Adrenergic regulation of cardiac ionic channels: Role of membrane microdomains in the regulation of kv4 channels

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 2, 2014, Pages 692-699

  Gallego, Mónica ^a   Alday, Aintzane ^a   Alonso, Hiart ^a   Casis, Oscar ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Arrhythmia; Compartmentation; Heart; Raft

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; CAVEOLIN 3; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; ION CHANNEL; NORADRENALIN; SHAL POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ADRENERGIC STIMULATION; ADRENERGIC SYSTEM; ARRHYTHMOGENESIS; ARTICLE; CALCIUM CURRENT; CAVEOLA; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; HEART MUSCLE POTENTIAL; HEART VENTRICLE HYPERTROPHY; HUMAN; LIPID RAFT; LONG QT SYNDROME; MUTATION; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUDDEN INFANT DEATH SYNDROME; SYMPATHETIC INNERVATION;

ARRHYTHMIA; COMPARTMENTATION; HEART; K(+) CHANNEL; RAFT;

ANIMALS; HEART; HUMANS; ION CHANNELS; MEMBRANE MICRODOMAINS; RECEPTORS, ADRENERGIC, ALPHA-1; SHAL POTASSIUM CHANNELS;

EID: 84892183593     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.06.025     Document Type: Review

References (92)

1. M. Gallego, E. Casis, M.J. Izquierdo, and O. Casis Restoration of cardiac transient potassium current by norepinephrine in diabetic rats Pflügers Arch. Eur. J. Physiol. 441 2000 102 107 (Pubitemid 32146963)
2. T. Volk, T.H.D. Nguyen, J.H. Schultz, and H. Ehmke Relationship between transient outward K + current and Ca + 2 influx in rat cardiac myocytes of endo- and epicardial origin J. Physiol. 519 1999 841 850 (Pubitemid 29462447)
3. N. Speralakis Regulation of calcium slow channels of heart by cyclic nucleotides and effects of ischemia Adv. Pharmacol. 31 1994 1 24
4. R.C. Balijepalli, J.D. Foell, D.D. Hall, J.W. Hell, and T.J. Kamp Localization of cardiac L-type Ca(2 +) channels to a caveolar macromolecular signaling complex is required for beta(2)-adrenergic regulation Proc. Natl. Acad. Sci. U. S. A. 103 2006 7500 7505 (Pubitemid 43727862)
5. M.C. Sanguinetti, M.E. Curran, A. Zou, J. Shen, P.S. Spector, D.L. Atkinson, and M.T. Keating Coassembly of KVLQT1 and minK (IsK) proteins to form cardiac IKS potassium channel Nature 384 1996 80 83 (Pubitemid 26374592)
6. J. Barhanin, F. Lesage, E. Guillemare, M. Fink, M. Lazdunski, and G. Romey KvLQT1 and IsK (minK) proteins associate to form the IKS cardiac potassium current Nature 384 1996 78 80 (Pubitemid 26374591)
7. S.O. Marx, J. Kurokawa, S. Reiken, H. Motoike, J. D'Armiento, A.R. Marks, and R.S. Kass Requirement of a macromolecular signaling complex for β-adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel Science 295 2002 496 499 (Pubitemid 34101639)
8. R.S. Kass, J. Kurokawa, S.O. Marx, and A.R. Marks Leucine/isoleucine zipper coordination of ion channel macromolecular signaling complexes in the heart. Roles in inherited arrhythmias Trends Cardiovasc. Med. 13 2003 52 56 (Pubitemid 36173859)
9. F.S. Cayabyab, and L.C. Schlichter Regulation of an ERG K + current by Src tyrosine kinase J. Biol. Chem. 277 2002 13673 13681 (Pubitemid 34967968)
10. D. Thomas, W. Zhang, C.A. Karle, S. Kathofer, W. Schols, W. Kubler, and J. Kiehn Deletion of protein kinase A phosphorylation sites in the HERG potassium channel inhibits activation shift by protein kinase A J. Biol. Chem. 274 1999 27457 27462
11. A. Kagan, Y.F. Merman, A. Krumerman, and T.V. McDonald 14-3-3 amplifies and prolongs adrenergic stimulation of HERG K + channel activity EMBO J. 21 2002 1889 1898 (Pubitemid 34437186)
