AMP-activated protein kinase controls exercise training- and AICAR-induced increases in SIRT3 and MnSOD

Frontiers in Physiology

Volumn 6, Issue MAR, 2015, Pages

  Brandauer, Josef ^a,b   Andersen, Marianne A ^a   Kellezi, Holti ^a   Risis, Steve ^a   Frøsig, Christian ^c   Vienberg, Sara G ^a   Treebak, Jonas T ^a  

^a Capital Region   (Denmark)

^b GETTYSBURG COLLEGE   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

AMPK; Exercise training; Mitochondrial biogenesis; MnSOD; OSCP; ROS; SIRT3; SOD2

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SIRTUIN 3;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXERCISE; FEMALE; HUMAN; HUMAN EXPERIMENT; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; NORMAL HUMAN; POLYMERASE CHAIN REACTION; QUADRICEPS FEMORIS MUSCLE; VASTUS LATERALIS MUSCLE; WESTERN BLOTTING; WILD TYPE;

EID: 84926456354     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00085     Document Type: Article

References (63)

1. Abbott, M. J., and Turcotte, L. P. (2014). AMPK-α2 is involved in exercise training-induced adaptations in insulin-stimulated metabolism in skeletal muscle following high-fat diet. J. Appl. Physiol. 117, 869-879. doi: 10.1152/japplphysiol.01380.2013
2. Ahn, B.-H., Kim, H.-S., Song, S., Lee, I. H., Liu, J., Vassilopoulos, A., et al. (2008). A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. U.S.A. 105, 14447-14452. doi: 10.1073/pnas.0803790105
3. Andersen, P., Adams, R. P., Sjogaard, G., Thorboe, A., and Saltin, B. (1985). Dynamic knee extension as model for study of isolated exercising muscle in humans. J. Appl. Physiol. 59, 1647-1653.
4. Bai, P., Cantó, C., Oudart, H., Brunyánszki, A., Cen, Y., Thomas, C., et al. (2011). PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 13, 461-468. doi: 10.1016/j.cmet.2011.03.004
5. Bamford, J. A., Lopaschuk, G. D., MacLean, I. M., Reinhart, M. L., Dixon, W. T., and Putman, C. T. (2003). Effects of chronic AICAR administration on the metabolic and contractile phenotypes of rat slow- and fast-twitch skeletal muscles. Can. J. Physiol. Pharmacol. 81, 1072-1082. doi: 10.1139/y03-110
6. Brandauer, J., Vienberg, S. G., Andersen, M. A., Ringholm, S., Risis, S., Larsen, P. S., et al. (2013). AMP-activated protein kinase regulates nicotinamide phosphoribosyl transferase expression in skeletal muscle. J. Physiol. 591(Pt 20), 5207-5220. doi: 10.1113/jphysiol.2013.259515
7. 5 is under the control of PGC-1α and AMPK and is involved in regulation of mitochondrial energy metabolism. FASEB J. 28, 3225-3237. doi: 10.1096/fj.13-245241
8. Cantó, C., Gerhart-Hines, Z., Feige, J. N., Lagouge, M., Noriega, L., Milne, J. C., et al. (2009). AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458, 1056-1060. doi: 10.1038/nature07813
9. Cantó, C., Jiang, L. Q., Deshmukh, A. S., Mataki, C., Coste, A., Lagouge, M., et al. (2010). Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab. 11, 213-219. doi: 10.1016/j.cmet.2010.02.006
10. Chabi, B., Adhihetty, P. J., O'Leary, M. F. N., Menzies, K. J., and Hood, D. A. (2009). Relationship between Sirt1 expression and mitochondrial proteins during conditions of chronic muscle use and disuse. J. Appl. Physiol. 107, 1730-1735. doi: 10.1152/japplphysiol.91451.2008
11. Chen, Y., Zhang, J., Lin, Y., Lei, Q., Guan, K.-L., Zhao, S., et al. (2011). Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 12, 534-541. doi: 10.1038/embor.2011.65
12. Egan, B., and Zierath, J. R. (2013). Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17, 162-184. doi: 10.1016/j.cmet.2012.12.012
