T3 increases lactate transport and the expression of MCT4, but not MCT1, in rat skeletal muscle

American Journal of Physiology - Endocrinology and Metabolism

Volumn 285, Issue 3 48-3, 2003, Pages

  Wang, Yuxiang ^a   Tonouchi, Mio ^a   Miskovic, Dragana ^a   Hatta, Hideo ^c   Bonen, Arend ^b  

^a UNIVERSITY OF WATERLOO   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Giant vesicles; Heart; Monocarboxylate transporter 1 mRNA; Monocarboxylate transporter 1 protein; Monocarboxylate transporter 4 mRNA; Monocarboxylate transporter 4 protein

Indexed keywords

LACTIC ACID; LIOTHYRONINE; MONOCARBOXYLATE TRANSPORTER; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 4; UNCLASSIFIED DRUG; COTRANSPORTER; MESSENGER RNA; MONOCARBOXYLATE TRANSPORT PROTEIN 1; MTC4 PROTEIN, RAT; MUSCLE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; FAST MUSCLE; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; HEART MUSCLE; MALE; MUSCLE CONTRACTION; MUSCLE METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SARCOLEMMA; SKELETAL MUSCLE; SLOW MUSCLE; UPREGULATION; WEIGHT GAIN; ANIMAL; DRUG EFFECT; GENETICS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; LACTIC ACID; MALE; MONOCARBOXYLIC ACID TRANSPORTERS; MUSCLE PROTEINS; MUSCLE, SKELETAL; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SARCOLEMMA; SYMPORTERS; TRIIODOTHYRONINE;

EID: 0042967491     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00069.2003     Document Type: Article

References (54)