12. D. Thomas, K. Wu, A.B. Wimmer, E. Zitron, B.C. Hammerling, S. Kathofer, S. Lueck, R. Bloehs, V.A. Kreye, J. Kiehn, H.A. Katus, W. Schoels, and C.A. Karle Activation of cardiac human ether-a-go-go related gene potassium currents is regulated by alpha(1A)-adrenoceptors J. Mol. Med. 82 2004 826 837
13. R. Sah, R.J. Ramirez, G.Y. Oudit, D. Gidrewicz, M.G. Trivieri, and C. Zobel et al. Regulation of cardiac excitation-contraction coupling by action potential repolarization: role of the transient outward potassium current I(to) J. Physiol. 546 2003 5 18 (Pubitemid 36104968)
14. J.C.L. Tseng-Crank, G.N. Tseng, A. Schwartz, and M.A. Tanouye Molecular cloning and functional expression of a potassium channel cDNA isolated from a rat cardiac library FEBS Lett. 268 1990 63 68 (Pubitemid 20233831)
15. + channel cloned from the cardiovascular system FEBS Lett. 295 1991 211 213
16. S.L. Roberds, and M.M. Tamkun Cloning and tissue-specific expression of five voltage-gated potassium channel cDNAs expressed in rat heart Proc. Natl. Acad. Sci. U. S. A. 88 1991 1798 1802 (Pubitemid 21916313)
17. + channel in ventricular muscle. A molecular correlate for the transient outward current Circ. Res. 79 1996 659 668 (Pubitemid 26317813)
18. Z. Wang, J. Feng, and S. Nattel The potential molecular basis of different physiological properties of transient outward current in rabbit versus human heart Circulation 96 Suppl. I-424 1997
19. M. Näbauer, D.J. Beuckelmann, P. Ueberfuhr, and G. Steinbeck Regional differences in current density and rate-dependent properties of the transient outward current in subepicardial and subendocardial myocytes of human left ventricle Circulation 93 1996 168 177 (Pubitemid 26006581)
20. + current in rat ventricle Am. J. Physiol. Heart Circ. Physiol. 276 1999 H1599 H1607
21. J.E. Dixon, and D. McKinnon Quantitative analysis of mRNA expression in atrial and ventricular muscle of rats Circ. Res. 75 1994 252 260 (Pubitemid 24228317)
22. B. Rosati, Z.M. Pan, S. Lypen, H.S. Wang, I. Cohen, J.E. Dixon, and D. McKinnon Regulation of KChIP potassium channel beta subunit gene expression underlies the gradient of transient outward current in canine and human ventricle J. Physiol. 533 2001 119 125 (Pubitemid 32499364)
23. M. Zheng, W. Zhu, Q. Han, and R.P. Xiao Emerging concepts and therapeutic implications of β-adrenergic receptor subtype signalling Pharmacol. Ther. 108 2005 257 268 (Pubitemid 41691867)
24. R.P. Xiao, and E.G. Lakatta Functional coupling of the β2-adrenoceptor to a pertussis toxin-sensitive G protein in cardiac myocytes Mol. Pharmacol. 47 1995 322 329
25. L.M. Luttrell, S.G. Ferguson, Y. Daaka, W.E. Miller, S. Maudsley, G.J. Della Roca, F.T. Lin, H. Kawakatsu, K. Owada, M.G. Luttrell, M.G. Caron, and R.J. Lefkowitz Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes Science 283 1999 655 661
26. Y. Daaka, L.M. Luttrell, and R.J. Lefkowitz Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A Nature 390 1997 88 91 (Pubitemid 27494762)
27. 2-adrenergic receptor regulates its coupling to Gs and Gi J. Biol. Chem. 277 2002 31249 31256
28. R. Setién, A. Alday, C. Diaz-Asensio, J. Urrutia, M. Gallego, and O. Casis Mechanisms responsible for the trophic effect of beta-adrenoceptors on the Ito current density in type 1 diabetic rat cardiomyocytes Cell. Physiol. Biochem. 31 2013 25 36
29. Y. Shimoni, H.S. Ewart, and D. Severson Type I and II models of diabetes produce different modifications of K + currents in rat heart: role of insulin J. Physiol. 507 1998 485 496 (Pubitemid 28135198)
30. Y. Shimoni, H.S. Ewart, and D. Severson Insulin stimulation of rat ventricular K + currents depends on the integrity of the cytoskeleton J. Physiol. 514 1999 735 745 (Pubitemid 29060320)
