Kv channel-interacting proteins as neuronal and non-neuronal calcium sensors

References

• An WF, Bowlby MR, Betty M, et al. Modulation of A-type potassium channels by a family of calcium sensors. Nature. 2000;403:553–556.
   PubMed Web of Science ®Google Scholar
• Pongs O, Schwarz JR. Ancillary subunits associated with voltage-dependent K+ channels. Physiol Rev. 2010;90:755–796.
   PubMed Web of Science ®Google Scholar
• Baldwin TJ, Tsaur ML, Lopez GA, et al. Characterization of a mammalian cDNA for an inactivating voltage-sensitive K+ channel. Neuron. 1991;7:471–483.
   PubMed Web of Science ®Google Scholar
• Pak MD, Baker K, Covarrubias M, et al. mShal, a subfamily of A-type K+ channel cloned from mammalian brain. Proc Natl Acad Sci U S A. 1991;88:4386–4390.
   PubMed Web of Science ®Google Scholar
• Jerng HH, Pfaffinger PJ, Covarrubias M. Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci. 2004;27:343–369.
   PubMed Web of Science ®Google Scholar
• Serodio P, Kentros C, Rudy B. Identification of molecular components of A-type channels activating at subthreshold potentials. J Neurophysiol. 1994;72:1516–1529.
   PubMed Web of Science ®Google Scholar
• Dixon JE, Shi W, Wang HS, et al. Role of the Kv4.3 K+ channel in ventricular muscle. A molecular correlate for the transient outward current. Circ Res. 1996;79:659–668.
   PubMed Web of Science ®Google Scholar
• Patel SP, Campbell DL. Transient outward potassium current, ‘Ito’, phenotypes in the mammalian left ventricle: underlying molecular, cellular and biophysical mechanisms. J Physiol. 2005;569:7–39.
   PubMed Web of Science ®Google Scholar
• Serodio P, Vega-Saenz De Miera E, Rudy B. Cloning of a novel component of A-type K+ channels operating at subthreshold potentials with unique expression in heart and brain. J Neurophysiol. 1996;75:2174–2179.
   PubMed Web of Science ®Google Scholar
• Chabala LD, Bakry N, Covarrubias M. Low molecular weight poly(A)+ mRNA species encode factors that modulate gating of a non-Shaker A-type K+ channel. J Gen Physiol. 1993;102:713–728.
   PubMed Web of Science ®Google Scholar
• Rudy B, Hoger JH, Lester HA, et al. At least two mRNA species contribute to the properties of rat brain A-type potassium channels expressed in Xenopus oocytes. Neuron. 1988;1:649–658.
   PubMed Web of Science ®Google Scholar
• Maffie J, Rudy B. Weighing the evidence for a ternary protein complex mediating A-type K+ currents in neurons. J Physiol. 2008;586:5609–5623.
   PubMed Web of Science ®Google Scholar
• Rhodes KJ, Carroll KI, Sung MA, et al. KChIPs and Kv4 α subunits as integral components of A-type potassium channels in mammalian brain. J Neurosci. 2004;24:7903–7915.
   PubMed Web of Science ®Google Scholar
• Burgoyne RD. Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci. 2007;8:182–193.
   PubMed Web of Science ®Google Scholar
• Holmqvist MH, Cao J, Hernandez-Pineda R, et al. Elimination of fast inactivation in Kv4 A-type potassium channels by an auxiliary subunit domain. Proc Natl Acad Sci U S A. 2002;99:1035–1040.
   PubMed Web of Science ®Google Scholar
• Morohashi Y, Hatano N, Ohya S, et al. Molecular cloning and characterization of CALP/KChIP4, a novel EF-hand protein interacting with presenilin 2 and voltage-gated potassium channel subunit Kv4. J Biol Chem. 2002;277:14965–14975.
   PubMed Web of Science ®Google Scholar
• Pruunsild P, Timmusk T. Structure, alternative splicing, and expression of the human and mouse KCNIP gene family. Genomics. 2005;86:581–593.
