Chronic AMPK stimulation attenuates adaptive signaling in dystrophic skeletal muscle

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 1, 2012, Pages

  Ljubicic, Vladimir ^a   Khogali, Shiemaa ^a   Renaud, Jean Marc ^a   Jasmin, Bernard J ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

5 aminoimidazole 4 carboxamide 1 d ribofuranoside; Coactivator 1 ; Mdx mice; p38 mitogen activated protein kinase; Peroxisome proliferatoractivated receptor ; Protein arginine methyltransferases

Indexed keywords

5 AMINOIMIDAZOLE 4 CARBOXAMIDE 1 BETA DEXTRO RIBOFURANOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN 140; SIRTUIN 1; UNCLASSIFIED DRUG;

ACUTE STRESS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; MUSCLE CONTRACTION; MUSCULAR DYSTROPHY; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SKELETAL MUSCLE; TREADMILL; TREATMENT DURATION; VELOCITY; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ADAPTATION, PHYSIOLOGICAL; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; PHYSICAL CONDITIONING, ANIMAL; RIBONUCLEOTIDES; SIGNAL TRANSDUCTION;

EID: 83455250428     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00183.2011     Document Type: Article

References (77)

1. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280: 19587-19593, 2005.
2. Angus LM, Chakkalakal JV, Méjat A, Eibl JK, Bélanger G, Megeney LA, Chin ER, Schaeffer L, Michel RN, Jasmin BJ. Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1α, drives utrophin gene expression at the neuromuscular junction. Am J Physiol Cell Physiol 289: C908-C917, 2005.
3. Bamford JA, Lopaschuk GD, MacLean IM, Reinhart ML, Dixon WT, Putman CT. 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, 2003.
4. Barton ER, Morris L, Musaro A, Rosenthal N, Sweeney HL. Musclespecific expression of insulin-like growth factor I counters muscle decline in mdx mice. J Cell Biol 157: 137-148, 2002.
5. Bergeron R, Ren JM, Cadman KS, Moore IK, Perret P, Pypaert M, Young LH, Semenkovich CF, Shulman GI. Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am J Physiol Endocrinol Metab 281: E1340-E1346, 2001.
6. Booth FW, Laye MJ, Spangenburg EE. Gold standards for scientists who are conducting animal-based exercise studies. J Appl Physiol 108: 219-221, 2010.
7. Boppart MD, Asp S, Wojtaszewski JF, Fielding RA, Mohr T, Goodyear LJ. Marathon running transiently increases c-Jun NH2-terminal kinase and p38 activities in human skeletal muscle. J Physiol 526: 663-669, 2000.
8. Boppart MD, Burkin DJ, Kaufman SJ. Activation of AKT signaling promotes cell growth and survival in α7β1 integrin-mediated alleviation of muscular dystrophy. Biochim Biophys Acta 1812: 439-446, 2011.
9. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
10. Buhl ES, Jessen N, Pold R, Ledet T, Flyvbjerg A, Pedersen SB, Pedersen O, Schmitz O, Lund S. Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome. Diabetes 51: 2199-2206, 2002.
11. Burdi R, Rolland JF, Fraysse B, Litvinova K, Cozzoli A, Giannuzzi V, Liantonio A, Camerino GM, Sblendorio V, Capogrosso RF, Palmieri B, Andreetta F, Confalonieri P, De Benedictis L, Montagnani M, De Luca A. Multiple pathological events in exercised dystrophic mdx mice are targeted by pentoxifylline: outcome of a large array of in vivo and ex vivo tests. J Appl Physiol 106: 1311-1324, 2009.
12. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L, Kaul A, Kinnett K, McDonald C, Pandya S, Poysky J, Shapiro F, Tomezsko J, Constantin C; DMD Care Considerations Working Group. Diagnosis and management of Duchenne muscular dystrophy, part 2: implementation of multidisciplinary care. Lancet Neurol 9: 177-189, 2010.
13. Chakkalakal JV, Harrison MA, Carbonetto S, Chin E, Michel RN, Jasmin BJ. Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum Mol Genet 13: 379-388, 2004.
14. Chakkalakal JV, Stocksley MA, Harrison MA, Angus LM, Deschenes- Furry J, St-Pierre S, Megeney LA, Chin ER, Michel RN, Jasmin BJ. Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc Natl Acad Sci USA 100: 7791-7796, 2003.