31. U. Ravens, X.L. Wang, and E. Wettwer Alpha adrenoceptor stimulation reduces outward currents in rat ventricular myocytes J. Pharmacol. Exp. Ther. 250 1989 364 370 (Pubitemid 19195014)
32. M. Gallego, and O. Casis Regulation of cardiac transient outward potassium current by norepinephrine in normal and diabetic rats Diabetes Metab. Res. 17 2001 304 309 (Pubitemid 32821663)
33. 0 J. Biol. Chem. 268 1993 7532 7537 (Pubitemid 23105654)
34. K. Horie, H. Itoh, and G. Tsujimoto Hamster alpha 1B-adrenergic receptor directly activates Gs in the transfected Chinese hamster ovary cells Mol. Pharmacol. 48 1995 392 400
35. + current via cAMP/PKA mediated pathway in rat heart Am. J. Physiol. Cell Physiol. 288 2005 C577 C583
36. J.D. Corbin, P.H. Sugden, T.M. Lincoln, and S.L. Keely Compartmentalization of adenosine 3′-5′-monophosphate and adenosine 3′-5′-monophosphate-dependent protein-kinase in heart-tissue J. Biol. Chem. 252 1977 3854 3861
37. L.L. Bruton, J.S. Hayes, and S.E. Mayer Functional compartmentalization of cyclic AMP and protein Adv. Cyclic Nucleotide Res. 14 1981 391 397
38. J.J. Carlisle Michel, and J.D. Scott AKAP mediated signal transduction Annu. Rev. Pharmacol. Toxicol. 42 2002 235 257 (Pubitemid 34160527)
39. L.J. Pike Rafts defined: a report on the Keystone symposium on lipid rafts and cell function J. Lipid Res. 47 2006 1597 1598 (Pubitemid 44079915)
40. R.W. Tsien, B.P. Bean, P. Hess, J.B. Lansman, B. Nilius, and M.C. Nowycky Mechanisms of calcium channel modulation by beta-adrenergic agents and dihydropyridine calcium agonists J. Mol. Cell. Cardiol. 18 1986 691 710 (Pubitemid 16056683)
41. H.M. Piper, and G. Isenberg Isolated Adult Cardiomyocytes Hans Michael Piper, Gerrit Isenberg, vol. 2 1989 C.R.C. Press. L.L.C. Boca Raton, FL 29 73
42. J.L. Garvey, E.G. Kranias, and R.G. Solaro Phosphorylation of C-protein, troponin I and phospholamban in isolated rabbit hearts Biochem. J. 249 1998 709 714
43. S. Kawano, F. Nakamura, T. Tanaka, and M. Hiraoka Cardiac sarcoplasmic reticulum chloride channels regulated by protein kinase A Circ. Res. 71 1992 585 589
44. P.C. Gray, B.D. Johnson, R.E. Westenbroek, L.G. Hays, J.R. Yates III, T. Scheuer, W.A. Catterall, and B.J. Murphy Primary structure and function of an A kinase anchoring protein associated with calcium channels Neuron 20 1998 1017 1026 (Pubitemid 28247406)
45. C.C. Malbon, J. Tao, and H. Wan AKAPs (A-Kinase anchoring proteins) and molecules that compose their G-protein-coupled receptor signaling complexes Biochem. J. 379 2004 1 9 (Pubitemid 38491353)
46. T. Harder, and K. Simons Caveolae, DIGs and the dynamics of sphingolipid-cholesterol microdomains Curr. Opin. Cell Biol. 9 1997 534 542 (Pubitemid 27354763)
47. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572 (Pubitemid 27248754)
48. T.M. Williams, and M.P. Lisanti The caveolin genes: from cell biology to medicine Ann. Med. 36 2004 584 595 (Pubitemid 40051435)
49. K.G. Rothberg, J.E. Heuser, W.C. Donzell, Y.S. Ying, J.R. Glenney, and R.G. Anderson Caveolin, a protein component of caveolae membrane coats Cell 68 1992 673 682
50. P.W. Shaul, and R.G. Anderson Role of plasmalemmal caveolae in signal transduction Am. J. Physiol. Lung Cell. Mol. Physiol. 275 1998 L843 L851
51. R. Govers, and T.J. Rabelink Cellular regulation of endothelial nitric oxide synthase Am. J. Physiol. Ren. Physiol. 280 2001 F193 F206
52. M.P. Lisanti, P.E. Scherer, Z. Tang, and M. Sargiacomo Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis Trends Cell Biol. 4 1994 231 235 (Pubitemid 24190653)
53. T. Okatomo, A. Schlegel, P.E. Scherer, and M.P. Lisanti Caveolins, a family of scaffolding proteins for organizing "preassembled signalling complexes" at the plasma membrane J. Biol. Chem. 273 1998 5419 5422 (Pubitemid 28123999)
