Fuel economy in food-deprived skeletal muscle: Signaling pathways and regulatory mechanisms

FASEB Journal

Volumn 21, Issue 13, 2007, Pages 3431-3441

  De Lange, Pieter ^a   Moreno, Maria ^b   Silvestri, Elena ^b   Lombardi, Assunta ^c   Goglia, Fernando ^b   Lanni, Antonia ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF SANNIO   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

AMP activated protein kinase; Fatty acids; Myosin heavy chain Ib; Peroxisome proliferator activated receptor coactivator 1 ; Peroxisome proliferator activated receptor ; Time course

Indexed keywords

ACETYL COENZYME A; ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; CD36 ANTIGEN; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; GENE PRODUCT; GLUCOSE; LIM PROTEIN; MESSENGER RNA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NUCLEAR PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SIRT3; SIRTUIN; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 3;

BIOGENESIS; ENDURANCE; ENERGY; EXERCISE; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FOOD DEPRIVATION; GENE ACTIVITY; KINETICS; MITOCHONDRIAL RESPIRATION; MUSCLE METABOLISM; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSCRIPTION INITIATION; TRANSLATION REGULATION;

ANIMALS; ENERGY METABOLISM; FOOD DEPRIVATION; MUSCLE, SKELETAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 35948975126     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-8527rev     Document Type: Review

References (97)

1. 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
2. Pette, D., and Staron, R. S. (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev. Physiol. Biochem. Pharmacol. 116, 1-76
3. Pette, D. (2002) The adaptive potential of skeletal muscle fibers. Can. J. Appl. Physiol. 27, 423-448
4. Kyrolainen, H., Kivela, R., Koskinen, S., McBride, J., Andersen, J. L., Takala, T., Sipila, S., and Komi, P. V. (2003) Interrelationships between muscle structure, muscle strength, and running economy. Med. Sci. Sports. Exerc. 35, 45-49
5. Pilegaard, H., Saltin, B., and Darrell Neufer, P. (2003) Effect of short term fasting and refeeding on transcriptional regulation of metabolic genes in human skeletal muscle. Diabetes 52, 657-662
6. De Lange, P., Ragni, M., Silvestri, E., Moreno, M., Schiavo, L., Lombardi, A., Farina, P., Feola, A., Goglia, F., and Lanni, A. (2004) Combined cDNA array/RT PCR analysis of gene expression profile in rat gastrocnemius muscle: relation to its adaptive function in energy metabolism during fasting. FASEB J. 18, 350-352
7. Jagoe, R. T., Lecker, S. R., Gomes, M., and Goldberg, A. L. (2002) Patterns of gene expression in atrophying skeletal muscle: response to food deprivation. FASEB J. 16, 1697-1712
8. Hardie, D. G., Hawley, S. A., and Scott, J. W. (2006) AMP-activated protein kinase - development of the energy sensor concept. J. Physiol. 574, 7-15
9. Hardie, D. G., Carling, D., and Carlson, M. (1998) The AMP activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryote cell? Annu. Rev. Biochem. 67, 821.855
10. Zhou, M., Lin, B.-Z., Coughlin, S., Vallega, G., and Philch, P. F. (2000) UCP-3 expression in skeletal muscle: effects of exercise, hypoxia, and AMP-activated protein kinase. Am. J. Physiol. Endocrinol. Metab. 279, 622-629
11. Suwa, M., Nakano, H., and Kugami, S. (2003) Effects of chronic AICAR treatment on fiber composition, enzyme activity, UCP3, and PGC-1 in rat muscles. J. Appl. Physiol. 95, 950-958
12. Putman, C. T., Kricsi, M., Pearcy, J., MacLean, I. M., Bamford, J. A., Murdoch, G. K., Dixon, W. T., and Pette, D. (2003) AMPK activation increases uncoupling protein-3 expression and mitochondrial enzyme activities in rat muscle without fibre type transitions. J. Physiol. 551, 169-178
