3,5-Diiodo-L-thyronine prevents high-fat-diet-induced insulin resistance in rat skeletal muscle through metabolic and structural adaptations

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3312-3324

  Moreno, Maria ^a   Silvestri, Elena ^a   De Matteis, Rita ^b   De Lange, Pieter ^c   Lombardi, Assunta ^d   Glinni, Daniela ^a   Senese, Rosalba ^c   Cioffi, Federica ^c   Salzano, Anna Maria ^e   Scaloni, Andrea ^e   Lanni, Antonia ^c   Goglia, Fernando ^a  

^a UNIVERSITY OF SANNIO   (Italy)

^b UNIVERSITY OF URBINO   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e CNR   (Italy)

Author keywords

Metabolism; Proteomics; Thyroid hormone

Indexed keywords

ADIPOPHILIN; CD36 ANTIGEN; CHOLESTEROL; DIIODOTHYRONINE; GLUCOSE TRANSPORTER 4; IODOTHYRONINE; PROTEIN KINASE B; TRIACYLGLYCEROL;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FIBER; GASTROCNEMIUS MUSCLE; HEART VENTRICLE HYPERTROPHY; HYPERLIPIDEMIA; INSULIN RESISTANCE; LIPID DIET; MALE; METABOLIC DISORDER; MUSCLE CELL; MUSCLE LEVEL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SARCOLEMMA; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION;

ANIMALS; ANTIGENS, CD36; DIETARY FATS; DIIODOTHYRONINES; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 4; INSULIN; INSULIN RESISTANCE; LIPIDS; MALE; MEMBRANE PROTEINS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SARCOLEMMA; SIGNAL TRANSDUCTION; TRIGLYCERIDES;

RATTUS;

EID: 80053913540     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-181982     Document Type: Article

References (45)

