Inhibition of Kir2.1 (KCNJ2) by the AMP-activated protein kinase

Biochemical and Biophysical Research Communications

Volumn 408, Issue 4, 2011, Pages 505-510

  Alesutan, Ioana ^a   Munoz, Carlos ^a   Sopjani, Mentor ^a   Dërmaku Sopjani, Miribane ^a   Michael, Diana ^a   Fraser, Scott ^b   Kemp, Bruce E ^c   Seebohm, Guiscard ^d   Föller, Michael ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b AUSTIN HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

AMPK; Cardiac action potential; Ischaemia; KCNJ2

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; SMALL CYTOPLASMIC RNA; UBIQUITIN PROTEIN LIGASE NEDD4;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; XENOPUS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DOWN-REGULATION; HUMANS; MUTATION; OOCYTES; PHOSPHORYLATION; POTASSIUM CHANNELS, INWARDLY RECTIFYING; XENOPUS;

EID: 79956193992     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2011.04.015     Document Type: Article

References (68)

1. Lopatin A.N., Nichols C.G. Inward rectifiers in the heart: an update on I(K1). J. Mol. Cell Cardiol. 2001, 33:625-638.
2. + channels from guinea-pig cardiomyocytes. J. Physiol. 2001, 532:115-126.
3. Preisig-Muller R., Schlichthorl G., Goerge T., Heinen S., Bruggemann A., Rajan S., Derst C., Veh R.W., Daut J. Heteromerization of Kir2.x potassium channels contributes to the phenotype of Andersen's syndrome. Proc. Natl. Acad. Sci. USA 2002, 99:7774-7779.
4. Xia M., Jin Q., Bendahhou S., He Y., Larroque M.M., Chen Y., Zhou Q., Yang Y., Liu Y., Liu B., Zhu Q., Zhou Y., Lin J., Liang B., Li L., Dong X., Pan Z., Wang R., Wan H., Qiu W., Xu W., Eurlings P., Barhanin J., Chen Y. A Kir2.1 gain-of-function mutation underlies familial atrial fibrillation. Biochem. Biophys. Res. Commun. 2005, 332:1012-1019.
5. Andersen E.D., Krasilnikoff P.A., Overvad H. Intermittent muscular weakness, extrasystoles, and multiple developmental anomalies. A new syndrome?. Acta Paediatr. Scand. 1971, 60:559-564.
6. Plaster N.M., Tawil R., Tristani-Firouzi M., Canun S., Bendahhou S., Tsunoda A., Donaldson M.R., Iannaccone S.T., Brunt E., Barohn R., Clark J., Deymeer F., George A.L., Fish F.A., Hahn A., Nitu A., Ozdemir C., Serdaroglu P., Subramony S.H., Wolfe G., Fu Y.H., Ptacek L.J. Mutations in Kir2.1 cause the developmental and episodic electrical phenotypes of Andersen's syndrome. Cell 2001, 105:511-519.
7. Sansone V., Griggs R.C., Meola G., Ptacek L.J., Barohn R., Iannaccone S., Bryan W., Baker N., Janas S.J., Scott W., Ririe D., Tawil R. Andersen's syndrome: a distinct periodic paralysis. Ann. Neurol. 1997, 42:305-312.
8. Tawil R., Ptacek L.J., Pavlakis S.G., DeVivo D.C., Penn A.S., Ozdemir C., Griggs R.C. Andersen's syndrome: potassium-sensitive periodic paralysis, ventricular ectopy, and dysmorphic features. Ann. Neurol. 1994, 35:326-330.
9. + channels to metabolic inhibitors. J. Biol. Chem. 2002, 277:35815-35818.
10. Lodge N.J., Normandin D.E. Alterations in Ito1, IKr and Ik1 density in the BIO TO-2 strain of syrian myopathic hamsters. J. Mol. Cell Cardiol. 1997, 29:3211-3221.
11. + channels (Kir2.1 or Kir2.2) abolishes protection by ischemic preconditioning in rabbit ventricular cardiomyocytes. Circ. Res. 2004, 95:325-332.
12. Towler M.C., Hardie D.G. AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 2007, 100:328-341.
13. Winder W.W., Thomson D.M. Cellular energy sensing and signaling by AMP-activated protein kinase. Cell Biochem. Biophys. 2007, 47:332-347.
14. McGee S.L., Hargreaves M., PK A.M. Transcriptional regulation. Front. Biosci. 2008, 13:3022-3033.
