Localisation of AMPK γ subunits in cardiac and skeletal muscles

Journal of Muscle Research and Cell Motility

Volumn 34, Issue 5-6, 2013, Pages 369-378

  Pinter, Katalin ^a   Grignani, Robert T ^a,b   Watkins, Hugh ^a   Redwood, Charles ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Subunits; AMPK; Cardiomyopathy; Sub cellular localisation

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ANIMAL; ARTICLE; C57BL MOUSE; CARDIOMYOPATHY; CONFOCAL MICROSCOPY; CYTOLOGY; ENZYMOLOGY; HEART MUSCLE; HUMAN; METABOLISM; MOUSE; PROTEIN SUBUNIT; SKELETAL MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARDIOMYOPATHIES; HUMANS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MUSCLE, SKELETAL; MYOCARDIUM; PROTEIN SUBUNITS;

EID: 84890124737     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-013-9359-4     Document Type: Article

References (55)

1. Alzamora R, Gong F, Rondanino C, Lee JK, Smolak C, Pastor-Soler NM, Hallows KR (2010) AMP-activated protein kinase inhibits KCNQ1 channels through regulation of the ubiquitin ligase Nedd4-2 in renal epithelial cells. Am J Physiol Renal Physiol 299(6):F1308-F1319
2. Andersen MN, Rasmussen HB (2012) AMPK: a regulator of ion channels. Commun Integr Biol 5(5):480-484
3. Andersson L (2003) Identification and characterization of AMPK gamma 3 mutations in the pig. Biochem Soc Trans 31(Pt 1):232-235
4. Arad M, Benson DW, Perez-Atayde AR, McKenna WJ, Sparks EA, Kanter RJ, McGarry K, Seidman JG, Seidman CE (2002) Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J Clin Invest 109(3):357-362
5. Banerjee SK, McGaffin KR, Pastor-Soler NM, Ahmad F (2009) SGLT1 is a novel cardiac glucose transporter that is perturbed in disease states. Cardiovasc Res 84(1):111-118
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 (2004) 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(37):38441-38447
7. Bendayan M, Londono I, Kemp BE, Hardie GD, Ruderman N, Prentki M (2009) Association of AMP-activated protein kinase subunits with glycogen particles as revealed in situ by immunoelectron microscopy. J Histochem Cytochem 57(10):963-971
8. Birk JB, Wojtaszewski JF (2006) Predominant alpha2/beta2/gamma3 AMPK activation during exercise in human skeletal muscle. J Physiol 577(Pt 3):1021-1032
9. Blair E, Redwood C, Ashrafian H, Oliveira M, Broxholme J, Kerr B, Salmon A, Ostman-Smith I, Watkins H (2001) 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(11):1215-1220
10. Bloemberg D, Quadrilatero J (2012) Rapid determination of myosin heavy chain expression in rat, mouse, and human skeletal muscle using multicolor immunofluorescence analysis. PLoS One 7(4):e35273
11. Boncompagni S, Rossi AE, Micaroni M, Beznoussenko GV, Polishchuk RS, Dirksen RT, Protasi F (2009) Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Mol Biol Cell 20(3):1058-1067
12. Cheung PC, Salt IP, Davies SP, Hardie DG, Carling D (2000) Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem J 346(Pt 3):659-669
13. Costford SR, Kavaslar N, Ahituv N, Chaudhry SN, Schackwitz WS, Dent R, Pennacchio LA, McPherson R, Harper ME (2007) Gain-of-function R225W mutation in human AMPKgamma(3) causing increased glycogen and decreased triglyceride in skeletal muscle. PLoS One 2(9):e903
14. Dong Y, Zhang M, Liang B, Xie Z, Zhao Z, Asfa S, Choi HC, Zou MH (2010) Reduction of AMP-activated protein kinase alpha2 increases endoplasmic reticulum stress and atherosclerosis in vivo. Circulation 121(6):792-803
15. Durante PE, Mustard KJ, Park SH, Winder WW, Hardie DG (2002) Effects of endurance training on activity and expression of AMP-activated protein kinase isoforms in rat muscles. Am J Physiol Endocrinol Metab 283(1):E178-E186
16. Eisenberg BR, Kuda AM, Peter JB (1974) Stereological analysis of mammalian skeletal muscle. I. Soleus muscle of the adult guinea pig. J Cell Biol 60(3):732-754