   PubMed Web of Science ®Google Scholar
• Buxbaum JD, Choi EK, Luo Y, et al. Calsenilin: a calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment. Nat Med. 1998;4:1177–1181.
   PubMed Web of Science ®Google Scholar
• Carrion AM, Link WA, Ledo F, et al. DREAM is a Ca2+-regulated transcriptional repressor. Nature. 1999;398:80–84.
   PubMed Web of Science ®Google Scholar
• Anderson D, Mehaffey WH, Iftinca M, et al. Regulation of neuronal activity by Cav3-Kv4 channel signaling complexes. Nat Neurosci. 2010;13:333–337.
   PubMed Web of Science ®Google Scholar
• Anderson D, Rehak R, Hameed S, et al. Regulation of the Kv4.2 complex by Cav3.1 calcium channels. Channels. 2010;4:163–167.
   PubMed Web of Science ®Google Scholar
• Groen C, Bähring R. Modulation of human Kv4.3/KChIP2 channel inactivation kinetics by cytoplasmic Ca2+. Pflügers Arch: Eur J Physiol. 2017;469:1457–1470.
   PubMed Web of Science ®Google Scholar
• Burgoyne RD, Haynes LP. Understanding the physiological roles of the neuronal calcium sensor proteins. Mol Brain. 2012;5:2.
   PubMed Web of Science ®Google Scholar
• Burgoyne RD, Weiss JL. The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J. 2001;353:1–12.
   PubMed Web of Science ®Google Scholar
• O’Callaghan DW, Hasdemir B, Leighton M, et al. Residues within the myristoylation motif determine intracellular targeting of the neuronal Ca2+ sensor protein KChIP1 to post-ER transport vesicles and traffic of Kv4 K+ channels. J Cell Sci. 2003;116:4833–4845.
   PubMed Web of Science ®Google Scholar
• Ames JB, Ishima R, Tanaka T, et al. Molecular mechanics of calcium-myristoyl switches. Nature. 1997;389:198–202.
   PubMed Web of Science ®Google Scholar
• Zozulya S, Stryer L. Calcium-myristoyl protein switch. Proc Natl Acad Sci U S A. 1992;89:11569–11573.
   PubMed Web of Science ®Google Scholar
• Ames JB, Levay K, Wingard JN, et al. Structural basis for calcium-induced inhibition of rhodopsin kinase by recoverin. J Biol Chem. 2006;281:37237–37245.
   PubMed Web of Science ®Google Scholar
• Takimoto K, Yang EK, Conforti L. Palmitoylation of KChIP splicing variants is required for efficient cell surface expression of Kv4.3 channels. J Biol Chem. 2002;277:26904–26911.
   PubMed Web of Science ®Google Scholar
• Pioletti M, Findeisen F, Hura GL, et al. Three-dimensional structure of the KChIP1-Kv4.3 T1 complex reveals a cross-shaped octamer. Nat Struct Mol Biol. 2006;13:987–995.
   PubMed Web of Science ®Google Scholar
• Scannevin RH, Wang K, Jow F, et al. Two N-terminal domains of Kv4 K+ channels regulate binding to and modulation by KChIP1. Neuron. 2004;41:587–598.
   PubMed Web of Science ®Google Scholar
• Zhou W, Qian Y, Kunjilwar K, et al. Structural insights into the functional interaction of KChIP1 with Shal-type K+ channels. Neuron. 2004;41:573–586.
   PubMed Web of Science ®Google Scholar
• Lusin JD, Vanarotti M, Li C, et al. NMR structure of DREAM: implications for Ca2+-dependent DNA binding and protein dimerization. Biochemistry. 2008;47:2252–2264.
   PubMed Web of Science ®Google Scholar
• Chang LS, Chen CY, Wu TT. Functional implication with the metal-binding properties of KChIP1. Biochem Biophys Res Commun. 2003;311:258–263.