13. De Lange, P., Farina, P., Moreno, M., Ragni, M., Lombardi, A., Silvestri, E., Burrone, L., Lanni, A., and Goglia, F. (2006) Sequential changes in the signal transduction responses of skeletal muscle following food deprivation. FASEB J. 20, 2579-2581
14. Jaschinski, F., Schuler, M., Peuker, H., and Pette, D. (1998) Changes in myosin heavy chain mRNA and protein isoforms of rat muscle during forced contractile activity. Am. J. Physiol. Cell Physiol. 274, C365-C370
15. Spiegelman, B. M., and Heinrich, R. (2004) Biological control through regulated transcriptional coactivators. Cell 119, 157-167
16. Knutti, D., Kaul, A., and Tralli, A. (2000) A tissue-specific coactivator of steroid receptors, identified in a functional genetic screen. Mol. Cell. Biol. 20, 2411-2422
17. Lin, J., Puigserver, P., Donovan, J., Tarr, P., and Spiegelman, B. M. (2002) Peroxisome proliferator-activated receptor gamma coactivator 1beta (PGC-1 beta), a novel PGC-1 related transcription coactivator associated with host cell factor. J. Biol. Chem. 277, 1645-1648
18. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., and Spiegellman, B. M. (1998) A cold-inducible coactivator of nuclear receptors is linked to adaptive thermogenesis. Cell 92, 829-839
19. Lin, J., Handschin, C., and Spiegelman, B. M. (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370
20. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124
21. Vega, R. B., Huss, J. M., and Kelly, D. P. (2000) The coactivator PGC-1 cooperates with peroxisome proliferators-activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol. Cell. Biol. 20, 1868-1876
22. Wang, Y. X., Lee, C. H., Tiep, S., Yu, R. T., Ham, J., Kang, H., and Evans, R. M. (2003) Peroxisome-proliferator-activated receptor δ activates fat metabolism to prevent obesity. Cell 113, 159-170
23. Huss, J. M., Kopp, R. P., and Kelly, D. P. (2002) Peroxisome proliferators-activated receptor coactivator-1alpha (PGC-1alpha) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-alpha and gamma. Identification of novel leucine-rich interaction motif within PGC-1alpha. J. Biol. Chem. 277, 40265-40274
24. Huss, J. M., Torra, I. P., Staels, B., Giguere, V., and Kelly, D. P. (2004) Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24, 9079-9091
25. Kamei, Y., Ohizumi, H., Fujitani, Y., Remoto, T., Tanaka, T., Takahashi, N., Kawada, T., Miyoshi, M., Ezaki, O., and Kakizuka, A. (2003) PPAR gamma coactivator 1 beta/ERR ligand 1 is an ERR protein ligand, whose expression induces a high-energy expenditure and antagonizes obesity. Proc. Natl. Acad. Sci. U. S. A. 100, 12378-12383
26. Mootha, V. K., Handschin, C., Arlow, D., Xie, X., St. Pierre, J., Sihag, S., Yang, W., Altshuler, D., Puigserver, P., Pattersom, N., et al. (2004) Err(alpha) and Gabpa/b specify PGC-1 (alpha)-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. U. S. A. 101, 6570-6575
27. Schreiber, S.N., Emter, R., Hock, M. B., Knutti, D., Cardenas, J., Podvinec, M., Oakeley, E. J., and Kralli, A. (2004) The estrogenrelated receptor α (ERRα) functions in PPARγ coactivator 1α (PGC-1α)-induced miochondrial biogenesis. Proc. Natl. Acad. Sci. U. S. A. 101, 6472-6477
28. Zhang, Y., Ma, K., Song, S., Elam, M. B., Cook, G. A., and Park, E. A. (2004) Peroxisomal proliferators-activated receptor gamma coactivator-1 alpha (PGC-1alpha) enhances the thyroid hormone induction of carnitine palmitoyl transferase I (CPT-I alpha). J. Biol. Chem. 279, 53963-53971
29. Kelly, D. P., and Scarpulla, R. C. (2004) Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18, 357-368
30. Puigserver, P., and Spiegelman, B. M. (2003) Peroxisome proliferators-activated receptor-gamma coactivator 1 alpha (PGC-1alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90
