Activation of AMPKa2 is not crucial for mitochondrial uncoupling-induced metabolic effects but required to maintain skeletal muscle integrity

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Ost, Mario ^a   Werner, Franziska ^a   Dokas, Janine ^a   Klaus, Susanne ^a   Voigt, Anja ^a  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; ADENYLATE KINASE ALPHA 2; CD36 ANTIGEN; FIBROBLAST GROWTH FACTOR 21; HEAT SHOCK PROTEIN 70; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE ULK1; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; AMPK ALPHA2 SUBUNIT, MOUSE; FATTY ACID; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; UNCOUPLING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMETRY; BODY WEIGHT; CALORIC INTAKE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENERGY BALANCE; ENERGY EXPENDITURE; ENZYME ACTIVATION; FAT MASS; FATTY ACID OXIDATION; GENE OVEREXPRESSION; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; HISTOPATHOLOGY; INSULIN SENSITIVITY; LEAN BODY WEIGHT; LOCOMOTION; MALE; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MITOPHAGY; MORPHOLOGY; MOUSE; MUSCLE ATROPHY; MUSCLE FUNCTION; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SKELETAL MUSCLE; TISSUE DISTRIBUTION; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; C57BL MOUSE; CROSS BREEDING; GENETICS; GLUCOSE TOLERANCE TEST; METABOLISM; MITOCHONDRION; PHOSPHORYLATION; PHYSIOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIGENS, CD36; BODY WEIGHT; CROSSES, GENETIC; FATTY ACIDS; GLUCOSE; GLUCOSE TOLERANCE TEST; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; PHENOTYPE; PHOSPHORYLATION; UNCOUPLING AGENTS;

EID: 84899623784     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094689     Document Type: Article

References (86)

1. Corpeleijn E, Saris WH, Blaak EE (2009) Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle. Obes Rev 10: 178-193.
2. Katterle Y, Keipert S, Hof J, Klaus S (2008) Dissociation of obesity and insulin resistance in transgenic mice with skeletal muscle expression of uncoupling protein 1. Physiol Genomics 32: 352-359. (Pubitemid 351328558)
3. Keipert S, Voigt A, Klaus S (2011) Dietary effects on body composition, glucose metabolism, and longevity are modulated by skeletal muscle mitochondrial uncoupling in mice. Aging Cell 10: 122-136.
4. Neschen S, Katterle Y, Richter J, Augustin R, Scherneck S, et al. (2008) Uncoupling protein 1 expression in murine skeletal muscle increases AMPK activation, glucose turnover, and insulin sensitivity in vivo. Physiol Genomics 33: 333-340. (Pubitemid 352755735)
5. Keipert S, Ost M, Chadt A, Voigt A, Ayala V, et al. (2013) Skeletal muscle uncoupling-induced longevity in mice is linked to increased substrate metabolism and induction of the endogenous antioxidant defense system. Am J Physiol Endocrinol Metab 304: E495-506.
6. Gates AC, Bernal-Mizrachi C, Chinault SL, Feng C, Schneider JG, et al. (2007) Respiratory uncoupling in skeletal muscle delays death and diminishes agerelated disease. Cell Metab 6: 497-505. (Pubitemid 350163051)
7. Klaus S, Keipert S, Rossmeisl M, Kopecky J (2011) Augmenting energy expenditure by mitochondrial uncoupling: a role of AMP-activated protein kinase. Genes Nutr.
8. Hardie DG, Ross FA, Hawley SA (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13: 251-262.
9. Zhang BB, Zhou G, Li C (2009) AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 9: 407-416.
10. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, et al. (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMPactivated protein kinase. J Biol Chem 271: 27879-27887. (Pubitemid 26367365)
11. O'Neill HM (2013) AMPK and Exercise: Glucose Uptake and Insulin Sensitivity. Diabetes Metab J 37: 1-21.
12. Hardie DG (2008) AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond) 32 Suppl 4: S7-12.
13. McGee SL, Hargreaves M (2010) AMPK-mediated regulation of transcription in skeletal muscle. Clin Sci (Lond) 118: 507-518.
14. Canto C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, et al. (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 11: 213-219.
15. Viollet B, Athea Y, Mounier R, Guigas B, Zarrinpashneh E, et al. (2009) AMPK: Lessons from transgenic and knockout animals. Front Biosci 14: 19-44.
