Skeletal muscle subsarcolemmal mitochondrial dysfunction in high-fat fed rats exhibiting impaired glucose homeostasis

International Journal of Obesity

Volumn 31, Issue 10, 2007, Pages 1596-1604

  Lionetti, L ^a   Mollica, M P ^a   Crescenzo, R ^a   D'Andrea, E ^a   Ferraro, M ^a   Bianco, F ^a   Liverini, G ^a   Iossa, S ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b Sezione di Fisiologia   (Italy)

Author keywords

Energy balance; Insulin resistance; Muscle mitochondrial compartment; Oxidative stress

Indexed keywords

ACONITATE HYDRATASE; ESSENTIAL FATTY ACID; GLUCOSE; INSULIN; LIPID; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY FAT; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY BALANCE; ENERGY CONSUMPTION; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTON TRANSPORT; RAT; SARCOLEMMA;

ANIMALS; BODY COMPOSITION; DIETARY FATS; ENERGY INTAKE; ENERGY METABOLISM; GLUCOSE INTOLERANCE; INSULIN RESISTANCE; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OBESITY; OXIDATIVE STRESS; RATS; RATS, WISTAR; SARCOLEMMA;

ANIMALIA; RATTUS;

EID: 34748856784     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/sj.ijo.0803636     Document Type: Article

References (60)

