Erratum: Muscle uncoupling protein 3 overexpression mimics endurance training and reduces circulating biomarkers of incomplete β-oxidation (FASEB Journal (2013) 27 (4213- 4225) DOI: 10.1096/fj.13-234302);Muscle uncoupling protein 3 overexpression mimics endurance training and reduces circulating biomarkers of incomplete β-oxidation

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 4213-4225

  Aguer, Céline ^a   Fiehn, Oliver ^c   Seifert, Erin L ^a   Bézaire, Véronic ^e   Meissen, John K ^c   Daniels, Amanda ^a   Scott, Kyle ^a   Renaud, Jean Marc ^a   Padilla, Marta ^a,b   Bickel, David R ^a,b   Dysart, Michael ^a   Adams, Sean H ^c,d   Harper, Mary Ellen ^a,b,f  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

^e CARLETON UNIVERSITY   (Canada)

^f THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Acylcarnitines; Exercise mimetic; Fatty acid oxidation; Mitochondria; Oxidative stress

Indexed keywords

ACETYLCARNITINE; ACYLCARNITINE; BIOLOGICAL MARKER; CARNITINE ACETYLTRANSFERASE; CARNITINE PALMITOYLTRANSFERASE; UNCOUPLING PROTEIN 3; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY MASS; BODY WEIGHT; CALORIC INTAKE; CONTROLLED STUDY; ENDURANCE TRAINING; ENERGY EXPENDITURE; ENZYME ACTIVITY; FATTY ACID OXIDATION; FOOD INTAKE; GASTROCNEMIUS MUSCLE; GENOTYPE; INSULIN SENSITIVITY; LOCOMOTION; MALE; METABOLIC DISORDER; MOUSE; MUSCLE FATIGUE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLEUS MUSCLE; TIBIALIS ANTERIOR MUSCLE; TREADMILL EXERCISE; WEIGHT REDUCTION; WHITE ADIPOSE TISSUE; WILD TYPE; ANIMAL; EATING; ENDURANCE; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SKELETAL MUSCLE; TRANSGENIC MOUSE;

MUS;

ANIMALS; BIOLOGICAL MARKERS; EATING; ENERGY METABOLISM; GENE EXPRESSION REGULATION; ION CHANNELS; MALE; MICE; MICE, TRANSGENIC; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE;

EID: 84885134786     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-234302ERR     Document Type: Erratum

References (55)

