Metabolism - Clinical and Experimental
Volume 55, Issue 3 , Pages 300-308 , March 2006

α2 Isoform–specific activation of 5′adenosine monophosphate–activated protein kinase by 5-aminoimidazole-4-carboxamide-1-β-d-ribonucleoside at a physiological level activates glucose transport and increases glucose transporter 4 in mouse skeletal muscle

  • Masako Nakano

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Taku Hamada

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Tatsuya Hayashi

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • Kyoto University Graduate School of Human and Environmental Studies, Kyoto 606-8501, Japan
    • Corresponding Author InformationCorresponding author. Kyoto University Graduate School of Human and Environmental Studies, Kyoto 606-8501, Japan. Tel.: +81 75 753 6640; fax: +81 75 753 6640.
    • ,
  • Shin Yonemitsu

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Licht Miyamoto

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Taro Toyoda

      Affiliations

    • Division of Food Science and Biotechnology, Kyoto University Graduate School of Agriculture, Kyoto 606-8502, Japan
    • ,
  • Satsuki Tanaka

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Hiroaki Masuzaki

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Ken Ebihara

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Yoshihiro Ogawa

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Kiminori Hosoda

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Gen Inoue

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Yasunao Yoshimasa

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
    • ,
  • Akira Otaka

      Affiliations

    • Department of Bioorganic Medicinal Chemistry, Kyoto University Graduate School of Pharmaceutical Sciences, Kyoto 606-8501, Japan
    • ,
  • Toru Fushiki

      Affiliations

    • Division of Food Science and Biotechnology, Kyoto University Graduate School of Agriculture, Kyoto 606-8502, Japan
    • ,
  • Kazuwa Nakao

      Affiliations

    • Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan

Received 27 October 2004 ,Accepted 24 September 2005.