16. Rockl KS, Hirshman MF, Brandauer J, Fujii N, Witters LA, et al. (2007) Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56: 2062-2069. (Pubitemid 47195818)
17. Geng T, Li P, Okutsu M, Yin X, Kwek J, 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: C572-579.
18. Zwetsloot KA, Westerkamp LM, Holmes BF, Gavin TP (2008) AMPK regulates basal skeletal muscle capillarization and VEGF expression, but is not necessary for the angiogenic response to exercise. J Physiol 586: 6021-6035.
19. O'Neill HM, Maarbjerg SJ, Crane JD, Jeppesen J, Jorgensen SB, et al. (2011) AMP-activated protein kinase (AMPK) beta1beta2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proc Natl Acad Sci U S A 108: 16092-16097.
20. Thomson DM, Porter BB, Tall JH, Kim HJ, Barrow JR, et al. (2007) Skeletal muscle and heart LKB1 deficiency causes decreased voluntary running and reduced muscle mitochondrial marker enzyme expression in mice. Am J Physiol Endocrinol Metab 292: E196-202. (Pubitemid 46052942)
21. Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, et al. (2007) The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 9: 218-224. (Pubitemid 46420865)
22. Salminen A, Kaarniranta K (2012) AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res Rev 11: 230-241.
23. Sanchez AM, Candau RB, Csibi A, Pagano AF, Raibon A, et al. (2012) The role of AMP-activated protein kinase in the coordination of skeletal muscle turnover and energy homeostasis. Am J Physiol Cell Physiol 303: C475-485.
24. Kroemer G, Marino G, Levine B (2010) Autophagy and the integrated stress response. Mol Cell 40: 280-293.
25. Kim KH, Jeong YT, Oh H, Kim SH, Cho JM, et al. (2013) Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med 19: 83-92.
26. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, et al. (2009) Autophagy is required to maintain muscle mass. Cell Metab 10: 507-515.
27. Sanchez AM, Csibi A, Raibon A, Cornille K, Gay S, et al. (2012) AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J Cell Biochem 113: 695-710.
28. Keipert S, Ost M, Johann K, Imber F, Jastroch M, et al. (2013) Skeletal muscle mitochondrial uncoupling drives endocrine cross-talk through induction of FGF21 as a myokine. Am J Physiol Endocrinol Metab in press.
29. Mu J, Brozinick JT, Jr., Valladares O, Bucan M, Birnbaum MJ (2001) A role for AMP-activated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094. (Pubitemid 32525754)
30. Mu J, Barton ER, Birnbaum MJ (2003) Selective suppression of AMP-activated protein kinase in skeletal muscle: update on 'lazy mice'. Biochem Soc Trans 31: 236-241. (Pubitemid 36241436)
31. Klaus S, Rudolph B, Dohrmann C, Wehr R (2005) Expression of uncoupling protein 1 in skeletal muscle decreases muscle energy efficiency and affects thermoregulation and substrate oxidation. Physiol Genomics 21: 193-200. (Pubitemid 40898479)
32. Keipert S, Klaus S, Heldmaier G, Jastroch M (2010) UCP1 ectopically expressed in murine muscle displays native function and mitigates mitochondrial superoxide production. Biochim Biophys Acta 1797: 324-330.
33. Davies SP, Carling D, Hardie DG (1989) Tissue distribution of the AMPactivated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studied using a specific and sensitive peptide assay. Eur J Biochem 186: 123-128. (Pubitemid 20015134)
34. Kudo N, Barr AJ, Barr RL, Desai S, Lopaschuk GD (1995) High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 59-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J Biol Chem 270: 17513-17520.
35. Barnes BR, Marklund S, Steiler TL, Walter M, Hjalm G, et al. (2004) The 59-AMP-activated protein kinase gamma3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle. J Biol Chem 279: 38441-38447. (Pubitemid 39295995)
36. Chadt A, Leicht K, Deshmukh A, Jiang LQ, Scherneck S, et al. (2008) Tbc1d1 mutation in lean mouse strain confers leanness and protects from diet-induced obesity. Nat Genet 40: 1354-1359.
37. Dokas J, Chadt A, Nolden T, Himmelbauer H, Zierath JR, et al. (2013) Conventional knockout of Tbc1d1 in mice impairs insulin-and AICARstimulated glucose uptake in skeletal muscle. Endocrinology 154: 3502-3514.
38. Seebacher F, Guderley H, Elsey RM, Trosclair PL, 3rd (2003) Seasonal acclimatisation of muscle metabolic enzymes in a reptile (Alligator mississippiensis). J Exp Biol 206: 1193-1200. (Pubitemid 36409161)
39. Boque N, Campion J, Paternain L, Garcia-Diaz DF, Galarraga M, et al. (2009) Influence of dietary macronutrient composition on adiposity and cellularity of different fat depots in Wistar rats. J Physiol Biochem 65: 387-395.