1. Argov Z, Renshaw P, Boden B, Winkokur A, and Bank W. Effects of thyroid hormone on skeletal muscle bioenergetics. J Clin Invest 81: 1695-1701, 1988.
2. 2-isoforms. Am J Physiol Cell Physiol 265: C680-C687, 1993.
3. Baker SK, Tarnopolsky MA, and Bonen A. Expression of MCT1 and MCT4 in a patient with mitochondrial myopathy. Muscle Nerve 24: 394-398, 2001.
4. Begum N, Leitner W, Reusch JE-B, Sussman KE, and Draznin B. GLUT-4 phosphorylation and its intrinsic activity. Mechanism of Ca2+-induced inhibition of insulin-stimulated glucose transport. J Biol Chem 268: 3352-3356, 1993.
5. Bonen A. Expression of lactate transporters (MCT1, MCT4) in heart and muscle. Eur J Appl Physiol 86: 6-11, 2001.
6. Bonen A, Luiken JJFP, Arumugam Y, Glatz JFC, and Tandon NN. Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. J Biol Chem 275: 14501-14508, 2000.
7. Bonen A, Luiken JJFP, Lui S, Dyck DJ, Kiens B, Kristiansen S, Turcotte L, van der Vusse GJ, and Glatz JFC. Palmitate transport and fatty acid transporters in red and white muscles. Am J Physiol Endocrinol Metab 275: E471-E478, 1998.
8. Bonen A, Megeney LA, McCarthy SC, McDermott JC, and Tan MH. Epinephrine administration stimulates GLUT4 translocation but reduces glucose transport in muscle. Biochem Biophys Res Commun 187: 685-691, 1992.
9. Bonen A, Miskovic D, Tonouchi M, Lemieux K, Wilson MC, Marette A, and Halestrap AP. Abundance and subcellular distribution of MCT1 and MCT4 in heart and fast-twitch skeletal muscles. Am J Physiol Endocrinol Metab 278: E1067-E1077, 2000.
10. Bonen A, Tonuchi M, Miskovic D, Heddle C, Heikkila JJ, and Halestrap AP. Isoform-specific regulation of the lactate transporters MCT1 and MCT4 by contractile activity. Am J Physiol Endocrinol Metab 279: E1131-E1138, 2000.
11. Broer S, Broer A, Schneider HP, Stegen C, Halestrap AP, and Deitmer JW. Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem J 341: 529-535, 1999.
12. Broer S, Schneider HP, Broer A, Rahman B, Hamprecht B, and Deitmer JW. Characterization of the monocarboxylate transporter 1 expressed in Xenopus laevis oocytes by changes in cytosolic pH. Biochem J 333: 167-174, 1998.
13. Clancy BM, Harrison SA, Buxton JM, and Czech MP. Protein synthesis inhibitors activate glucose transport without increasing plasma membrane glucose transporters in 3T3-L1 adipocytes. J Biol Chem 266: 10122-10130, 1991.
14. Dimmer K-S, Friedrich B, Lang F, Deitmer JW, and Broer S. The low affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem J 350: 219-227, 2000.
15. Dubouchaud H, Butterfield GE, Wolfel EE, Bergman BC, and Brooks GA. Endurance training, expression, and physiology of LDH, MCT1, and MCT4 in human skeletal muscle. Am J Physiol Endocrinol Metab 278: E571-E579, 2000.
16. Fisher MD and Frost SC. Translocation of GLUT1 does not account for elevated glucose transport in glucose-deprived 3T3-L1 adipocytes. J Biol Chem 271: 118906-11809, 1996.
17. Garcia CK, Brown MS, Pathak RK, and Goldstein JL. cDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1. J Biol Chem 270: 1843-1849, 1995.
18. Gerhart DZ, Enerson BE, Zhdankina OY, Leino RL, and Drewes LR. Expression of the monocarboxylate transporter MCT2 by rat brain glia. Glia 22: 272-281, 1998.
19. Halestrap AP and Price NT. The proton-linked monocarboxylate transporter family: structure, function and regulation. Biochem J 343: 281-299, 1999.
20. Han X-X and Bonen A. Epinephrine translocates GLUT-4 but inhibits insulin-stimulated glucose transport in rat muscle. Am J Physiol Endocrinol Metab 274: E700-E707, 1998.
21. Hatta H, Tonouchi M, and Bonen A. Tissue-specific and isoform-specific changes in MCT1 and -4 in heart and soleus muscle during a 1-yr period. Am J Physiol Endocrinol Metab 281: E749-E756, 2001.
22. Jackson VN, Price NT, and Halestrap AP. cDNA cloning of MCT1, a monocarboxylate transporter from rat skeletal muscle. Biochim Biophys Acta 1238: 193-196, 1995.
23. Jackson VN, Price NT, and Halestrap AP. Cloning of the monocarboxylate transporter isoform MCT2 from rat testis provides evidence that the expression is species specific and may involve post-transcriptional regulation. Biochem J 324: 447-453, 1997.
24. Johannsson E, Lunde PK, Heddle C, Sjaastad I, Thomas MJ, Bergersen LJ, Halestrap AP, Blackstad TW, Ottersen OP, and Sejersted OM. Upregulation of the cardiac monocarboxylate transporter MCT1 in a rat model of congestive heart failure. Circulation 104: 729-734, 2001.
25. Juel C. Muscle lactate transport studied in sarcolemmal giant vesicles. Biochim Biophys Acta 1065: 15-20, 1991.
26. Juel C. Lactate-proton cotransport in skeletal muscle. Physiol Rev 77: 1-37, 1997.
27. Juel C, Honig A, and Pilegaard H. Muscle lactate transport studied in sarcolemmal giant vesicles: dependence on fiber type and age. Acta Physiol Scand 143: 361-365, 1991.
