Recovered insulin response by 2 weeks of leptin administration in high-fat fed rats is associated with restored AS160 activation and decreased reactive lipid accumulation

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 301, Issue 1, 2011, Pages

  Stefanyk, Leslie E ^a   Gulli, Roberto A ^a   Ritchie, Ian R ^a   Chabowski, Adrian ^b   Snook, Laelie A ^a   Bonen, Arend ^a   Dyck, David J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

Author keywords

Ceramide; Diacylglycerol; Fatty acid transport proteins; Insulin signaling; Leptin; Mitochondria

Indexed keywords

AKT SUBSTRATE; CD36 ANTIGEN; CERAMIDE; CITRATE SYNTHASE; DIACYLGLYCEROL; GLUCOSE; INSULIN; LEPTIN; MUSCLE ENZYME; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY MASS; CALORIC INTAKE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATIONAL STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FAST MUSCLE; FEMALE; GLUCOSE TRANSPORT; INSULIN BLOOD LEVEL; INSULIN RESPONSE; LIPID DIET; LIPID STORAGE; LOW FAT DIET; MITOCHONDRION; MOLECULAR MECHANICS; MUSCLE FIBRIL; NONHUMAN; PRIORITY JOURNAL; RAT; SARCOLEMMA; SIGNAL TRANSDUCTION; SLOW MUSCLE; SOLEUS MUSCLE;

ANIMALS; BODY COMPOSITION; CITRATE (SI)-SYNTHASE; DIETARY FATS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLUCOSE TRANSPORTER TYPE 4; GTPASE-ACTIVATING PROTEINS; INSULIN; LEPTIN; LIPID METABOLISM; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OBESITY; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 79959958107     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00636.2010     Document Type: Article

References (59)

