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Journal of Neuroscience, Vol 13, 167-180, Copyright © 1993 by Society for Neuroscience
Development of larval muscle properties in the embryonic myotubes of Drosophila melanogaster
KS Broadie and M Bate
Department of Zoology, University of Cambridge, United Kingdom.
The entire developmental history of muscle membrane electrogenesis can be
observed in the embryonic myotubes of Drosophila. We have examined the
development of ionic currents and muscle properties using whole- cell
patch-clamp techniques throughout embryonic myogenesis. In the early stages
of myogenesis, from myoblast fusion through to establishing epidermal
insertions, the myotubes are electrically inert and are electrically and
dye coupled to adjacent myotubes. Membrane electrogenesis begins in the
mid-embryonic stages (early stage 16), when the myotubes abruptly uncouple,
revealing the first of five prominent extrajunctional currents: a small,
inward, voltage-gated calcium current (ICa). The uncoupling of the
embryonic myotubes heralds the onset of extremely rapid electrogenesis;
within several minutes both the fast, inactivating (IA; Shaker) and
delayed, noninactivating (IK) outward potassium currents, the
stretch-activated outward potassium current, and the junctional
glutamate-gated inward current all appear and begin to develop in a
current-specific manner. Very late in embryogenesis (late stage 17), the
calcium-dependent, outward potassium currents [rapid, inactivating (ICF;
slowpoke) then delayed, noninactivating (ICS)] develop, completing the
complement of macroscopic currents in the mature larval muscle. Hence, the
voltage- gated currents (ICa, IA, and IK, respectively) appear relatively
early, and the calcium-dependent currents (ICF, ICS) appear only very late
during myogenesis. This developmental progression of current maturation is
reflected in dynamic changes in the voltage responses of the embryonic
membrane, from wholly passive response to current injection in the early,
coupled myotubes to regenerating, overshooting action potentials in the
mature embryonic muscle. The earliest embryonic IA current has a midpoint
of inactivation 40 mV more negative than the IA current in the mature
embryo. As myogenesis proceeds, the inactivation curve develops a biphasic
character, suggesting that a low-inactivation IA channel is present in
early development and progressively replaced by the mature form as
development proceeds. The current at all stages can be completely
eliminated in Shaker mutants (ShKS133). These findings suggest that an
embryonic form of the Shaker IA channel is present during early myogenesis.
The prominent IA current present in early development is almost entirely
inactivated at the physiological resting potential; the significance and
mechanism of this developmental shift are unclear.
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