Activation of AMP-activated protein kinase stimulates Na+,K +-ATPase activity in skeletal muscle cells

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 23451-23463

  Benziane, Boubacar ^a   Björnholm, Marie ^a   Pirkmajer, Sergej ^a   Austin, Reginald L ^a   Kotova, Olga ^a   Viollet, Benoit ^b   Zierath, Juleen R ^a   Chibalin, Alexander V ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMP-ACTIVATED PROTEIN KINASE; ATP-ASE ACTIVITY; CATALYTIC SUBUNITS; DEPHOSPHORYLATIONS; ION PUMPING; METABOLIC STRESS; MUSCLE CELL; MYOTUBES; POTENTIAL MECHANISM; PROTEIN PHOSPHATASE; SHORT TERM; SKELETAL MUSCLE; SKELETAL MUSCLE CELLS;

ACTIVATION ENERGY; BIOELECTRIC POTENTIALS; CELL MEMBRANES; CYANIDES; MOLECULAR BIOLOGY; MUSCLE; PHOSPHATASES; PHOSPHORYLATION; PUMPING PLANTS; PUMPS;

SODIUM COMPOUNDS;

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) ALPHA1 SUBUNIT; ESTERASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN PHOSPHATASE METHYLESTERASE 1; SERINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL HYPOXIA; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE SILENCING; MOUSE; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN METHYLATION; PROTEIN TRANSPORT; RAT; SKELETAL MUSCLE;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BLOTTING, WESTERN; CARBOXYLIC ESTER HYDROLASES; CELL HYPOXIA; CELLS, CULTURED; ENZYME ACTIVATION; METHYLATION; MICE; MICE, KNOCKOUT; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN SUBUNITS; PYRONES; RATS; RIBONUCLEOTIDES; RNA INTERFERENCE; SODIUM-POTASSIUM-EXCHANGING ATPASE; THIOPHENES;

RATTUS; STROPHANTHUS GRATUS;

EID: 84863633664     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.331926     Document Type: Article

References (62)