13. Frøsig, C., Jørgensen, S. B., Hardie, D. G., Richter, E. A., and Wojtaszewski, J. F. P. (2004). 5'-AMP-activated protein kinase activity and protein expression are regulated by endurance training in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 286, E411-E417. doi: 10.1152/ajpendo.00317.2003
14. Geng, T., Li, P., Okutsu, M., Yin, X., Kwek, J., Zhang, M., et al. (2010). PGC-1alpha plays a functional role in exercise-induced mitochondrial biogenesis and angiogenesis but not fiber-type transformation in mouse skeletal muscle. Am. J. Physiol. Cell Physiol. 298, C572-C579. doi: 10.1152/ajpcell.00481.2009
15. Gerhart-Hines, Z., Rodgers, J. T., Bare, O., Lerin, C., Kim, S.-H., Mostoslavsky, R., et al. (2007). Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J. 26, 1913-1923. doi: 10.1038/sj.emboj.7601633
16. 3 is present in mitochondria and not in the nucleus; and SIRT3 is upregulated by chronic muscle contraction in an adenosine monophosphate-activated protein kinase-independent manner. Metab. Clin. Exp. 61, 733-741. doi: 10.1016/j.metabol.2011.09.016
17. Gurd, B. J., Perry, C. G. R., Heigenhauser, G. J. F., Spriet, L. L., and Bonen, A. (2010). High-intensity interval training increases SIRT1 activity in human skeletal muscle. Appl. Physiol. Nutr. Metab. 35, 350-357. doi: 10.1139/H10-030
18. Hallows, W. C., Lee, S., and Denu, J. M. (2006). Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. U.S.A. 103, 10230-10235. doi: 10.1073/pnas.0604392103
19. Hardie, D. G. (2011). Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism. Proc. Nutr. Soc. 70, 92-99. doi: 10.1017/S0029665110003915
20. 3a dependent gene expression. Int. J. Biol. Sci. 4, 291-299.
21. Jäger, S., Handschin, C., St-Pierre, J., and Spiegelman, B. M. (2007). AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. U.S.A. 104, 12017-12022. doi: 10.1073/pnas.0705070104
22. Jenkins, R. R., Friedland, R., and Howald, H. (1984). The relationship of oxygen uptake to superoxide dismutase and catalase activity in human skeletal muscle. Int. J. Sports Med. 5, 11-14. doi: 10.1055/s-2008-1025872
23. Jensen, T. E., Wojtaszewski, J. F. P., and Richter, E. A. (2009). AMP-activated protein kinase in contraction regulation of skeletal muscle metabolism: necessary and/or sufficient? Acta Physiol. (Oxf). 196, 155-174. doi: 10.1111/j.1748-1716.2009.01979.x
24. 4, hexokinase II, and mitochondrial protein expression in mouse muscle. Am. J. Physiol. Endocrinol. Metab. 292, E331-E339. doi: 10.1152/ajpendo.00243.2006
25. Jørgensen, S. B., Wojtaszewski, J. F. P., Viollet, B., Andreelli, F., Birk, J. B., Hellsten, Y., et al. (2005). Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J. 19, 1146-1148. doi: 10.1096/fj.04-3144fje
26. Koh, H.-J., Brandauer, J., and Goodyear, L. J. (2008). LKB1 and AMPK and the regulation of skeletal muscle metabolism. Curr. Opin. Clin. Nutr. Metab. Care 11, 227-232. doi: 10.1097/MCO.0b013e3282fb7b76
27. Kong, X., Wang, R., Xue, Y., Liu, X., Zhang, H., Chen, Y., et al. (2010). Sirtuin 3, a new target of PGC-1alpha, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS ONE 5:e11707. doi: 10.1371/journal.pone.0011707
28. Lanza, I. R., Short, D. K., Short, K. R., Raghavakaimal, S., Basu, R., Joyner, M. J., et al. (2008). Endurance exercise as a countermeasure for aging. Diabetes 57, 2933-2942. doi: 10.2337/db08-0349
29. Lee, W. J., Kim, M., Park, H.-S., Kim, H. S., Jeon, M. J., Oh, K. S., et al. (2006). AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPARalpha and PGC-1. Biochem. Biophys. Res. Commun. 340, 291-295. doi: 10.1016/j.bbrc.2005.12.011