28. Koehler-Stec EM, Simpson IA, Vannucci SJ, Landschulz KT, and Landschulz WH. Monocarboxylate transporter expression in mouse brain. Am J Physiol Endocrinol Metab 275: E516-E524, 1998.
29. Kristiansen S, Wojtaszewski JF, Juel C, and Richter EA. Effect of glucose-6-phosphate and pH on glucose transport in skeletal muscle plasma membrane giant vesicles. Acta Physiol Scand 150: 227-233, 1994.
30. Lin RY, Vera JC, Chaganti RS, and Golde DW. Human monocarboxylate transporter 2 (MCT2) is a high affinity pyruvate transporter. J Biol Chem 273: 28959-28965, 1998.
31. Luiken JJ, Willems J, Coort SL, Coumans WA, Bonen A, Van Der Vusse GJ, and Glatz JF. Effects of cAMP modulators on long-chain fatty-acid uptake and utilization by electrically stimulated rat cadiac myocytes. Biochem J 367: 881-887, 2002.
32. Manning Fox JE, Meredith D, and Halestrap AP. Characterisation of human monocarboxylate transporter 4 substantiates its role in lactic acid efflux from skeletal muscle. J Physiol 529: 285-293, 2000.
33. McCullagh KJA, Juel C, O'Brien M, and Bonen A. Chronic muscle stimulation increases lactate transport in rat skeletal muscle. Mol Cell Biochem 156: 51-57, 1996.
34. McCullagh KJA, Poole RC, Halestrap AP, O'Brien M, and Bonen A. Role of the lactate transporter (MCT1) in skeletal muscles. Am J Physiol Endocrinol Metab 271: E143-E150, 1996.
35. McCullagh KJA, Poole RC, Halestrap AP, O'Brien M, and Bonen A. Chronic electrical stimulation increases MCT1 and lactate uptake in red and white skeletal muscle. Am J Physiol Endocrinol Metab 273: E239-E246, 1997.
36. McDermott JC and Bonen A. Lactate transport by skeletal muscle sarcolemmal vesicles. Mol Cell Biochem 122: 113-121, 1993.
37. McDermott JC and Bonen A. Lactate transport in rat sarcolemmal vesicles and intact skeletal muscle, and after muscle contraction. Acta Physiol Scand 151: 17-28, 1994.
38. Oppenheimer JH. The Nuclear Receptor-Triiodothyronine Complex: Realtionship to Thyroid Hormone Distribution, Metabolism and Biologic Action. New York: Academic, 1983.
39. Pellerin L, Pellegri G, Bittar PG, Charnay Y, Bouras C, Martin JL, Stella N, and Magistretti PJ. Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci 20: 291-299, 1998.
40. Pellerin L, Pellegri G, Martin JL, and Magistretti PJ. Expression of monocarboxylate transporter mRNAs in mouse brain: support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc Natl Acad Sci USA 95: 3990-3995, 1998.
41. + transport capacity in human skeletal muscle. Am J Physiol Endocrinol Metab 276: E255-E261, 1999.
42. Price NT, Jackson VN, and Halestrap AP. Cloning and sequencing of four new mammalian monocarboxylate transporter (MCT) homologues confirms the existence of a transporter family with an ancient past. Biochem J 329: 321-328, 1998.
43. Reusch JE-B, Sussman KE, and Draznin B. Inverse relationship between GLUT-4 phosphorylation and its intrinsic activity. J Biol Chem 268: 3348-3351, 1993.
44. Roth DA and Brooks GA. Lactate transport is mediated by a membrane-bound carrier in rat skeletal muscle sarcolemmal membranes. Arch Biochem Biophys 279: 377-385, 1990.
45. Sambrook J, Fritisch EF, and Maniatis T. Molecular Cloning: A Laboratory Manual. Cold Springs Harbor, NY: Cold Springs Harbor Laboratory, 1989.
46. Shi Y, Liu H, Vanderburg G, Samuel SJ, Ismail-Beigi F, and Yung CY. Modulation of GLUT1 intrinsic activity in clone 9 cells by inhibition of oxidative phosphorylation. J Biol Chem 270: 21772-21778, 1995.
47. 3 increases mitochondrial ATP production in oxidative muscle despite increased expression of UCP2 and -3. Am J Physiol Endocrinol Metab 280: E761-E769, 2001.
48. Stevens R, Nishio M, and Hood D. Effect of hyperthyroidism on the expression of cytochrome c and cytochrome oxidase in heart and muscle during development. Mol Cell Biochem 143: 119-127, 1995.
49. Takanaga H, Tamai I, Inaba S, Sai Y, Higashida H, Yamamoto H, and Tsuji A. cDNA cloning and functional characterization of rat intestinal monocarboxylate transporter. Biochem Biophys Res Commun 217: 370-377, 1995.
50. Tonouchi M, Hatta H, and Bonen A. Muscle contraction increases lactate transport while reducing sarcolemmal MCT4, but not MCT1. Am J Physiol Endocrinol Metab 282: E1062-E1069, 2002.
51. 2+-ATPase isoform expression by thyroid hormone in rat skeletal muscle. Am J Physiol Cell Physiol 271: C1908-C1919, 1996.
52. Weinstein SP, O'Boyle E, and Haber RS. Thyroid hormone increases basal and insulin-stimulated glucose transport in skeletal muscle. The role of GLUT4 glucose transporter expression. Diabetes 43: 1185-1189, 1994.
53. Weinstein SP, Watts J, and Haber RS. Thyroid hormone increases muscle/ fat glucose transporter gene expression in rat skeletal muscle. Endocrinology 129: 455-464, 1991.
54. Wilson MC, Jackson VN, Hedle C, Price NT, Pilegaard H, Juel C, Bonen A, Montgomery I, Hutter OF, and Halestrap AP. Lactic acid efflux from white skeletal muscle is catalyzed by the monocarboxylate transporter MCT3. J Biol Chem 273: 15920-15926, 1998.