1. Han D, Hansen PA, Host HH, Holloszy JO. Insulin resistance of muscle glucose transport in rats fed a high fat diet. Diabetes 1997; 46: 1761-1767.
2. Bernstein RS, Marshall MC, Caney AL. Effects of dietary composition on adipose tissue hexokinase-2 and glucose utilization in normal and streptozotocin-diabetic rats. Diabetes 1977; 26: 770-779.
3. Kraegen EW, Clark PW, Jenkins AB, Daley E, Chisholm DJ, Storlien LH. Development of muscle insulin resistance after liver insulin resistance in the high fat fed rat. Diabetes 1991; 40: 1397-1403.
4. Kelley DE, Mintun MA, Watkins SC, Simoneau JA, Jadili F, Fredrickson A et al. The effect of non-insulin-dependent diabetes mellitus and obesity on glucose transport and phosphorylation in skeletal muscle. J Clin Invest 1996; 97: 2705-2713.
5. Furler SM, Oakes ND, Watkinson AL, Kraegen EW. A high-fat diet influences insulin-stimulated posttransport muscle glucose metabolism in rat. Metabolism 1997; 46: 1101-1106.
6. Ikemoto S, Thompson KS, Takahashi M, Itakura H, Lane MD, Ezaki O. High fat diet induced hyperglicemia. prevention by low level expression of a glucose transporter (GLUT4) minigene in transgenic mouse. Proc Natl Acad Sci USA 1995; 92: 3096-3099.
7. Zhou YP, Grill VE. Long term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J Clin Invest 1994; 93: 870-876.
8. Sako Y, Grill VE. A 48-hour lipid infusion in the rat time-dependently inhibits glucose-induced insulin secretion and B cell oxidation through a process likely coupled to fatty acid oxidation. Endocrinology 1990; 127: 1580-1589.
9. Carpentier A, Mittelman SD, Lamarche B, Bergman RN, Giacca A, Lewis GF. Acute enhancement of insulin secretion by FFA in humans is lost with prolonged FFA elevation. Am J Physiol Endocrinol Metab 1999; 276: E1055-E1066.
10. Paolisso G, Gambardella A, Amato L, Tortoriello R, D'Amore A, Varricchio M et al. Opposite effects of short- and long-term fatty acid infusion on insulin secretion in healthy subjects. Diabetologia 1995; 38: 1295-1299.
11. Oakes ND, Bell KS, Furler SM, Camilleri S, Saha AK, Ruderman NB et al. Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulation of glucose uptake and suppression of long-chain fatty acyl CoA. Diabetes 1997; 46: 2022-2028.
12. Chalkley SM, Hettiarachchi M, Chisholm DJ, Kraegen EW. Longterm high fat feeding leads to severe insulin resistance but not diabetes in Wistar rats. Am J Physiol Endocrinol Metab 2002; 282: E1231-E1238.
13. Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, Kraegen EW. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes 1991; 40: 280-289.
14. Stark AH, Timar B, Madar Z. Adaptation of Sprague Dawley rats to long-term feeding of high fat or high fructose diets. Eur J Nutr 2000; 39: 229-234.
15. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 2005; 54: 8-14.
16. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant qoffspring of patients with type 2 diabetes. N Engl J Med 2004; 350: 664-671.
17. Stannard SR, Johnson NA. Insulin resistance and elevated triglyceride in muscle: more important for survival than thrifty genes? J Physiol 2003; 554: 595-607.
18. Iossa S, Lionetti L, Mollica MP, Crescenzo R, Botta M, Barletta A et al. Effect of high fat feeding on metabolic efficiency and mitochondrial oxidative capacity in adult rats. Br J Nutr 2003; 90: 953-960.
19. Mollica MP, Lionetti L, Crescenzo R, D'Andrea E, Ferraro M, Liverini G et al. Heterogeneous bioenergetic behaviour of subsarcolemmal and intermyofibrillar mitochondria in fed and fasted rats. Cell Mol Life Sci 2005; 63: 358-366.
20. Sreekumar R, Unnikrishnan J, Fu A, Nygren J, Short KR, Shimke J et al. Impact of high-fat diet and antioxidant supplement on mitochondrial funcions and gene transcripts in rat muscle. Am J Physiol Endocrinol Metab 2002; 282: E1055-E1061.
21. Slim RM, Toborek M, Watkins BA, Boissonneault GA, Hennig B. Susceptibility to hepatic oxidative stress in rabbits fed different animal and plant fats. J Am Coll Nutr 1996; 15: 289-294.
22. Iossa S, Mollica MP, Lionetti L, Crescenzo R, Botta M, Liverini G. Skeletal muscle oxidative capacity in rats fed high-fat diet. Int J Obes 2002; 26: 65-72.
23. Folch J, Lees M, Stanley GHS. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 1957; 226: 497-510.
24. Iossa S, Lionetti L, Mollica MP, Barletta A, Liverini G. Energy intake and utilization vary during development in rats. J Nutr 1999; 129: 1593-1596.
25. Pullar JD, Webster AJF. The energy cost of fat and protein deposition in the rat. Br J Nutr 1977; 37: 355-363.
26. Rothwell NJ, Stock MJ, Warwick BP. Energy balance and brown fat activity in rats fed cafeteria diets or high fat, semisynthetic diets at several levels of intake. Metab 1985; 34: 474-480.
27. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412-419.
28. Iossa S, Mollica MP, Lionetti L, Crescenzo R, Botta M, Samec S et al. Skeletal muscle mitochondrial efficiency and uncoupling protein 3 in overeating rats with increased thermogenesis. Pflug Arch 2002; 445: 431-436.