1. Pedersen, B. K., and Saltin, B. (2006) Evidence for prescribing exercise as therapy in chronic disease. Scand. J. Med. Sci. Sports 16(Suppl. 1), 3-63
2. Egan, B., and Zierath, J. R. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17, 162-184
3. Knowler, W. C, Barrett-Connor, E., Fowler, S. E., Hamman, R. F., Lachin, J. M., and Nathan, D. M. (2002) Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N. Engl. J. Med. 346, 393-403
4. Calvo, J. A, Daniels, T. G., Wang, X., Paul, A, Lin, J., Spiegelman, B. M., Stevenson, S. C, and Rangwala, S. M. (2008) Muscle-specific expression of PPARγ coactivator-1α improves exercise performance and increases peak oxygen uptake. J. Appl. Physiol. 104, 1304-1312
5. Bostrom, P., Wu, J., Jedrychowski, M. P., Korde, A, Ye, L., Long, J. Z., Kajimura, S., Zingaretti, M. C, Vind, B. F., Tu, H., Cinti, S., Hojlund, K., Gygi, S. P., and Spiegelman, B. M. (2012) A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463-468
6. Narkar, V. A, Downes, M., Yu, R. T., Embler, E., Wang, Y. X., Mihaylova, M. M., Nelson, M. C, Zou, Y., Juguilon, H., Kang, H., Shaw, R. J., and Evans, R. M. (2008) AMPK and PPARδ agonists are exercise mimetics. Cell 134, 405-415
7. Anderson, E. J., Lustig, M. E., Boyle, K. E., Woodlief, T. L., Price, J. W., 3rd, Kang, L., Rabinovitch, P. S., Szeto, H. H., Houmard, J. A, Cortright, R. N., Wasserman, D. H., and Neufer, P. D. (2009) Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J. Clin. Invest. 119, 573-581
8. Houstis, N., Rosen, E. D., and Lander, E. S. (2006) Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440, 944-948
9. Powers, S. K., Kavazis, A. N., and McClung, J. M. (2007) Oxidative stress and disuse muscle atrophy. J. Appl. Physiol. 102, 2389-2397
10. Di Meo, S., and Venditti, P. (2001) Mitochondria in exerciseinduced oxidative stress. Biol. Signals Recept. 10, 125-140
11. Pecqueur, C., Couplan, E., Bouillaud, F., and Ricquier, D. (2001) Genetic and physiological analysis of the role of uncoupling proteins in human energy homeostasis. J. Mol. Med. 79, 48-56
12. Toime, L. J., and Brand, M. D. (2010) Uncoupling protein-3 lowers reactive oxygen species production in isolated mitochondria. Free Radic. Biol. Med. 49, 606-611
13. Anderson, E. J., Yamazaki, H., and Neufer, P. D. (2007) Induction of endogenous uncoupling protein 3 suppresses mitochondrial oxidant emission during fatty acid-supported respiration. J. Biol. Chem. 282, 31257-31266
14. MacLellan, J. D., Gerrits, M. F., Gowing, A, Smith, P. J., 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
15. Bezaire, V., Spriet, L. L., Campbell, S., Sabet, N., Bonen, A, and Harper, M. E. (2005) Constitutive UCP3 over-expression at physiological levels increases mouse skeletal muscle capacity for fatty acid transport and oxidation. FASEB J. 19, 977-979
16. Costford, S. R, Chaudhry, S. N., Salkhordeh, M., and Harper, M. E. (2006) Effects of the presence, absence, and overexpression of uncoupling protein-3 on adiposity and fuel metabolism in congenic mice. Am. J. Physiol. Endocrinol. Metab. 290, E1304-E1312
17. Choi, C. S., Fillmore, J. J., Kim, J. K., Liu, Z. X., Collier, E. F., Kulkarni, A, Distefano, A, Hwang, Y. J., Kahn, M., Chen, Y, Yu, C, Moore, I. K., Reznick, R. M., Higashimori, T., and Shulman, G. I. (2007) Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J. Clin. Invest. 117, 1995-2003
18. Clapham, J. C, Arch, J. R, Chapman, H., Haynes, A, Lister, C, Moore, G. B., Piercy, V., Carter, S. A, Lehner, I., Godden, R. J., Herrity, N., Skehel, M., Changani, K. K., Hockings, P. D., Reid, D. G., Squires, S. M., Hatcher, J., Trail, B., Latcham, J., Rastan, S., Harper, A. J., Cadenas, S., Buckingham, J. A, Brand, M. D., and Abuin, A. (2000) Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406, 415-418
19. Leick, L., Wojtaszewski, J. F., Johansen, S. T., Kiilerich, K., Hellsten, Y., Hidalgo, J., and Pilegaard, H. (2008) PGC-1a is not mandatory for exercise-and training-induced adaptive gene responses in mouse skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 294, E463-E474