1. DeFronzo, R. A., and Tripathy, D. (2009) Skeletal muscle IR is the primary defect in type 2 diabetes. Diabetes Care 32, S157-S163
2. Kelley, D. E., Mokan, M., Simoneau, J. A., and Mandarino, L. S. (1993) Interaction between glucose and free fatty acid metabolism in human skeletal muscle. J. Clin. Invest. 92, 91-98 (Pubitemid 23208984)
3. Itani, S. I., Ruderman, N. B., Schmieder, F., and Boden, G. (2002) Lipid-induced IR in human muscle is associated with changes in diacylglycerol, protein kinase C and IκB-α. Diabetes 51, 2005-2011 (Pubitemid 34729001)
4. Stump, C. S., Henriksen, E. J., Wei, Y., and Sowers, J. R. (2006) The metabolic syndrome: role of skeletal muscle metabolism. Ann. Med. 38, 389-402 (Pubitemid 44484877)
5. Bonen, A., Parolin, M. L., Steinberg, G. R., Calles-Escandon, J., Tandon, N. N., Glatz, J. F., Luiken, J. J., Heigenhauser, G. J., and Dyck, D. J. (2004) 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 (Pubitemid 39561551)
6. Chabowski, A., Chatham, J. C., Tandon, N. N., Calles-Escandon, J., Glatz, J. F., Luiken, J. J., and Bonen, A. (2006) Fatty acid transport and FAT/CD36 are increased in red but not in white skeletal muscle of ZDF rats. Am. J. Physiol. Endocrinol. Metab. 291, E675-E682 (Pubitemid 44352276)
7. Kelley, D. E., Goodpaster, B., Wing, R. R., and Simoneau, J. A. (1999) Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am. J. Physiol. 277, E1130-E1141 (Pubitemid 30046009)
8. Kim, J. Y., Hickner, R. C., Cortright, R. L., Dohm, G. L., and Houmard, J. A. (2000) Lipid oxidation is reduced in obese human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279, E1039-E1044
9. McGarry, J. D. (2002) Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51, 7-18
10. Watt, M. J. (2009) Storing up trouble: does accumulation of intramyocellular triglyceride protect skeletal muscle from insulin resistance? Clin. Exp. Pharmacol. Physiol. 36, 5-11
11. Son, N. H., Yu, S., Tuinei, J., Arai, K., Hamai, H., Homma, S., Shulman, G. I., Abel, E. D., and Goldberg, I. J. (2010) PPARγ-induced cardiolipotoxicity in mice is ameliorated by PPARα deficiency despite increases in fatty acid oxidation. J. Clin. Invest. 120, 3443-3454
12. Hajduch, E., Alessi, D. R., Hemmings, B. A., and Hundal, H. S. (1998) Constitutive activation of protein kinase Bα by membrane targeting promotes glucose and system A amino acid transport, protein synthesis, and inactivation of glycogen synthase kinase 3 in L6 muscle cells. Diabetes 47, 1006-1013 (Pubitemid 28294540)
13. Ueki, K., Yamamoto-Honda, R., Kaburagi, Y., Yamauchi, T., Tobe, K., Burgering, B. M., Coffer, P. J., Komuro, I., Akanuma. Y., Yazaki, Y., and Kadowaki, T. (1998) Potential role of protein kinase B in insulin-induced glucose transport, glycogen synthesis, and protein synthesis. J. Biol. Chem. 273, 5315-5322 (Pubitemid 28108698)
14. Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., Zlotchenko, E., Scrimgeour, A., Lawrence, J. C., Glass, D. J., and Yancopoulos, G. D. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014-1019 (Pubitemid 34428747)
15. Tremblay, F., and Marette, A. (2001) Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J. Biol. Chem. 276, 38052-38060
16. Belfort, R., Mandarino, L., Kashyap, S., Wirfel, K., Pratipanawatr, T., Berria, R., Defronzo, R. A., and Cusi, K. (2005) Dose-response effect of elevated plasma free fatty acid on insulin signaling. Diabetes 54, 1640-1648 (Pubitemid 40770753)
17. Van Loon, L. J., and Goodpaster, B. H. (2006) Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state. Pflügers Arch. 451, 606-616 (Pubitemid 43042172)
18. Tanner, C. J., Barakat, H. A., Dohm, G. L., Pories, W. J., MacDonald, K. G., Cunningham, P. R., Swanson, M. S., and Houmard, J. A. (2002) Muscle fiber type is associated with obesity and weight loss. Am. J. Physiol. Endocrinol. Metab. 282, E1191-E1196 (Pubitemid 34654686)
19. Levin, M. C., Monetti, M., Watt, M. J., Sajan, M. P., Stevens, R. D., Bain, J. R., Newgard, C. B., Farese, R. V., Sr., and Farese, R. V., Jr. (2007) Increased lipid accumulation and insulin resistance in transgenic mice expressing DGAT2 in glycolytic (type II) muscle. Am. J. Physiol. Endocrinol. Metab. 293, E1772-E1781 (Pubitemid 350255131)
20. Izumiya, Y., Hopkins, T., Morris, C., Sato, K., Zeng, L., Viereck, J., Hamilton, J. A., Ouchi, N., LeBrasseur, N. K., and Walsh, K. (2008) Fast/glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab. 7, 159-172 (Pubitemid 351168553)
21. Oppenheimer, J. H., Schwartz, H. L., Lane, J. T., and Thompson, M. P. (1991) Functional relationship of thyroid hormone-induced lipogenesis, lipolysis, and thermogenesis in the rat. J. Clin. Invest. 87, 125-132
22. Weinstein, S. P., O'Boyle, E., and Haber, R. S. (1994) Thyroid hormone increases basal and insulin-stimulated glucose transport in skeletal muscle. The role of GLUT4 glucose transporter expression. Diabetes 43, 1185-1189 (Pubitemid 24361182)
23. Dimitriadis, G., Parry-Billings, M., Bevan, S., Leighton, B., Krause, U., Piva, T., Tegos, K., Challiss, R. A., Wegener, G., and Newsholme, E. A. (1997) The effects of insulin on transport and metabolism of glucose in skeletal muscle from hyperthyroid and hypothyroid rats. Eur. J. Clin. Invest. 27, 475-483 (Pubitemid 27288357)
24. Weinstein, S. P., Watts, J., and Haber, R. S. (1991) Thyroid hormone increases muscle/fat glucose transporter gene expression in rat skeletal muscle. Endocrinology 129, 455-464
