Physiology and Evolution of Voltage-Gated Calcium Channels in Early Diverging Animal Phyla: Cnidaria, Placozoa, Porifera and Ctenophora.

Adriano Senatore,Hamad Raiss,Phuong Le

doi:10.3389/fphys.2016.00481

Abstract

Voltage-gated calcium (Cav) channels serve dual roles in the cell, where they can both depolarize the membrane potential for electrical excitability, and activate transient cytoplasmic Ca2+ signals. In animals, Cav channels play crucial roles including driving muscle contraction (excitation-contraction coupling), gene expression (excitation-transcription coupling), pre-synaptic and neuroendocrine exocytosis (excitation-secretion coupling), regulation of flagellar/ciliary beating, and regulation of cellular excitability, either directly or through modulation of other Ca2+-sensitive ion channels. In recent years, genome sequencing has provided significant insights into the molecular evolution of Cav channels. Furthermore, expanded gene datasets have permitted improved inference of the species phylogeny at the base of Metazoa, providing clearer insights into the evolution of complex animal traits which involve Cav channels, including the nervous system. For the various types of metazoan Cav channels, key properties that determine their cellular contribution include: Ion selectivity, pore gating, and, importantly, cytoplasmic protein-protein interactions that direct sub-cellular localization and functional complexing. It is unclear when these defining features, many of which are essential for nervous system function, evolved. In this review, we highlight some experimental observations that implicate Cav channels in the physiology and behavior of the most early-diverging animals from the phyla Cnidaria, Placozoa, Porifera, and Ctenophora. Given our limited understanding of the molecular biology of Cav channels in these basal animal lineages, we infer insights from better-studied vertebrate and invertebrate animals. We also highlight some apparently conserved cellular functions of Cav channels, which might have emerged very early on during metazoan evolution, or perhaps predated it.

Highlights

The coupling of fast electrical impulses, driven by voltagegated potassium (Kv) and sodium (Nav) channels, with calciumdependent synaptic signaling, allows the nervous system to coordinate cellular activities rapidly and over long distances
The nature and purpose of electrical signaling in Trichoplax remains a mystery. It is likely of significant importance, where in addition to Cav channels, the animal expresses mRNAs of a core set of genes required for generating action potentials and propagating fast electrical signals: One of the two Nav2 channels predicted from the genome (Srivastava et al, 2008; Liebeskind et al, 2011), Kv channels of the Shaker, Shab, Shal, and Shaw varieties, a Ca2+-activated K+ channel, a Kv channel accessory β subunit, and 2-pore K+ (K2P) leak channels and inward rectifying K+ (KIR) channels, essential for setting the polarized resting membrane potential of excitable cells (Figure 5D)
Cellular Contractility It is interesting that of the three Cav channel types, the Cav1 channel appears to be the most highly expressed in the Trichoplax transcriptome (Figure 5D), considering the specialized role that Cav1 channels play in excitation-contraction coupling in muscle, and the absence of ultrastructural markers for muscle in Trichoplax (Smith et al, 2014)

Summary

Introduction

The coupling of fast electrical impulses, driven by voltagegated potassium (Kv) and sodium (Nav) channels, with calciumdependent synaptic signaling, allows the nervous system to coordinate cellular activities rapidly and over long distances.

Results

Conclusion