30. Leick, L., Fentz, J., Biensø, R. S., Knudsen, J. G., Jeppesen, J., Kiens, B., et al. (2010a). PGC-1{alpha} is required for AICAR-induced expression of GLUT4 and mitochondrial proteins in mouse skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 299, E456-E465. doi: 10.1152/ajpendo.00648.2009
31. Leick, L., Hellsten, Y., Fentz, J., Lyngby, S. S., Wojtaszewski, J. F. P., Hidalgo, J., et al. (2009). PGC-1alpha mediates exercise-induced skeletal muscle VEGF expression in mice. Am. J. Physiol. Endocrinol. Metab. 297, E92-E103. doi: 10.1152/ajpendo.00076.2009
32. Leick, L., Lyngby, S. S., Wojtaszewski, J. F. P., Wojtasewski, J. F. P., and Pilegaard, H. (2010b). PGC-1alpha is required for training-induced prevention of age-associated decline in mitochondrial enzymes in mouse skeletal muscle. Exp. Gerontol. 45, 336-342. doi: 10.1016/j.exger.2010.01.011
33. Ljubicic, V., Miura, P., Burt, M., Boudreault, L., Khogali, S., Lunde, J. A., et al. (2011). Chronic AMPK activation evokes the slow, oxidative myogenic program and triggers beneficial adaptations in mdx mouse skeletal muscle. Hum. Mol. Genet. 20, 3478-3493. doi: 10.1093/hmg/ddr265
34. Lombard, D. B., Alt, F. W., Cheng, H.-L., Bunkenborg, J., Streeper, R. S., Mostoslavsky, R., et al. (2007). Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol. Cell. Biol. 27, 8807-8814. doi: 10.1128/MCB.01636-07
35. McArdle, A., van der Meulen, J., Close, G. L., Pattwell, D., Van Remmen, H., Huang, T. T., et al. (2004). Role of mitochondrial superoxide dismutase in contraction-induced generation of reactive oxygen species in skeletal muscle extracellular space. Am. J. Physiol. Cell Physiol. 286, C1152-C1158. doi: 10.1152/ajpcell.00322.2003
36. Mu, J., Brozinick, J. T. Jr., Valladares, O., Bucan, M., and Birnbaum, M. J. (2001). A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol. Cell 7, 1085-1094. doi: 10.1016/S1097-2765(01)00251-9
37. Naya, F. J., Mercer, B., Shelton, J., Richardson, J. A., Williams, R. S., and Olson, E. N. (2000). Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J. Biol. Chem. 275, 4545-4548. doi: 10.1074/jbc.275.7.4545
38. Nemoto, S., Fergusson, M. M., and Finkel, T. (2005). SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1{alpha}. J. Biol. Chem. 280, 16456-16460. doi: 10.1074/jbc.M501485200
39. Olesen, J., Ringholm, S., Nielsen, M. M., Brandt, C. T., Pedersen, J. T., Halling, J. F., et al. (2013). Role of PGC-1a in exercise training- and resveratrol-induced prevention of age-associated inflammation. Exp. Gerontol. 48, 1274-1284. doi: 10.1016/j.exger.2013.07.015
40. 3 and activate AMPK and PGC-1a in skeletal muscle. Aging (Albany. NY) 1, 771-783.
41. Parise, G., Phillips, S. M., Kaczor, J. J., and Tarnopolsky, M. A. (2005). Antioxidant enzyme activity is up-regulated after unilateral resistance exercise training in older adults. Free Radic. Biol. Med. 39, 289-295. doi: 10.1016/j.freeradbiomed.2005.03.024
42. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., and Spiegelman, B. M. (1998). A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839. doi: 10.1016/S0092-8674(00)81410-5
43. Putman, C. T., Kiricsi, M., Pearcey, J., MacLean, I. M., Bamford, J. A., Murdoch, G. K., et al. (2003). AMPK activation increases uncoupling protein-3 expression and mitochondrial enzyme activities in rat muscle without fibre type transitions. J. Physiol. 551, 169-178. doi: 10.1111/j.1469-7793.2003.00169.x
44. Qiu, X., Brown, K., Hirschey, M. D., Verdin, E., and Chen, D. (2010). Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 12, 662-667. doi: 10.1016/j.cmet.2010.11.015
45. 3 in metabolic pathways. Proc. Natl. Acad. Sci. U.S.A. 110, 6601-6606. doi: 10.1073/pnas.1302961110