References 

  1. Hayashi T, Wojtaszewski JF, Goodyear LJ. Exercise regulation of glucose transport in skeletal muscle. Am J Physiol. 1997;273:E1039–E1051
  2. MacLean PS, Zheng D, Dohm GL. Muscle glucose transporter (GLUT 4) gene expression during exercise. Exerc Sport Sci Rev. 2000;28:148–152
  3. Etgen GJ, Jensen J, Wilson CM, et al. Exercise training reverses insulin resistance in muscle by enhanced recruitment of GLUT-4 to the cell surface. Am J Physiol. 1997;272:E864–E869
  4. Hayashi T, Hirshman MF, Kurth EJ, et al. Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes. 1998;47:1369–1373
  5. Kurth-Kraczek EJ, Hirshman MF, Goodyear LJ, et al. 5′ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes. 1999;48:1667–1671
  6. Hayashi T, Hirshman MF, Fujii N, et al. Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes. 2000;49:527–531
  7. Mu J, Brozinick JT, Valladares O, et al. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell. 2001;7:1085–1094
  8. Musi N, Hayashi T, Fujii N, et al. AMP-activated protein kinase activity and glucose uptake in rat skeletal muscle. Am J Physiol Endocrinol Metab. 2001;280:E677–E684
  9. Jorgensen SB, Viollet B, Andreelli F, et al. 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. 2004;279:1070–1079
  10. 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. 1999;87:1990–1995
  11. Ojuka EO, Nolte LA, Holloszy JO. Increased expression of GLUT-4 and hexokinase in rat epitrochlearis muscles exposed to AICAR in vitro. J Appl Physiol. 2000;88:1072–1075
  12. Buhl ES, Jessen N, Schmitz O, et al. Chronic treatment with 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside increases insulin-stimulated glucose uptake and GLUT4 translocation in rat skeletal muscles in a fiber type–specific manner. Diabetes. 2001;50:12–17
  13. Zheng D, MacLean PS, Pohnert SC, et al. Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase. J Appl Physiol. 2001;91:1073–1083
  14. MacLean PS, Zheng D, Jones JP, et al. Exercise-induced transcription of the muscle glucose transporter (GLUT 4) gene. Biochem Biophys Res Commun. 2002;292:409–414
  15. Holmes BF, Lang DB, Birnbaum MJ, et al. AMP kinase is not required for the GLUT4 response to exercise and denervation in skeletal muscle. Am J Physiol Endocrinol Metab. 2004;287:E739–E743
  16. Stapleton D, Mitchelhill KI, Gao G, et al. Mammalian AMP-activated protein kinase subfamily. J Biol Chem. 1996;271:611–614
  17. Fujii N, Hayashi T, Hirshman MF, et al. Exercise induces isoform-specific increase in 5′AMP-activated protein kinase activity in human skeletal muscle. Biochem Biophys Res Commun. 2000;273:1150–1155
  18. Wojtaszewski JF, Nielsen P, Hansen BF, et al. Isoform-specific and exercise intensity-dependent activation of 5′-AMP–activated protein kinase in human skeletal muscle. J Physiol. 2000;528(Pt 1):221–226
  19. Stephens TJ, Chen ZP, Canny BJ, et al. Progressive increase in human skeletal muscle AMPKalpha2 activity and ACC phosphorylation during exercise. Am J Physiol Endocrinol Metab. 2002;282:E688–E694
  20. Musi N, Fujii N, Hirshman MF, et al. AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes. 2001;50:921–927
  21. Chen ZP, McConell GK, Michell BJ, et al. AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation. Am J Physiol Endocrinol Metab. 2000;279:E1202–E1206
  22. Matsumoto K, Ishihara K, Tanaka K, et al. An adjustable-current swimming pool for the evaluation of endurance capacity of mice. J Appl Physiol. 1996;81:1843–1849
  23. Masuzaki H, Ogawa Y, Aizawa-Abe M, et al. Glucose metabolism and insulin sensitivity in transgenic mice overexpressing leptin with lethal yellow agouti mutation: usefulness of leptin for the treatment of obesity-associated diabetes. Diabetes. 1999;48:1615–1622
  24. Toyoda T, Hayashi T, Miyamoto L, et al. 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. 2004;287:E166–E173
  25. Bruning JC, Michael MD, Winnay JN, et al. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell. 1998;2:559–569
  26. Hayashi T, Hirshman MF, Dufresne SD, et al. Skeletal muscle contractile activity in vitro stimulates mitogen-activated protein kinase signaling. Am J Physiol. 1999;277:C701–C707
  27. Stein SC, Woods A, Jones NA, et al. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J. 2000;3:437–443
  28. Davies SP, Sim AT, Hardie DG. Location and function of three sites phosphorylated on rat acetyl-CoA carboxylase by the AMP-activated protein kinase. Eur J Biochem. 1990;187:183–190
  29. Hardie DG, Carling D. The AMP-activated protein kinase—fuel gauge of the mammalian cell?. Eur J Biochem. 1997;246:259–273
  30. Salt I, Celler JW, Hawley SA, et al. AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem J. 1998;334(Pt 1):177–187
  31. 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. 1996;382:43–47
  32. Vincent MF, Erion MD, Gruber HE, et al. Hypoglycaemic effect of AICAriboside in mice. Diabetologia. 1996;39:1148–1155
  33. Vincent MF, Marangos PJ, Gruber HE, et al. Inhibition by AICA riboside of gluconeogenesis in isolated rat hepatocytes. Diabetes. 1991;40:1259–1266
  34. Balon TW, Jasman AP. Acute exposure to AICAR increases glucose transport in mouse EDL and soleus muscle. Biochem Biophys Res Commun. 2001;282:1008–1011
  35. Winder WW, Holmes BF, Rubink DS, et al. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol. 2000;88:2219–2226
  36. Ai H, Ihlemann J, Hellsten Y, et al. Effect of fiber type and nutritional state on AICAR- and contraction-stimulated glucose transport in rat muscle. Am J Physiol Endocrinol Metab. 2002;282:E1291–E1300
  37. Leturque A, Loizeau M, Vaulont S, et al. Improvement of insulin action in diabetic transgenic mice selectively overexpressing GLUT4 in skeletal muscle. Diabetes. 1996;45:23–27
  38. Tsao TS, Burcelin R, Katz EB, et al. Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes. 1996;45:28–36
  39. Fiedler M, Zierath JR, Selen G, et al. 5-Aminoimidazole-4-carboxy-amide-1-beta-d-ribofuranoside treatment ameliorates hyperglycaemia and hyperinsulinaemia but not dyslipidaemia in KKAy-CETP mice. Diabetologia. 2001;44:2180–2186

PII: S0026-0495(05)00359-8

doi: 10.1016/j.metabol.2005.09.003

Metabolism - Clinical and Experimental
Volume 55, Issue 3 , Pages 300-308 , March 2006

Article Tools

* Image Usage & Resolution