Muscle activity and the loss of electrical coupling between striated muscle cells in Xenopus embryos

Abstract

The gap junctions between embryonic striated muscle cells are lost during development. The time course of their elimination has been examined with electrophysiological techniques in myotomes of Xenopus laevis embryos. Gap junctions were detected by the passage of electronic current or the fluorescent dye, Lucifer Yellow, from one muscle cell to another. These tracers only spread to neighboring cells when injected intracellularly. All the muscle cells are electrically coupled at stage 24 when neuromuscular transmission begins, but normally many cells become uncoupled during the next 48 hr. In contrast, the muscle cells remain electrically coupled if neuromuscular transmission is blocked during that period with tricaine or alpha-bungarotoxin. When muscle activity recovers, the loss of coupling resumes. Once the coupling has disappeared, neuromuscular blockade does not restore it. Muscle contraction is blocked during development in a mutant of Xenopus, even though the muscle cells remain electrically excitable. After stage 32 in these immobile embryos, the muscle cells are stimulated repeatedly by regular bursts of neural activity. Although they never contract, the mutant muscle cells become uncoupled at the same time as the muscle cells in normal embryos. The results suggest that some consequence of repeated cholinergic activation, other than contraction, stimulates the loss of gap junctions between striated muscle cells during development. The elimination of gap junctions may be required for neural control of subsequent muscle differentiation.