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Journal of Neuroscience, Vol 8, 1704-1711, Copyright © 1988 by Society for Neuroscience
Neurite outgrowth in individual neurons of a neuronal population is differentially regulated by calcium and cyclic AMP
MP Mattson, A Taylor-Hunter and SB Kater
Department of Anatomy and Neurobiology, Colorado State University, Fort Collins 80523.
In identified Helisoma neurons, intracellular calcium can regulate neurite
elongation and growth cone motility. Neurotransmitters such as 5-HT
suppress both neurite elongation and the filopodial and lamellipodial
movements of growth cones by causing increases in intracellular calcium
(Haydon et al., 1984; Cohan et al., 1987; Mattson and Kater, 1987). Since
an additional second messenger, cyclic AMP (cAMP), is known to mediate many
physiological effects of neurotransmitters, we tested (1) the possible
involvement of cAMP in the regulation of neurite outgrowth from Helisoma
buccal neurons and (2) calcium-cAMP interrelationships in the regulation of
outgrowth. The cAMP-elevating agents forskolin (5 x 10(-6)-10(-4) M) and
dibutyryl cAMP (dbcAMP; 5 x 10(-3)-10(-2) M) suppressed neurite elongation
and growth cone movements in identified neurons B19 (5-HT sensitive) and B5
(5-HT insensitive); the suppression was reversible. Exposure of these
particular identified neurons to the calcium channel blocker La3+ (10(- 5)
M) or a culture medium with reduced calcium prevented and reversed the
suppressive effects of forskolin and dbcAMP. In order to determine if the
results on neurons B5 and B19 were representative of all neurons or only a
subset, we examined a larger population of neurons. Calcium ionophore
A23187 suppressed outgrowth from all neurons in mass dissociate cultures of
buccal neurons, while forskolin or dbcAMP plus IBMX suppressed outgrowth
from only one-half of buccal neurons. Finally, we found that 2
subpopulations exist among the neurons whose outgrowth is suppressed by
cAMP: One subpopulation requires calcium influx for cAMP to act, while the
other does not. Thus, even within the relatively small population of
neuronal types comprising the buccal ganglion of Helisoma, second
messengers within different neurons can act and interact in different ways
to regulate outgrowth.
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