40. Mutsaers CA, Wishart TM, Lamont DJ, Riessland M, Schreml J, et al. (2011) Reversible molecular pathology of skeletal muscle in spinal muscular atrophy. Hum Mol Genet 20: 4334-4344.
41. Eaton SL, Roche SL, Llavero Hurtado M, Oldknow KJ, Farquharson C, et al. (2013) Total protein analysis as a reliable loading control for quantitative fluorescent Western blotting. PLoS One 8: e72457.
42. Jacobs RA, Diaz V, Meinild AK, Gassmann M, Lundby C (2013) The C57Bl/6 mouse serves as a suitable model of human skeletal muscle mitochondrial function. Exp Physiol 98: 908-921.
43. Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, Mark W, et al. (2004) Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion. Am J Physiol Heart Circ Physiol 286: H1633-1641. (Pubitemid 38525448)
44. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, et al. (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3: 965-976. (Pubitemid 351818685)
45. Pesta D, Gnaiger E (2012) High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol Biol 810: 25-58.
46. Jorgensen SB, Treebak JT, Viollet B, Schjerling P, Vaulont S, et al. (2007) Role of AMPKalpha2 in basal, training-, and AICAR-induced GLUT4, hexokinase II, and mitochondrial protein expression in mouse muscle. Am J Physiol Endocrinol Metab 292: E331-339. (Pubitemid 46052958)
47. Klip A, Paquet MR (1990) Glucose transport and glucose transporters in muscle and their metabolic regulation. Diabetes Care 13: 228-243. (Pubitemid 20092110)
48. Merrill GF, Kurth EJ, Hardie DG, Winder WW (1997) AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol 273: E1107-1112.
49. Carling D, Clarke PR, Zammit VA, Hardie DG (1989) Purification and characterization of the AMP-activated protein kinase. Copurification of acetyl-CoA carboxylase kinase and 3-hydroxy-3-methylglutaryl-CoA reductase kinase activities. Eur J Biochem 186: 129-136. (Pubitemid 20015135)
50. Alkhateeb H, Holloway GP, Bonen A (2011) Skeletal muscle fatty acid oxidation is not directly associated with AMPK or ACC2 phosphorylation. Appl Physiol Nutr Metab 36: 361-367.
51. Dzamko N, Schertzer JD, Ryall JG, Steel R, Macaulay SL, et al. (2008) AMPKindependent pathways regulate skeletal muscle fatty acid oxidation. J Physiol 586: 5819-5831.
52. Coburn CT, Knapp FF, Jr., Febbraio M, Beets AL, Silverstein RL, et al. (2000) Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J Biol Chem 275: 32523-32529.
53. Nahle Z, Hsieh M, Pietka T, Coburn CT, Grimaldi PA, et al. (2008) CD36-dependent regulation of muscle FoxO1 and PDK4 in the PPAR delta/betamediated adaptation to metabolic stress. J Biol Chem 283: 14317-14326.
54. Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA (1999) Reduced differentiation potential of primary MyoD-/-myogenic cells derived from adult skeletal muscle. J Cell Biol 144: 631-643. (Pubitemid 29234543)
55. Couplan E, Gelly C, Goubern M, Fleury C, Quesson B, et al. (2002) High level of uncoupling protein 1 expression in muscle of transgenic mice selectively affects muscles at rest and decreases their IIb fiber content. J Biol Chem 277: 43079-43088. (Pubitemid 35285690)
56. Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, et al. (2012) A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481: 463-468.
57. Haddad F, Zaldivar F, Cooper DM, Adams GR (2005) IL-6-induced skeletal muscle atrophy. J Appl Physiol (1985) 98: 911-917. (Pubitemid 40283672)
58. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, et al. (2011) Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331: 456-461.
59. Bjorkoy G, Lamark T, Pankiv S, Overvatn A, Brech A, et al. (2009) Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 452: 181-197.
60. Zong H, Ren JM, Young LH, Pypaert M, Mu J, et al. (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99: 15983-15987. (Pubitemid 35462735)
61. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, et al. (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296: 349-352. (Pubitemid 34303690)
62. Holmes BF, Lang DB, Birnbaum MJ, Mu J, Dohm GL (2004) AMP kinase is not required for the GLUT4 response to exercise and denervation in skeletal muscle. Am J Physiol Endocrinol Metab 287: E739-743. (Pubitemid 39237903)
63. Jeppesen J, Albers PH, Rose AJ, Birk JB, Schjerling P, et al. (2011) Contractioninduced skeletal muscle FAT/CD36 trafficking and FA uptake is AMPK independent. J Lipid Res 52: 699-711.