1. Skou, J. C. (1988) The Na,K-pump. Methods Enzymol. 156, 1-25
2. Blanco, G., and Mercer, R. W. (1998) Isozymes of the Na,K-ATPase. Heterogeneity in structure, diversity in function. Am. J. Physiol. Renal Physiol. 275, F633-F650
3. Hundal, H. S., Maxwell, D. L., Ahmed, A., Darakhshan, F., Mitsumoto, Y., and Klip, A. (1994) Subcellular distribution and immunocytochemical localization of Na,K-ATPase subunit isoforms in human skeletal muscle. Mol. Membr. Biol. 11, 255-262
4. + pump subunits to the plasma membrane in human skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R1107-R1110
5. +-ATPase isoform mRNA, but not protein expression in human skeletal muscle. J. Physiol. 556, 507-519
6. + pump protects muscle excitability and contractility during exercise. Exerc. Sport Sci. Rev. 28, 159-164
7. + pump regulation and skeletal muscle contractility. Physiol. Rev. 83, 1269-1324
8. Benziane, B., and Chibalin, A. V. (2008) Frontiers. Skeletal muscle sodium pump regulation. A translocation paradigm. Am. J. Physiol. Endocrinol. Metab. 295, E553-558
9. Hardie, D. G. (2003) Minireview. The AMP-activated protein kinase cascade. The key sensor of cellular energy status. Endocrinology 144, 5179-5183
10. Kemp, B. E., Stapleton, D., Campbell, D. J., Chen, Z. P., Murthy, S., Walter, M., Gupta, A., Adams, J. J., Katsis, F., van Denderen, B., Jennings, I. G., Iseli, T., Michell, B. J., and Witters, L. A. (2003) AMP-activated protein kinase, super metabolic regulator. Biochem. Soc. Trans. 31, 162-168 (Pubitemid 36241420)
11. Hardie, D. G. (2004) AMP-activated protein kinase. A key system mediating metabolic responses to exercise. Med. Sci. Sports Exerc. 36, 28-34
12. Hardie, D. G., and Sakamoto, K. (2006) AMPK. A key sensor of fuel and energy status in skeletal muscle. Physiology 21, 48-60 (Pubitemid 43752517)
13. Corton, J. M., Gillespie, J. G., Hawley, S. A., and Hardie, D. G. (1995) 5-Aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur. J. Biochem. 229, 558-565
14. Cool, B., Zinker, B., Chiou, W., Kifle, L., Cao, N., Perham, M., Dickinson, R., Adler, A., Gagne, G., Iyengar, R., Zhao, G., Marsh, K., Kym, P., Jung, P., Camp, H. S., and Frevert, E. (2006) Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab. 3, 403-416 (Pubitemid 43811782)
15. +-ATPase. Am. J. Physiol. Cell Physiol. 297, 1554-1566
16. + channels through Nedd4-2 and causes an epithelial phenotype when mutated. Pflugers Arch. 458, 713-721
17. + channel through functional regulation of the ubiquitin ligase Nedd4-2. J. Biol. Chem. 281, 26159-26169
18. Carattino, M. D., Edinger, R. S., Grieser, H. J., Wise, R., Neumann, D., Schlattner, U., Johnson, J. P., Kleyman, T. R., and Hallows, K. R. (2005) Epithelial sodium channel inhibition by AMP-activated protein kinase in oocytes and polarized renal epithelial cells. J. Biol. Chem. 280, 17608-17616 (Pubitemid 41388995)
19. Hallows, K. R., Raghuram, V., Kemp, B. E., Witters, L. A., and Foskett, J. K. (2000) Inhibition of cystic fibrosis transmembrane conductance regulator by novel interaction with the metabolic sensor AMP-activated protein kinase. J. Clin. Invest. 105, 1711-1721 (Pubitemid 30421752)
20. - secretion by AMPK in vivo. Pflugers Arch. 457, 1071-1078
21. - co-transporter NKCC2 by AMP-activated protein kinase (AMPK). Biochem. J. 405, 85-93
22. Woollhead, A. M., Scott, J. W., Hardie, D. G., and Baines, D. L. (2005) Phenformin and 5-aminoimidazole-4-carboxamide-1-β-d-RIBOFURANOSIDE (AICAR) ACTIVATION OF AMP-ACTIVATED PROTEIN KINASE INHIBITS TRANSEPITHELIAL NA+ TRANSPORT ACROSS H441 LUNG CELLS. J. PHYSIOL. 566, 781-792 (Pubitemid 41122661)
23. + transport processes across human lung epithelial cells. Br. J. Pharmacol. 151, 1204-1215
24. 2-induced alveolar epithelial dysfunction in rats and human cells by promoting Na,K-ATPase endocytosis. J. Clin. Invest. 118, 752-762
25. +-ATPase. J. Biol. Chem. 269, 19659-19662
26. +-ATPase and mediates the adenosine monophosphate- stimulated protein kinase-dependent regulation of sodium pump surface expression. Mol. Biol. Cell 21, 4400-4408
27. Hulo, S., Tiesset, H., Lancel, S., Edmé, J. L., Viollet, B., Sobaszek, A., and Nevière, R. (2011) AMP-activated protein kinase deficiency reduces ozone-induced lung injury and oxidative stress in mice. Respir. Res. 12, 64
28. +]. Am. J. Physiol. Cell Physiol. 294, C126-C135
29. +-adenosine triphosphatase α-subunits in rat skeletal muscle. Endocrinology 142, 3474-3482
30. +-ATPase activity in cultured rat skeletal muscle cells. J. Biol. Chem. 272, 23653-23658
31. Mounier, R., Lantier, L., Leclerc, J., Sotiropoulos, A., Pende, M., Daegelen, D., Sakamoto, K., Foretz, M., and Viollet, B. (2009) Important role for AMPKα1 in limiting skeletal muscle cell hypertrophy. FASEB J. 23, 2264-2273
32. Lantier, L., Mounier, R., Leclerc, J., Pende, M., Foretz, M., and Viollet, B. (2010) Coordinated maintenance of muscle cell size control by AMPactivated protein kinase. FASEB J. 24, 3555-3561