15. Chaturvedi RK, Adhihetty P, Shukla S, Hennessy T, Calingasan N, Yang L, Starkov A, Kiaei M, Cannella M, Sassone J, Ciammola A, Squitieri F, Beal MF. Impaired PGC-1alpha function in muscle in Huntington's disease. Hum Mol Genet 18: 3048-3065, 2009.
16. Chen SL, Loffler KA, Chen D, Stallcup MR, Muscat GE. The coactivator- associated arginine methyltransferase is necessary for muscle differentiation: CARM1 coactivates myocyte enhancer factor-2. J Biol Chem 277: 4324-4333, 2002.
17. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS. A calcineurindependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12: 2499-2509, 1998.
18. Copp SW, Davis RT, Poole DC, Musch TI. Reproducibility of endurance capacity and VO2peak in male Sprague-Dawley rats. J Appl Physiol 106: 1072-1078, 2009.
19. Dacwag CS, Bedford MT, Sif S, Imbalzano AN. Distinct protein arginine methyltransferases promote ATP-dependent chromatin remodeling function at different stages of skeletal muscle differentiation. Mol Cell Biol 29: 1909-1921, 2009.
20. 31P]-nuclear magnetic resonance study of mdx mice. Proc Biol Sci 251: 201-206, 1993.
21. Ehrenborg E, Krook A. Regulation of skeletal muscle physiology and metabolism by peroxisome proliferator-activated receptor delta. Pharmacol Rev 61: 373-393, 2009.
22. Fillmore N, Jacobs DL, Mills DB, Winder WW, Hancock CR. Chronic AMP-activated protein kinase activation and a high-fat diet have an additive effect on mitochondria in rat skeletal muscle. J Appl Physiol 109: 511-520, 2010.
23. Frasca D, Romero M, Landin AM, Diaz A, Riley RL, Blomberg BB. Protein phosphatase 2A (PP2A) is increased in old murine B cells and mediates p38 MAPK/tristetraprolin dephosphorylation and E47 mRNA instability. Mech Ageing Dev 131: 306-314, 2010.
24. Goodyear LJ, Chang PY, Sherwood DJ, Dufresne SD, Moller DE. Effects of exercise and insulin on mitogen-activated protein kinase signaling pathways in rat skeletal muscle. Am J Physiol Endocrinol Metab 271: E403-E408, 1996.
25. Gramolini AO, Bélanger G, Thompson JM, Chakkalakal JV, Jasmin BJ. Increased expression of utrophin in a slow vs. a fast muscle involves posttranscriptional events. Am J Physiol Cell Physiol 281: C1300-C1309, 2001.
26. Handschin C, Kobayashi YM, Chin S, Seale P, Campbell KP, Spiegelman BM. PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev 21: 770-783, 2007.
27. Iwasaki H, Yada T. Protein arginine methylation regulates insulin signaling in L6 skeletal muscle cells. Biochem Biophys Res Commun 364: 1015-1021, 2007.
28. Jørgensen SB, Treebak JT, Viollet B, Schjerling P, Vaulont S, Wojtaszewski JF, Richter EA. Role of AMPKα2 in basal, training-, and AICAR-induced GLUT4, hexokinase II, and mitochondrial protein expression in mouse muscle. Am J Physiol Endocrinol Metab 292: E331-E339, 2007.
29. Kickstein E, Krauss S, Thornhill P, Rutschow D, Zeller R, Sharkey J, Williamson R, Fuchs M, Köhler A, Glossmann H, Schneider R, Sutherland C, Schweiger S. Biguanide metformin acts on tau phosphorylation via mTOR/protein phosphatase 2A (PP2A) signaling. Proc Natl Acad Sci USA 107: 21830-21835, 2010.
30. Kim D, Lee MS, Jo K, Lee KE, Hwang JK. Therapeutic potential of panduratin A, LKB1-dependent AMP-activated protein kinase stimulator, with activation of PPARα/δ for the treatment of obesity. Diabetes Obes Metab 13: 584-593, 2011.
31. Kim SJ, Yoo BC, Uhm CS, Lee SW. Posttranslational arginine methylation of lamin A/C during myoblast fusion. Biochim Biophys Acta 1814: 308-317, 2011.
32. Knab AM, Bowen RS, Moore-Harrison T, Hamilton AT, Turner MJ, Lightfoot JT. Repeatability of exercise behaviors in mice. Physiol Behav 98: 433-440, 2009.
33. Krzysik B, Vergnes JP, McManus I. Enzymatic methylation of skeletal muscle contractile proteins. Arch Biochem Biophys 146: 34-45, 1971.
34. Kumar A, Bhatnagar S, Kumar A. Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Am J Pathol 177: 248-260, 2010.
35. Lang JM, Esser KA, Dupont-Versteegden EE. Altered activity of signaling pathways in diaphragm and tibialis anterior muscle of dystrophic mice. Exp Biol Med (Maywood) 229: 503-511, 2004.
