AICAR stimulation metabolome widely mimics electrical contraction in isolated rat epitrochlearis muscle

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 12, 2013, Pages

  Miyamoto, Licht ^a   Egawa, Tatsuro ^b   Oshima, Rieko ^b   Kurogi, Eriko ^b   Tomida, Yosuke ^a   Tsuchiya, Koichiro ^a   Hayashi, Tatsuya ^b  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

5' AMP activated protein kinase; AICAR; Isolated skeletal muscle; Metabolome; Muscle contraction

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ALANINE; ASPARTIC ACID; GLUTATHIONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LYSINE;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAPILLARY ELECTROPHORESIS; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME ACTIVATION; EPITROCHLEARIS MUSCLE; EX VIVO STUDY; GLUCOSE TRANSPORT; MALE; METABOLOME; METABOLOMICS; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; TIME OF FLIGHT MASS SPECTROMETRY;

5′-AMP-ACTIVATED PROTEIN KINASE; AICAR; ISOLATED SKELETAL MUSCLE; METABOLOME; MUSCLE CONTRACTION;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL LINE; ELECTRIC STIMULATION; FACTOR ANALYSIS, STATISTICAL; GLUCOSE; GLUTATHIONE; HYPOGLYCEMIC AGENTS; MALE; METABOLOME; MUSCLE CONTRACTION; MUSCLE, SKELETAL; PRINCIPAL COMPONENT ANALYSIS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RIBONUCLEOTIDES; TRANSCRIPTOME;

EID: 84890390626     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00162.2013     Document Type: Article

References (59)

