Skeletal muscle AMP-activated protein kinase γ1H151R overexpression enhances whole body energy homeostasis and insulin sensitivity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 309, Issue 7, 2015, Pages E679-E690

  Schönke, Milena ^a   Myers, Martin G ^b   Zierath, Juleen R ^a   Björnholm, Marie ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

AMP activated protein kinase; Metabolism; Skeletal muscle

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; AMP ACTIVATED PROTEIN KINASE GAMMA 1; CARBOHYDRATE; GLYCOGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; LEPTIN; UNCLASSIFIED DRUG; ARGININE; HISTIDINE; PRKAG1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY FAT DISTRIBUTION; BODY WEIGHT; ENERGY BALANCE; ENERGY EXPENDITURE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXTENSOR DIGITORUM LONGUS MUSCLE; FEMALE; FOOD INTAKE; GASTROCNEMIUS MUSCLE; GENE OVEREXPRESSION; GLYCOGEN MUSCLE LEVEL; INSULIN SENSITIVITY; MALE; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; WHITE ADIPOSE TISSUE; AMINO ACID SUBSTITUTION; ANIMAL; C57BL MOUSE; ENERGY METABOLISM; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HOMEOSTASIS; INSULIN RESISTANCE; METABOLISM; MISSENSE MUTATION; TRANSGENIC MOUSE; UPREGULATION;

AMINO ACID SUBSTITUTION; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ARGININE; ENERGY METABOLISM; FEMALE; HISTIDINE; HOMEOSTASIS; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUTATION, MISSENSE; TRANSFECTION; UP-REGULATION;

EID: 84943311604     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00195.2015     Document Type: Article

References (44)