   PubMed Web of Science ®Google Scholar
• Chen CP, Lee L, Chang LS. Effects of metal-binding properties of human Kv channel-interacting proteins on their molecular structure and binding with Kv4.2 channel. Protein J. 2006;25:345–351.
   PubMed Web of Science ®Google Scholar
• Craig TA, Benson LM, Venyaminov SY, et al. The Metal-binding Properties of DREAM. Evidence for calcium-mediated changes in DREAM structure. J Biol Chem. 2002;277:10955–10966.
   PubMed Web of Science ®Google Scholar
• Lee L, Chen KC, Chang LS. Functional roles of EF-hands in human potassium channel-interacting protein 2.2. Protein Pept Lett. 2009;16:1081–1087.
   PubMed Web of Science ®Google Scholar
• Lin YL, Chen CY, Cheng CP, et al. Protein-protein interactions of KChIP proteins and Kv4.2. Biochem Biophys Res Commun. 2004;321:606–610.
   PubMed Web of Science ®Google Scholar
• Osawa M, Dace A, Tong KI, et al. Mg2+ and Ca2+ differentially regulate DNA binding and dimerization of DREAM. J Biol Chem. 2005;280:18008–18014.
   PubMed Web of Science ®Google Scholar
• Yu L, Sun C, Mendoza R, et al. Solution structure and calcium-binding properties of EF-hands 3 and 4 of calsenilin. Protein Sci. 2007;16:2502–2509.
   PubMed Web of Science ®Google Scholar
• Osawa M, Tong KI, Lilliehook C, et al. Calcium-regulated DNA binding and oligomerization of the neuronal calcium-sensing protein, calsenilin/DREAM/KChIP3. J Biol Chem. 2001;276:41005–41013.
   PubMed Web of Science ®Google Scholar
• Ramachandran PL, Craig TA, Atanasova EA, et al. The potassium channel interacting protein 3 (DREAM/KChIP3) heterodimerizes with and regulates calmodulin function. J Biol Chem. 2012;287:39439–39448.
   PubMed Web of Science ®Google Scholar
• Kuo HC, Cheng CF, Clark RB, et al. A defect in the Kv Channel-Interacting Protein 2 (KChIP2) gene leads to a complete loss of Ito and confers susceptibility to ventricular tachycardia. Cell. 2001;107:801–813.
   PubMed Web of Science ®Google Scholar
• Rosati B, Pan Z, Lypen S, et al. Regulation of KChIP2 potassium channel β subunit gene expression underlies the gradient of transient outward current in canine and human ventricle. J Physiol. 2001;533:119–125.
   PubMed Web of Science ®Google Scholar
• Shen J, Kelleher RJ 3rd. The presenilin hypothesis of Alzheimer’s disease: evidence for a loss-of-function pathogenic mechanism. Proc Natl Acad Sci U S A. 2007;104:403–409.
   PubMed Web of Science ®Google Scholar
• Jo DG, Jang J, Kim BJ, et al. Overexpression of calsenilin enhances gamma-secretase activity. Neurosci Lett. 2005;378:59–64.
   PubMed Web of Science ®Google Scholar
• Pham K, Miksovska J. Molecular insight of DREAM and presenilin 1 C-terminal fragment interactions. FEBS Lett. 2016;590:1114–1122.
   PubMed Web of Science ®Google Scholar
• Cheung KH, Shineman D, Muller M, et al. Mechanism of Ca2+ disruption in Alzheimer’s disease by presenilin regulation of InsP3 receptor channel gating. Neuron. 2008;58:871–883.
   PubMed Web of Science ®Google Scholar
• Hayrapetyan V, Rybalchenko V, Rybalchenko N, et al. The N-terminus of presenilin-2 increases single channel activity of brain ryanodine receptors through direct protein-protein interaction. Cell Calcium. 2008;44:507–518.
   PubMed Web of Science ®Google Scholar
• Payne AJ, Gerdes BC, Naumchuk Y, et al. Presenilins regulate the cellular activity of ryanodine receptors differentially through isotype-specific N-terminal cysteines. Exp Neurol. 2013;250:143–150.