1. Anonymous. The diabetes pandemic. Lancet 378: 99, 2011.
2. Anonymous. Diabetes Atlas IDF. Brussels, Belgium: International Diabetes Federation, 2012.
3. Albright A, Franz M, Hornsby G, Kriska A, Marrero D, Ullrich I, Verity LS. American College of Sports Medicine position stand. Exercise and type 2 diabetes. Med Sci Sports Exerc 32: 1345-1360, 2000.
4. Bae EJ, Cho MJ, Kim SG. Metformin prevents an adaptive increase in GSH and induces apoptosis under the conditions of GSH deficiency in H4IIE cells. J Toxicol Environ Health 70: 1371-1380, 2007.
5. Beg ZH, Stonik JA, Brewer HB Jr. Characterization and regulation of reductase kinase, a protein kinase that modulates the enzymic activity of 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Proc Natl Acad Sci USA 76: 4375-4379, 1979.
6. Bergeron R, Previs SF, Cline GW, Perret P, Russell RR 3rd, Young LH, Shulman GI. Effect of 5-aminoimidazole-4-carboxamide-1-beta-Dribofuranoside infusion on in vivo glucose and lipid metabolism in lean and obese Zucker rats. Diabetes 50: 1076-1082, 2001.
7. Berglund L, Brunzell JD, Goldberg AC, Goldberg IJ, Sacks F, Murad MH, Stalenhoef AF. Evaluation and treatment of hypertriglyceridemia: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97: 2969-2989, 2012.
8. Bright NJ, Thornton C, Carling D. The regulation and function of mammalian AMPK-related kinases. Acta Physiol (Oxf) 196: 15-26, 2009.
9. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J. AMPK regulates energy expenditure by modulating NAD metabolism and SIRT1 activity. Nature 458: 1056-1060, 2009.
10. Carling D, Zammit VA, Hardie DG. A common bicyclic protein kinase cascade inactivates the regulatory enzymes of fatty acid and cholesterol biosynthesis. FEBS Lett 223: 217-222, 1987.
11. Fujii N, Hirshman MF, Kane EM, Ho RC, Peter LE, Seifert MM, Goodyear LJ. AMP-activated protein kinase alpha2 activity is not essential for contraction-and hyperosmolarity-induced glucose transport in skeletal muscle. J Biol Chem 280: 39033-39041, 2005.
12. Gao G, Fernandez CS, Stapleton D, Auster AS, Widmer J, Dyck JR, Kemp BE, Witters LA. Non-catalytic beta-and gamma-subunit isoforms of the 5'-AMP-activated protein kinase. J Biol Chem 271: 8675-8681, 1996.
13. Goto-Inoue N, Manabe Y, Miyatake S, Ogino S, Morishita A, Hayasaka T, Masaki N, Setou M, Fujii NL. Visualization of dynamic change in contraction-induced lipid composition in mouse skeletal muscle by matrix-assisted laser desorption/ionization imaging mass spectrometry. Anal Bioanal Chem 403: 1863-1871, 2012.
14. Hardie DG, Carling D. The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur J Biochem 246: 259-273, 1997.
15. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 271: 27879-27887, 1996.
16. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2: 9-19, 2005.
17. Hayashi T, Hirshman MF, Fujii N, Habinowski SA, Witters LA, Goodyear LJ. Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49: 527-531, 2000.
18. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ. Evidence for 5' AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47: 1369-1373, 1998.
19. Hayashi T, Wojtaszewski JF, Goodyear LJ. Exercise regulation of glucose transport in skeletal muscle. Am J Physiol Endocrinol Metab 273: E1039-E1051, 1997.
20. Holmes BF, Kurth-Kraczek EJ, Winder WW. Chronic activation of 5'-AMP-activated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle. J Appl Physiol 87: 1990-1995, 1999.
21. Hossain P, Kawar B, El Nahas M. Obesity and diabetes in the developing world-a growing challenge. N Engl J Med 356: 213-215, 2007.
22. Iglesias MA, Ye JM, Frangioudakis G, Saha AK, Tomas E, Ruderman NB, Cooney GJ, Kraegen EW. AICAR administration causes an apparent enhancement of muscle and liver insulin action in insulin-resistant high-fat-fed rats. Diabetes 51: 2886-2894, 2002.
23. Jaques H. NICE guideline on lipid modification. Eur Heart J 34: 481-482, 2013.
24. Jorgensen SB, Viollet B, Andreelli F, Frosig C, Birk JB, Schjerling P, Vaulont S, Richter EA, Wojtaszewski JF. Knockout of the alpha2 but not alpha1 5'-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranosidebut not contraction-induced glucose uptake in skeletal muscle. J Biol Chem 279: 1070-1079, 2004.
25. Koh HJ, Toyoda T, Fujii N, Jung MM, Rathod A, Middelbeek RJ, Lessard SJ, Treebak JT, Tsuchihara K, Esumi H, Richter EA, Wojtaszewski JF, Hirshman MF, Goodyear LJ. Sucrose nonfermenting AMPK-related kinase (SNARK) mediates contraction-stimulated glucose transport in mouse skeletal muscle. Proc Natl Acad Sci USA 107: 15541-15546, 2010.
26. Kurth-Kraczek EJ, Hirshman MF, Goodyear LJ, Winder WW. 5' AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48: 1667-1671, 1999.
27. Lee-Young RS, Griffee SR, Lynes SE, Bracy DP, Ayala JE, McGuinness OP, Wasserman DH. Skeletal muscle AMP-activated protein kinase is essential for the metabolic response to exercise in vivo. J Biol Chem 284: 23925-23934, 2009.
28. Lehmann R, Zhao X, Weigert C, Simon P, Fehrenbach E, Fritsche J, Machann J, Schick F, Wang J, Hoene M, Schleicher ED, Haring HU, Xu G, Niess AM. Medium chain acylcarnitines dominate the metabolite pattern in humans under moderate intensity exercise and support lipid oxidation. PLoS One 5: e11519, 2010.
29. Lewis GD, Farrell L, Wood MJ, Martinovic M, Arany Z, Rowe GC, Souza A, Cheng S, McCabe EL, Yang E, Shi X, Deo R, Roth FP, Asnani A, Rhee EP, Systrom DM, Semigran MJ, Vasan RS, Carr SA, Wang TJ, Sabatine MS, Clish CB, Gerszten RE. Metabolic signatures of exercise in human plasma. Sci Transl Med 2: 33ra37, 2010.
30. Ma X, Iwanaka N, Masuda S, Karaike K, Egawa T, Hamada T, Toyoda T, Miyamoto L, Nakao K, Hayashi T. Morus alba leaf extract stimulates 5'-AMP-activated protein kinase in isolated rat skeletal muscle. J Ethnopharmacol 122: 54-59, 2009.