15. Breen D.M., Sanli T., Giacca A., Tsiani E. Stimulation of muscle cell glucose uptake by resveratrol through sirtuins and AMPK. Biochem. Biophys. Res. Commun. 2008, 374:117-122.
16. Kim T., Davis J., Zhang A.J., He X., Mathews S.T. Curcumin activates AMPK and suppresses gluconeogenic gene expression in hepatoma cells. Biochem. Biophys. Res. Commun. 2009, 388:377-382.
17. Kohan A.B., Talukdar I., Walsh C.M., Salati L.M. A role for AMPK in the inhibition of glucose-6-phosphate dehydrogenase by polyunsaturated fatty acids. Biochem. Biophys. Res. Commun. 2009, 388:117-121.
18. Ota S., Horigome K., Ishii T., Nakai M., Hayashi K., Kawamura T., Kishino A., Taiji M., Kimura T. Metformin suppresses glucose-6-phosphatase expression by a complex I inhibition and AMPK activation-independent mechanism. Biochem. Biophys. Res. Commun. 2009, 388:311-316.
19. Song H., Guan Y., Zhang L., Li K., Dong C. SPARC interacts with AMPK and regulates GLUT4 expression. Biochem. Biophys. Res. Commun. 2010, 396:961-966.
20. Zygmunt K., Faubert B., MacNeil J., Tsiani E. Naringenin, a citrus flavonoid, increases muscle cell glucose uptake via AMPK. Biochem. Biophys. Res. Commun. 2010, 398:178-183.
21. Carling D. The role of the AMP-activated protein kinase in the regulation of energy homeostasis. Novartis Found. Symp. 2007, 286:72-81.
22. Guan F., Yu B., Qi G.X., Hu J., Zeng D.Y., Luo J. Chemical hypoxia-induced glucose transporter-4 translocation in neonatal rat cardiomyocytes. Arch. Med. Res. 2008, 39:52-60.
23. Horie T., Ono K., Nagao K., Nishi H., Kinoshita M., Kawamura T., Wada H., Shimatsu A., Kita T., Hasegawa K. Oxidative stress induces GLUT4 translocation by activation of PI3-K/Akt and dual AMPK kinase in cardiac myocytes. J. Cell Physiol. 2008, 215:733-742.
24. Jensen T.E., Rose A.J., Hellsten Y., Wojtaszewski J.F., Richter E.A. Caffeine-induced Ca(2+) release increases AMPK-dependent glucose uptake in rodent soleus muscle. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E286-E292.
25. Jessen N., Pold R., Buhl E.S., Jensen L.S., Schmitz O., Lund S. Effects of AICAR and exercise on insulin-stimulated glucose uptake, signaling, and GLUT-4 content in rat muscles. J. Appl. Physiol. 2003, 94:1373-1379.
26. Lei B., Matsuo K., Labinskyy V., Sharma N., Chandler M.P., Ahn A., Hintze T.H., Stanley W.C., Recchia F.A. Exogenous nitric oxide reduces glucose transporters translocation and lactate production in ischemic myocardium in vivo. Proc. Natl. Acad. Sci. USA 2005, 102:6966-6971.
27. Li J., Hu X., Selvakumar P., Russell R.R., Cushman S.W., Holman G.D., Young L.H. Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am. J. Physiol. Endocrinol. Metab. 2004, 287:E834-E841.
28. Luiken J.J., Coort S.L., Koonen D.P., Van der Horst D.J., Bonen A., Zorzano A., Glatz J.F. Regulation of cardiac long-chain fatty acid and glucose uptake by translocation of substrate transporters. Pflugers Arch. 2004, 448:1-15.
29. MacLean P.S., Zheng D., Jones J.P., Olson A.L., Dohm G.L. Exercise-induced transcription of the muscle glucose transporter (GLUT 4) gene. Biochem. Biophys. Res. Commun. 2002, 292:409-414.
30. Natsuizaka M., Ozasa M., Darmanin S., Miyamoto M., Kondo S., Kamada S., Shindoh M., Higashino F., Suhara W., Koide H., Aita K., Nakagawa K., Kondo T., Asaka M., Okada F., Kobayashi M. Synergistic up-regulation of Hexokinase-2, glucose transporters and angiogenic factors in pancreatic cancer cells by glucose deprivation and hypoxia. Exp. Cell Res. 2007, 313:3337-3348.
