Hypercholesterolemia induces up-regulation of K ACh cardiac currents via a mechanism independent of phosphatidylinositol 4,5-bisphosphate and Gβγ

Journal of Biological Chemistry

Volumn 287, Issue 7, 2012, Pages 4925-4935

  Deng, Wu ^b   Bukiya, Anna N ^c   Rodríguez Menchaca, Aldo A ^b   Zhang, Zhe ^b   Baumgarten, Clive M ^b   Logothetis, Diomedes E ^b   Levitan, Irena ^a   Rosenhouse Dantsker, Avia ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIO-VASCULAR DISEASE; CARDIOMYOCYTES; CHANNEL ACTIVITY; CHOLESTEROL DEPLETION; CHRONOTROPIC EFFECT; HEART RATES; HYPERCHOLESTEROLEMIA; MYOCYTES; PHOSPHATIDYLINOSITOL 4 ,5-BISPHOSPHATE; RISK FACTORS; UP-REGULATION; XENOPUS OOCYTE;

MAMMALS; NUTRITION;

CHOLESTEROL;

CHOLESTEROL; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN KIR3.1; PROTEIN KIR3.4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLESTEROL DIET; CONTROLLED STUDY; DEPLETION; FEMALE; HEART ATRIUM; HEART MUSCLE CELL; HYPERCHOLESTEROLEMIA; MALE; METABOLIC REGULATION; NONHUMAN; OOCYTE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; RAT; SIGNAL TRANSDUCTION; UPREGULATION; XENOPUS;

ANIMALS; CHOLESTEROL; DIETARY FATS; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; HEART ATRIA; HYPERHOMOCYSTEINEMIA; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; RABBITS; UP-REGULATION; XENOPUS LAEVIS;

ORYCTOLAGUS CUNICULUS; RODENTIA;

EID: 84863163891     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.306134     Document Type: Article

References (52)