1. Adams J, Chen ZP, Van Denderen BJ, Morton CJ, Parker MW, Witters LA, Stapleton D, Kemp BE. Intrasteric control of AMPK via the gamma1 subunit AMP allosteric regulatory site. Protein Sci 13: 155-165, 2004.
2. Allen T, van Tuyl M, Iyengar P, Jothy S, Post M, Tsao MS, Lobe CG. Grg1 acts as a lung-specific oncogene in a transgenic mouse model. Cancer Res 66: 1294-1301, 2006.
3. Andersson L. Identification and characterization of AMPK gamma 3 mutations in the pig. Biochem Soc Trans 31: 232-235, 2003.
4. Arad M, Moskowitz IP, Patel VV, Ahmad F, Perez-Atayde AR, Sawyer DB, Walter M, Li GH, Burgon PG, Maguire CT, Stapleton D, Schmitt JP, Guo XX, Pizard A, Kupershmidt S, Roden DM, Berul CI, Seidman CE, Seidman JG. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff-Parkinson-White syndrome in glycogen storage cardiomyopathy. Circulation 107: 2850 -2856, 2003.
5. Barnes BR, Glund S, Long YC, Hjalm G, Andersson L, Zierath JR. 5'-AMP-activated protein kinase regulates skeletal muscle glycogen content and ergogenics. FASEB J 19: 773-779, 2005.
6. Barnes BR, Marklund S, Steiler TL, Walter M, Hjalm G, Amarger V, Mahlapuu M, Leng Y, Johansson C, Galuska D, Lindgren K, Abrink M, Stapleton D, Zierath JR, Andersson L. The 5'-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, 2004.
7. Barnes BR, Marklund S, Steiler TL, Walter M, Hjalm G, Amarger V, Mahlapuu M, Leng Y, Johansson C, Galuska D, Lindgren K, Abrink M, Stapleton D, Zierath JR, Andersson L. The 5'-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, 2004.
8. Barre L, Richardson C, Hirshman MF, Brozinick J, Fiering S, Kemp BE, Goodyear LJ, Witters LA. Genetic model for the chronic activation of skeletal muscle AMP-activated protein kinase leads to glycogen accumulation. Am J Physiol Endocrinol Metab 292: E802-E811, 2007.
9. Bergeron R, Russell RR 3rd, Young LH, Ren JM, Marcucci M, Lee A, Shulman GI. Effect of AMPK activation on muscle glucose metabolism in conscious rats. Am J Physiol Endocrinol Metab 276: E938 -E944, 1999.
10. Blair E, Redwood C, Ashrafian H, Oliveira M, Broxholme J, Kerr B, Salmon A, Ostman-Smith I, Watkins H. Mutations in the gamma(2) subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum Mol Genet 10: 1215-1220, 2001.
11. Bothe GW, Haspel JA, Smith CL, Wiener HH, Burden SJ. Selective expression of Cre recombinase in skeletal muscle fibers. Genesis 26: 165-166, 2000.
12. Cheung PC, Salt IP, Davies SP, Hardie DG, Carling D. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem J 346: 659-669, 2000.
13. Costford SR, Kavaslar N, Ahituv N, Chaudhry SN, Schackwitz WS, Dent R, Pennacchio LA, McPherson R, Harper ME. Gain-of-function R225W mutation in human AMPKgamma(3) causing increased glycogen and decreased triglyceride in skeletal muscle. PLoS One 2: e903, 2007.
14. D'Eon TM, Rogers NH, Stancheva ZS, Greenberg AS. Estradiol and the estradiol metabolite, 2-hydroxyestradiol, activate AMP-activated protein kinase in C2C12 myotubes. Obesity (Silver Spring) 16: 1284-1288, 2008.
15. Dyck JR, Gao G, Widmer J, Stapleton D, Fernandez CS, Kemp BE, Witters LA. Regulation of 5'-AMP-activated protein kinase activity by the noncatalytic beta and gamma subunits. J Biol Chem 271: 17798-17803, 1996.
16. Fujii N, Ho RC, Manabe Y, Jessen N, Toyoda T, Holland WL, Summers SA, Hirshman MF, Goodyear LJ. Ablation of AMP-activated protein kinase alpha2 activity exacerbates insulin resistance induced by high-fat feeding of mice. Diabetes 57: 2958-2966, 2008.
17. Garcia-Roves PM, Osler ME, Holmstrom MH, Zierath JR. Gain-offunction R225Q mutation in AMP-activated protein kinase gamma3 subunit increases mitochondrial biogenesis in glycolytic skeletal muscle. J Biol Chem 283: 35724-35734, 2008.
18. Hardie DG. AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond) 32, Suppl 4: S7-S12, 2008.
19. Hardie DG, Carling D, Gamblin SJ. AMP-activated protein kinase: also regulated by ADP? Trends Biochem Sci 36: 470-477, 2011.
20. Henin N, Vincent MF, Gruber HE, Van den Berghe G. Inhibition of fatty acid and cholesterol synthesis by stimulation of AMP-activated protein kinase. FASEB J 9: 541-546, 1995.
21. Hunter RW, Treebak JT, Wojtaszewski JF, Sakamoto K. Molecular mechanism by which AMP-activated protein kinase activation promotes glycogen accumulation in muscle. Diabetes 60: 766-774, 2011.