25. Dimitriadis, G. D., Leighton, B., Parry-Billings, M., West, D., and Newsholme, E. A. (1989) Effects of hypothyroidism on the sensitivity of glycolysis and glycogen synthesis to insulin in the soleus muscle of the rat. Biochem. J. 257, 369-373 (Pubitemid 19040906)
26. Lanni, A., Moreno, M., Lombardi, A., de Lange, P., Silvestri, E., Ragni, M., Farina, P., Baccari, G. C., Fallahi, P., Antonelli, A., and Goglia, F. (2005) 3,5-Diiodo-L-thyronine powerfully reduces adiposity in rats by increasing the burning of fats. FASEB J. 19, 1552-1554 (Pubitemid 41279028)
27. De Lange, P., Senese, R., Cioffi, F., Moreno, M., Lombardi, A., Silvestri, E., Goglia, F., and Lanni, A. (2008) Rapid activation by 3,5,3′-L-triiodothyronine of adenosine 5′-monophosphate-activated protein kinase/acetyl-coenzyme a carboxylase and akt/protein kinase B signaling pathways: relation to changes in fuel metabolism and myosin heavy-chain protein content in rat gastrocnemius muscle in vivo. Endocrinology 149, 6462-6470
28. Opie, L. H., and Newsholme, E. A. (1967) The activities of fructose 1,6-diphosphatase, phosphofructokinase and phosphoenolpyruvate carboxykinase in white muscle and red muscle. Biochem. J. 103, 391-399
29. Behan, W. M., Cossar, D. W., Madden, H. A., and McKay, I. C. (2002) Validation of a simple, rapid, and economical technique for distinguishing type 1 and 2 fibres in fixed and frozen skeletal muscle. J. Clin. Pathol. 55, 375-380 (Pubitemid 34494178)
30. Koopman, R., Schaart, G., and Hesselink, M. K. (2001) Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem. Cell Biol. 116, 63-68 (Pubitemid 32695819)
31. Silvestri, E., Burrone, L., de Lange, P., Lombardi, A., Farina, P., Chambery, A., Parente, A., Lanni, A., Goglia, F., and Moreno, M. (2007) Thyroid-state influence on protein-expression profile of rat skeletal muscle. J. Proteome Res. 6, 3187-3196 (Pubitemid 47310203)
32. Talamo, F., D'Ambrosio, C., Arena, S., Del Vecchio, P., Ledda, L., and Zehender, G. (2003) Proteins from bovine tissues and biological fluids: defining a reference electrophoresis map for liver, kidney, muscle, plasma and red blood cells. Proteomics 3, 440-460 (Pubitemid 36428297)
33. Scippa, G. S., Rocco, M., Ialicicco, M., Trupiano, D., Viscosi, V., Di Michele, M., Arena, S., Chiatante, D., and Scaloni, A. (2010) The proteome of lentil (Lens culinaris Medik.) seeds: discriminating between landraces. Electrophoresis 31, 497-506
34. Qian, W. J., Liu, T., Monroe, M. D. E., Strittmatter, E. F., Jacobs, J. M., Kangas, L. J., Petritis, K., Camp, D. G. 2nd, and Smith, R. D. (2005) Probability-based evaluation of peptide and protein identification from tandem mass spectrometry and SEQUEST analysis: the human proteome. J. Proteome Res. 4, 53-62 (Pubitemid 40352578)
35. Fluck, M., and Hoppeler, H. (2003) Molecular basis of skeletal muscle plasticity - from gene to form and function. Rev. Physiol. Biochem. Pharmacol. 146, 159-216
36. Phillips, S. A., Choe, C. C., Ciaraldi, T. P., Greenberg, A. S., Kong, A. P., Baxi, S. C., Christiansen, L., Mudaliar, S. R., and Henry, R. R. (2005) Adipocyte differentiation-related protein in human skeletal muscle: relationship to insulin sensitivity. Obes. Res. 13, 1321-1329
37. Minnaard, R., Schrauwen, P., Schaart, G., Jorgensen, J. A., Lenaers, E., Mensink, M., and Hesselink, M. K. (2009) Adipocyte differentiation-related protein and OXPAT in rat and human skeletal muscle: involvement in lipid accumulation and type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 94, 4077-4085
38. Muoio, D. M., and Newgard, C. B. (2006) Obesity-related derangements in metabolic regulation. Annu. Rev. Biochem. 75, 367-401 (Pubitemid 44118037)
39. Pimenta, A. S., Gaidhu, M. P., Habib, S., So, M., Fediuc, S., Mirpourian, M., Curi, R., and Ceddia, R. B. (2008) Prolonged exposure to palmitate impairs fatty acid oxidation despite activation of AMP-activated protein kinase in skeletal muscle cells. J. Cell. Physiol. 217, 478-485
40. Randle, P. J., Garland, P. B., Hales, C. N., and Newsholme, E. A. (1963) The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1, 785-789
41. Saltiel, A. R., and Kahn, C. R. (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799-806 (Pubitemid 34000783)
42. Tremblay, F., Lavigne, C., Jacques, H., and Marette, A. (2001) Defective insulin-induced GLUT4 translocation in skeletal muscle of high fat-fed rats is associated with alterations in both Akt/protein kinase B and atypical protein kinase C (ζ/λ) activities. Diabetes 50, 1901-1910 (Pubitemid 33641612)
43. Albright, A., Franz, M., Hornsby, G., Kriska, A., Marrero, D., Ullrich, I., and Varity, L. S. (2000) American College of Sports Medicine position stand. Exercise and type 2 diabetes. Med. Sci. Sports Exerc. 32, 1345-1360 (Pubitemid 30483962)
44. Schmitz, K. H., Hannan, P. J., Stovitz, S. D., Bryan, C. J., Warren, M., and Jensen, M. D. (2007) Strength training and adiposity in premenopausal women: strong, healthy, and empowered study. Am. J. Clin. Nutr. 86, 566-572 (Pubitemid 47435821)
45. Miyabara, E. H., Aoki, M. S., Soares, A. G., Saltao, R. M., Vilicev, C. M., Passarelli, M., Scanlan, T. S., Gouveia, C. H., and Moriscot, A. S. (2005) Thyroid hormone receptor-β-selective agonist GC-24 spares skeletal muscle type I to II fiber shift. Cell Tissue Res. 321, 233-241 (Pubitemid 41127030)