   PubMed Web of Science ®Google Scholar
• Rybalchenko V, Hwang SY, Rybalchenko N, et al. The cytosolic N-terminus of presenilin-1 potentiates mouse ryanodine receptor single channel activity. Int J Biochem Cell Biol. 2008;40:84–97.
   PubMed Web of Science ®Google Scholar
• Leissring MA, Yamasaki TR, Wasco W, et al. Calsenilin reverses presenilin-mediated enhancement of calcium signaling. Proc Natl Acad Sci U S A. 2000;97:8590–8593.
   PubMed Web of Science ®Google Scholar
• LaFerla FM. Calcium dyshomeostasis and intracellular signalling in Alzheimer’s disease. Nat Rev Neurosci. 2002;3:862–872.
   PubMed Web of Science ®Google Scholar
• Nassal DM, Wan X, Liu H, et al. KChIP2 regulates the cardiac Ca2+ transient and myocyte contractility by targeting ryanodine receptor activity. PLoS One. 2017;12:e0175221.
   PubMed Web of Science ®Google Scholar
• Gomez-Villafuertes R, Torres B, Barrio J, et al. Downstream regulatory element antagonist modulator regulates Ca2+ homeostasis and viability in cerebellar neurons. J Neurosci. 2005;25:10822–10830.
   PubMed Web of Science ®Google Scholar
• Link WA, Ledo F, Torres B, et al. Day-night changes in downstream regulatory element antagonist modulator/potassium channel interacting protein activity contribute to circadian gene expression in pineal gland. J Neurosci. 2004;24:5346–5355.
   PubMed Web of Science ®Google Scholar
• Nassal DM, Wan X, Liu H, et al. KChIP2 is a core transcriptional regulator of cardiac excitability. Elife. 2017;6. pii:e17304. doi:10.7554/eLife.17304.
   PubMed Web of Science ®Google Scholar
• Ronkainen JJ, Hanninen SL, Korhonen T, et al. Ca2+-calmodulin-dependent protein kinase II represses cardiac transcription of the L-type calcium channel α1C-subunit gene (Cacna1c) by DREAM translocation. J Physiol. 2011;589:2669–2686.
   PubMed Web of Science ®Google Scholar
• Sanz C, Mellstrom B, Link WA, et al. Interleukin 3-dependent activation of DREAM is involved in transcriptional silencing of the apoptotic Hrk gene in hematopoietic progenitor cells. EMBO J. 2001;20:2286–2292.
   PubMed Web of Science ®Google Scholar
• Savignac M, Pintado B, Gutierrez-Adan A, et al. Transcriptional repressor DREAM regulates T-lymphocyte proliferation and cytokine gene expression. EMBO J. 2005;24:3555–3564.
   PubMed Web of Science ®Google Scholar
• Scsucova S, Palacios D, Savignac M, et al. The repressor DREAM acts as a transcriptional activator on Vitamin D and retinoic acid response elements. Nucleic Acids Res. 2005;33:2269–2279.
   PubMed Web of Science ®Google Scholar
• Ledo F, Kremer L, Mellstrom B, et al. Ca2+-dependent block of CREB-CBP transcription by repressor DREAM. EMBO J. 2002;21:4583–4592.
   PubMed Web of Science ®Google Scholar
• Rivas M, Mellstrom B, Naranjo JR, et al. Transcriptional repressor DREAM interacts with thyroid transcription factor-1 and regulates thyroglobulin gene expression. J Biol Chem. 2004;279:33114–33122.
   PubMed Web of Science ®Google Scholar
• Zaidi NF, Kuplast KG, Washicosky KJ, et al. Calsenilin interacts with transcriptional co-repressor C-terminal binding protein(s). J Neurocem. 2006;98:1290–1301.