20. Cifelli, C., Bourassa, F., Gariepy, L., Banas, K., and Renaud, J. M. (2007) KATP channel deficiency in mouse flexor digitorum brevis causes fibre damage and impairs Ca + release and force development during fatigue in vitro. J. Physiol. 582, 843-857
21. Estey, C., Seifert, E. L., Aguer, C., Moffat, C, and Harper, M. E. (2012) Calorie restriction in mice overexpressing UCP3: evidence that prior mitochondrial uncoupling alters response. Exp. Gerontol. 47, 361-371
22. Gerrits, M. F., Ghosh, S., Kavaslar, N., Hill, B., Beauchamp, B., Gorman, S., Stuart, J., Dent, R, McPherson, R, and Harper, M. E. Distinct skeletal muscle fiber characteristics and gene expression in diet-sensitive versus dietresistant obesity. J. Lipid Res. 51, 2394-2404
23. Seifert, E. L., Fiehn, O., Bezaire, V., Bickel, D. R, Wohlgemuth, G, Adams, S. H., and Harper, M. E. (2010) Long-chain fatty acid combustion rate is associated with unique metabolite profiles in skeletal muscle mitochondria. PLoS One 5, e9834
24. Mailloux, R. J., Adjeitey, C. N., Xuan, J. Y., and Harper, M. E. (2011) Crucial yet divergent roles of mitochondrial redox state in skeletal muscle vs. brown adipose tissue energetics. FASEB J. 26, 363-375
25. Baillet, L., Mullur, R. S., Esser, V., and McGarry, J. D. (2000) Elucidation of the mechanism by which (+)-acylcarnitines inhibit mitochondrial fatty acid transport. J. Biol. Chem. 275, 36766-36768
26. Aguer, C., Mercier, J., Man, C. Y, Metz, L., Bordenave, S., Jean, E., Lantier, L., Bounoua, L., Brun, J. F., Raynaud De Mauverger, E., Andreelli, F., Foretz, M., and Kitzmann, M. (2010) Intramyocellular lipid accumulation is associated with permanent relocation ex vivo and in vitro of fatty acid translocase (FAT)/CD36 in obese patients. Diabetologia 53, 1151-1163
27. Jaudzems, K., Kuka, J., Gutsaits, A, Zinovjevs, K., Kalvinsh, I., and Dambrova, M. (2009) Inhibition of carnitine acetyltransferase by mildronate, a regulator of energy metabolism. J. Enzyme Inhib. Med. Chem. 24, 1269-1275
28. Mailloux, R. J., Dumouchel, T., Aguer, C., De Kemp, R, Beanlands, R, and Harper, M. E. (2011) Hexokinase II acts through UCP3 to suppress mitochondrial reactive oxygen species production and maintain aerobic respiration. Biochem. J. 437, 301-311
29. Glatz, J. F., Jacobs, A. E., and Veerkamp, J. H. (1984) Fatty acid oxidation in human and rat heart. Comparison of cell-free and cellular systems. Biochim. Biophys. Acta 794, 454-465
30. Veerkamp, J. H., Van Moerkerk, H. T., Glatz, J. F., and Van Hinsbergh, V. W. (1983) Incomplete palmitate oxidation in cell-free systems of rat and human muscles. Biochim. Biophys. Acta 753, 399-410
31. Kitzmann, M., Lantier, L., Hebrard, S., Mercier, J., and Aguer, C. (2011) Abnormal metabolism flexibility in response to high palmitate concentrations in myotubes derived from obese type 2 diabetic patients. Biochim. Biophys. Acta 1812, 423-430
32. Efron, B. (2004) Large-scale simultaneous hypothesis testing: the choice of a null hypothesis. J. Am. Stat. Assoc. 99, 96-104
33. Bickel, D. R. (2013) Simple estimators of false discovery rates given as few as one or two p-values without strong parametric assumptions. [E-pub ahead of print] Stat. Appl. Genet. Mol. Biol. doi: 10.1515/sagmb-2013-0003
34. Efron, B., Turnbull, B., and Narasimhan, B. (2011) locfdr: Computes local false discovery rates. R package version 1.1-7. R Foundation for Statistical Computing, Vienna, Austria
35. Padilla, M., and Bickel, D. R. (2012) Empirical Bayes methods corrected for small number of tests. Stat. Appl. Genet. Mol. Biol. 11, 4
36. Efron, B. L. (2010) Large-scale inference: empirical Bayes methods for estimation, testing, and prediction. Cambridge University Press, Cambridge, UK
37. Bickel, D. R. (2004) Error-rate and decision-theoretic methods of multiple testing: which genes have high objective probabilities of differential expression? Stat. Appl. Genet. Mol. Biol. 3, Article8
38. Holloszy, J. O., and Coyle, E. F. (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. 56, 831-838
39. Majerczak, J., Rychlik, B., Grzelak, A., Grzmil, P., Pierzchalski, P., Pulaski, L., Bartosz, G., and Zoladz, J. A. (2010) Effect of 5-week moderate intensity endurance training on the oxidative stress, muscle specific uncoupling protein (UCP3) and superoxide dismutase (SOD2) contents in vastus lateralis of young, healthy men. J. Physiol. Pharmacol. 61, 743-751