54. M. Way, and R.G. Parton M-caveolin a muscle-specific caveolin-related protein FEBS Lett. 376 1995 108 112
55. K.S. Song, M. Sargiacomo, F. Galbiati, and M.P. Lisanti Targeting of a Gα subunit (Gi1α) and c-Src tyrosine kinase to caveolae membranes: clarifying the role of N-myristoylation Cell. Mol. Biol. 43 1997 293 303
56. B. Aravamudan, D. Volonte, R. Ramani, E. Gursoy, M.P. Lisanti, B. London, and F. Galbiati Transgenic overexpression of caveolin-3 in the heart induces a cardiomyopathic phenotype Hum. Mol. Genet. 12 2003 2777 2788 (Pubitemid 37407114)
57. S.E. Woodman, D.S. Park, A.W. Cohen, M. Cheung, M. Chandra, J. Shirani, B. Tang, L.A. Jelicks, R.N. Kitsis, G.J. Christ, S.M. Factor, H.B. Tanowitz, and M.P. Lisanti Caveolin-3 knock-out mice develop a progressive cardiomyopathy and show hyperactivation of the p42/44 MAPK cascade J. Biol. Chem. 277 2002 38988 38997 (Pubitemid 35154765)
58. A.W. Cohen, R. Hnasko, W. Schubert, and M.P. Lisanti Role of caveolae and caveolins in health and disease Physiol. Rev. 84 2004 1341 1379 (Pubitemid 39287953)
59. V.O. Rybin, X. Xu, M.P. Lisanti, and S.F. Steinberg Differential targeting of beta-adrenergic receptor subtypes and adenylyl cyclase to cardiomyocytes caveolae. A mechanism to functionally regulate the cAMP signalling pathway J. Biol. Chem. 275 2000 41447 41457 (Pubitemid 32054981)
60. T. Fujita, Y. Toya, K. Iwatsubo, T. Onda, K. Kimura, U. Satoshi, and Y. Ishikawa Accumulation of molecules involved in α1-adrenergic signal within caveolae: caveolin expression and the development of cardiac hypertrophy Cardiovasc. Res. 51 2001 709 716 (Pubitemid 32800712)
61. R.S. Ostrom, R.A. Bundey, and P.A. Insel Nitric oxide inhibition of adenylate cyclase type 6 activity is independent upon lipid rafts and caveolin signalling complexes J. Biol. Chem. 279 2004 19846 19853 (Pubitemid 38623425)
62. 2 + entry requires localization in cholesterol-rich domains J. Biol. Chem. 275 2000 26530 26537
63. C.V. Carman, M.P. Lisanti, and J.F. Benovic Regulation of G protein-coupled receptor kinases by caveolin J. Biol. Chem. 274 1999 8858 8864 (Pubitemid 29164686)
64. B. Razani, C.S. Rubin, and M.P. Lisanti Regulation of cAMP-mediated signal transduction via interaction of caveolins with the catalytic subunit of protein kinase A J. Biol. Chem. 274 1999 26353 26360
65. M.O. Parat, and P.L. Fox Palmitoylation of caveolin-1 in endothelial cells is post-translational but irreversible J. Cell Biol. 276 2001 15776 15782
66. H. Lee, S.E. Woodman, J.A. Engelman, D. Volonte, and F. Galbiati Palmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase: targeting of dually acylated molecules (GPI-linked, transmembrane, or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (TYR-14) J. Biol. Chem. 43 2001 293 303
67. + channel protein in explanted cardiac tissue J. Clin. Invest. 1 1995 282 292
68. R.H. Scannevin, H. Murakaski, K.J. Roodees, and J.S. Trimmer J. Cell Biol. 135 1996 1619 1632
69. J.R. Martens, R. Navarro-Polanco, E.A. Coppock, A. Nishiyama, L. Parsheley, T.D. Grobaski, and M.M. Tamkun Differential targeting of Shaker-like potassium channels to lipid rafts J. Biol. Chem. 275 2000 7443 7446 (Pubitemid 30159634)
70. J. Abi-Char, A. Maguy, A. Coulombe, E. Balse, P. Ratajczak, J.L. Samuel, S. Nattel, and S.N. Hatem Membrane cholesterol modulates Kv1.5 potassium channel distribution and function in rat cardiomyocytes J. Physiol. 582 2007 1205 1217 (Pubitemid 47104349)
71. + channels to distinct lipid raft populations. Targeting of Kv 1.5 to caveolae J. Biol. Chem. 276 2001 8409 8414
72. A. Alday, J. Urrutia, M. Gallego, and O. Casis α1-Adrenoreceptors regulate only the caveolae-located subpopulation of cardiac Kv4 channels Channels 4 2010 168 178