17. Gollob MH (2003) Glycogen storage disease as a unifying mechanism of disease in the PRKAG2 cardiac syndrome. Biochem Soc Trans 31(Pt 1):228-231
18. Gollob MH, Green MS, Tang AS, Gollob T, Karibe A, Ali Hassan AS, Ahmad F, Lozado R, Shah G, Fananapazir L, Bachinski LL, Roberts R (2001) Identification of a gene responsible for familial Wolff-Parkinson-White syndrome. N Engl J Med 344(24):1823-1831
19. Graham TE, Yuan Z, Hill AK, Wilson RJ (2010) The regulation of muscle glycogen: the granule and its proteins. Acta Physiol (Oxf) 199(4):489-498
20. Gregor M, Zeold A, Oehler S, Marobela KA, Fuchs P, Weigel G, Hardie DG, Wiche G (2006) Plectin scaffolds recruit energy-controlling AMP-activated protein kinase (AMPK) in differentiated myofibres. J Cell Sci 119(Pt 9):1864-1875
21. Hamilton SR, Stapleton D, O'Donnell JB Jr, Kung JT, Dalal SR, Kemp BE, Witters LA (2001) An activating mutation in the gamma1 subunit of the AMP-activated protein kinase. FEBS Lett 500(3):163-168
22. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8(10):774-785
23. Hardie DG, Carling D, Carlson M (1998) The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu Rev Biochem 67:821-855
24. Ikematsu N, Dallas ML, Ross FA, Lewis RW, Rafferty JN, David JA, Suman R, Peers C, Hardie DG, Evans AM (2011) Phosphorylation of the voltage-gated potassium channel Kv2.1 by AMP-activated protein kinase regulates membrane excitability. Proc Natl Acad Sci USA 108(44):18132-18137
25. 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 USA 104(29):12017-12022
26. Katz AM (1975) Congestive heart failure: role of altered myocardial cellular control. N Engl J Med 293(23):1184-1191
27. Kim M, Tian R (2011) Targeting AMPK for cardiac protection: opportunities and challenges. J Mol Cell Cardiol 51(4):548-553
28. Kim AS, Miller EJ, Young LH (2009) AMP-activated protein kinase: a core signalling pathway in the heart. Acta Physiol (Oxf) 196(1):37-53
29. Lang T, Yu L, Tu Q, Jiang J, Chen Z, Xin Y, Liu G, Zhao S (2000) Molecular cloning, genomic organization, and mapping of PRKAG2, a heart abundant gamma2 subunit of 5′-AMP-activated protein kinase, to human chromosome 7q36. Genomics 70(2):258-263
30. Mahlapuu M, Johansson C, Lindgren K, Hjalm G, Barnes BR, Krook A, Zierath JR, Andersson L, Marklund S (2004) Expression profiling of the gamma-subunit isoforms of AMP-activated protein kinase suggests a major role for gamma3 in white skeletal muscle. Am J Physiol Endocrinol Metab 286(2):E194-E200
31. 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 (2000) A mutation in PRKAG3 associated with excess glycogen content in pig skeletal muscle. Science 288(5469):1248-1251
32. Murphy RT, Mogensen J, McGarry K, Bahl A, Evans A, Osman E, Syrris P, Gorman G, Farrell M, Holton JL, Hanna MG, Hughes S, Elliott PM, Macrae CA, McKenna WJ (2005) Adenosine monophosphate-activated protein kinase disease mimicks hypertrophic cardiomyopathy and Wolff-Parkinson-White syndrome: natural history. J Am Coll Cardiol 45(6):922-930
33. Oakhill JS, Steel R, Chen ZP, Scott JW, Ling N, Tam S, Kemp BE (2011) AMPK is a direct adenylate charge-regulated protein kinase. Science 332(6036):1433-1435
34. O'Connell KM, Whitesell JD, Tamkun MM (2008) Localization and mobility of the delayed-rectifer K + channel Kv2.1 in adult cardiomyocytes. Am J Physiol Heart Circ Physiol 294(1):H229-H237
35. Oliveira SM, Zhang YH, Sancho Solis R, Isackson H, Bellahcene M, Yavari A, Pinter K, Davies JD, Ge Y, Ashrafian H, Walker JW, Carling D, Watkins H, Casadei B, Redwood C (2012) AMP-activated protein kinase phosphorylates cardiac troponin I and alters contractility of murine ventricular myocytes. Circ Res 110(9):1192-1201
36. Pinter K, Grignani RT, Czibik G, Farza H, Watkins H, Redwood C (2012a) Embryonic expression of AMPK gamma subunits and the identification of a novel gamma2 transcript variant in adult heart. J Mol Cell Cardiol 53(3):342-349
