Genetic dissection of ion currents underlying all-or-none action potentials in C. elegans body-wall muscle cells.
Although the neuromuscular system of C. elegans has been studied intensively, little is known about the properties of muscle action potentials (APs). By combining mutant analyses with in vivo electrophysiological recording techniques and Ca2+ imaging, we have established the fundamental properties and molecular determinants of body-wall muscle APs. We show that, unlike mammalian skeletal muscle APs, C. elegans muscle APs occur in spontaneous trains, do not require the function of postsynaptic receptors, and are all-or-none overshooting events, rather than graded potentials as has been previously reported. Furthermore, we show that muscle APs depend on Ca2+ entry through the L-type Ca2+ channel EGL-19 with a contribution from the T-type Ca2+ channel CCA-1. Both the Shaker K+ channel SHK-1 and the Ca2+/Cl−-gated K+ channel SLO-2 play important roles in controlling the speed of membrane repolarization, the amplitude of afterhyperpolarization (AHP) and the pattern of AP firing; SLO-2 is also important in setting the resting membrane potential. Finally, AP-elicited elevations of [Ca2+]i require both EGL-19 and the ryanodine receptor UNC-68. Thus, like mammalian skeletal muscle, C. elegans body-wall myocytes generate all-or-none APs, which evoke Ca2+ release from the sarcoplasmic reticulum (SR), although the specific ion channels used for AP upstroke and repolarization differ.
Department of Neuroscience, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, CT 06030-3401, USA.
Ping
P
Liu
Qian
Q
Ge
Bojun
B
Chen
Lawrence
L
Salkoff
Michael I
MI
Kotlikoff
Zhao-Wen
ZW
Wang
D000200:Action Potentials / Q000235:genetics; D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D015220:Calcium Channels / Q000378:metabolism; D020747:Calcium Channels, T-Type / Q000378:metabolism; D056966:Excitation Contraction Coupling; D007473:Ion Channels / Q000235:genetics / Q000378:metabolism*; D026901:Membrane Transport Proteins / Q000378:metabolism; D009046:Motor Neurons / Q000502:physiology; D032342:Muscle Cells / Q000378:metabolism*; D009124:Muscle Proteins / Q000378:metabolism; D009132:Muscles / Q000294:innervation*; D009154:Mutation; D018408:Patch-Clamp Techniques; D019837:Ryanodine Receptor Calcium Release Channel / Q000378:metabolism; D012519:Sarcoplasmic Reticulum / Q000378:metabolism; D051637:Shaker Superfamily of Potassium Channels / Q000378:metabolism; D013997:Time Factors
D029742:Caenorhabditis elegans Proteins; D015220:Calcium Channels; D020747:Calcium Channels, T-Type; C109164:Egl-19 protein, C elegans; D007473:Ion Channels; D026901:Membrane Transport Proteins; D009124:Muscle Proteins; D019837:Ryanodine Receptor Calcium Release Channel; C402625:SLO-2 protein, C elegans; D051637:Shaker Superfamily of Potassium Channels; C438601:Unc-68 protein, C elegans