   PubMed Web of Science ®Google Scholar
• Cheng HY, Pitcher GM, Laviolette SR, et al. DREAM is a critical transcriptional repressor for pain modulation. Cell. 2002;108:31–43.
   PubMed Web of Science ®Google Scholar
• Woo HN, Chang JW, Choi YH, et al. Characterization of subcellular localization and Ca2+ modulation of calsenilin/DREAM/KChIP3. Neuroreport. 2008;19:1193–1197.
   PubMed Web of Science ®Google Scholar
• Winther SV, Tuomainen T, Borup R, et al. Potassium channel interacting protein 2 (KChIP2) is not a transcriptional regulator of cardiac electrical remodeling. Sci Rep. 2016;6:28760.
   PubMed Web of Science ®Google Scholar
• Thomsen MB, Foster E, Nguyen KH, et al. Transcriptional and electrophysiological consequences of KChIP2-mediated regulation of Cav1.2. Channels. 2009;3:308–310.
   PubMed Web of Science ®Google Scholar
• Thomsen MB, Wang C, Özgen N, et al. The accessory subunit KChIP2 modulates the cardiac L-type calcium current. Circ Res. 2009;104:1382–1389.
   PubMed Web of Science ®Google Scholar
• Bähring R, Dannenberg J, Peters HC, et al. 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.
   PubMed Web of Science ®Google Scholar
• Beck EJ, Bowlby M, An WF, et al. Remodelling inactivation gating of Kv4 channels by KChIP1, a small-molecular-weight calcium-binding protein. J Physiol. 2002;538:691–706.
   PubMed Web of Science ®Google Scholar
• Gonzalez WG, Pham K, Miksovska J. Modulation of the voltage-gated potassium channel (Kv4.3) and the auxiliary protein (KChIP3) interactions by the current activator NS5806. J Biol Chem. 2014;289:32201–32213.
   PubMed Web of Science ®Google Scholar
• Kitazawa M, Kubo Y, Nakajo K. The stoichiometry and biophysical properties of the Kv4 potassium channel complex with K+ channel-interacting protein (KChIP) subunits are variable, depending on the relative expression level. J Biol Chem. 2014;289:17597–17609.
   PubMed Web of Science ®Google Scholar
• Callsen B, Isbrandt D, Sauter K, et al. Contribution of N- and C-terminal Kv4.2 channel domains to KChIP interaction. J Physiol. 2005;568:397–412.
   PubMed Web of Science ®Google Scholar
• Wang H, Yan Y, Liu Q, et al. Structural basis for modulation of Kv4 K+ channels by auxiliary KChIP subunits. Nat Neurosci. 2007;10:32–39.
   PubMed Web of Science ®Google Scholar
• Patel SP, Campbell DL, Strauss HC. Elucidating KChIP effects on Kv4.3 inactivation and recovery kinetics with a minimal KChIP2 isoform. J Physiol. 2002;545:5–11.
   PubMed Web of Science ®Google Scholar
• Gebauer M, Isbrandt D, Sauter K, et al. N-type inactivation features of Kv4.2 channel gating. Biophys J. 2004;86:210–223.
   PubMed Web of Science ®Google Scholar
• Barghaan J, Tozakidou M, Ehmke H, et al. Role of N-terminal domain and accessory subunits in controlling deactivation-inactivation coupling of Kv4.2 channels. Biophys J. 2008;94:1276–1294.
   PubMed Web of Science ®Google Scholar
• Shibata R, Misonou H, Campomanes CR, et al. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J Biol Chem. 2003;278:36445–36454.
   PubMed Web of Science ®Google Scholar
• Hasdemir B, Fitzgerald DJ, Prior IA, et al. Traffic of Kv4 K+ channels mediated by KChIP1 is via a novel post-ER vesicular pathway. J Cell Biol. 2005;171:459–469.
   PubMed Web of Science ®Google Scholar
• Tang YQ, Liang P, Zhou J, et al. Auxiliary KChIP4a suppresses A-type K+ current through endoplasmic reticulum (ER) retention and promoting closed-state inactivation of Kv4 channels. J Biol Chem. 2013;288:14727–14741.
