Accessory subunit KChIP2 modulates the cardiac L-Type calcium current

Circulation Research

Volumn 104, Issue 12, 2009, Pages 1382-1389

  Thomsen, Morten B ^a   Wang, Chaojian ^b   Özgen, Nazira ^a   Wang, Hong Gang ^b   Rosen, Michael R ^a   Pitt, Geoffrey S ^b  

^a Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Amino terminal inhibitory module; Auxiliary subunit; CaV1.2; Ion channels; Mouse models

Indexed keywords

CALCIUM CHANNEL L TYPE; POTASSIUM CHANNEL INTERACTING PROTEIN 2; PROTEIN SUBUNIT; UNCLASSIFIED DRUG; CALCIUM; CAV1.2 PROTEIN, MOUSE; KCNIP2 PROTEIN, MOUSE; KV CHANNEL INTERACTING PROTEIN; MUSCLE PROTEIN; SHAL POTASSIUM CHANNEL;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BIOCHEMISTRY; C57BL 6 MOUSE; CELL ISOLATION; CELL MEMBRANE; CELL MIGRATION; CONTROLLED STUDY; ELECTROCARDIOGRAM; GENOTYPE; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; IMMUNOBLOTTING; ION CURRENT; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; ST SEGMENT ELEVATION; VOLTAGE CLAMP; WHOLE CELL; ANIMAL; CELL CULTURE; CELL MEMBRANE POTENTIAL; GENETICS; ION TRANSPORT; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CELL MEMBRANE; CELLS, CULTURED; ION TRANSPORT; KV CHANNEL-INTERACTING PROTEINS; MALE; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; PROTEIN STRUCTURE, TERTIARY; SHAL POTASSIUM CHANNELS;

EID: 67650215355     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.196972     Document Type: Article

References (39)