31. Ojuka E.O., Nolte L.A., Holloszy J.O. Increased expression of GLUT-4 and hexokinase in rat epitrochlearis muscles exposed to AICAR in vitro. J. Appl. Physiol. 2000, 88:1072-1075.
32. Park S., Scheffler T.L., Gunawan A.M., Shi H., Zeng C., Hannon K.M., Grant A.L., Gerrard D.E. Chronic elevated calcium blocks AMPK-induced GLUT-4 expression in skeletal muscle. Am. J. Physiol. Cell Physiol. 2009, 296:C106-C115.
33. +-coupled glucose carrier SGLT1 by AMP-activated protein kinase. Mol. Membr. Biol. 2010, 27:137-144.
34. Walker J., Jijon H.B., Diaz H., Salehi P., Churchill T., Madsen K.L. 5-aminoimidazole-4-carboxamide riboside (AICAR) enhances GLUT2-dependent jejunal glucose transport: a possible role for AMPK. Biochem. J. 2005, 385:485-491.
35. Winder W.W., Holmes B.F., Rubink D.S., Jensen E.B., Chen M., Holloszy J.O. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 2000, 88:2219-2226.
36. Zheng D., MacLean P.S., Pohnert S.C., Knight J.B., Olson A.L., Winder W.W., Dohm G.L. Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase. J. Appl. Physiol. 2001, 91:1073-1083.
37. Taub M., Springate J.E., Cutuli F. Targeting of renal proximal tubule Na K-ATPase by salt-inducible kinase. Biochem. Biophys. Res. Commun. 2010, 393:339-344.
38. Foller M., Sopjani M., Koka S., Gu S., Mahmud H., Wang K., Floride E., Schleicher E., Schulz E., Munzel T., Lang F. Regulation of erythrocyte survival by AMP-activated protein kinase. FASEB J. 2009, 23:1072-1080.
39. Hardie D.G. The AMP-activated protein kinase pathway - new players upstream and downstream. J. Cell Sci. 2004, 117:5479-5487.
40. Almaca J., Kongsuphol P., Hieke B., Ousingsawat J., Viollet B., Schreiber R., Amaral M.D., Kunzelmann K. AMPK controls epithelial Na(+) channels through Nedd4-2 and causes an epithelial phenotype when mutated. Pflugers Arch. 2009, 458:713-721.
41. Bhalla V., Oyster N.M., Fitch A.C., Wijngaarden M.A., Neumann D., Schlattner U., Pearce D., Hallows K.R. AMP-activated kinase inhibits the epithelial Na+ channel through functional regulation of the ubiquitin ligase Nedd4-2. J. Biol. Chem. 2006, 281:26159-26169.
42. Carattino M.D., Edinger R.S., Grieser H.J., Wise R., Neumann D., Schlattner U., Johnson J.P., Kleyman T.R., Hallows K.R. Epithelial sodium channel inhibition by AMP-activated protein kinase in oocytes and polarized renal epithelial cells. J. Biol. Chem. 2005, 280:17608-17616.
43. Hallows K.R., Kobinger G.P., Wilson J.M., Witters L.A., Foskett J.K. Physiological modulation of CFTR activity by AMP-activated protein kinase in polarized T84 cells. Am. J. Physiol. Cell Physiol. 2003, 284:C1297-C1308.
44. + channel KCNQ1/KCNE1 by the AMP-activated protein kinase. Mol. Memb. Biol. 2011, 28:79-89.
45. Liu X.S., Jiang M., Zhang M., Tang D., Clemo H.F., Higgins R.S., Tseng G.N. Electrical remodeling in a canine model of ischemic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H560-H571.
46. Henrion U., Strutz-Seebohm N., Duszenko M., Lang F., Seebohm G. Long QT syndrome-associated mutations in the voltage sensor of I(Ks) channels. Cell Physiol. Biochem. 2009, 24:11-16.
47. + channels Kir2. 3. Cell Physiol. Biochem. 2008, 21:347-356.
48. - co-transporter NKCC2 by AMP-activated protein kinase (AMPK). Biochem. J. 2007, 405:85-93.
49. +-nucleoside cotransporter rCNT1. J. Biol. Chem. 2001, 276:27981-27988.
50. Boehmer C., Laufer J., Jeyaraj S., Klaus F., Lindner R., Lang F., Palmada M. Modulation of the voltage-gated potassium channel Kv1. 5 by the SGK1 protein kinase involves inhibition of channel ubiquitination. Cell Physiol. Biochem. 2008, 22:591-600.
