3,5-Diiodo-L-thyronine rapidly enhances mitochondrial fatty acid oxidation rate and thermogenesis in rat skeletal muscle: AMP-activated protein kinase involvement

American Journal of Physiology - Endocrinology and Metabolism

Volumn 296, Issue 3, 2009, Pages

  Lombardi, A ^a   De Lange, P ^b   Silvestri, E ^c   Busiello, R A ^b   Lanni, A ^b   Goglia, F ^c,d   Moreno, M ^c,d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c Dipartimento di Scienze Biologiche ed Ambientali   (Italy)

^d UNIVERSITY OF SANNIO   (Italy)

Author keywords

Adenosine 5 monophosphate; Mitochondria; Thyroid hormone

Indexed keywords

DIIODOTHYRONINE; FATTY ACID; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MALONYL COENZYME A; PALMITOYL COENZYME A; PALMITOYLCARNITINE; PYRUVIC ACID; SUCCINIC ACID; 3,5-DIIODOTHYRONINE; ACETYL COENZYME A CARBOXYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENERGY METABOLISM; ENZYME ACTIVITY; FATTY ACID OXIDATION; GASTROCNEMIUS MUSCLE; HYPOTHYROIDISM; MALE; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SINGLE DRUG DOSE; SKELETAL MUSCLE; THERMOGENESIS; TIBIALIS ANTERIOR MUSCLE; ANIMAL; DISEASE MODEL; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; PHYSIOLOGY; THERMOREGULATION; WISTAR RAT;

ACETYL-COA CARBOXYLASE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BODY TEMPERATURE REGULATION; DIIODOTHYRONINES; DISEASE MODELS, ANIMAL; FATTY ACIDS; HYPOTHYROIDISM; MALE; MITOCHONDRIA; MUSCLE, SKELETAL; OXIDATION-REDUCTION; PHOSPHORYLATION; RATS; RATS, WISTAR;

EID: 64749099765     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90642.2008     Document Type: Article

References (39)