1. Sheng M, Tsaur ML, Jan YN, Jan LY. Subcellular segregation of two A-type K+ channel proteins in rat central neurons. Neuron. 1992;9: 271-284.
2. Dixon JE, Shi W, Wang HS, McDonald C, Yu H, Wymore RS, Cohen IS, McKinnon D. Role of the Kv4.3 K+ channel in ventricular muscle. A molecular correlate for the transient outward current. Circ Res. 1996;79: 659-668
3. An WF, Bowlby MR, Betty M, Cao J, Ling HP, Mendoza G, Hinson JW, Mattsson KI, Strassle BW, Trimmer JS, Rhodes KJ. Modulation of A-type potassium channels by a family of calcium sensors. Nature. 2000;403:553-556.
4. Morohashi Y, Hatano N, Ohya S, Takikawa R, Watabiki T, Takasugi N, Imaizumi Y, Tomita T, Iwatsubo T. Molecular cloning and characterization of CALP/KChIP4, a novel EF-hand protein interacting with pre-senilin 2 and voltage-gated potassium channel subunit Kv4. J Biol Chem. 2002;277:14965-14975.
5. Deschenes I, DiSilvestre D, Juang GJ, Wu RC, An WF, Tomaselli GF. Regulation of Kv4.3 current by KChIP2 splice variants: a component of native cardiac I(to)? Circulation. 2002;106:423-429.
6. Thomsen MB, Sosunov EA, Anyukhovsky EP, Ozgen N, Boyden PA, Rosen MR. Deleting the accessory subunit KChIP2 results in loss of Ito,f and increased IK,slow that maintains normal action potential configuration. Heart Rhythm. 2009;6:370-377.
7. Shibata R, Misonou H, Campomanes CR, Anderson AE, Schrader LA, Doliveira LC, Carroll KI, Sweatt JD, Rhodes KJ, Trimmer JS. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J Biol Chem. 2003;278: 36445-36454.
8. Venn N, Haynes LP, Burgoyne RD. Specific effects of KChIP3/ calsenilin/DREAM, but not KChIPs 1, 2 and 4, on calcium signalling and regulated secretion in PC12 cells. Biochem J. 2008;413:71-80.
9. Bahring R, Dannenberg J, Peters HC, Leicher T, Pongs O, Isbrandt D. Conserved Kv4 N-terminal domain critical for effects of Kv channel-interacting protein 2.2 on channel expression and gating. J Biol Chem. 2001;276:23888-23894.
10. Holmqvist MH, Cao J, Hernandez-Pineda R, Jacobson MD, Carroll KI, Sung MA, Betty M, Ge P, Gilbride KJ, Brown ME, Jurman ME, Lawson D, Silos-Santiago I, Xie Y, Covarrubias M, Rhodes KJ, Distefano PS, An WF. Elimination of fast inactivation in Kv4 A-type potassium channels by an auxiliary subunit domain. Proc Natl Acad Sci USA. 2002;99: 1035-1040.
11. Burgoyne RD. Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci. 2007;8:182-193.
12. Burgoyne RD, Weiss JL. The neuronal calcium sensor family of Ca2 +-binding proteins. Biochem J. 2001;353:1-12.
13. Haeseleer F, Imanishi Y, Sokal I, Filipek S, Palczewski K. Calcium-binding proteins: intracellular sensors from the calmodulin superfamily. Biochem Biophys Res Commun. 2002;290:615-623.
14. Zuhlke RD, Pitt GS, Deisseroth K, Tsien RW, Reuter H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature. 1999;399:159-162.
15. Peterson BZ, DeMaria CD, Adelman JP, Yue DT. Calmodulin is the Ca2+ sensor for Ca2 +-dependent inactivation of L-type calcium channels [published erratum in Neuron. 1999;22:893]. Neuron. 1999;22: 549-558.
16. Ivanina T, Blumenstein Y, Shistik E, Barzilai R, Dascal N. Modulation of L-type Ca2 + channels by Gbg and calmodulin via interactions with N and C termini of a1C. J Biol Chem. 2000;275:39846-39854.
17. Dick IE, Tadross MR, Liang H, Tay LH, Yang W, Yue DT. A modular switch for spatial Ca2 + selectivity in the calmodulin regulation of CaV channels. Nature. 2008;451:830-834.
18. Zhou H, Yu K, McCoy KL, Lee A. Molecular mechanism for divergent regulation of Cav1.2 Ca2+ channels by calmodulin and Ca2 +-binding protein-1. J Biol Chem. 2005;280:29612-29619.
19. Cui G, Meyer AC, Calin-Jageman I, Neef J, Haeseleer F, Moser T, Lee A. Ca2 +-binding proteins tune Ca2 +-feedback to Cav1.3 channels in mouse auditory hair cells. J Physiol. 2007;585:791-803.
20. Yang PS, Alseikhan BA, Hiel H, Grant L, Mori MX, Yang W, Fuchs PA, Yue DT. Switching of Ca2 +-dependent inactivation of CaV1.3 channels by calcium binding proteins of auditory hair cells. J Neurosci. 2006;26: 10677-10689.
21. Lee A, Westenbroek RE, Haeseleer F, Palczewski K, Scheuer T, Catterall WA. Differential modulation of Ca(v) 2.1 channels by calmodulin and Ca2 +-binding protein 1. Nat Neurosci. 2002;5:210-217.