1. Breitwieser, G. E., and Szabo, G. (1985) Uncoupling of cardiac muscarinic and β-adrenergic receptors from ion channels by a guanine nucleotide analogue. Nature 317, 538-540 (Pubitemid 16224161)
2. + channels in cell-free membrane of atrial cells. Am. J. Physiol. 251, H681-H684
3. Pfaffinger, P. J., Martin, J. M., Hunter, D. D., Nathanson, N. M., and Hille, B. (1985) GTP-binding proteins couple cardiac muscarinic receptors to a K channel. Nature 317, 536-538 (Pubitemid 16224160)
4. Soejima, M., and Noma, A. (1984) Mode of regulation of the ACh-sensitive K channel by the muscarinic receptor in rabbit atrial cells. Pflügers Arch. 400, 424-431 (Pubitemid 14115046)
5. βγ subunit activation. J. Physiol. 555, 643-657
6. Wickman, K., Nemec, J., Gendler, S. J., and Clapham, D. E. (1998) Abnormal heart rate regulation in GIRK4 knockout mice. Neuron 20, 103-114 (Pubitemid 28078353)
7. Signorini, S., Liao, Y. J., Duncan, S. A., Jan, L. Y., and Stoffel, M. (1997) Normal cerebellar development but susceptibility to seizures in mice lacking G protein-coupled, inwardly rectifying K+ channel GIRK2. Proc. Natl. Acad. Sci. U.S.A. 94, 923-927 (Pubitemid 27074423)
8. + currents in cerebellar granule cells isolated from weaver and Girk2-null mutant mice. Proc. Natl. Acad. Sci. U.S.A. 94, 12210-12217
9. Blednov, Y. A., Stoffel, M., Chang, S. R., and Harris, R. A. (2001) Potassium channels as targets for ethanol: studies of G protein-coupled inwardly rectifying potassium channel 2 (GIRK2)-null mutant mice. J. Pharmacol. Exp. Ther. 298, 521-530 (Pubitemid 32673402)
10. + channel proteins. Nature 374, 135-141
11. + channel (GIRK1/GIRK4) expressed in oocytes. Am. J. Physiol. 272, H195-H206
12. Logothetis, D. E., Kurachi, Y., Galper, J., Neer, E. J., and Clapham, D. E. (1987) The βγ subunits of GTP-binding proteins activate the muscarinic K+ channel in heart. Nature 325, 321-326 (Pubitemid 17053169)
13. Kobayashi, T., and Ikeda, K. (2006)Gprotein-activated inwardly rectifying potassium channels as potential therapeutic targets. Curr. Pharm. Des. 12, 4513-4523 (Pubitemid 44835160)
14. ACh) in atrial fibrillation using a mouse knockout model. J. Am. Coll Cardiol. 37, 2136-2143
15. Menke, J., Lüthje, L., Kastrup, A., and Larsen, J. (2010) Thromboembolism in atrial fibrillation. Am. J. Cardiol. 105, 502-510
16. Hughes, M., and Lip, G. Y. (2008) Stroke and thromboembolism in atrial fibrillation: a systematic review of stroke risk factors, risk stratification schema, and cost effectiveness data. Thromb. Haemost. 99, 295-304 (Pubitemid 351230959)
17. Bettahi, I., Marker, C. L., Roman, M. I., and Wickman, K. (2002) Contribution of the Kir3.1 subunit to the muscarinic-gated atrial potassium channel IKACh. J. Biol. Chem. 277, 48282-48288 (Pubitemid 35470781)
18. Rosenhouse-Dantsker, A., Leal-Pinto, E., Logothetis, D. E., and Levitan, I. (2010) Comparative analysis of cholesterol sensitivity of Kir channels: role of the CD loop. Channels 4, 63-66
19. Vivaudou, M., Chan, K. W., Sui, J. L., Jan, L. Y., Reuveny, E., and Logothetis, D. E. (1997) Probing theGprotein regulation of GIRK1 and GIRK4, the two subunits of the KACh channel, using functional homomeric mutants. J. Biol. Chem. 272, 31553-31560 (Pubitemid 28013297)
20. Lee, A. G. (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta 1612, 1-40
21. Marius, P., Zagnoni, M., Sandison, M. E., East, J. M., Morgan, H., and Lee, A. G. (2008) Binding of anionic lipids to at least three nonannular sites on the potassium channel KcsA is required for channel opening. Biophys. J. 94, 1689-1698
22. Sunshine, C., and McNamee, M. G. (1994) Lipid modulation of nicotinic acetylcholine receptor function: the role of membrane lipid composition and fluidity. Biochim. Biophys. Acta 1191, 59-64 (Pubitemid 24133529)
23. Jones, O. T., and McNamee, M. G. (1988) Annular and nonannular binding sites for cholesterol associated with the nicotinic acetylcholine receptor. Biochemistry 27, 2364-2374
24. Rankin, S. E., Addona, G. H., Kloczewiak, M. A., Bugge, B., and Miller, K. W. (1997) The cholesterol dependence of activation and fast desensitization of the nicotinic acetylcholine receptor. Biophys. J. 73, 2446-2455 (Pubitemid 27471453)
25. Shouffani, A., and Kanner, B. I. (1990) Cholesterol is required for the reconstruction of the sodium- and chloride-coupled, γ-aminobutyric acid transporter from rat brain. J. Biol. Chem. 265, 6002-6008
26. + channel activity through interactions with the βγsubunits of G proteins. J. Biol. Chem. 277, 6088-6096
27. 2interactions. Nat. Cell Biol. 1, 183-188
28. Murata, Y., and Okamura, Y. (2007) Depolarization activates the phosphoinositide phosphatase Ci-VSP, as detected in Xenopus oocytes coexpressing sensors of PIP2. J. Physiol. 583, 875-889 (Pubitemid 47423706)