73. F. Xia, X. Gao, E. Kwan, P.P. Lam, L. Chan, and K. Sy Disruption of pancreatic beta-cell lipid rafts modifies Kv2.1 channels gaiting and insulin exocytose J. Biol. Chem. 279 2004 24685 24691 (Pubitemid 38725336)
74. D.A. Zacharias, J.D. Violin, A.C. Newton, and R.Y. Tsien Partitioning of lipid-modified monomeric GFPs into the membrane microdomains of live cells Science 296 2002 913 916 (Pubitemid 34464897)
75. D.E. Saslowsky, J. Lawrence, X. Ren, D.A. Brown, and J.M. Henderson Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers J. Biol. Chem. 277 2002 26966 26970 (Pubitemid 34951707)
76. S. Munro A comparation of the transmembrane domains of Golgi and plasma membrane proteins Biochem. Soc. Trans. 23 1995 527 530
77. R. Vicente, N. Villalonga, M. Calvo, A. Escalada, C. Solsona, C. Soler, M.M. Tamkun, and A. Felipe Kv1.5 association modifies Kv1.3 traffic and membrane localization J. Biol. Chem. 283 2008 8756 8764
78. J. Abi-Char, S. El-Haou, E. Balse, N. Neyroud, R. Vranckx, A. Coulombe, and S.N. Hatem The anchoring protein SAP97 retains Kv1.5 channels in the plasma membrane of cardiac myocytes Am. J. Physiol. Heart Circ. Physiol. 294 2008 H1851 H1861
79. E.J. Folco, G.X. Liu, and G. Koren Caveolin-3 and SAP97 from a scaffolding protein complex that regulates the voltage-gated potassium channels Kv1.5 Am. J. Physiol. Heart Circ. Physiol. 287 2004 H681 H690
80. P.A. Conrad, E.J. Smart, Y.S. Ying, R.G. Anderson, and G.S. Bloom Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps J. Cell Biol. 131 1995 1421 1433 (Pubitemid 26001748)
81. 2 + waves preferentially originate at specific loci in caveolin-rich cell edges Proc. Natl. Acad. Sci. U. S. A. 95 1998 5009 5014
82. H.H. Patel, F. Murray, and P.A. Insel Caveolae as organizers of pharmacologically relevant signal transduction molecules Annu. Rev. Pharmacol. Toxicol. 48 2008 359 391 (Pubitemid 351738158)
83. + currents Circ. Res. 90 2002 586 593 (Pubitemid 34640909)
84. S.F. Steinberg, and L.L. Brunton Compartmentalization of G protein-coupled signaling pathways in cardiac myocytes Annu. Rev. Pharmacol. Toxicol. 41 2001 751 773 (Pubitemid 32385905)
85. M.S. Kapiloff Contributions of protein kinase A anchoring proteins to compartmentalization of cAMP signaling in the heart Mol. Pharmacol. 62 2002 193 199 (Pubitemid 34804096)
86. W. Wong, and L.C. Schlichter Differential recruitment of Kv1.4 and Kv4.2 to lipid rafts by PSD-95 J. Biol. Chem. 279 2004 444 452 (Pubitemid 38044845)
87. A. Bacher, and R.A. McIlhinney Consequences of lipid raft association on G-protein-coupled receptor function Biochem. Soc. Symp. 72 2005 151 164 (Pubitemid 44804743)
88. B. Chini, and M. Parenti G-protein coupled receptors in lipid rafts and caveolae: how, when and why do they go there? J. Mol. Endocrinol. 32 2004 325 338 (Pubitemid 38584639)
89. M. Panneerselvam, H.H. Patel, and D.M. Roth Caveolins and heart diseases Adv. Exp. Med. Biol. 729 2012 145 156
90. E. Gazzerro, F. Sotgia, C. Bruno, M.P. Lisanti, and C. Minetti Caveolinopathies: from the biology of caveolin-3 to human diseases Eur. J. Hum. Genet. 18 2010 137 145
91. M. Vatta, M.J. Ackerman, B. Ye, J.C. Makielski, E.E. Ughanze, E.W. Taylor, D.J. Tester, R.C. Balijepalli, J.D. Foell, Z. Li, T.J. Kamp, and J.A. Towbin Mutant caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome Circulation 114 2006 2104 2112 (Pubitemid 44747890)
92. L.B. Cronk, B. Ye, T. Kaku, D.J. Tester, M. Vatta, J.C. Makielski, and M.J. Ackerman Novel mechanism for sudden infant death syndrome: persistent late sodium current secondary to mutations in caveolin-3 Heart Rhythm 4 2007 161 166 (Pubitemid 46158709)