1. Alkhateeb H, Chabowski A, Glatz JF, Gurd B, Luiken JJ, Bonen A. Restoring As160 phosphorylation rescues skeletal muscle insulin resistance and fatty acid oxidation while not reducing intramuscular lipids. Am J Physiol Endocrinol Metab 297: E1056-E1066, 2009.
2. Aoi W, Naito Y, Takanami Y, Ishii T, Kawai Y, Akagiri S, Kato Y, Osawa T, Yoshikawa T. Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification. Biochem Biophys Res Commun 366: 892-897, 2008.
3. Ayre KJ, Hulbert AJ. Effects of changes in dietary fatty acids on isolated skeletal muscle functions in rats. J Appl Physiol 80: 464-471, 1996.
4. Benton CR, Nickerson JG, Lally J, Han XX, Holloway GP, Glatz JF, Luiken JJ, Graham TE, Heikkila JJ, Bonen A. Modest PGC-1alpha overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria. J Biol Chem 283: 4228-4240, 2008.
5. Berthon PM, Howlett RA, Heigenhauser GJ, Spriet LL. Human skeletal muscle carnitine palmitoyltransferase I activity determined in isolated intact mitochondria. J Appl Physiol 85: 148-153, 1998.
6. Bezaire V, Bruce CR, Heigenhauser GJ, Tandon NN, Glatz JF, Luiken JJ, Bonen A, Spriet LL. Identification of fatty acid translocase on human skeletal muscle mitochondrial membranes: essential role in fatty acid oxidation. Am J Physiol Endocrinol Metab 290: E509-E515, 2006.
7. Biddinger SB, Miyazaki M, Boucher J, Ntambi JM, Kahn CR. Leptin suppresses stearoyl-CoA desaturase 1 by mechanisms independent of insulin and sterol regulatory element-binding protein-1c. Diabetes 55: 2032-2041, 2006.
8. Bonen A, Campbell SE, Benton CR, Chabowski A, Coort SL, Han XX, Koonen DP, Glatz JF, Luiken JJ. Regulation of fatty acid transport by fatty acid translocase/CD36. Proc Nutr Soc 63: 245-249, 2004.
9. Bonen A, Parolin ML, Steinberg GR, Calles-Escandon J, Tandon NN, Glatz JF, Luiken JJ, Heigenhauser GJ, Dyck DJ. Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36. FASEB J 18: 1144-1146, 2004.
10. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ, Dyck DJ. Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 291: E99-E107, 2006.
11. Buettner R, Newgard CB, Rhodes CJ, O'Doherty RM. Correction of diet-induced hyperglycemia, hyperinsulinemia, and skeletal muscle insulin resistance by moderate hyperleptinemia. Am J Physiol Endocrinol Metab 278: E563-E569, 2000.
12. Campbell SE, Tandon NN, Woldegiorgis G, Luiken JJ, Glatz JF, Bonen A. A novel function for fatty acid translocase (FAT)/CD36: involvement in long chain fatty acid transfer into the mitochondria. J Biol Chem 279: 36235-36241, 2004.
13. Cartee GD, Wojtaszewski JF. Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl Physiol Nutr Metab 32: 557-566, 2007.
14. Chavez JA, Knotts TA, Wang LP, Li G, Dobrowsky RT, Florant GL, Summers SA. A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids. J Biol Chem 278: 10297-10303, 2003.
15. Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264: C383-C389, 1993.
16. Cohen P, Miyazaki M, Socci ND, Hagge-Greenberg A, Liedtke W, Soukas AA, Sharma R, Hudgins LC, Ntambi JM, Friedman JM. Role for stearoyl-CoA desaturase-1 in leptin-mediated weight loss. Science 297: 240-243, 2002.
17. Dube JJ, Bhatt BA, Dedousis N, Bonen A, O'Doherty RM. Leptin, skeletal muscle lipids, and lipid-induced insulin resistance. Am J Physiol Regul Integr Comp Physiol 293: R642-R650, 2007.
18. Fillmore N, Jacobs DL, Mills DB, Winder WW, Hancock CR. Chronic AMP-activated protein kinase activation and a high fat diet have an additive effect on mitochondria in rat skeletal muscle. J Appl Physiol 109: 511-520, 2010.
19. Han XX, Chabowski A, Tandon NN, Calles-Escandon J, Glatz JF, Luiken JJ, Bonen A. Metabolic challenges reveal impaired fatty acid metabolism and translocation of FAT/CD36 but not FABPpm in obese Zucker rat muscle. Am J Physiol Endocrinol Metab 293: E566-E575, 2007.
20. Helge JW, Kriketos AD, Storlien LH. Insulin sensitivity, muscle fibre types, and membrane lipids. Adv Exp Med Biol 441: 129-138, 1998.
21. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature 420: 333-336, 2002.