29. Srere PA. Citrate synthase. Methods Enzymol 1969; 13: 3-5.
30. Estabrook RW. Mitochondrial respiratory control and the polarographic measurement of ADP:O ratios. Methods Enzymol 1967; 10: 41-47.
31. Nedergaard J. The relationship between extramitochondrial Ca2+ concentration, respiratory rate, and membrane potential in mitochondria from brown adipose tissue of the rat. Eur J Biochem 1983; 133: 185-191.
32. Iossa S, Mollica MP, Lionetti L, Crescenzo R, Tasso R, Liverini G. A possible link between skeletal muscle mitochondrial efficiency and age-induced insulin resistance. Diabetes 2004; 53: 2861-2866.
33. Richieri GV, Anel A, Kleinfeld AM. Interactions of long chain fatty acids and albumin: determination of free fatty acid levels using the fluorescent probe ADIFAB. Biochemistry 1993; 32: 7574-7580.
34. Gardner PR. Aconitase: sensitive target and measure of superoxide. Methods Enzymol 2002; 349: 9-16.
35. Hausladen A, Fridovich I. Measuring nitric oxide and superoxide: rate constants for aconitase reactivity. Methods Enzymol 1996; 269: 37-41.
36. Flohè L, Otting F. Superoxide Dismutase Assay. Methods Enzymol 1984; 105: 93-104.
37. Krieger DA, Tate CA, McMillin-Wood J, Booth FW. Populations of rat skeletal muscle mitocondria after exercise and immobilization. J Appl Physiol 1980; 48: 23-28.
38. Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol 1993; 264: C383-C389.
39. Bizeau ME, Willis WT, Hazel JR. Differential responses to endurance training in subsarcolemmal and intermyofibrillar mitochondria. J Appl Physiol 1998; 85: 1279-1284.
40. Rolfe DSF, Brown CG. Cellular energy utilisation and molecular origin of standard metabolic rate in mammals. Physiol Rev 1997; 77: 731-758.
41. Skulachev VP. Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett 1991; 294: 158-162.
42. Jezek P, Engstova H, Zackova M, Vercesi AE, Costa ADT, Arruta P et al. Fatty acid cycling mechanism and mitochondrial uncoupling proteins. Biochim Biophys Acta 1998; 1365: 319-327.
43. Boozer CN, Schoenbach B, Atkinson RL. Dietary fat and adiposity: a dose-response relationship in adult male rats fed isocalorically. Am J Physiol 1995; 268: E546-E550.
44. Boozer CN, Brasseur A, Atkinson RL. Dietary fat affects weight loss and adiposity during energy restriction in rats. Am J Clin Nutr 1993; 58: 846-852.
45. Flatt JP. The biochemistry of energy expenditure. In: Bjorntorp P and Bordoff BN (eds). Obesity. Lippincott: Philadelphia, PA, 1992; 110-116.
46. Jequier E. Pathways to obesity. Int J Obes 2002; 26: S12-S17.
47. Kaloyianni M, Freedland RA. Contribution of several aminoacids and lactate to gluconeogenesis in hepatocytes isolated from rats fed various diets. J Nutr 1990; 120: 116-122.
48. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA et al. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 2005; 54: 1926-1933.
49. Jagoe RT, Lecker SH, Gomes M, Goldberg AL. Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J 2002; 16: 1697-1712.
50. Robblee NM, Clandinin MT. Effect of dietary fat level and polyunsaturated fatty acid content on the phospholipid composition of rat cardiac mitochondrial membranes and mitochondrial ATPase activity. J Nutr 1984; 114: 263-269.
51. 2 production in liver. Comp Biochem Physiol 2005; 140: 99-108.
52. Weiss R, Dufour S, Taksali SE, Tamborlane WV, Petersen KF, Bonadonna RC et al. Prediabetes in obese youth: a syndrome of impaired glucose tolerance, severe insulin resistance, and altered myocellular and abdominal fat partitioning. Lancet 2003; 362: 951-957.
53. Petersen KF, Befroy D, Dofour S, Dziura J, Arijan C, Rothman DL et al. Mitochondrial disfunction in the elderly: possible role in insulin resistance. Science 2003; 300: 1140-1142.
54. Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD et al. Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J Clin Endocrinol Metab 2003; 88: 5444-5451.
55. Pamploma R, Portero-Otin M, Sanz A, Requena J, Barja G. Modification of the longevity-related degree of fatty acid unsaturation modulates oxidative damage to proteins and mitochondrial DNA in liver and brain. Exp Gerontol 2004; 39: 725-733.
56. 2 production and lipid and protein oxidative damage. Mech Ageing Dev 2001; 122: 427-443.
57. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997; 416: 15-18.
58. Crescenzo R, Lionetti L, Mollica MP, Ferraro M, D'Andrea E, Mainieri D et al. Altered skeletal muscle subsarcolemmal mitochondrial compartment during catch-up fat after caloric restriction. Diabetes 2006; 55: 2286-2293.
59. Kerner J, Turkaly PJ, Minkler PE, Hoppel CL. Aging skeletal muscle mitochondria in the rat: decreased uncoupling protein-3 content. Am J Physiol 2001; 281: E1054-E1062.
60. Hoeks J, Hesselink MKC, Schrauwen P. Involvement of UCP3 in mild uncoupling and lipotoxicity. Exp Gerontol 2006; 41: 658-662.