29. Christian, A. E., Haynes, M. P., Phillips, M. C., and Rothblat, G. H. (1997) Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 38, 2264-2272 (Pubitemid 27495385)
30. + channels in rabbit cardiac myocytes. J. Pharmacol. Exp. Ther. 293, 196-205
31. Wang, Z., Yue, L., White, M., Pelletier, G., and Nattel, S. (1998) Differential distribution of inward rectifier potassium channel transcripts in human atrium versus ventricle. Circulation 98, 2422-2428 (Pubitemid 28549786)
32. Epshtein, Y., Chopra, A. P., Rosenhouse-Dantsker, A., Kowalsky, G. B., Logothetis, D. E., and Levitan, I. (2009) Identification of a C terminus domain critical for the sensitivity of Kir2.1 to cholesterol. Proc. Natl. Acad. Sci. U.S.A. 106, 8055-8060
33. Romanenko, V. G., Fang, Y., Byfield, F., Travis, A. J., Vandenberg, C. A., Rothblat, G. H., and Levitan, I. (2004) Cholesterol sensitivity and lipid raft targeting of Kir2.1 channels. Biophys. J. 87, 3850-3861 (Pubitemid 39602891)
34. + current by optical isomers of cholesterol. Biophys J. 83, 3211-3222
35. Gurdon, J. B., Lane, C. D., Woodland, H. R., and Marbaix, G. (1971) Use of frog eggs and oocytes for the study of messenger RNA and its translation in living cells. Nature 233, 177-182
36. Rishal, I., Porozov, Y., Yakubovich, D., Varon, D., and Dascal, N. (2005) Gβγ-dependent and Gβγ-independent basal activity of G protein-activated K+ channels. J. Biol. Chem. 280, 16685-16694 (Pubitemid 41389126)
37. Huang, C. L., Feng, S., and Hilgemann, D. W. (1998) Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gβγ. Nature 391, 803-806 (Pubitemid 28099680)
38. 2 interactions underlie channelopathies. Neuron 34, 933-944
39. 2. Nat. Chem. Biol. 4, 624-631
40. Bourne, H. R., Sanders, D. A., and McCormick, F. (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348, 125-132
41. Bourne, H. R., Sanders, D. A., and McCormick, F. (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117-127 (Pubitemid 21912023)
42. Reuveny, E., Slesinger, P. A., Inglese, J., Morales, J. M., Iñiguez-Lluhi, J. A., Lefkowitz, R. J., Bourne, H. R., Jan, Y. N., and Jan, L. Y. (1994) Activation of the cloned muscarinic potassium channel by G protein βγ subunits. Nature 370, 143-146 (Pubitemid 24229126)
43. He, C., Zhang, H., Mirshahi, T., and Logothetis, D. E. (1999) Identification of a potassium channel site that interacts with G protein βγ subunits to mediate agonist-induced signaling. J. Biol. Chem. 274, 12517-12524
44. Carman, C. V., Barak, L. S., Chen, C., Liu-Chen, L. Y., Onorato, J. J., Kennedy, S. P., Caron M. G., and Benovic, J. L. (2000) Mutational analysis of Gβγ and phospholipid interaction with G protein-coupled receptor kinase 2. J. Biol. Chem. 275, 10443-10452 (Pubitemid 30202105)
45. Rosenhouse-Dantsker, A., Logothetis, D. E., and Levitan, I. (2011) Cholesterol sensitivity of KIR2.1 is controlled by a belt of residues around the cytosolic pore. Biophys. J. 100, 381-389
46. Pegan, S., Arrabit, C., Zhou, W., Kwiatkowski, W., Collins, A., Slesinger, P. A., and Choe, S. (2005) Cytoplasmic domain structures of Kir2.1 and Kir3.1 show sites for modulating gating and rectification. Nat. Neurosci. 8, 279-287 (Pubitemid 40300184)
47. + channels in aortic endothelium in vitro and in vivo. Circ. Res. 98, 1064-1071
48. Dobrev, D., Friedrich, A., Voigt, N., Jost, N., Wettwer, E., Christ, T., Knaut, M., and Ravens, U. (2005) The G protein-gated potassium current I(K,ACh) is constitutively active in patients with chronic atrial fibrillation. Circulation 112, 3697-3706 (Pubitemid 43739509)
49. Cha, T. J., Ehrlich, J. R., Chartier, D., Qi, X. Y., Xiao, L., and Nattel, S. (2006) Kir3-based inward rectifier potassium current: potential role in atrial tachycardia remodeling effects on atrial repolarization and arrhythmias. Circulation 113, 1730-1737 (Pubitemid 43958465)
50. Ehrlich, J. R., Cha, T. J., Zhang, L., Chartier, D., Villeneuve, L., Hébert, T. E., and Nattel, S. (2004) Characterization of a hyperpolarization-activated time-dependent potassium current in canine cardiomyocytes from pulmonary vein myocardial sleeves and left atrium. J. Physiol. 557, 583-597 (Pubitemid 38807396)
51. Fauchier, L., Pierre, B., de Labriolle, A., Grimard, C., Zannad, N., and Babuty, D. (2008) Antiarrhythmic effect of statin therapy and atrial fibrillation a meta-analysis of randomized controlled trials. J. Am. Coll Cardiol. 51, 828-835 (Pubitemid 351255618)
52. Adam, O., Neuberger, H. R., Böhm, M., and Laufs, U. (2008) Prevention of atrial fibrillation with 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Circulation 118, 1285-1293