22. Holloway GP, Benton CR, Mullen KL, Yoshida Y, Snook LA, Han XX, Glatz JF, Luiken JJ, Lally J, Dyck DJ, Bonen A. In obese rat muscle transport of palmitate is increased and is channeled to triacylglycerol storage despite an increase in mitochondrial palmitate oxidation. Am J Physiol Endocrinol Metab 296: E738-E747, 2009.
23. Holloway GP, Jain SS, Bezaire V, Han XX, Glatz JF, Luiken JJ, Harper ME, Bonen A. FAT/CD36-null mice reveal that mitochondrial FAT/CD36 is required to upregulate mitochondrial fatty acid oxidation in contracting muscle. Am J Physiol Regul Integr Comp Physiol 297: R960-R967, 2009.
24. Holloway GP, Thrush AB, Heigenhauser GJ, Tandon NN, Dyck DJ, Bonen A, Spriet LL. Skeletal muscle mitochondrial FAT/CD36 content and palmitate oxidation are not decreased in obese women. Am J Physiol Endocrinol Metab 292: E1782-E1789, 2007.
25. Jeppesen J, Mogensen M, Prats C, Sahlin K, Madsen K, Kiens B. FAT/CD36 is localized in sarcolemma and in vesicle-like structures in subsarcolemma regions but not in mitochondria. J Lipid Res 51: 1504-1512.
26. Junkin KA, Dyck DJ, Mullen KL, Chabowski A, Thrush AB. Resistin acutely impairs insulin-stimulated glucose transport in rodent muscle in the presence, but not absence, of palmitate. Am J Physiol Regul Integr Comp Physiol 296: R944-R951, 2009.
27. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest 106: 473-481, 2000.
28. King KL, Stanley WC, Rosca M, Kerner J, Hoppel CL, Febbraio M. Fatty acid oxidation in cardiac and skeletal muscle mitochondria is unaffected by deletion of CD36. Arch Biochem Biophys 467: 234-238, 2007.
29. Koonen DP, Coumans WA, Arumugam Y, Bonen A, Glatz JF, Luiken JJ. Giant membrane vesicles as a model to study cellular substrate uptake dissected from metabolism. Mol Cell Biochem 239: 121-130, 2002.
30. Luiken JJ, Arumugam Y, Dyck DJ, Bell RC, Pelsers MM, Turcotte LP, Tandon NN, Glatz JF, Bonen A. Increased rates of fatty acid uptake and plasmalemmal fatty acid transporters in obese Zucker rats. J Biol Chem 276: 40567-40573, 2001.
31. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, Carling D, Kahn BB. Leptin stimulates fatty-acid oxidation by activating AMPactivated protein kinase. Nature 415: 339-343, 2002.
32. Montell E, Turini M, Marotta M, Roberts M, Noe V, Ciudad CJ, Mace K, andGomez-Foix AM. DAG accumulation from saturated fatty acids desensitizes insulin stimulation of glucose uptake in muscle cells. Am J Physiol Endocrinol Metab 280: E229-E237, 2001.
33. Nickerson JG, Alkhateeb H, Benton CR, Lally J, Nickerson J, Han XX, Wilson MH, Jain SS, Snook LA, Glatz JF, Chabowski A, Luiken JJ, Bonen A. Greater transport efficiencies of the membrane fatty acid transporters FAT/CD36 and FATP4 compared with FABPpm and FATP1 and differential effects on fatty acid esterification and oxidation in rat skeletal muscle. J Biol Chem 284: 16522-16530, 2009.
34. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlien LH. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46: 983-988, 1997.
35. Peters SJ, Harris RA, Heigenhauser GJ, Spriet LL. Muscle fiber type comparison of PDH kinase activity and isoform expression in fed and fasted rats. Am J Physiol Regul Integr Comp Physiol 280: R661-R668, 2001.
36. Schenk S, Cook JN, Kaufman AE, Horowitz JF. Postexercise insulin sensitivity is not impaired after an overnight lipid infusion. Am J Physiol Endocrinol Metab 288: E519-E525, 2005.
37. Schenk S, Horowitz JF. Coimmunoprecipitation of FAT/CD36 and CPT I in skeletal muscle increases proportionally with fat oxidation after endurance exercise training. Am J Physiol Endocrinol Metab 291: E254-E260, 2006.
38. Sebastian D, Guitart M, Garcia-Martinez C, Mauvezin C, Orellana-Gavalda JM, Serra D, Gomez-Foix AM, Hegardt FG, Asins G. Novel role of FATP1 in mitochondrial fatty acid oxidation in skeletal muscle cells. J Lipid Res 50: 1789-1799, 2009.
39. Shimabukuro M, Koyama K, Chen G, Wang MY, Trieu F, Lee Y, Newgard CB, Unger RH. Direct antidiabetic effect of leptin through triglyceride depletion of tissues. Proc Natl Acad Sci USA 94: 4637-4641, 1997.
40. Simoneau JA, Veerkamp JH, Turcotte LP, Kelley DE. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J 13: 2051-2060, 1999.