64. Raney MA, Yee AJ, Todd MK, Turcotte LP (2005) AMPK activation is not critical in the regulation of muscle FA uptake and oxidation during low-intensity muscle contraction. Am J Physiol Endocrinol Metab 288: E592-598. (Pubitemid 40250555)
65. Olson AL, Pessin JE (1996) Structure, function, and regulation of the mammalian facilitative glucose transporter gene family. Annu Rev Nutr 16: 235-256. (Pubitemid 26286854)
66. Fueger PT, Shearer J, Bracy DP, Posey KA, Pencek RR, et al. (2005) Control of muscle glucose uptake: test of the rate-limiting step paradigm in conscious, unrestrained mice. J Physiol 562: 925-935. (Pubitemid 40246804)
67. Thomson DM, Winder WW (2009) AMP-activated protein kinase control of fat metabolism in skeletal muscle. Acta Physiol (Oxf) 196: 147-154.
68. Turcotte LP, Raney MA, Todd MK (2005) ERK1/2 inhibition prevents contraction-induced increase in plasma membrane FAT/CD36 content and FA uptake in rodent muscle. Acta Physiol Scand 184: 131-139. (Pubitemid 40776360)
69. Viollet B, Athea Y, Mounier R, Guigas B, Zarrinpashneh E, et al. (2009) AMPK: Lessons from transgenic and knockout animals. Front Biosci (Landmark Ed) 14: 19-44.
70. Milne KJ, Noble EG (2002) Exercise-induced elevation of HSP70 is intensity dependent. J Appl Physiol (1985) 93: 561-568. (Pubitemid 34810219)
71. Senf SM, Howard TM, Ahn B, Ferreira LF, Judge AR (2013) Loss of the inducible Hsp70 delays the inflammatory response to skeletal muscle injury and severely impairs muscle regeneration. PLoS One 8: e62687.
72. Senf SM, Dodd SL, McClung JM, Judge AR (2008) Hsp70 overexpression inhibits NF-kappaB and Foxo3a transcriptional activities and prevents skeletal muscle atrophy. FASEB J 22: 3836-3845.
73. Lawler JM, Song W, Kwak HB (2006) Differential response of heat shock proteins to hindlimb unloading and reloading in the soleus. Muscle Nerve 33: 200-207. (Pubitemid 43208676)
74. Kabakov AE, Budagova KR, Latchman DS, Kampinga HH (2002) Stressful preconditioning and HSP70 overexpression attenuate proteotoxicity of cellular ATP depletion. Am J Physiol Cell Physiol 283: C521-534. (Pubitemid 34787535)
75. Adair TH (2005) Growth regulation of the vascular system: an emerging role for adenosine. Am J Physiol Regul Integr Comp Physiol 289: R283-R296. (Pubitemid 41060476)
76. Hepple RT, Mackinnon SL, Goodman JM, Thomas SG, Plyley MJ (1997) Resistance and aerobic training in older men: effects on VO2peak and the capillary supply to skeletal muscle. J Appl Physiol (1985) 82: 1305-1310. (Pubitemid 27172334)
77. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, et al. (2007) ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14: 230-239. (Pubitemid 46092226)
78. Wong CH, Iskandar KB, Yadav SK, Hirpara JL, Loh T, et al. (2010) Simultaneous induction of non-canonical autophagy and apoptosis in cancer cells by ROS-dependent ERK and JNK activation. PLoS One 5: e9996.
79. Mizushima N (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22: 132-139.
80. Lee JW, Park S, Takahashi Y, Wang HG (2010) The association of AMPK with ULK1 regulates autophagy. PLoS One 5: e15394.
81. Egan D, Kim J, Shaw RJ, Guan KL (2011) The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 7: 643-644.
82. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13: 132-141.
83. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, et al. (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20: 1992-2003.
84. Jorgensen SB, Wojtaszewski JF, Viollet B, Andreelli F, Birk JB, et al. (2005) Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J 19: 1146-1148. (Pubitemid 40946446)
85. Jager S, Handschin C, St-Pierre J, Spiegelman BM (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. (Pubitemid 47185622)
86. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, et al. (2005) Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280: 19587-19593. (Pubitemid 41379480)