PKA phosphorylation of HERG protein regulates the rate of channel synthesis

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 296, Issue 5, 2009, Pages

  Chen, Jian ^a   Sroubek, Jakub ^a   Krishnan, Yamini ^a   Li, Yan ^a   Bian, Jinsong ^b   McDonald, Thomas V ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Adenosine 3 ,5 cyclic monophosphate; Human ether a go go related gene; Potassium channel; Protein kinase A

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; POTASSIUM CHANNEL; POTASSIUM CHANNEL HERG;

ARTICLE; CELL STRAIN HEK293; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOPLASMIC RETICULUM; ETHER-A-GO-GO POTASSIUM CHANNELS; FORSKOLIN; GOLGI APPARATUS; HEAT-SHOCK PROTEINS; HUMANS; KINETICS; MEMBRANE POTENTIALS; MYOCYTES, CARDIAC; PHOSPHORYLATION; POTASSIUM; PROTEIN STABILITY; PROTEIN TRANSPORT; RABBITS; SIGNAL TRANSDUCTION; THIONUCLEOTIDES; TRANSFECTION; UP-REGULATION;

EID: 66149125148     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01252.2008     Document Type: Article

References (54)

1. Anderson CL, Delisle BP, Anson BD, Kilby JA, Will ML, Tester DJ, Gong Q, Zhou Z, Ackerman MJ, January CT. Most LQT2 mutations reduce Kv11.1 (hERG) current by a class 2 (trafficking-deficient) mechanism. Circulation 113: 365-373, 2006. (Pubitemid 43803197)
2. Anh D, Marine JE. Beta blockers as anti-arrhythmic agents. Heart Fail Rev 9: 139-147, 2004. (Pubitemid 39485475)
3. Kr. Am J Physiol Heart Circ Physiol 287: H2154-H2163, 2004.
4. Bose S, Weikl T, Bugl H, Buchner J. Chaperone function of Hsp90-associated proteins. Science 274: 1715-1717, 1996. (Pubitemid 26414904)
5. Bukau B, Horwich AL. The Hsp70 and Hsp60 chaperone machines. Cell 92: 351-366, 1998. (Pubitemid 28093013)
6. Caron JM, Jones AL, Kirschner MW. Autoregulation of tubulin synthesis in hepatocytes and fibroblasts. J Cell Biol 101: 1763-1772, 1985.
7. Chirico WJ, Waters MG, Blobel G. 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332: 805-810, 1988.
8. Connolly BJ, Willits PB, Warrington BH, Murray KJ. 8-(4-Chlorophenyl) thio-cyclic AMP is a potent inhibitor of the cyclic GMP-specific phosphodiesterase (PDE VA). Biochem Pharmacol 44: 2303-2306, 1992.
9. Corbin JD, Beebe SJ, Blackmore PF. cAMP-dependent protein kinase activation lowers hepatocyte cAMP. J Biol Chem 260: 8731-8735, 1985.
10. Cui J, Kagan A, Qin D, Mathew J, Melman YF, McDonald TV. Analysis of the cyclic nucleotide binding domain of the HERG potassium channel and interactions with KCNE2. J Biol Chem 276: 17244-17251, 2001. (Pubitemid 37411531)
11. Cui J, Melman Y, Palma E, Fishman GI, McDonald TV. Cyclic AMP regulates the HERG K+ channel by dual pathways. Curr Biol 10: 671-674, 2000. (Pubitemid 30354704)
12. Curran ME, Splawski I, Timothy KW, Vincent GM, Green ED, Keating MT. A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell 80: 795-803, 1995.
13. Ficker E, Dennis AT, Obejero-Paz CA, Castaldo P, Taglialatela M, Brown AM. Retention in the endoplasmic reticulum as a mechanism of dominant-negative current suppression in human long QT syndrome. J Mol Cell Cardiol 32: 2327-2337, 2000. (Pubitemid 32039783)
14. Ficker E, Dennis AT, Wang L, Brown AM. Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel HERG. Circ Res 92: e87-e100, 2003.
15. Fink AL. Chaperone-mediated protein folding. Physiol Rev 79: 425-449, 1999.
16. Gao T, Newton AC. The turn motif is a phosphorylation switch that regulates the binding of Hsp70 to protein kinase C. J Biol Chem 277: 31585-31592, 2002.