41. Singh MK, Krisan AD, Crain AM, Collins DE, Yaspelkis BB, 3rd. High-fat diet and leptin treatment alter skeletal muscle insulin-stimulated phosphatidylinositol 3-kinase activity and glucose transport. Metabolism 52: 1196-1205, 2003.
42. Smith AC, Mullen KL, Junkin KA, Nickerson J, Chabowski A, Bonen A, Dyck DJ. Metformin and exercise reduce muscle FAT/CD36 and lipid accumulation and blunt the progression of high-fat diet-induced hyperglycemia. Am J Physiol Endocrinol Metab 293: E172-E181, 2007.
43. Srere PA, Brooks GC. The circular dichroism of glucagon solutions. Arch Biochem Biophys 129: 708-710, 1969.
44. Stefanyk LE, Coverdale N, Roy BD, Peters SJ, LeBlanc PJ. Skeletal muscle type comparison of subsarcolemmal mitochondrial membrane phospholipid fatty acid composition in rat. J Membr Biol 234: 207-215.
45. Steinberg GR, Bonen A, Dyck DJ. Fatty acid oxidation and triacylglycerol hydrolysis are enhanced after chronic leptin treatment in rats. Am J Physiol Endocrinol Metab 282: E593-E600, 2002.
46. Steinberg GR, Dyck DJ, Calles-Escandon J, Tandon NN, Luiken JJ, Glatz JF, Bonen A. Chronic leptin administration decreases fatty acid uptake and fatty acid transporters in rat skeletal muscle. J Biol Chem 277: 8854-8860, 2002.
47. Steinberg GR, Rush JW, Dyck DJ. AMPK expression and phosphorylation are increased in rodent muscle after chronic leptin treatment. Am J Physiol Endocrinol Metab 284: E648-E654, 2003.
48. Straczkowski M, Kowalska I, Baranowski M, Nikolajuk A, Otziomek E, Zabielski P, Adamska A, Blachnio A, Gorski J, Gorska M. Increased skeletal muscle ceramide level in men at risk of developing type 2 diabetes. Diabetologia 50: 2366-2373, 2007.
49. Suzuki A, Okamoto S, Lee S, Saito K, Shiuchi T, Minokoshi Y. Leptin stimulates fatty acid oxidation and peroxisome proliferator-activated receptor alpha gene expression in mouse C2C12 myoblasts by changing the subcellular localization of the alpha2 form of AMP-activated protein kinase. Mol Cell Biol 27: 4317-4327, 2007.
50. Thrush AB, Brindley DN, Chabowski A, Heigenhauser GJ, Dyck DJ. Skeletal muscle lipogenic protein expression is not different between lean and obese individuals: a potential factor in ceramide accumulation. J Clin Endocrinol Metab 94: 5053-5061, 2009.
51. Todd MK, Yaspelkis BB, 3rd, Turcotte LP. Short-term leptin treatment increases fatty acids uptake and oxidation in muscle of high fat-fed rats. Metabolism 54: 1218-1224, 2005.
52. Tsalouhidou S, Argyrou C, Theofilidis G, Karaoglanidis D, Orfanidou E, Nikolaidis MG, Petridou A, Mougios V. Mitochondrial phospholipids of rat skeletal muscle are less polyunsaturated than whole tissue phospholipids: implications for protection against oxidative stress. J Anim Sci 84: 2818-2825, 2006.
53. Unger RH. Longevity, lipotoxicity and leptin: the adipocyte defense against feasting and famine. Biochimie 87: 57-64, 2005.
54. Unger RH. Minireview: weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology 144: 5159-5165, 2003.
55. Wallberg-Henriksson H, Zetan N, Henriksson J. Reversibility of decreased insulin-stimulated glucose transport capacity in diabetic muscle with in vitro incubation. Insulin is not required. J Biol Chem 262: 7665-7671, 1987.
56. Yaspelkis BB, 3rd, Ansari L, Ramey EL, Holland GJ, Loy SF. Chronic leptin administration increases insulin-stimulated skeletal muscle glucose uptake and transport. Metabolism 48: 671-676, 1999.
57. Yaspelkis BB, 3rd, Davis JR, Saberi M, Smith TL, Jazayeri R, Singh M, Fernandez V, Trevino B, Chinookoswong N, Wang J, Shi ZQ, Levin N. Leptin administration improves skeletal muscle insulin responsiveness in diet-induced insulin-resistant rats. Am J Physiol Endocrinol Metab 280: E130-E142, 2001.
58. Yaspelkis BB, 3rd, Saberi M, Singh MK, Trevino B, Smith TL. Chronic leptin treatment normalizes basal glucose transport in a fiber type-specific manner in high-fat-fed rats. Metabolism 51: 859-863, 2002.
59. Yaspelkis BB, 3rd, Singh MK, Krisan AD, Collins DE, Kwong CC, Bernard JR, Crain AM. Chronic leptin treatment enhances insulinstimulated glucose disposal in skeletal muscle of high-fat fed rodents. Life Sci 74: 1801-1816, 2004.