46. Reid, M. B. (2001). Invited review: redox modulation of skeletal muscle contraction: what we know and what we don't. J. Appl. Physiol. 90, 724-731.
47. Ringholm, S., Olesen, J., Pedersen, J. T., Brandt, C. T., Halling, J. F., Hellsten, Y., et al. (2013). Effect of lifelong resveratrol supplementation and exercise training on skeletal muscle oxidative capacity in aging mice; impact of PGC-1α. Exp. Gerontol. 48, 1311-1318. doi: 10.1016/j.exger.2013.08.012
48. Röckl, K. S. C., Hirshman, M. F., Brandauer, J., Fujii, N., Witters, L. A., and Goodyear, L. J. (2007). Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56, 2062-2069. doi: 10.2337/db07-0255
49. Schwer, B., Bunkenborg, J., Verdin, R. O., Andersen, J. S., and Verdin, E. (2006). Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. U.S.A. 103, 10224-10229. doi: 10.1073/pnas.0603968103
50. Schwer, B., North, B. J., Frye, R. A., Ott, M., and Verdin, E. (2002). The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase. J. Cell Biol. 158, 647-657. doi: 10.1083/jcb.200205057
51. Shinmura, K., Tamaki, K., Saito, K., Nakano, Y., Tobe, T., and Bolli, R. (2007). Cardioprotective effects of short-term caloric restriction are mediated by adiponectin via activation of AMP-activated protein kinase. Circulation 116, 2809-2817. doi: 10.1161/CIRCULATIONAHA.107.725697
52. Someya, S., Yu, W., Hallows, W. C., Xu, J., Vann, J. M., Leeuwenburgh, C., et al. (2010). Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143, 802-812. doi: 10.1016/j.cell.2010.10.002
53. Spina, R. J., Chi, M. M., Hopkins, M. G., Nemeth, P. M., Lowry, O. H., and Holloszy, J. O. (1996). Mitochondrial enzymes increase in muscle in response to 7-10 days of cycle exercise. J Appl Physiol 80, 2250-2254.
54. Tanner, C. B., Madsen, S. R., Hallowell, D. M., Goring, D. M. J., Moore, T. M., Hardman, S. E., et al. (2013). Mitochondrial and performance adaptations to exercise training in mice lacking skeletal muscle LKB1. Am. J. Physiol. Endocrinol. Metab. 305, E1018-E1029. doi: 10.1152/ajpendo.00227.2013
55. Tao, R., Coleman, M. C., Pennington, J. D., Ozden, O., Park, S.-H., Jiang, H., et al. (2010). Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell 40, 893-904. doi: 10.1016/j.molcel.2010.12.013
56. Tiidus, P. M., Pushkarenko, J., and Houston, M. E. (1996). Lack of antioxidant adaptation to short-term aerobic training in human muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 271, R832-R836.
57. Tonkonogi, M., Walsh, B., Svensson, M., and Sahlin, K. (2000). Mitochondrial function and antioxidative defence in human muscle: effects of endurance training and oxidative stress. J. Physiol. 528, 379-388. doi: 10.1111/j.1469-7793.2000.00379.x
58. 4 proteins in human skeletal muscle. J. Physiol. 592, 351-375. doi: 10.1113/jphysiol.2013.266338
59. 3 to protect mitochondria against oxidative damage. Free Radic. Biol. Med. 63, 222-234. doi: 10.1016/j.freeradbiomed.2013.05.002
60. 3 deacetylates ATP synthase F1 complex proteins in response to nutrient- and exercise-induced stress. Antioxid. Redox Signal. 21, 551-564. doi: 10.1089/ars.2013.5420
61. White, A. T., and Schenk, S. (2012). NAD+/NADH and skeletal muscle mitochondrial adaptations to exercise. Am. J. Physiol. Endocrinol. Metab. 303, E308-E321. doi: 10.1152/ajpendo.00054.2012
62. 3-catalyzed deacetylation and its deficiency in human cells harboring 4977bp deletion of mitochondrial DNA. Biochim. Biophys. Acta 1832, 216-227. doi: 10.1016/j.bbadis.2012.10.002
63. 3 regulates mitochondrial protein synthesis by deacetylation of the ribosomal protein MRPL10. J. Biol. Chem. 285, 7417-7429. doi: 10.1074/jbc.M109.053421