Development of ionic currents of zebrafish slow and fast skeletal muscle fibers

Abstract

Voltage-gated Na+ and K+ channels play key roles in the excitability of skeletal muscle fibers. In this study we investigated the steady-state and kinetic properties of voltage-gated Na+ and K+ currents of slow and fast skeletal muscle fibers in zebrafish ranging in age from 1 day postfertilization (dpf) to 4-6 dpf. The inner white (fast) fibers possess an A-type inactivating K+ current that increases in peak current density and accelerates its rise and decay times during development. As the muscle matured, the V50s of activation and inactivation of the A-type current became more depolarized, and then hyperpolarized again in older animals. The activation kinetics of the delayed outward K+ current in red (slow) fibers accelerated within the first week of development. The tail currents of the outward K+ currents were too small to allow an accurate determination of the V50s of activation. Red fibers did not show any evidence of inward Na+ currents; however, white fibers expressed Na+ currents that increased their peak current density, accelerated their inactivation kinetics, and hyperpolarized their V50 of inactivation during development. The action potentials of white fibers exhibited significant changes in the threshold voltage and the half width. These findings indicate that there are significant differences in the ionic current profiles between the red and white fibers and that a number of changes occur in the steady-state and kinetic properties of Na+ and K+ currents of developing zebrafish skeletal muscle fibers, with the most dramatic changes occurring around the end of the first day following egg fertilization.

Development of Skeletal Muscle Sodium and Potassium Currents in Zebrafish <i>sofa potato</i> Mutants

“…Zebrafish red muscle fibers are recruited primarily during slow swimming rates [Buss and Drapeau, 2002], and express voltage-gated potassium currents, but not sodium currents. Zebrafish white muscle fibers, in contrast, exhibit both potassium and sodium currents [Buckingham and Ali, 2004;Coutts et al, 2006] and are responsible for fast swimming behaviors [Buss and Drapeau, 2002] and escape responses.…”

“…The zebrafish (Danio rerio) is an important animal model for developmental studies of the vertebrate nervous system and musculature [Westerfield et al, 1986;Devoto et al, 1996;Ali et al, 2000;Drapeau, 2000, 2002;Coutts et al, 2006]. It has proven to be especially valuable for studying aspects of neuromuscular physiology in vivo.…”

“…For instance, the progression of motor behaviors has been well characterized [Kimmel et al, 1995;Saint-Amant and Drapeau, 1998], beginning at approximately 16-18 h after fertilization when the axons of primary motorneurons make their initial contact with muscle fibers and cholinergic synaptic transmission begins [Melancon et al, 1997]. Muscle fibers are relatively easy to record electrical activity from Drapeau, 2000, 2002;Buckingham and Ali, 2004;Lefebvre et al, 2004;Coutts et al, 2006], and a wide range of transgenics and locomotor mutants are readily available [Westerfield et al, 1990;Ono et al, 2001;Lefebvre et al, 2004]. Here, we investigate one such mutant known as sofa potato (sop).…”

“…The axial muscle of larval zebrafish is composed of both red and white muscle fibers, which have different behavioral roles [Buss and Drapeau, 2002] and electrical phenotypes [Buckingham and Ali, 2004;Coutts et al, 2006]. Zebrafish red muscle fibers are recruited primarily during slow swimming rates [Buss and Drapeau, 2002], and express voltage-gated potassium currents, but not sodium currents.…”

“…We have previously characterized the development of ionic currents and action potentials in wild-type zebrafish skeletal muscle [Coutts et al, 2006]. The axial muscle of larval zebrafish is composed of both red and white muscle fibers, which have different behavioral roles [Buss and Drapeau, 2002] and electrical phenotypes [Buckingham and Ali, 2004;Coutts et al, 2006].…”