22. Li H, Guo W, Mellor RL, Nerbonne JM. KChIP2 modulates the cell surface expression of Kv 1.5-encoded K( + ) channels. J Mol Cell Cardiol. 2005;39:121-132.
23. Deschenes I, Armoundas AA, Jones SP, Tomaselli GF. Post-transcriptional gene silencing of KChIP2 and Navbeta1 in neonatal rat cardiac myocytes reveals a functional association between Na and Ito currents. J Mol Cell Cardiol. 2008;45:336-346.
24. Kuo HC, Cheng CF, Clark RB, Lin JJ, Lin JL, Hoshijima M, Nguyen-Tran VT, Gu Y, Ikeda Y, Chu PH, Ross J, Giles WR, Chien KR. A defect in the Kv channel-interacting protein 2 (KChIP2) gene leads to a complete loss of I(to) and confers susceptibility to ventricular tachycardia. Cell. 2001;107:801-813.
25. Protas L, Barbuti A, Qu J, Rybin VO, Palmiter RD, Steinberg SF, Robinson RB. Neuropeptide Y is an essential in vivo developmental regulator of cardiac ICa,L. Circ Res. 2003;93:972-979.
26. Grabner M, Dirksen RT, Beam KG. Tagging with green fluorescent protein reveals a distinct subcellular distribution of L-type and non-L-type Ca2+ channels expressed in dysgenic myotubes. Proc Natl Acad Sci USA. 1998;95:1903-1908.
27. Ozgen N, Dun W, Sosunov EA, Anyukhovsky EP, Hirose M, Duffy HS, Boyden PA, Rosen MR. Early electrical remodeling in rabbit pulmonary vein results from trafficking of intracellular SK2 channels to membrane sites. Cardiovasc Res. 2007;75:758-769.
28. Ventura A, Maccarana M, Raker VA, Pelicci PG. A cryptic targeting signal induces isoform-specific localization of p46Shc to mitochondria. J Biol Chem. 2004;279:2299-2306.
29. Wang C, Wang HG, Xie H, Pitt GS. Ca2+/CaM controls Ca2 +-dependent inactivation of NMDA receptors by dimerizing the NR1 C termini. J Neurosci. 2008;28:1865-1870.
30. Zhou H, Kim SA, Kirk EA, Tippens AL, Sun H, Haeseleer F, Lee A. Ca2 +-binding protein-1 facilitates and forms a postsynaptic complex with Cav1.2 (L-type) Ca2+ channels. J Neurosci. 2004;24:4698-4708.
31. Kim J, Ghosh S, Nunziato DA, Pitt GS. Identification of the components controlling inactivation of voltage-gated Ca2+ channels. Neuron. 2004; 41:745-754.
32. Shistik E, Ivanina T, Blumenstein Y, Dascal N. Crucial role of N terminus in function of cardiac L-type Ca2 + channel and its modulation by protein kinase C. J Biol Chem. 1998;273:17901-17909.
33. Kanevsky N, Dascal N. Regulation of maximal open probability is a separable function of Ca(v)beta subunit in L-type Ca2 + channel, dependent on NH2 terminus of alpha1C (Ca(v)1.2alpha). J Gen Physiol. 2006;128:15-36.
34. Wei X, Neely A, Olcese R, Lang W, Stefani E, Birnbaumer L. Increase in Ca2 + channel expression by deletions at the amino terminus of the cardiac alpha 1C subunit. Receptors Channels. 1996;4:205-215.
35. Savignac M, Pintado B, Gutierrez-Adan A, Palczewska M, Mellstrom B, Naranjo JR. Transcriptional repressor DREAM regulates T-lymphocyte proliferation and cytokine gene expression. EMBO J. 2005;24: 3555-3564.
36. Saada N, Dai B, Echetebu C, Sarna SK, Palade P. Smooth muscle uses another promoter to express primarily a form of human Cav1.2 L-type calcium channel different from the principal heart form. Biochem Biophys Res Commun. 2003;302:23-28.
37. Guo W, Jung WE, Marionneau C, Aimond F, Xu H, Yamada KA, Schwarz TL, Demolombe S, Nerbonne JM. Targeted deletion of Kv4.2 eliminates I(to,f) and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circ Res. 2005;97:1342-1350.
38. Radicke S, Cotella D, Graf EM, Banse U, Jost N, Varro A, Tseng GN, Ravens U, Wettwer E. Functional modulation of the transient outward current Ito by KCNE beta-subunits and regional distribution in human non-failing and failing hearts. Cardiovasc Res. 2006;71:695-703.
39. Antzelevitch C, Pollevick GD, Cordeiro JM, Casis O, Sanguinetti MC, Aizawa Y, Guerchicoff A, Pfeiffer R, Oliva A, Wollnik B, Gelber P, Bonaros EP Jr, Burashnikov E, Wu Y, Sargent JD, Schickel S, Oberheiden R, Bhatia A, Hsu LF, Haissaguerre M, Schimpf R, Borggrefe M, Wolpert C. Loss-of-function mutations in the cardiac calcium channel underlie a new clinical entity characterized by ST-segment elevation, short QT intervals, and sudden cardiac death. Circulation. 2007;115:442-449.