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Journal of Neuroscience, Vol 7, 3600-3611, Copyright © 1987 by Society for Neuroscience
Cyclic AMP induces changes in distribution and transport of organelles within growth cones of Aplysia bag cell neurons
P Forscher, LK Kaczmarek, JA Buchanan and SJ Smith
Howard Hughes Medical Institute Section of Molecular Neurobiology, Yale School of Medicine, New Haven, Connecticut 06510.
This report examines cAMP-induced regulation of directed organelle
transport in bag cell neuron growth cones using video-enhanced differential
interference contrast (DIC) microscopy (Allen et al., 1981; Inoue, 1981)
and digital image analysis techniques. Under control conditions, organelle
transport is evident in the central cytoplasmic regions of bag cell neuron
growth cones, but not in lamellae. Motility of lamellae takes the form of
slow (less than 0.01 micron/sec) extension of margins and ruffling motions
that propagate as waves (velocity, approximately 0.07 micron/sec) in a
retrograde direction. Application of forskolin and a phosphodiesterase
(PDE) inhibitor at concentrations known to induce changes in bag cell
protein phosphorylation resulted in (1) rapid extension of directed
organelle transport into lamellae, and (2) inhibition of the retrograde
ruffling waves. These changes effected transformation of lamellae into
neurite endings packed with microtubules and organelles, a large proportion
of which appeared to be neurosecretory granules. The effects were
reversible, dose-dependent, potentiated by a variety of PDE inhibitors, and
mimicked by 6-N-butyl-8-benzyl-thio-cAMP (BT-cAMP). Though forskolin may
normally promote depolarization and Ca entry, these changes in growth cone
structure are not secondary to influx of external Ca, as they persist in
Ca-free/EGTA solutions; furthermore, they do not resemble the effects of
depolarization induced by perfusion with elevated K solutions. The
cAMP-induced changes in growth cone morphology that we report here suggest
a possible role for protein phosphorylation in promoting growth cone
differentiation and structural changes accompanying secretion.
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