Voltage-Gated Na+ Channel Isoforms and Their mRNA Expression Levels and Protein Abundance in Three Electric Organs and the Skeletal Muscle of the Electric Eel Electrophorus electricus.

Jia M. Woo,Kum C. Hiong,Biyun Ching,Wai P. Wong,Yuen K. Ip,Shit F. Chew,Mel V. Boo

doi:10.1371/journal.pone.0167589

Jia M. Woo, Kum C. Hiong + Show 5 more

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https://doi.org/10.1371/journal.pone.0167589

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Abstract

This study aimed to obtain the coding cDNA sequences of voltage-gated Na+ channel (scn) α-subunit (scna) and β-subunit (scnb) isoforms from, and to quantify their transcript levels in, the main electric organ (EO), Hunter’s EO, Sach’s EO and the skeletal muscle (SM) of the electric eel, Electrophorus electricus, which can generate both high and low voltage electric organ discharges (EODs). The full coding sequences of two scna (scn4aa and scn4ab) and three scnb (scn1b, scn2b and scn4b) were identified for the first time (except scn4aa) in E. electricus. In adult fish, the scn4aa transcript level was the highest in the main EO and the lowest in the Sach’s EO, indicating that it might play an important role in generating high voltage EODs. For scn4ab/Scn4ab, the transcript and protein levels were unexpectedly high in the EOs, with expression levels in the main EO and the Hunter’s EO comparable to those of scn4aa. As the key domains affecting the properties of the channel were mostly conserved between Scn4aa and Scn4ab, Scn4ab might play a role in electrogenesis. Concerning scnb, the transcript level of scn4b was much higher than those of scn1b and scn2b in the EOs and the SM. While the transcript level of scn4b was the highest in the main EO, protein abundance of Scn4b was the highest in the SM. Taken together, it is unlikely that Scna could function independently to generate EODs in the EOs as previously suggested. It is probable that different combinations of Scn4aa/Scn4ab and various Scnb isoforms in the three EOs account for the differences in EODs produced in E. electricus. In general, the transcript levels of various scn isoforms in the EOs and the SM were much higher in adult than in juvenile, and the three EOs of the juvenile fish could be functionally indistinct.

Highlights

Some fishes have acquired the ability to generate and/or sense electricity [1]
The hydrophobic constriction sites (HCS), which are located in the core of the voltage-sensing domain (VSD), line the narrowest part of the gating charge movement pathway and form a seal to avoid ion leakage as the S4 segments rotate during activation as proposed in the helical screw model [47]
We have obtained the full coding sequences of scn4aa, scn4ab, scn1b, scn2b and scn4b from the electric organ (EO) and the skeletal muscle (SM) of E. electricus. Both scn4aa and scn4ab were highly expressed in the EOs, while in the SM, scn4aa was barely detectable compared to scn4ab

Summary

Introduction

Some fishes have acquired the ability to generate and/or sense electricity [1]. Electric fishes can generate strong electric organ discharges (EODs) for predation and defense or weak EODs for communication and sensing of the surroundings [2]. E. electricus has three electric organs (EOs), the main EO, the Hunter’s EO and the Sach’s EO. The low-frequency, low-voltage EODs generated by the Sach’s EO and the posterior one-third of the Hunter’s EO are mainly used for navigation and communication purposes [8]. Electrophorus electricus hunts its prey using high-frequency voltage pulses which are targeted to motor neurons, resulting in the induction of uncontrolled muscle seizures [9]. It can generate a doublet of electric discharge during hunting to cause muscle twitching in stationary or hidden prey, revealing the prey’s location [9]

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