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Palmitoylation of the pore-forming subunit of Ca(v)1.2 controls channel voltage sensitivity and calcium transients in cardiac myocytes

Chien-Wen S. Kuoa, Sara Dobia, Caglar Göka, Ana Da Silva Costaa, Alice Maina, Olivia Robertson-Graya, Daniel Baptista-Honb,c, Krzysztof J. Wypijewskia, Hannah Costellob, Tim G. Halesb, Niall MacQuaidea, Godfrey L. Smitha, and William Fuller

Abstract

Mammalian voltage-activated L-type Ca2+ channels, such as Ca(v)1.2, control transmem-brane Ca2+ fluxes in numerous excitable tissues. Here, we report that the pore-forming α1C subunit of Ca(v)1.2 is reversibly palmitoylated in rat, rabbit, and human ventricular myocytes. We map the palmitoylation sites to two regions of the channel: The N termi-nus and the linker between domains I and II. Whole-cell voltage clamping revealed a rightward shift of the Ca(v)1.2 current–voltage relationship when α1C was not palmi-toylated. To examine function, we expressed dihydropyridine-resistant α1C in human induced pluripotent stem cell-derived cardiomyocytes and measured Ca2+ transients in the presence of nifedipine to block the endogenous channels. The transients generated by  unpalmitoylatable  channels  displayed  a  similar  activation  time  course  but  signifi-cantly reduced amplitude compared to those generated by wild-type channels. We thus conclude  that  palmitoylation  controls  the  voltage  sensitivity  of  Ca(v)1.2.  Given  that  the identified Ca(v)1.2 palmitoylation sites are also conserved in most Ca(v)1 isoforms, we  propose  that  palmitoylation  of  the  pore-forming  α1C  subunit  provides  a  means  to regulate the voltage sensitivity of voltage-activated Ca2+ channels in excitable cells.

Voltage-activated channels facilitate the movement of ions across the membranes of excit-able  tissues  in  response  to  changes  in  membrane  potential.  The  L-type  Ca2+  channel  mediates  the  depolarization-induced  entry  of  Ca2+  into  numerous  cell  types,  thereby  controlling excitation–contraction coupling in smooth and striated muscles, excitation–secretion coupling in endocrine cells, and neurotransmitter release in neurons (1). The precise control of L-type Ca2+ channel activity is therefore important in a diverse range of physiological settings—from the contraction of cardiac muscle in the control of cardiac output to the contraction of blood vessels in the control of blood pressure and the secretion of insulin in glucose homeostasis.Voltage-activated  Ca2+  channels  are  composed  of  multiple  subunits,  including  a  pore-forming α subunit and an accessory β subunit (2). The α subunit (α1C in the cardiac L-type Ca2+ channel Ca(v)1.2) is a transmembrane protein that has four domains (I to IV, each with six membrane-spanning units), which are connected by intracellular loops.

The β subunit is cytosolic, interacts with the intracellular loop between domains I and II of the α subunit, and regulates numerous aspects of channel behavior (3).There are four subfamilies of β subunits (β1 to β4) encoded by distinct genes which can be alternatively spliced (4). Specifically, β subunits enhance Ca(v)1.2-mediated cur-rents by promoting channel exit from the endoplasmic reticulum (4). Once Ca(v)1.2 is at the cell surface, β subunits promote channel activation by shifting the voltage depend-ence of opening to more hyperpolarized potentials and accelerating channel activation (5, 6). Two forms of activity-dependent inactivation control most voltage-sensitive Ca2+channels:  Voltage-dependent  inactivation  (VDI)  and  calcium-dependent  inactivation  (CDI). Both VDI and CDI contribute to regulation of neuronal P/Q-type (Ca(v)2.1) Ca2+ channels, (7, 8) whereas CDI usually dominates for L-type channels such as Ca(v)1.2 in the heart (8–10). Most β subunits enhance both VDI and CDI, but β2a specifically reduces VDI.

 


First published: 23 February 2023