjected to prolonged physical exercise-training. Physiol Behav 1994;56:1049-1055.
41. Dyck DJ, Heigenhauser GJ, Bruce CR: The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol (Oxf) 2006;186:5-16.
42. Rondinone CM: Adipocyte-derived hormones, cytokines, and mediators. Endocrine 2006;29:81-90.
43. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ: Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 2007;56:2085-2092.
44. Chou CJ, Cha MC, Jung DW, Boozer CN, Hashim SA, Pi-Sunyer FX: High-fat diet feeding elevates skeletal muscle uncoupling protein 3 levels but not its activity in rats. Obes Res 2001;9:313-319.
45. Echtay KS, Esteves TC, Pakay JL, Jekabsons MB, Lambert AJ, Portero-Otin M, Pamplona R, Vidal-Puig AJ, Wang S, Roebuck SJ, Brand MD: A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. Embo J 2003;22:4103-4110.
46. Minnaard R, Schrauwen P, Schaart G, Hesselink MK: UCP3 in muscle wasting, a role in modulating lipotoxicity? FEBS Lett 2006;580:5172-5176.
47. Hoeks J, Hesselink MK, van Bilsen M, Schaart G, van der Vusse GJ, Saris WH, Schrauwen P: Differential response of UCP3 to medium versus long chain triacylglycerols; manifestation of a functional adaptation. FEBS Lett 2003;555:631-637.
48. Kontani Y, Wang Z, Furuyama T, Sato Y, Mori N, Yamashita H: Effects of aging and denervation on the expression of uncoupling proteins in slow- and fast-twitch muscles of rats. J Biochem (Tokyo) 2002;132:309-315.
49. Garcia-Palmer FJ, Pericas J, Matamala JC, Puigserver P, Bonet ML, Palou A, Gianotti M: Diminished response to food deprivation of the rat brown adipose tissue mitochondrial uncoupling system with age. Biochem Mol Biol Int 1997;42:1151-1161.
50. Puigserver P, Llado I, Palou A, Gianotti M: Evidence for masking of brown adipose tissue mitochondrial GDP-binding sites in response to fasting in rats made obese by dietary manipulation. Effects of reversion to standard diet. Biochem J 1991;279 ( Pt 2):575-579.
51. Tiraby C, Tavernier G, Capel F, Mairal A, Crampes F, Rami J, Pujol C, Boutin JA, Langin D: Resistance to high-fat-diet-induced obesity and sexual dimorphism in the metabolic responses of transgenic mice with moderate uncoupling protein 3 overexpression in glycolytic skeletal muscles. Diabetologia 2007;50:2190-2199.
52. Huppertz C, Fischer BM, Kim YB, Kotani K, Vidal-Puig A, Slieker LJ, Sloop KW, Lowell BB, Kahn BB: Uncoupling protein 3 (UCP3) stimulates glucose uptake in muscle cells through a phosphoinositide 3-kinase-dependent mechanism. J Biol Chem 2001;276:12520-12529.
53. Zorzano A, Palacin M, Guma A: Mechanisms regulating GLUT4 glucose transporter expression and glucose transport in skeletal muscle. Acta Physiol Scand 2005;183:43-58.
54. Kahn BB: Dietary regulation of glucose transporter gene expression: tissue specific effects in adipose cells and muscle. J Nutr 1994;124:1289S- 1295S.
55. Koranyi L, James D, Mueckler M, Permutt MA: Glucose transporter levels in spontaneously obese (db/db) insulin-resistant mice. J Clin Invest 1990;85:962-967.
56. King PA, Horton ED, Hirshman MF, Horton ES: Insulin resistance in obese Zucker rat (fa/fa) skeletal muscle is associated with a failure of glucose transporter translocation. J Clin Invest 1992;90:1568-1575.