The NH2 terminus regulates voltage-dependent gating of CALHM ion channels

Am J Physiol Cell Physiol. 2017 Aug 1;313(2):C173-C186. doi: 10.1152/ajpcell.00318.2016. Epub 2017 May 17.

Abstract

Calcium homeostasis modulator protein-1 (CALHM1) and its Caenorhabditis elegans (ce) homolog, CLHM-1, belong to a new family of physiologically important ion channels that are regulated by voltage and extracellular Ca2+ (Ca2+o) but lack a canonical voltage-sensing domain. Consequently, the intrinsic voltage-dependent gating mechanisms for CALHM channels are unknown. Here, we performed voltage-clamp experiments on ceCLHM-1 chimeric, deletion, insertion, and point mutants to assess the role of the NH2 terminus (NT) in CALHM channel gating. Analyses of chimeric channels in which the ceCLHM-1 and human (h)CALHM1 NH2 termini were interchanged showed that the hCALHM1 NT destabilized channel-closed states, whereas the ceCLHM-1 NT had a stabilizing effect. In the absence of Ca2+o, deletion of up to eight amino acids from the ceCLHM-1 NT caused a hyperpolarizing shift in the conductance-voltage relationship with little effect on voltage-dependent slope. However, deletion of nine or more amino acids decreased voltage dependence and induced a residual conductance at hyperpolarized voltages. Insertion of amino acids into the NH2-terminal helix also decreased voltage dependence but did not prevent channel closure. Mutation of ceCLHM-1 valine 9 and glutamine 13 altered half-maximal activation and voltage dependence, respectively, in 0 Ca2+ In 2 mM Ca2+o, ceCLHM-1 NH2-terminal deletion and point mutant channels closed completely at hyperpolarized voltages with apparent affinity for Ca2+o indistinguishable from wild-type ceCLHM-1, although the ceCLHM-1 valine 9 mutant exhibited an altered conductance-voltage relationship and kinetics. We conclude that the NT plays critical roles modulating voltage dependence and stabilizing the closed states of CALHM channels.

Keywords: Ca2+ regulation; calcium homeostasis modulator channel; channel gating; voltage sensing.

MeSH terms

  • Amino Acids / genetics
  • Amino Acids / metabolism
  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Calcium / metabolism*
  • Calcium Channels / chemistry
  • Calcium Channels / genetics
  • Calcium Channels / metabolism*
  • Electrophysiology
  • Humans
  • Membrane Glycoproteins / chemistry
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Membrane Potentials / genetics
  • Mutant Proteins / chemistry
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism*
  • Patch-Clamp Techniques
  • Point Mutation
  • Sequence Deletion / genetics

Substances

  • Amino Acids
  • CALHM1 protein, human
  • CLHM-1 protein, C elegans
  • Caenorhabditis elegans Proteins
  • Calcium Channels
  • Membrane Glycoproteins
  • Mutant Proteins
  • Calcium