36. Lilling G, Beitner R. Altered allosteric properties of cytoskeleton-bound phosphofructokinase in muscle from mice with X chromosome-linked muscular dystrophy (mdx). Biochem Med Metab Biol 45: 319-325, 1991.
37. Lira VA, Benton CR, Yan Z, Bonen A. PGC-1α regulation by exercise training and its influences on muscle function and insulin sensitivity. Am J Physiol Endocrinol Metab 299: E145-E161, 2010.
38. Ljubicic V, Hood DA. Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle. Aging Cell 8: 394-404, 2009.
39. Ljubicic V, Hood DA. Specific attenuation of protein kinase phosphorylation in muscle with a high mitochondrial content. Am J Physiol Endocrinol Metab 297: E749-E758, 2009.
40. Ljubicic V, Miura P, Burt M, Boudreault L, Khogali S, Renaud JM, Jasmin BJ. Chronic AMPK activation evokes the slow, oxidative myogenic program and triggers beneficial adaptations in mdx mouse skeletal muscle. Hum Mol Genet 20: 3478-3493, 2011.
41. Mallappa C, Hu YJ, Shamulailatpam P, Tae S, Sif S, Imbalzano AN. The expression of myogenic microRNAs indirectly requires protein arginine methyltransferase (Prmt)5 but directly requires Prmt4. Nucleic Acids Res 39: 1243-1255, 2011.
42. Markert CD, Ambrosio F, Call JA, Grange RW. Exercise and Duchenne muscular dystrophy: toward evidence-based exercise prescription. Muscle Nerve 43: 464-478, 2011.
43. McConell GK, Manimmanakorn A, Lee-Young RS, Kemp BE, Linden KC, Wadley GD. Differential attenuation of AMPK activation during acute exercise following exercise training or AICAR treatment. J Appl Physiol 105: 1422-1427, 2008.
44. Merrill GF, Kurth EJ, Hardie DG, Winder WW. AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol Endocrinol Metab 273: E1107-E1112, 1997.
45. Miura P, Chakkalakal JV, Boudreault L, Bélanger G, Hébert RL, Renaud JM, Jasmin BJ. Pharmacological activation of PPARbeta/delta stimulates utrophin A expression in skeletal muscle fibers and restores sarcolemmal integrity in mature mdx mice. Hum Mol Genet 18: 4640-4649, 2009.
46. Mizobuchi M, Inoue R, Miyaka M, Kakimoto Y. Accelerated protein turnover in the skeletal muscle of dystrophic mice. Biochim Biophys Acta 843: 78-82, 1985.
47. Moens P, Baatsen PH, Maréchal G. Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J Muscle Res Cell Motil 14: 446-451, 1993.
48. Mostaqul Huq MD, Gupta P, Tsai NP, White R, Parker MG, Wei LN. Suppression of receptor interacting protein 140 repressive activity by protein arginine methylation. EMBO J 25: 5094-5104, 2006.
49. Musi N, Goodyear LJ. Targeting the AMP-activated protein kinase for the treatment of type 2 diabetes. Curr Drug Targets Immune Endocr Metabol Disord 2: 119-127, 2002.
50. Mussini E, Cornelio F, Dworzak F, Cotellessa L, Morandi L, Colombo L, De Ponte G, Marcucci F. Content of methylhistidines in normal and pathological human skeletal muscles. Muscle Nerve 6: 423-429, 1983.
51. Mylabathula DB, Rice KM, Wang Z, Uddemarri S, Kinnard RS, Blough ER. Age-associated changes in MAPK activation in fast- and slow-twitch skeletal muscle of the F344/NNiaHSD × Brown Norway/ BiNia rat model. Exp Gerontol 41: 205-214, 2006.
52. Nader GA, Esser KA. Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J Appl Physiol 90: 1936-1942, 2001.
53. Nakamura A, Yoshida K, Ueda H, Takeda S, Ikeda S. Up-regulation of mitogen activated protein kinases in mdx skeletal muscle following chronic treadmill exercise. Biochim Biophys Acta 1740: 326-331, 2005.
54. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, Banayo E, Mihaylova MM, Nelson MC, Zou Y, Juguilon H, Kang H, Shaw RJ, Evans RM. AMPK and PPARdelta agonists are exercise mimetics. Cell 134: 405-415, 2008.
55. Peter AK, Ko CY, Kim MH, Hsu N, Ouchi N, Rhie S, Izumiya Y, Zeng L, Walsh K, Crosbie RH. Myogenic Akt signaling upregulates the utrophin-glycoprotein complex and promotes sarcolemma stability in muscular dystrophy. Hum Mol Genet 18: 318-327, 2009.
56. Pette D. Plasticity of mammalian skeletal muscle. J Appl Physiol 90: 1119-1124, 2001.
57. Ren JM, Ohira Y, Holloszy JO, Hämäläinen N, Traub I, Pette D. Effects of beta-guanidinopropionic acid-feeding on the patterns of myosin isoforms in rat fast-twitch muscle. Pflügers Arch 430: 389-393, 1995.