31. Barish, G. D., Narkar, V. H., and Evans, R. M. (2006) PPARδ: a dagger in the heart of the metabolic syndrome. J. Clin. Invest. 116, 590-597
32. Reznick, R. M., and Shulman, G. I. (2006) The role of AMP-activated protein kinase in mitochondrial biogenesis. J. Physiol. 574, 33-39
33. Lin, J., Wu, H., Tarr, P. T., Zhang, C.-Y., Wu, Z., Boss, O., Michael, L. F., Puigserver, P., Isotani, E., Olson, E. N., et al. (2002) Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibers. Nature 419, 797-801
34. Wang, Y.X., Zhang, C.-L., Yu, R. T., Cho, H. K., Nelson, M. C., Bayugu-Ocampo, C. R., Ham, J., Kang, H., and Evans, R. M. (2004) Regulation of muscle fiber-type and running endurance by PPARδ. PloS. Biol. 2, e294
35. Leone, T. C., Lehman, J. J., Finck, B. N., Schaeffer, P. J., Wende, A. R., Boudina, S., Courtois, M., Wozniak, D. F., Sambandam, N., Bernal-Mizrachi, C., et al. (2005) PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PloS Biol. 3, e101
36. Vescovo, G., Ravara, B., Gobbo, V., Angelini, A., and Dalla Libera, L. (2005) Skeletal muscle fibres synthesis in heart failure: role of PGC-1alpha, calcineurin and GH. Int. J. Cardiol. 104, 298-306
37. Irrcher, I., Adhihetty, P. J., Sheehan, T., Joseph, A. M., and Hood, D. A. (2003) PPAR gamma coactivator-1 alpha expression during thyroid hormone- and contractile activity- induced mitochondrial adaptations. Am. J. Physiol. Cell. Physiol. 284, C1699-C1677
38. Terada, S., Goto, M., Kato, M., Kawanaka, K., Shimokawa, T., and Tabata, I. (2002) Effects of low-intensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle. Biochem. Biophys. Res. Commun. 296, 350-354
39. Zong, H., Ren., J. M., Young, L. H., Pypaert, M., Mu, J., Birnbaum, M. J., and Shulman, G. I. (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc. Natl. Acad. Sci. U. S. A. 25, 15983-15987
40. Jobgen, W. S., Fried, S. K., Fu, W. J., Meininger, C. J., and Wu, G. (2006) Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J. Nutr. Biochem. 17, 571-588
41. Escher, P., Braissant, O., Basu-Modak, S., Michalik, L., Wahli, W., and Desvergne, B. (2001) Rat PPARs: Quantitative analysis in adult rat tissues and regulation in fasting and refeeding. Endocrinology 142, 4195-4202
42. Luquet, S., Lopez-Soriano, J., Holst, D., Fredenrich, A., Malki, J., Rassoulzadegan, M., and Grimaldi, P. A. (2003) Peroxisome proliferator-activated receptor δ controls muscle development and oxidative capability. FASEB J. 17, 2299-2301
43. Brunmair, B., Staniek, K., Dorig, J., Szocs, Z., Stadlbauer, K., Marian, V., Gras, F., Anderwald, C., Nohl, H., Waldhsausl, W., et al. (2006) Activation of PPAR-delta in isolated rat skeletal muscle switches fuel preference from glucose to fatty acids. Diabetologia 49, 2713-2722
44. Tanaka, T., Yamamoto, J., Iwasaki, S., Asaba, H., Hamura, H., Ikeda, Y., Watanabe, M., Magoori, K., Ioka, R. X., Tachibana, K., et al. (2003) Activation of peroxisome proliferators-activated receptor δ induces fatty acid - oxidation in skeletal muscle and attenuates metabolic syndrome. Proc. Natl. Acad. Sci. U. S. A. 100, 15924-15929
45. Tsintzas, K., Jewell, K., Kamran, M., Laithwaite, D., Boonsong, T., Littlewood, J., MacDonald, I., and Bennet, A. (2006) Differential regulation of metabolic genes in skeletal muscle during starvation and refeeding in humans. J. Physiol. 575, 291-303
46. Holst, D., Luquet, S., Nogueira, V., Kristiansen, K., Leverve, X., and Grimaldi, P. A. (2003) Nutritional regulation and role of peroxisome proliferators-activated receptor delta in fatty acid catabolism in skeletal muscle. Biochim. Biophys. Acta 1633, 43-50
47. Stavinoha, M. A., RaySpellicy, J. W., Essop, M. F., Graveleau, C., Abel, E. D., Hart-Sailors, M. L., Mersmann, H. J., Bray, M. S., and Young, M. E. (2004) Evidence for mitochondrial thioesterase 1 as a peroxisome proliferator-activated receptor alpha-regulated gene in cardiac and skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 287, E888-E895