40. Dekany, M., Nemeskeri, V., Gyore, I., Harbula, I., and Pucsok, J. (2006) Antioxidant status of interval-trained athletes in various sports. Int. J. Sports Med. 27, 112-116
41. Hollander, J., Fiebig, R., Gore, M., Ookawara, T., and Ji, L. L. (2001) Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflugers Arch. 442, 426-434
42. Hitomi, Y., Watanabe, S., Kizaki, T., Sakurai, T., Haga, S., Ookawara, T., Suzuki, K., and Ohno, H. (2008) Acute exercise increases expression of extracellular superoxide dismutase in skeletal muscle and the aorta. Redox Rep. 13, 213-216
43. Pimenta Ada, S., Lambertucci, R. H., Gorjao, R., Silveira Ldos, R., and Curi, R. (2007) Effect of a single session of electrical stimulation on activity and expression of citrate synthase and antioxidant enzymes in rat soleus muscle. Eur. J. Appl. Physiol. 102, 119-126
44. Steinberg, J., Gainnier, M., Michel, F., Faucher, M., and Jammes, Y. (2002) The post-exercise oxidative stress is depressed by acetylsalicylic acid. Respir. Physiol. Neurobiol. 130, 189-199
45. Jones, R. E., Askew, E. W., Hecker, A. L., and Hofeldt, F. D. (1981) Salicylic acid stimulation of palmitic acid oxidation by rat skeletal muscle mitochondria. Biochim. Biophys. Acta 666, 120-126
46. Hawley, S. A., Fullerton, M. D., Ross, F. A., Schertzer, J. D., Walker, K. J., Peggie, M. W., Zibrova, D., Green, K. A., Mustard, K. J., Kemp, B. E., Sakamoto, K, Steinberg, G. R., and Hardie, D. G. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 336, 918-922
47. Jorgensen, T. G., Weis-Fogh, U. S., Nielsen, H. H., and Olesen, H. P. (1976) Salicylate-and aspirin-induced uncoupling of oxidative phosphorylation in mitochondria isolated from the mucosal membrane of the stomach. Scand. J. Clin. Lab. Invest. 36, 649-654
48. Senese, R., Valli, V., Moreno, M., Lombardi, A., Cioffi, F., Silvestri, E., Goglia, F., Lanni, A., and De Lange, P. (2011) Uncoupling protein 3 expression levels influence insulin sensitivity, fatty acid oxidation, and related signaling pathways. Pflugers Arch. 461, 153-164
49. Argyropoulos, G., Brown, A. M., Willi, S. M., Zhu, J., Reitman, M., Gevao, S. M., Spruill, I., and Garvey, W. T. (1998) Effects of mutations in the human uncoupling protein 3 gene on the respiratory quotient and fat oxidation in severe obesity and type 2 diabetes. J. Clin. Invest. 102, 1345-1351
50. Koves, T. R., Ussher, J. R., Noland, R. C., Slentz, D., Ilkayeva, O., Bain, J., Stevens, R., Dyck, J. R., Newgard, C. B., Lopaschuk, G. D., and Muoio, D. M. (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 7, 45-56
51. Adams, S. H., Hoppel, C. L., Lok, K. H., Zhao, L., Minkler, P. E., Hwang, D. H., Newman, J. W., and Garvey, W. T. (2009) Plasma acylcarnitine profiles suggest incomplete longchain fatty acid β-oxidation and altered tricarboxylic acid cycle activity in type 2 diabetic African-American women. J. Nutr. 139, 1073-1081
52. Lehmann, R., Zhao, X., Weigert, C., Simon, P., Fritsche, J., Machann, J., Schick, F., Wang, J., Hoene, M., Schleicher, E. D., Haring, H. U., Xu, G., and Niess, A. M. (2010) Medium chain acylcarnitines dominate the metabolite pattern in humans under moderate intensity exercise and support lipid oxidation. PloS One 5, e11519
53. Thyfault, J. P., Cree, M. G., Tapscott, E. B., Bell, J. A., Ilkayeva, O., Wolfe, R. R., Dohm, G. L., and Muoio, D. M. (2010) Metabolic profiling of muscle contraction in lean compared with obese rodents. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R926-R934
54. Jong-Yeon, K, Hickner, R. C., Dohm, G. L., and Houmard, J. A (2002) Long-and medium-chain fatty acid oxidation is increased in exercise-trained human skeletal muscle. Metabolism 51, 460-464
55. Muoio, D. M., Noland, R. C, Kovalik, J. P., Seiler, S. E., Davies, M. N., Ilkayeva, O. R., Stevens, R. D., Kheterpal, I., Zhang, J., Covington, J. D., Bajpeyi, S., Ravussin, E., Kraus, W., Koves, T. R., and Mynatt, R. L. (2012) Muscle-specific deletion of carnitine acetyltransferase compromises glucose tolerance and metabolic flexibility. Cell Metab. 15, 764-777