31. 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.
32. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, Carling D, Kahn BB. Leptin stimulates fatty-acid oxidation by activating AMPactivated protein kinase. Nature 415: 339-343, 2002.
33. Miyamoto L, Ebihara K, Kusakabe T, Aotani D, Yamamoto-Kataoka S, Sakai T, Aizawa-Abe M, Yamamoto Y, Fujikura J, Hayashi T, Hosoda K, Nakao K. Leptin activates hepatic 5'-AMP-activated protein kinase through sympathetic nervous system and alpha1-adrenergic receptor: a potential mechanism for improvement of fatty liver in lipodystrophy by leptin. J Biol Chem 287: 40441-40447, 2012.
34. Miyamoto L, Toyoda T, Hayashi T, Yonemitsu S, Nakano M, Tanaka S, Ebihara K, Masuzaki H, Hosoda K, Ogawa Y, Inoue G, Fushiki T, Nakao K. Effect of acute activation of 5'-AMP-activated protein kinase on glycogen regulation in isolated rat skeletal muscle. J Appl Physiol 102: 1007-1013, 2007.
35. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ. A role for AMP-activated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094, 2001.
36. Musi N, Hirshman MF, Nygren J, Svanfeldt M, Bavenholm P, Rooyackers O, Zhou G, Williamson JM, Ljunqvist O, Efendic S, Moller DE, Thorell A, Goodyear LJ. Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes 51: 2074-2081, 2002.
37. Nakano M, Hamada T, Hayashi T, Yonemitsu S, Miyamoto L, Toyoda T, Tanaka S, Masuzaki H, Ebihara K, Ogawa Y, Hosoda K, Inoue G, Yoshimasa Y, Otaka A, Fushiki T, Nakao K. Alpha2 isoform-specific activation of 5'adenosine monophosphate-activated protein kinase by 5-aminoimidazole-4-carboxamide-1-beta-D-ribonucleoside at a physiological level activates glucose transport and increases glucose transporter 4 in mouse skeletal muscle. Metabolism 55: 300-308, 2006.
38. Perez-Sampietro M, Casas C, Herrero E. The AMPK family member Snf1 protects Saccharomyces cerevisiae cells upon glutathione oxidation. PLoS One 8: e58283, 2013.
39. Roca-Rivada A, Al-Massadi O, Castelao C, Senin LL, Alonso J, Seoane LM, Garcia-Caballero T, Casanueva FF, Pardo M. Muscle tissue as an endocrine organ: comparative secretome profiling of slowoxidative and fast-glycolytic rat muscle explants and its variation with exercise. J Proteomics 75: 5414-5425, 2012.
40. Sakamoto K, McCarthy A, Smith D, Green KA, Grahame Hardie D, Ashworth A, Alessi DR. Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO J 24: 1810-1820, 2005.
41. Sandstrom ME, Zhang SJ, Bruton J, Silva JP, Reid MB, Westerblad H, Katz A. Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 575: 251-262, 2006.
42. Sandstrom ME, Zhang SJ, Westerblad H, Katz A. Mechanical load plays little role in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 579: 527-534, 2007.
43. Sim K, International Diabetes Federation Clinical Guidelines Task Force. Global Guideline for Type 2 Diabetes. Brussels, Belgium: International Diabetes Federation, 2012.
44. Soga T, Ohashi Y, Ueno Y, Naraoka H, Tomita M, Nishioka T. Quantitative metabolome analysis using capillary electrophoresis mass spectrometry. J Proteome Res 2: 488-494, 2003.
45. Stapleton D, Mitchelhill KI, Gao G, Widmer J, Michell BJ, Teh T, House CM, Fernandez CS, Cox T, Witters LA, Kemp BE. Mammalian AMPactivated protein kinase subfamily. J Biol Chem 271: 611-614, 1996.
46. Swinburn BA, Sacks G, Hall KD, McPherson K, Finegood DT, Moodie ML, Gortmaker SL. The global obesity pandemic: shaped by global drivers and local environments. Lancet 378: 804-814, 2011.
47. Toyoda T, Hayashi T, Miyamoto L, Yonemitsu S, Nakano M, Tanaka S, Ebihara K, Masuzaki H, Hosoda K, Inoue G, Otaka A, Sato K, Fushiki T, Nakao K. Possible involvement of the alpha1 isoform of 5'-AMP-activated protein kinase in oxidative stress-stimulated glucose transport in skeletal muscle. Am J Physiol Endocrinol Metab 287: E166-E173, 2004.
48. Toyoda T, Tanaka S, Ebihara K, Masuzaki H, Hosoda K, Sato K, Fushiki T, Nakao K, Hayashi T. Low-intensity contraction activates the alpha1-isoform of 5'-AMP-activated protein kinase in rat skeletal muscle. Am J Physiol Endocrinol Metab 290: E583-E590, 2006.
49. 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.
50. 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.
51. Wojtaszewski JF, Nielsen P, Hansen BF, Richter EA, Kiens B. Isoform-specific and exercise intensity-dependent activation of 5'-AMPactivated protein kinase in human skeletal muscle. J Physiol 528: 221-226, 2000.
52. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13: 2004-2008, 2003.
53. Wu Y, Viana M, Thirumangalathu S, Loeken MR. AMP-activated protein kinase mediates effects of oxidative stress on embryo gene expression in a mouse model of diabetic embryopathy. Diabetologia 55: 245-254, 2012.
54. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8: 1288-1295, 2002.
55. Yan B, AJ, Wang G, Lu H, Huang X, Liu Y, Zha W, Hao H, Zhang Y, Liu L, Gu S, Huang Q, Zheng Y, Sun J. Metabolomic investigation into variation of endogenous metabolites in professional athletes subject to strength-endurance training. J Appl Physiol 106: 531-538, 2009.
56. Young JC. Exercise prescription for individuals with metabolic disorders. Practical considerations. Sports Med 19: 43-54, 1995.
57. Zheng D, MacLean PS, Pohnert SC, Knight JB, Olson AL, Winder WW, Dohm GL. Regulation of muscle GLUT-4 transcription by AMPactivated protein kinase. J Appl Physiol 91: 1073-1083, 2001.
58. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174, 2001.
59. Zmijewski JW, Banerjee S, Bae H, Friggeri A, Lazarowski ER, Abraham E. Exposure to hydrogen peroxide induces oxidation and activation of AMP-activated protein kinase. J Biol Chem 285: 33154-33164, 2010.