17. Gong Q, Anderson CL, January CT, Zhou Z. Pharmacological rescue of trafficking defective HERG channels formed by coassembly of wildtype and long QT mutant N470D subunits. Am J Physiol Heart Circ Physiol 287: H652-H658, 2004. (Pubitemid 38955296)
18. Gong Q, Jones MA, Zhou Z. Mechanisms of pharmacological rescue of trafficking-defective hERG mutant channels in human long QT syndrome. J Biol Chem 281: 4069-4074, 2006. (Pubitemid 43847832)
19. Gong Q, Keeney DR, Molinari M, Zhou Z. Degradation of traffickingdefective long QT syndrome type II mutant channels by the ubiquitin-proteasome pathway. J Biol Chem 280: 19419-19425, 2005. (Pubitemid 41379650)
20. Hurt CM, Feng FY, Kobilka B. Cell-type specific targeting of the alpha 2c-adrenoceptor. Evidence for the organization of receptor microdomains during neuronal differentiation of PC12 cells. J Biol Chem 275: 35424-35431, 2000.
21. Iaccarino G, Tomhave ED, Lefkowitz RJ, Koch WJ. Reciprocal in vivo regulation of myocardial G protein-coupled receptor kinase expression by beta-adrenergic receptor stimulation and blockade. Circulation 98: 1783-1789, 1998. (Pubitemid 28492500)
22. + channel activity. EMBO J 21: 1889-1898, 2002.
23. Kagan A, Yu Z, Fishman GI, McDonald TV. The dominant negative LQT2 mutation A561V reduces wild-type HERG expression. J Biol Chem 275: 11241-11248, 2000. (Pubitemid 30212770)
24. Kiehn J, Karle C, Thomas D, Yao X, Brachmann J, Kubler W. HERG potassium channel activation is shifted by phorbol esters via protein kinase A-dependent pathways. J Biol Chem 273: 25285-25291, 1998. (Pubitemid 28443294)
25. Kleber AG, Rudy Y. Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 84: 431-488, 2004. (Pubitemid 38365490)
26. Kopperud R, Krakstad C, Selheim F, Doskeland SO. cAMP effector mechanisms. Novel twists for an ' old' signaling system. FEBS Lett 546: 121-126, 2003. (Pubitemid 36782292)
27. Kosik KS, Shimura H. Phosphorylated tau and the neurodegenerative foldopathies. Biochim Biophys Acta 1739: 298-310, 2005. (Pubitemid 40018546)
28. Landray MJ. Sudden death: ACE inhibitors and beta-blockers. Basic Res Cardiol 95 Suppl 1: I37-I40, 2000.
29. Levin G, Keren T, Peretz T, Chikvashvili D, Thornhill WB, Lotan I. Regulation of RCK1 currents with a cAMP analog via enhanced protein synthesis and direct channel phosphorylation. J Biol Chem 270: 14611-14618, 1995.
30. Levitan IB. Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu Rev Physiol 56: 193-212, 1994.
31. Li Y, Sroubek J, Krishnan Y, McDonald TV. A-kinase anchoring protein targeting of protein kinase a and regulation of HERG channels. J Membr Biol 223: 107-116, 2008.
32. Lohse MJ, Engelhardt S, Eschenhagen T. What is the role of beta-adrenergic signaling in heart failure? Circ Res 93: 896-906, 2003. (Pubitemid 37433227)
33. Marx SO, Kurokawa J, Reiken S, Motoike H, D'Armiento J, Marks AR, Kass RS. Requirement of a macromolecular signaling complex for beta adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel. Science 295: 496-499, 2002. (Pubitemid 34101639)
34. McDonald TV, Yu Z, Ming Z, Palma E, Meyers MB, Wang KW, Goldstein SA, Fishman GI. A minK-HERG complex regulates the cardiac potassium current IKr. Nature 388: 289-292, 1997. (Pubitemid 27317974)
35. Meacham GC, Lu Z, King S, Sorscher E, Tousson A, Cyr DM. The Hdj-2/Hsc70 chaperone pair facilitates early steps in CFTR biogenesis. EMBO J 18: 1492-1505, 1999. (Pubitemid 29127063)