48. Watt, M. J., Southgate, R. J., Holmes, A. G., and Febbraio, M. A. (2004) Suppression of plasma free fatty acids upregulates peroxisome proliferators-activated (PPAR) alpha and delta and PPAR coactivator 1 alpha in human skeletal muscle, but not lipid regulatory genes. J. Mol. Endocrinol. 33, 533-544
49. Mahoney, D. J., Parise, G., Melov., S., Safidar, A., and Tarnopolky, M. A. (2005) Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 19, 1498-1500
50. Hawley, S.A., Boudeau, J., Reid, J. L., Mustard, K. J., Udd, L., Makela, T. P., Alessi, D. R., and Hardie, D. G. (2003) Complexes between the LKB1 tumor suppressor, STRAD α/-β and MO25 α/β- are upstream kinases in the AMP-activated protein kinase cascade. J. Biol. 2, 28
51. Sakamoto, K., Zarrinpashneh, E., Budas, G. R., Pouleur, A. C., Dutta, A., Prescott, A. R., Ashworth, A., Jovanovic, A., Alessi, D. R., and Bertrand, L. (2006) Deficiency of LKB1 in heart prevents ischemia-mediated activation of AMPKα2 but not AMPKα1. Am. J. Physiol. Endocrinol. Metab. 290, E780-E788
52. Lizcano, J. M., Goransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Makela, T. P., Hardie, D. G., et al. (2004) LKB is a master kinase that activates 13 protein kinases of the AMPK subfamily, including the MARK/PAR-1 kinases. EMBO J. 23, 833-843
53. Sakamoto, K., Goransson, O., Hardie, D. G., and Alessi, D. R. (2004) Activity of LKB1 and AMPK-related kinases in skeletal muscle: effects of contraction, phenformin, and AICAR. Am. J. Physiol. Endocrinol. Metab. 287, E310-E317
54. Winder, W. W., Hardie, D. G., Mustard, K.J., Greenwood, L. J., Paxton, B. E., Park, S. H., Rubink, D. S., and Taylor, E. B. (2003) Long-term regulation of AMP-activated protein kinase and acetyl-CoA carboxylase in skeletal muscle. Biochem. Soc. Trans. 31, 182-185
55. Park, H., Kaushik, V. K., Constant, S., Prentki, M., Przybytkowski, E., Ruderman, N. B., and Saha, A. K. (2002) Coordinate regulation of malonyl-CoA decarboxylase, sn-glycerol-3-phosphate acyltransferase, and acetyl-CoA carboxylase by AMP-activated protein kinase in rat tissues in response to exercise. J. Biol. Chem. 277, 32571-32577
56. Long, Y. C., Barnes, B. R., Mahlapuu, M., Steiler, T. L., Martinsson, S., Leng, Y., Wallberg-Hendriksson, H., Andersson, L., and Zierath, J. R. (2005) Role of AMP-activated protein kinase in the coordinated expression of genes controlling glucose and lipid metabolism in mouse white skeletal muscle. Diabetologia 48, 2354-2365
57. Jorgensen, S. B., Wojtaszewski, J. F., Viollet, B., Andreelli, F., Birk, J. B., Hellsten, Y., Schjerling, P., Vaulont, S., Neufer, P. D., Richter, E. A., et al. (2005) Effects of α-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J. 19, 1146-1148
58. Itani, S. I., Saha, A. K., Kurowski, T. G., Coffin, H. R., Tornheim, K., and Ruderman, N. B. (2003) Glucose autoregulates its uptake in skeletal muscle. Diabetes 53, 1635-1640
59. Jing, M., and Ismail-Beigi, F. (2007) Critical role of 5′-AMP-activated protein kinase in the stimulation of glucose transport in response to inhibition of oxidative phosphorylation. Am. J. Physiol. Cell. Physiol. 292, C477-C487
60. Lin, J., Wu, P. H., Tarr, P. T., Lindenberg, K. S., St-Pierre, J., Zhang, W., Mootha, V. K., Jager, S., Vianna, C. R., Reznick, R. M., et al. (2004) Defects in adaptative energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119, 121-135
61. Sriwijitkamol, A., Ivy, J. L., Christ-Roberts, C., Defronzo, R. A., Mandarino, L. J., and Musi, N. (2006) LKB1-AMPK signaling in muscle from obese insulin-resistant Zucker rats and effects of training. Am. J. Physiol. Endocrinol. Metab. 290, E925-E932