58. Schiaffino S, Sandri M, Murgia M. Activity-dependent signaling pathways controlling muscle diversity and plasticity. Physiology (Bethesda) 22: 269-278, 2007.
59. Seth A, Steel JH, Nichol D, Pocock V, Kumaran MK, Fritah A, Mobberley M, Ryder TA, Rowlerson A, Scott J, Poutanen M, White R, Parker M. The transcriptional corepressor RIP140 regulates oxidative metabolism in skeletal muscle. Cell Metab 6: 236-245, 2007.
60. Singh R, Millman G, Turin E, Polisiakeiwicz L, Lee B, Gatti F, Berge J, Smith E, Rutter J, Sumski C, Winders WT, Samadi A, Carlson CG. Increases in nuclear p65 activation in dystrophic skeletal muscle are secondary to increases in the cellular expression of p65 and are not solely produced by increases in IkappaB-alpha kinase activity. J Neurol Sci 285: 159-171, 2009.
61. Spangenburg EE, Brown DA, Johnson MS, Moore RL. Alterations in peroxisome proliferator-activated receptor mRNA expression in skeletal muscle after acute and repeated bouts of exercise. Mol Cell Biochem 332: 225-231, 2009.
62. Stupka N, Michell BJ, Kemp BE, Lynch GS. Differential calcineurin signalling activity and regeneration efficacy in diaphragm and limb muscles of dystrophic mdx mice. Neuromuscul Disord 16: 337-346, 2006.
63. Stupka N, Schertzer JD, Bassel-Duby R, Olson EN, Lynch GS. Stimulation of calcineurin Aα activity attenuates muscle pathophysiology in mdx dystrophic mice. Am J Physiol Regul Integr Comp Physiol 294: R983-R992, 2008.
64. Suchankova G, Nelson LE, Gerhart-Hines Z, Kelly M, Gauthier MS, Saha AK, Ido Y, Puigserver P, Ruderman NB. Concurrent regulation of AMP-activated protein kinase and SIRT1 in mammalian cells. Biochem Biophys Res Commun 378: 836-841, 2009.
65. Suwa M, Nakano H, Radak Z, Kumagai S. Short-term adenosine monophosphate-activated protein kinase activator 5-aminoimidazole-4- carboxamide-1-β-D-ribofuranoside treatment increases the sirtuin 1 protein expression in skeletal muscle. Metabolism 60: 394-403, 2011.
66. Teyssier C, Ma H, Emter R, Kralli A, Stallcup MR. Activation of nuclear receptor coactivator PGC-1alpha by arginine methylation. Genes Dev 19: 1466-1473, 2005.
67. Thabet M, Miki T, Seino S, Renaud JM. Treadmill running causes significant fiber damage in skeletal muscle of KATP channel-deficient mice. Physiol Genomics 22: 204-212, 2005.
68. Thomson DM, Gordon SE. Impaired overload-induced muscle growth is associated with diminished translational signalling in aged rat fast-twitch skeletal muscle. J Physiol 574: 291-305, 2006.
69. Villa-Moruzzi E, Puntoni F, Marin O. Activation of protein phosphatase-1 isoforms and glycogen synthase kinase-3 beta in muscle from mdx mice. Int J Biochem Cell Biol 28: 13-22, 1996.
70. Vinciguerra M, Fulco M, Ladurner A, Sartorelli V, Rosenthal N. SirT1 in muscle physiology and disease: lessons from mouse models. Dis Model Mech 3: 298-303, 2010.
71. Wang T, Yu Q, Chen J, Deng B, Qian L, Le Y. PP2A mediated AMPK inhibition promotes HSP70 expression in heat shock response. PLoS One 5: e13096, 2010.
72. Webster C, Silberstein L, Hays AP, Blau HM. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52: 503-513, 1988.
73. Williams DB, Sutherland LN, Bomhof MR, Basaraba SA, Thrush AB, Dyck DJ, Field CJ, Wright DC. Muscle-specific differences in the response of mitochondrial proteins to β-GPA feeding: an evaluation of potential mechanisms. Am J Physiol Endocrinol Metab 296: E1400-E1408, 2009.
74. Winder WW, Hardie DG. Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol Endocrinol Metab 270: E299-E304, 1996.
75. Winder WW, Holmes BF, Rubink DS, Jensen EB, Chen M, Holloszy JO. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 88: 2219-2226, 2000.
76. Witczak CA, Sharoff CG, Goodyear LJ. AMP-activated protein kinase in skeletal muscle: from structure and localization to its role as a master regulator of cellular metabolism. Cell Mol Life Sci 65: 3737-3755, 2008.
77. Young ME, Radda GK, Leighton B. Activation of glycogen phosphorylase and glycogenolysis in rat skeletal muscle by AICAR-an activator of AMP-activated protein kinase. FEBS Lett 382: 43-47, 1996.