36. Nathan DF, Vos MH, Lindquist S. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 94: 12949-12956, 1997. (Pubitemid 27518457)
37. Nerbonne JM, Guo W. Heterogeneous expression of voltage-gated potassium channels in the heart: roles in normal excitation and arrhythmias. J Cardiovasc Electrophysiol 13: 406-409, 2002. (Pubitemid 34407609)
38. Noda Y, Sasaki S. Molecular mechanisms and drug development in aquaporin water channel diseases: molecular mechanism of water channel aquaporin-2 trafficking. J Pharm Sci 96: 249-254, 2004. (Pubitemid 40013330)
39. Novara M, Baldelli P, Cavallari D, Carabelli V, Giancippoli A, Carbone E. Exposure to cAMP and beta-adrenergic stimulation recruits Ca(V)3 T-type channels in rat chromaffin cells through Epac cAMP-receptor proteins. J Physiol 558: 433-449, 2004. (Pubitemid 39117593)
40. + channel (ROMK). Proc Natl Acad Sci USA 102: 9954-9959, 2005.
41. Qian SB, Princiotta MF, Bennink JR, Yewdell JW. Characterization of rapidly degraded polypeptides in mammalian cells reveals a novel layer of nascent protein quality control. J Biol Chem 281: 392-400, 2006.
42. Rockman HA, Koch WJ, Lefkowitz RJ. Seven-transmembrane-spanning receptors and heart function. Nature 415: 206-212, 2002.
43. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774, 2000. (Pubitemid 30212405)
44. Spiegelman BM, Penningroth SM, Kirschner MW. Turnover of tubulin and the N site GTP in Chinese hamster ovary cells. Cell 12: 587-600, 1977.
45. Thomas D, Kiehn J, Katus HA, Karle CA. Defective protein trafficking in hERG-associated hereditary long QT syndrome (LQT2): molecular mechanisms and restoration of intracellular protein processing. Cardiovasc Res 60: 235-241, 2003. (Pubitemid 37412356)
46. Thomas D, Zhang W, Karle CA, Kathofer S, Schols W, Kubler W, Kiehn J. Deletion of protein kinase A phosphorylation sites in the HERG potassium channel inhibits activation shift by protein kinase A. J Biol Chem 274: 27457-27462, 1999. (Pubitemid 129527787)
47. Tomaselli GF, Marban E. Electrophysiological remodeling in hypertrophy and heart failure. Cardiovasc Res 42: 270-283, 1999. (Pubitemid 29243156)
48. Ungerer M, Bohm M, Elce JS, Erdmann E, Lohse MJ. Altered expression of beta-adrenergic receptor kinase and beta 1-adrenergic receptors in the failing human heart. Circulation 87: 454-463, 1993. (Pubitemid 23040915)
49. Witchel HJ, Hancox JC. Familial and acquired long qt syndrome and the cardiac rapid delayed rectifier potassium current. Clin Exp Pharmacol Physiol 27: 753-766, 2000.
50. Young JC, Moarefi I, Hartl FU. Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154: 267-273, 2001. (Pubitemid 34286138)
51. Zhang Y, Nijbroek G, Sullivan ML, McCracken AA, Watkins SC, Michaelis S, Brodsky JL. Hsp70 molecular chaperone facilitates endoplasmic reticulum-associated protein degradation of cystic fibrosis transmembrane conductance regulator in yeast. Mol Biol Cell 12: 1303-1314, 2001. (Pubitemid 33044412)
52. Zhou Z, Gong Q, January CT. Correction of defective protein trafficking of a mutant HERG potassium channel in human long QT syndrome. Pharmacological and temperature effects. J Biol Chem 274: 31123-31126, 1999. (Pubitemid 129501552)
53. Zhou Z, Gong Q, Ye B, Fan Z, Makielski JC, Robertson GA, January CT. Properties of HERG channels stably expressed in HEK 293 cells studied at physiological temperature. Biophys J 74: 230-241, 1998. (Pubitemid 28041752)
54. Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94: 471-480, 1998. (Pubitemid 28391863)