62. Liu, Y., Wan, Q., Guan, Q., Gao, L., and Zhao, J. (2006) High-fat diet feeding impairs both the expression and activity of AMPKα in rats' skeletal muscle. Biochem. Biophys. Res. Commun. 339, 701-707
63. Hojlund, K., Mustard, K. J., Staehr, P., Hardie, D. G., Beck-Nielsen, H., Richter, E. A., and Wojtaszweski, J. F. (2004) AMPK activity and subunit protein expression are similar in muscle of obese subjects with and without type 2 diabetes. Am. J. Physiol. Endocrinol. Metab. 286, E239-E244
64. Steinberg, G. R., Smith, A. C., Van Denderen, B. J., Chen, Z., Murthy, S., Campbell, D. J., Heigenhauser, G. J., Dyck, D. J., and Kemp, B. E. (2004) AMP-activated protein kinase is not downregulated in human skeletal muscle of obese females. J. Clin. Endocrinol. Metab. 89, 4575-4580
65. Sriwijitkamol, A., Coletta, D. K., Wajcberg, E., Balbontin, G. B., Reyna, S. M., Barrientes, J., Eagan, P. A., Jenkinson, C. P., Cersosimo, E., Defronzo, R. A., et al. (2007) Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: A time-course and dose-response study. Diabetes 56, 836-848
66. Gonzalez, A. A., Kumar, R., Mulligan, J. D., Davis, A. J., Weindruch, R., and Saupe, K. (2004) Metabolic adaptations to fasting and chronic caloric restriction in heart, muscle and liver do not include changes in AMPK activity. Am. J. Physiol. Endocrinol. Metab. 287, R1270-1275
67. Furuyama, T., Kitamaya, K., Yamashita, H., and Mori, N. (2003) Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem. J. 375, 365-371
68. Sugden, M. C., Howard, R. M., Munday, M. R., and Holness, M. J. (1993) Mechanisms involved in the coordinated regulation of strategic enzymes of glucose metabolism. Ad. Enzyme Regul. 33, 71-95
69. Heilbronn, L. K., Civitarese, A. E., Bogacka, I., Smith, S. R., Hulver, M., and Ravussin, E. (2005) Glucose tolerance and skeletal muscle gene expression in response to alternate day fasting. Obes. Res. 13, 574-581
70. Nisoli, E., Clementi, E., Paolucci, C., Cozzi, V., Tonello, C., Sciorinati, C., Bracale, R., Valerio, A., Francolini, M., Moncada, S., et al.(2003) Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299, 896-899
71. Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., et al. (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310, 314-317
72. Sauve, A. A., Wolberger, C., Schramm, V. L., and Boeke, J. D. (2006) The biochemistry of sirtuins. Annu. Rev. Biochem. 75, 435-465
73. Gerhart-Hines, Z., Rodgers, J. T., Bare, O., Lerin, C., Kim, S. H., Mostoslavsky, R., Alt, F. W., Wu, Z., and Puigserver, P. (2007) Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J. 26, 1913-1923
74. Lagouge, M., Argmann, C., Gerhart-Hines, Z., Meziane, H., Lerin, C., Daussin, F., Messadeq, N., Milne, J., Lambert, P., Elliott, P., et al. (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell 127, 1109-1122
75. Shi, T., Wang, F., Stieren, E., and Tong, Q. (2005) SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J. Biol. Chem. 14, 13560-13567
76. Mornagui, B., Grissa, A., Duvareille, M., Gharib, C., Kamoun, A., El-Fazaa, S., and Gharbi, N. (2006) Vasopressin and nitric oxide synthesis after three days of water or food deprivation. Acta Biol. Hung. 57, 1-11
77. Chen, Z. P., McConell, G. K., Michell, B. J., Snow, R. J., Canny, B. J., and Kemp, B. E. (2000) AMPK signaling in contracting human skeletal muscle. Acetyl-CoA carboxylase and NO synthase phosphorylation. Am. J. Physiol. Endocrinol. Metab. 279, E1202-E1206
78. Stephens, T. J., Canny, B. J., Snow, R. J., and McConell, G. K. (2004) 5′-aminoimidazole-4-carboxyamide-ribonucleoside-activated glucose transport is not prevented by nitric oxide synthase inhibition in rat isolated skeletal muscle. Clin. Exp. Pharmacol. Physiol. 31, 419-423