51. Mohamed M.R., Alesutan I., Foller M., Sopjani M., Bress A., Baur M., Salama R.H., Bakr M.S., Mohamed M.A., Blin N., Lang F., Pfister M. Functional analysis of a novel I71N mutation in the GJB2 gene among Southern Egyptians causing autosomal recessive hearing loss. Cell Physiol. Biochem. 2010, 26:959-966.
52. Bohmer C., Sopjani M., Klaus F., Lindner R., Laufer J., Jeyaraj S., Lang F., Palmada M. The serum and glucocorticoid inducible kinases SGK1-3 stimulate the neutral amino acid transporter SLC6A19. Cell Physiol. Biochem. 2010, 25:723-732.
53. Laufer J., Boehmer C., Jeyaraj S., Knuwer M., Klaus F., Lindner R., Palmada M., Lang F. The C-terminal PDZ-binding motif in the Kv1. 5 potassium channel governs its modulation by the Na+/H+ exchanger regulatory factor 2. Cell Physiol. Biochem. 2009, 23:25-36.
54. Eckey K., Strutz-Seebohm N., Katz G., Fuhrmann G., Henrion U., Pott L., Linke W.A., Arad M., Lang F., Seebohm G. Modulation of human ether a gogo related channels by CASQ2 contributes to etiology of catecholaminergic polymorphic ventricular tachycardia (CPVT). Cell Physiol. Biochem. 2010, 26:503-512.
55. Alesutan I.S., Ureche O.N., Laufer J., Klaus F., Zurn A., Lindner R., Strutz-Seebohm N., Tavare J.M., Boehmer C., Palmada M., Lang U.E., Seebohm G., Lang F. Regulation of the glutamate transporter EAAT4 by PIKfyve. Cell Physiol. Biochem. 2010, 25:187-194.
56. Lang F., Messner G., Rehwald W. Electrophysiology of sodium-coupled transport in proximal renal tubules. Am. J. Physiol. 1986, 250:F953-F962.
57. Lang F., Busch G.L., Ritter M., Volkl H., Waldegger S., Gulbins E., Haussinger D. Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 1998, 78:247-306.
58. Lang F., Rehwald W. Potassium channels in renal epithelial transport regulation. Physiol. Rev. 1992, 72:1-32.
59. Becker S., Reinehr R., Graf D., vom D.S., Haussinger D. Hydrophobic bile salts induce hepatocyte shrinkage via NADPH oxidase activation. Cell Physiol. Biochem. 2007, 19:89-98.
60. Bortner C.D., Cidlowski J.A. The role of apoptotic volume decrease and ionic homeostasis in the activation and repression of apoptosis. Pflugers Arch. 2004, 448:313-318.
61. Foller M., Kasinathan R.S., Duranton C., Wieder T., Huber S.M., Lang F. PGE2-induced apoptotic cell death in K562 human leukaemia cells. Cell Physiol. Biochem. 2006, 17:201-210.
62. + loss. Cell Physiol. Biochem. 2007, 20:35-44.
63. Shimizu T., Wehner F., Okada Y. Inhibition of hypertonicity-induced cation channels sensitizes HeLa cells to shrinkage-induced apoptosis. Cell Physiol. Biochem. 2006, 18:295-302.
64. Lupescu A., Geiger C., Zahir N., Aberle S., Lang P.A., Kramer S., Wesselborg S., Kandolf R., Foller M., Lang F., Bock C.T. Inhibition of Na+/H+ exchanger activity by parvovirus B19 protein NS1. Cell Physiol. Biochem. 2009, 23:211-220.
65. Boiteux A., Hess B. Design of glycolysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1981, 293:5-22.
66. Rotte A., Pasham V., Eichenmuller M., Bhandaru M., Foller M., Lang F. Upregulation of Na+/H+ exchanger by the AMP-activated protein kinase. Biochem. Biophys. Res. Commun. 2010, 398:677-682.
67. Evans A.M., Mustard K.J., Wyatt C.N., Peers C., Dipp M., Kumar P., Kinnear N.P., Hardie D.G. Does AMP-activated protein kinase couple inhibition of mitochondrial oxidative phosphorylation by hypoxia to calcium signaling in O2-sensing cells?. J. Biol. Chem. 2005, 280:41504-41511.
68. Lira V.A., Soltow Q.A., Long J.H., Betters J.L., Sellman J.E., Criswell D.S. Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1062-E1068.