22. Jensen TE, Ross FA, Kleinert M, Sylow L, Knudsen JR, Gowans GJ, Hardie DG, Richter EA. PT-1 selectively activates AMPK-gamma1 complexes in mouse skeletal muscle, but activates all three gamma subunit complexes in cultured human cells by inhibiting the respiratory chain. Biochem J 467: 461-472, 2015.
23. Kim JY, Jo KJ, Kim BJ, Baik HW, Lee SK. 17α-estradiol induces an interaction between adenosine monophosphate-activated protein kinase and the insulin signaling pathway in 3T3-L1 adipocytes. Int J Mol Med 30: 979-985, 2012.
24. Koistinen HA, Galuska D, Chibalin AV, Yang J, Zierath JR, Holman GD, Wallberg-Henriksson H 5-amino-imidazole carboxamide riboside increases glucose transport and cell-surface GLUT4 content in skeletal muscle from subjects with type 2 diabetes. Diabetes 52: 1066 -1072, 2003.
25. 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.
26. Lundsgaard AM, Kiens B. Gender differences in skeletal muscle substrate metabolism -molecular mechanisms and insulin sensitivity. Front Endocrinol (Lausanne) 5: 195, 2014.
27. Mahlapuu M, Johansson C, Lindgren K, Hjälm G, Barnes BR, Krook A, Zierath JR, Andersson L, Marklund S. Expression profiling of the γ-subunit isoforms of AMP-activated protein kinase suggests a major role for γ3 in white skeletal muscle. Am J Physiol Endocrinol Metab 286: E194-E200, 2004.
28. 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.
29. Milan D, Jeon JT, Looft C, Amarger V, Robic A, Thelander M, Rogel-Gaillard C, Paul S, Iannuccelli N, Rask L, Ronne H, Lundstrom K, Reinsch N, Gellin J, Kalm E, Roy PL, Chardon P, Andersson L. A mutation in PRKAG3 associated with excess glycogen content in pig skeletal muscle. Science 288: 1248-1251, 2000.
30. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferre P, Birnbaum MJ, Stuck BJ, Kahn BB. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428: 569-574, 2004.
31. Musi N, Fujii N, Hirshman MF, Ekberg I, Froberg S, Ljungqvist O, Thorell A, Goodyear LJ. AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 50: 921-927, 2001.
32. 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.
33. Rajakumari S, Wu J, Ishibashi J, Lim HW, Giang AH, Won KJ, Reed RR, Seale P. EBF2 determines and maintains brown adipocyte identity. Cell Metab 17: 562-574, 2013.
34. Rockl KS, Hirshman MF, Brandauer J, Fujii N, Witters LA, Goodyear LJ. Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift. Diabetes 56: 2062-2069, 2007.
35. Roepstorff C, Thiele M, Hillig T, Pilegaard H, Richter EA, Wojtaszewski JF, Kiens B. Higher skeletal muscle alpha2AMPK activation and lower energy charge and fat oxidation in men than in women during submaximal exercise. J Physiol 574: 125-138, 2006.
36. Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, Wolfe RR. Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol Endocrinol Metab 265: E380-E391, 1993.
37. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D. Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403: 139-148, 2007.
38. Steinberg GR, Kemp BE. AMPK in Health and Disease. Physiol Rev 89: 1025-1078, 2009.
39. 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.
40. Viollet B, Andreelli F, Jorgensen SB, Perrin C, Flamez D, Mu J, Wojtaszewski JF, Schuit FC, Birnbaum M, Richter E, Burcelin R, Vaulont S. Physiological role of AMP-activated protein kinase (AMPK): insights from knockout mouse models. Biochem Soc Trans 31: 216-219, 2003.
41. Viollet B, Athea Y, Mounier R, Guigas B, Zarrinpashneh E, Horman S, Lantier L, Hebrard S, Devin-Leclerc J, Beauloye C, Foretz M, Andreelli F, Ventura-Clapier R, Bertrand L. AMPK: Lessons from transgenic and knockout animals. Front Biosci (Landmark Ed) 14: 19-44, 2009.
42. Yu H, Hirshman MF, Fujii N, Pomerleau JM, Peter LE, Goodyear LJ. Muscle-specific overexpression of wild type and R225Q mutant AMPactivated protein kinase gamma3-subunit differentially regulates glycogen accumulation. Am J Physiol Endocrinol Metab 291: E557-E565, 2006.
43. Zhang BB, Zhou G, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 9: 407-416, 2009.
44. Zhu L, Martinez MN, Emfinger CH, Palmisano BT, Stafford JM. Estrogen signaling prevents diet-induced hepatic insulin resistance in male mice with obesity. Am J Physiol Endocrinol Metab 306: E1188-E1197, 2014.