1. Alexson SE, Nedergaard J. A novel type of short- and medium-chain acyl-CoA hydrolases in brown adipose tissue mitochondria. J Biol Chem 263: 13564-13571, 1988. (Pubitemid 18232318)
2. Demori I, Gerdoni E, Fugassa E, Voci A. 3,5-Diiodothyronine mimics the effect of triiodothyronine on insulin-like growth factor binding protein-4 expression in cultured rat hepatocytes. Horm Metab Res 36: 679-685, 2004. (Pubitemid 39486967)
3. Dobbins RL, Szczepaniak LS, Bentley B, Esser V, Myhill J, McGarry JD. Prolonged inhibition of muscle carnitine palmitoyltransferase-1 promotes intramyocellular lipid accumulation and insulin resistance in rats. Diabetes 50: 123-130, 2001. (Pubitemid 32047990)
4. Eaton S. Control of mitochondrial beta-oxidation flux. Prog Lipid Res 41:197-239, 2002.
5. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509, 1957.
6. Gambert S, Ricquier D. Mitochondrial thermogenesis and obesity. Curr Opin Clin Nutr Metab Care 10: 664-670, 2007. (Pubitemid 350293765)
7. Gerbitz KD, Gempel K, Brdiczka D. Mitochondria and diabetes. Genetic, biochemical, and clinical implications of the cellular energy circuit. Diabetes 45: 113-126, 1996. (Pubitemid 26045791)
8. Giudetti AM, Leo M, Geelen MS, Gnoni GV. Short-term stimulation of lipogenesis by 3,5-L-diiodothyronine in cultured rat hepatocytes. Endocrinology 146: 3959-3966, 2005. (Pubitemid 41175767)
9. Goglia F. Biological effects of 3,5-diiodothyronine (T2). Biochemistry (Moscow) 70: 164-172, 2005.
10. Goglia F, Lanni A, Horst C, Moreno M, Thoma R. In vitro binding of 3,5-di-iodo-L-thyronine to rat liver mitochondria. J Mol Endocrinol 13: 275-288, 1994. (Pubitemid 24380333)
11. Goglia F, Moreno M, Lanni A. Action of thyroid hormones at the cellular level: the mitochondrial target. FEBS Lett 452: 115-120, 1999. (Pubitemid 29301729)
12. Grasselli E, Canesi L, Voci A, De Matteis R, Demori I, Fugassa E, Vergani L. Effects of 3,5-diiodo-L-thyronine administration on the liver of high fat diet-fed rats. Exp Biol Med (Maywood) 233: 549-557, 2008.
13. Hartree EF. Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal Biochem 48: 422-427, 1972.
14. Horst C, Rokos H, Seitz HJ. Rapid stimulation of hepatic oxygen consumption by 3,5-di-iodo-L-thyronine. Biochem J 261: 945-950, 1989. (Pubitemid 19209537)
15. Houmard JA. Intramuscular lipid oxidation and obesity. Am J Physiol Regul Integr Comp Physiol 294: R1111-R1116, 2008.
16. Kelley DE, Goodpaster B, Wing RR, Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol Endocrinol Metab 277: E1130-E1141, 1999.
17. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
18. Kelley DE, Mandarino LJ. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 49: 677-683, 2000.
19. Klein I, Ojamaa K. Thyroid hormone and the cardiovascular system. N Engl J Med 344: 501-509, 2001. (Pubitemid 32164903)
20. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7: 45-56, 2008.
21. Lanni A, Beneduce L, Lombardi A, Moreno M, Boss O, Muzzin P, Giacobino JP, Goglia F. Expression of uncoupling protein-3 and mitochondrial activity in the transition from hypothyroid to hyperthyroid state in rat skeletal muscle. FEBS Lett 444: 250-254, 1999. (Pubitemid 29092812)
22. Lanni A, Cioffi M, Moreno M, Goglia F. Effect of 3,3′-di- iodothyronine and 3,5-di-iodothyronine on rat liver mitochondria. J Endocrinol 136: 59-64, 1993. (Pubitemid 23016114)
23. Lanni A, Moreno M, Lombardi A, de Lange P, Silvestri E, Ragni M, Farina P, Chieffi-Baccari G, Fallahi P, Antonelli A, Goglia F. 3,5-diiodo-L-thyronine powerfully reduces adiposity in rats by increasing the burning of fats. FASEB J 19: 1552-1554, 2005. (Pubitemid 41279028)
24. Lanni A, Moreno M, Lombardi A, Goglia F. Calorigenic effect of diiodothyronines in the rat. J Physiol 494: 831-837, 1996. (Pubitemid 26278858)
25. Lanni A, Moreno M, Lombardi A, Goglia F. 3,5-Diiodo-L-thyronine and 3,5,3′-triiodo-L-thyronine both improve the cold tolerance of hypothyroid rats, but possibly via different mechanisms. Pflugers Arch 436: 407-414, 1998. (Pubitemid 28329101)
26. Lombardi A, Lanni A, Moreno M, Brand MD, Goglia F. Effect of 3,5-di-iodo-L-thyronine on the mitochondrial energy-transduction apparatus. Biochem J 330: 521-526, 1998. (Pubitemid 28075782)
27. Lombardi A, Lanni A, de Lange P, Silvestri E, Grasso P, Senese R, Goglia F, Moreno M. Acute administration of 3,5-diiodo-L-thyronine to hypothyroid rats affects bioenergetic parameters in rat skeletal muscle mitochondria. FEBS Lett 581: 5911-5916, 2007. (Pubitemid 50009362)
28. Lonn L, Stenlof K, Ottosson M, Lindroos AK, Nystrom E, Sjostrom L. Body weight and body composition changes after treatment of hyperthyroidism. J Clin Endocrinol Metab 83: 4269-4273, 1998. (Pubitemid 29100120)
29. Moreno M, Lanni A, Lombardi A, Goglia F. How the thyroid controls metabolism in the rat: different roles for triiodothyronine and diiodothyronines. J Physiol 505: 529-538, 1997. (Pubitemid 28043394)
30. Moreno M, Lombardi A, Lanni A, Beneduce L, Silvestri E, Pinna G, Goglia F. Are the effects of T3 on resting metabolic rate in euthyroid rats entirely caused by T3 itself? Endocrinol 143: 504-510, 2002. (Pubitemid 34107203)
31. Mutomba MC, Yuan H, Konyavko M, Adachi S, Yokoyama CB, Esser V, McGarry JD, Babior BM, Gottlieb RA. Regulation of the activity of caspases by L-carnitine and palmitoyl-carnitine. FEBS Lett 478: 19-25, 2000. (Pubitemid 30462251)
32. Ness GC, Lopez D, Chambers CM, Newsome WP, Cornelius P, Long CA, Harwood HJ Jr. Effects of L-triiodothyronine and the thyromimetic L-94901 on serum lipoprotein levels and hepatic LDL-receptor, 3-hydroxy-3-methylglutaryl coenzyme A reductase, and Apo a-1 gene expression. Biochem Pharm 56: 121-129, 1998. (Pubitemid 28477459)
33. O'Reilly I, Murphy MP. Studies on the rapid stimulation of mitochondrial respiration by thyroid hormones. Acta Endocrinol 127: 542-546, 1992. (Pubitemid 23029984)
34. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8-14, 2005. (Pubitemid 40105089)
35. Rolfe DF, Brand MD. Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate. Am J Physiol Cell Physiol 271: C1380-C1389, 1996.
36. 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. Biochem Biophys Acta 1118: 405-416, 1994.
37. Ruderman NB, Saha AK. Metabolic syndrome: adenosine monophosphate- activated protein kinase and malonyl coenzyme A. Obesity 14, Suppl 1: 25S-33S, 2006.
38. Shrago E, Woldegiorgis G, Ruoho AE, DiRusso CC. Fatty acyl-CoA esters as regulators of cell metabolism. Prostaglandins Leukot Essent Fatty Acids 52: 163-166, 1995.
39. Unger RH, Orci L. Diseases of liporegulation: new perspective on obesity and related disorders. FASEB J 15: 312-321, 2001. (Pubitemid 32141423)