79. Zou, M. H., Hou, X. Y., Shi, M., Kirkpatrick, S., Liu, F., Goldman, M. H., and Cohen, R. A. (2003) Activation of 5′AMP-activated kinase is mediated through c-Scr and phosphoinositide 3-kinase activity during hypoxia-reoxygenation of bovine aortic endothelial cells. Role of peroxynitrite. J. Biol. Chem. 279, 20767-20774
80. Shearer, J., Fueger, P. T., Vorndick, B., Bracy, D. P., Rottman, J. N., Clanton, J. A., and Wasserman, D. H. (2004) AMP kinase-induced skeletal muscle glucose but not long-chain fatty acid uptake is dependent on nitric oxide. Diabetes 53, 1429-1435
81. Jungas, R. L., Halperin, M. L., and Brosnan, J. T. (1992) Quantitative analysis of amino acid oxidation and related gluconeogenesis in humans. Physiol. Rev. 72, 419-448
82. Rasmussen, B. B., and Wolfe, R. R. (1999) Regulation of fatty acid oxidation in skeletal muscle. Annu. Rev. Nutr. 19, 463-484
83. Ruderman, N. B., Saha, A. K., and Kragen, E. W. (2003) Minireview: Malonyl CoA, AMP-activated protein kinase, and adiposity. Endocrinology 144, 5166-5177
84. Bonen, A., Luiken, J. J., Arumugam, Y., Glatz, J. F., and Tandon, N. (2000) Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. J. Biol. Chem. 275, 14501-14508
85. Luiken, J. J., Coort, S. L. M., Willems, J., Coumans, W. A., Bonen, A., van der Vusse, G. J., and Glatz, J. F. (2003) Contraction-induced fatty acid translocase/CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling. Diabetes 52, 1627-1634
86. Campbell, S. A., Tandon, N. A., Woldegiorgis, G., Luiken, J. J. F. P., Glatz, J. F. C., and Bonen, A. (2004) A novel function for fatty acid translocase (FAT)/CD36. J. Biol. Chem. 279, 36235-36241
87. Bezaire, V., Spriet, L. L., Campbell, S., Sabet, N., Gerrits, M., Bonen, A., and Harper, M. E. (2005) Constitutive UCP3 overexpression at physiological levels increases mouse skeletal muscle capacity for fatty acid transport and oxidation. FASEB J. 19, 977-979
88. MacLellan, J. D., Gerrits, M. F., Gowing, A., Smith, P. J. S., Wheeler, M. B., and Harper, M. E. (2005) Physiological increases in uncoupling protein 3 augment fatty acid oxidation and decrease reactive oxygen species production without uncoupling respiration in muscle cells. Diabetes 54, 2343-2350
89. Goglia, F., and Skulachev, V. P. (2003) A function for novel uncoupling proteins: antioxidant defense of mitochondrial matrix by translocating fatty acid peroxides from the inner to the outer membrane leaflet. FASEB J. 17, 1585-1591
90. Solanes, G., Pedraza, N., Iglesias, R., Giralt, M., and Villaroya, F. (2000) The human uncoupling protein-3 gene promoter requires MyoD and is induced by retinoic acid in muscle cells. FASEB J. 14, 2141-2143
91. Solanes, G., Pedraza, N., Iglesias, R., Giralt, M., and Villarroya, F. (2003) Functional relationship between MyoD and peroxisome proliferator- activated receptor-dependent regulatory pathways in the control of the human uncoupling protein-3 gene transcription. Mol. Endocrinol. 217, 1944-1958
92. Kong, Y., Flick, M. J., Kudla, A. J., and Konieczny, S. F. (1997) Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD. Mol. Cell. Biol. 17, 4750-4769
93. Khurana, T., Khurana, B., and Noegel, A. A. (2002) LIM proteins: association with the actin cytoskeleton. Protoplasma 219, 1-12
94. Schrauwen, P., Hardie, D. G., Boorda, B., Clapham, J. C., Abuin, A., Thomason-Hughes, M., Green, K., Frederik, P. M., and Hesselink, M. K. (2004) Improved glucose homeostasis in mice overexpressing human UCP3: a role for AMP kinase? Int. J. Obes. 28, 824-828
95. Freyssenet, D. (2007) Energy sensing and regulation of gene expression in skeletal muscle J. Appl. Physiol. 102, 529-540
96. 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
97. Petersen, K. F., and Shulman, G. I. (2006) Etiology of insulin resistance. Am. J. Med. 119, 10S-16S