37. Pinter K, Jefferson A, Czibik G, Watkins H, Redwood C (2012b) Subunit composition of AMPK trimers present in the cytokinetic apparatus: implications for drug target identification. Cell Cycle 11(5):917-921
38. Ponticos M, Lu QL, Morgan JE, Hardie DG, Partridge TA, Carling D (1998) Dual regulation of the AMP-activated protein kinase provides a novel mechanism for the control of creatine kinase in skeletal muscle. EMBO J 17(6):1688-1699
39. Prats C, Cadefau JA, Cusso R, Qvortrup K, Nielsen JN, Wojtaszewski JF, Hardie DG, Stewart G, Hansen BF, Ploug T (2005) Phosphorylation-dependent translocation of glycogen synthase to a novel structure during glycogen resynthesis. J Biol Chem 280(24):23165-23172
40. Russell RR III, Bergeron R, Shulman GI, Young LH (1999) Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol 277(2 Pt 2):H643-H649
41. Salt I, Celler JW, Hawley SA, Prescott A, Woods A, Carling D, Hardie DG (1998) AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem J 334(Pt 1):177-187
42. Scott JW, Hawley SA, Green KA, Anis M, Stewart G, Scullion GA, Norman DG, Hardie DG (2004) CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest 113(2):274-284
43. Sears CE, Bryant SM, Ashley EA, Lygate CA, Rakovic S, Wallis HL, Neubauer S, Terrar DA, Casadei B (2003) Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ Res 92(5):e52-e59
44. Soeller C, Cannell MB (1999) Examination of the transverse tubular system in living cardiac rat myocytes by 2-photon microscopy and digital image-processing techniques. Circ Res 84(3):266-275
45. Sopjani M, Bhavsar SK, Fraser S, Kemp BE, Foller M, Lang F (2010) Regulation of Na+-coupled glucose carrier SGLT1 by AMP-activated protein kinase. Mol Membr Biol 27(2-3):137-144
46. Stanley WC, Hall JL, Hacker TA, Hernandez LA, Whitesell LF (1997) Decreased myocardial glucose uptake during ischemia in diabetic swine. Metabolism 46(2):168-172
47. Stapleton D, Woollatt E, Mitchelhill KI, Nicholl JK, Fernandez CS, Michell BJ, Witters LA, Power DA, Sutherland GR, Kemp BE (1997) AMP-activated protein kinase isoenzyme family: subunit structure and chromosomal location. FEBS Lett 409(3):452-456
48. Steinberg GR, Kemp BE (2009) AMPK in Health and Disease. Physiol Rev 89(3):1025-1078
49. Thornton C, Snowden MA, Carling D (1998) Identification of a novel AMP-activated protein kinase beta subunit isoform that is highly expressed in skeletal muscle. J Biol Chem 273(20):12443-12450
50. Turnley AM, Stapleton D, Mann RJ, Witters LA, Kemp BE, Bartlett PF (1999) Cellular distribution and developmental expression of AMP-activated protein kinase isoforms in mouse central nervous system. J Neurochem 72(4):1707-1716
51. Viana R, Towler MC, Pan DA, Carling D, Viollet B, Hardie DG, Sanz P (2007) A conserved sequence immediately N-terminal to the Bateman domains in AMP-activated protein kinase gamma subunits is required for the interaction with the beta subunits. J Biol Chem 282(22):16117-16125
52. Wilson AJ, Quinn KV, Graves FM, Bitner-Glindzicz M, Tinker A (2005) Abnormal KCNQ1 trafficking influences disease pathogenesis in hereditary long QT syndromes (LQT1). Cardiovasc Res 67(3):476-486
53. Winder WW, Hardie DG, Mustard KJ, Greenwood LJ, Paxton BE, Park SH, Rubink DS, Taylor EB (2003) Long-term regulation of AMP-activated protein kinase and acetyl-CoA carboxylase in skeletal muscle. Biochem Soc Trans 31(Pt 1):182-185
54. Yu H, Fujii N, Hirshman MF, Pomerleau JM, Goodyear LJ (2004) Cloning and characterization of mouse 5′-AMP-activated protein kinase gamma3 subunit. Am J Physiol Cell Physiol 286(2):C283-C292
55. Zhang YH, Zhang MH, Sears CE, Emanuel K, Redwood C, El-Armouche A, Kranias EG, Casadei B (2008) Reduced phospholamban phosphorylation is associated with impaired relaxation in left ventricular myocytes from neuronal NO synthase-deficient mice. Circ Res 102(2):242-249