   PubMed Web of Science ®Google Scholar
• Ren X, Shand SH, Takimoto K. Effective association of Kv channel-interacting proteins with Kv4 channel is mediated with their unique core peptide. J Biol Chem. 2003;278:43564–43570.
   PubMed Web of Science ®Google Scholar
• Liang P, Wang H, Chen H, et al. Structural insights into KChIP4a modulation of Kv4.3 inactivation. J Biol Chem. 2009;284:4960–4967.
   PubMed Web of Science ®Google Scholar
• Schwenk J, Zolles G, Kandias NG, et al. NMR analysis of KChIP4a reveals structural basis for control of surface expression of Kv4 channel complexes. J Biol Chem. 2008;283:18937–18946.
   PubMed Web of Science ®Google Scholar
• Jerng HH, Pfaffinger PJ. Multiple Kv channel-interacting proteins contain an N-terminal transmembrane domain that regulates Kv4 channel trafficking and gating. J Biol Chem. 2008;283:36046–36059.
   PubMed Web of Science ®Google Scholar
• Li M, Lei L, Jia L, et al. Interactions of KChIP4a and its mutants with Ca2+ or Kv4.3 N-terminus by affinity capillary electrophoresis. Anal Biochem. 2014;449:99–105.
   PubMed Web of Science ®Google Scholar
• Chen QX, Wong RK. Intracellular Ca2+ suppressed a transient potassium current in hippocampal neurons. J Neurosci. 1991;11:337–343.
   PubMed Web of Science ®Google Scholar
• Wang X, Bao J, Zeng XM, et al. Elevation of intracellular Ca2+ modulates A-currents in rat cerebellar granule neurons. J Neurosci Res. 2005;81:530–540.
   PubMed Web of Science ®Google Scholar
• Holmqvist MH, Cao J, Knoppers MH, et al. Kinetic modulation of Kv4-mediated A-current by arachidonic acid is dependent on potassium channel interacting proteins. J Neurosci. 2001;21:4154–4161.
   PubMed Web of Science ®Google Scholar
• Turner RW, Zamponi GW. T-type channels buddy up. Pflügers Arch: Eur J Physiol. 2014;466:661–675.
   PubMed Web of Science ®Google Scholar
• Heath NC, Rizwan AP, Engbers JD, et al. The expression pattern of a Cav3-Kv4 complex differentially regulates spike output in cerebellar granule cells. J Neurosci. 2014;34:8800–8812.
   PubMed Web of Science ®Google Scholar
• Anderson D, Engbers JD, Heath NC, et al. The Cav3-Kv4 complex acts as a calcium sensor to maintain inhibitory charge transfer during extracellular calcium fluctuations. J Neurosci. 2013;33:7811–7824.
   PubMed Web of Science ®Google Scholar
• Kuo YL, Cheng JK, Hou WH, et al. K+ channel modulatory subunits KChIP and DPP participate in Kv4-mediated mechanical pain control. J Neurosci. 2017;37:4391–4404.
   PubMed Web of Science ®Google Scholar
• Colinas O, Gallego M, Setien R, et al. Differential modulation of Kv4.2 and Kv4.3 channels by calmodulin-dependent protein kinase II in rat cardiac myocytes. Am J Physiol Heart Circ Physiol. 2006;291:H1978–H1987.
   PubMed Web of Science ®Google Scholar
• El-Haou S, Balse E, Neyroud N, et al. Kv4 potassium channels form a tripartite complex with the anchoring protein SAP97 and CaMKII in cardiac myocytes. Circ Res. 2009;104:758–769.
   PubMed Web of Science ®Google Scholar
• Keskanokwong T, Lim HJ, Zhang P, et al. Dynamic Kv4.3-CaMKII unit in heart: an intrinsic negative regulator for CaMKII activation. Eur Heart J. 2010;32:305–315.
   PubMed Web of Science ®Google Scholar