33. Konrad, D., Rudich, A., Bilan, P. J., Patel, N., Richardson, C., Witters, L. A., and Klip, A. (2005) Troglitazone causes acute mitochondrial membrane depolarization and an AMPK-mediated increase in glucose phosphorylation in muscle cells. Diabetologia 48, 954-966 (Pubitemid 40767990)
34. +-ATPase by phosphorylation of the α-subunit in human skeletal muscle cells. J. Biol. Chem. 279, 25211-25218
35. 18 in the rat α-subunit and is responsible for the decreased activity in epithelial cells. J. Biol. Chem. 274, 1920-1927
36. +-ATPase endocytosis. J. Biol. Chem. 273, 8814-8819
37. Dada, L. A., Chandel, N. S., Ridge, K. M., Pedemonte, C., Bertorello, A. M., and Sznajder, J. I. (2003) Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-ζ. J. Clin. Invest. 111, 1057-1064 (Pubitemid 36397482)
38. +-ATPase α-subunit is essential for AP-2 binding and clathrindependent endocytosis. J. Biol. Chem. 277, 17108-17111
39. +-ATPase. J. Physiol. 518, 37-46
40. 1-subunit in HEK-293 cells. Am. J. Physiol. Cell Physiol. 281, C1797-1803
41. 1-subunit dephosphorylation by protein phosphatase 2A is necessary for its recruitment to the plasma membrane. FASEB J. 20, 2618-2620
42. Fellner, T., Lackner, D. H., Hombauer, H., Piribauer, P., Mudrak, I., Zaragoza, K., Juno, C., and Ogris, E. (2003) A novel and essential mechanism determining specificity and activity of protein phosphatase 2A (PP2A) in vivo. Genes Dev. 17, 2138-2150 (Pubitemid 37052293)
43. Kim, K. Y., Baek, A., Hwang, J. E., Choi, Y. A., Jeong, J., Lee, M. S., Cho, D. H., Lim, J. S., Kim, K. I., and Yang, Y. (2009) Adiponectin-activated AMPK stimulates dephosphorylation of AKT through protein phosphatase 2A activation. Cancer Res. 69, 4018-4026
44. Sjöström, M., Stenström, K., Eneling, K., Zwiller, J., Katz, A. I., Takemori, H., and Bertorello, A. M. (2007) SIK1 is part of a cell sodium-sensing network that regulates active sodium transport through a calcium-dependent process. Proc. Natl. Acad. Sci. U.S.A. 104, 16922-16927 (Pubitemid 350210966)
45. 1-AMP-activated protein kinase regulates hypoxia-induced Na,K-ATPase endocytosis via direct phosphorylation of protein kinase Cζ. Mol. Cell. Biol. 29, 3455-3464
46. +-ATPase translocation to the plasma membrane in a process mediated by the action of Akt. J. Cell Sci. 123, 1343-1351
47. Barlet-Bas, C., Khadouri, C., Marsy, S., and Doucet, A. (1990) Enhanced intracellular sodium concentration in kidney cells recruits a latent pool of Na,K-ATPase whose size is modulated by corticosteroids. J. Biol. Chem. 265, 7799-7803
48. Efendiev, R., Das-Panja, K., Cinelli, A. R., Bertorello, A. M., and Pedemonte, C. H. (2007) Localization of intracellular compartments that exchange Na,K-ATPase molecules with the plasma membrane in a hormone- dependent manner. Br. J. Pharmacol. 151, 1006-1013 (Pubitemid 47195524)
49. Hardie, D. G. (2011) Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism. Proc. Nutr. Soc. 70, 92-99
50. Seo-Mayer, P. W., Thulin, G., Zhang, L., Alves, D. S., Ardito, T., Kashgarian, M., and Caplan, M. J. (2011) Preactivation of AMPK by metformin may ameliorate the epithelial cell damage caused by renal ischemia. Am. J. Physiol. Renal Physiol. 301, F1346-1357
51. Rolfe, D. F., and Brown, G. C. (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758 (Pubitemid 27328739)
52. Erecińska, M., and Silver, I. A. (1989) ATP and brain function. J. Cereb. Blood Flow Metab. 9, 2-19 (Pubitemid 19053430)
53. +- dependent adenosine triphosphatase-mediated ion transport in the intact renal cell. J. Biol. Chem. 256, 10319-10328
54. Clausen, T., Van Hardeveld, C., and Everts, M. E. (1991) Significance of cation transport in control of energy metabolism and thermogenesis. Physiol. Rev. 71, 733-774
55. Crambert, G., Fuzesi, M., Garty, H., Karlish, S., and Geering, K. (2002) Phospholemman (FXYD1) associates with Na,K-ATPase and regulates its transport properties. Proc. Natl. Acad. Sci. U.S.A. 99, 11476-11481 (Pubitemid 34920950)
56. +-ATPase by vasopressin in the cortical collecting duct. J. Membr. Biol. 153, 233-239
57. Lecuona, E., Garcia, A., and Sznajder, J. I. (2000) A novel role for protein phosphatase 2A in the dopaminergic regulation of Na,K-ATPase. FEBS Lett. 481, 217-220
58. Wang, M. Y., and Unger, R. H. (2005) Role of PP2C in cardiac lipid accumulation in obese rodents and its prevention by troglitazone. Am. J. Physiol. Endocrinol. Metab. 288, E216-221
59. Wu, Y., Song, P., Xu, J., Zhang, M., and Zou, M. H. (2007) Activation of protein phosphatase 2A by palmitate inhibits AMP-activated protein kinase. J. Biol. Chem. 282, 9777-9788 (Pubitemid 47104626)
60. Xing, Y., Li, Z., Chen, Y., Stock, J. B., Jeffrey, P. D., and Shi, Y. (2008) Structural mechanism of demethylation and inactivation of protein phosphatase 2A. Cell 133, 154-163 (Pubitemid 351442993)
61. Ortega-Gutiérrez, S., Leung, D., Ficarro, S., Peters, E. C., and Cravatt, B. F. (2008) Targeted disruption of the PME-1 gene causes loss of demethylated PP2A and perinatal lethality in mice. PLoS One 3, e2486
62. Hombauer, H., Weismann, D., Mudrak, I., Stanzel, C., Fellner, T., Lackner, D. H., and Ogris, E. (2007) Generation of active protein phosphatase 2A is coupled to holoenzyme assembly. PLoS Biol. 5, e155