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Journal of Neuroscience, Vol 14, 5187-5201, Copyright © 1994 by Society for Neuroscience
NGF and NT-3 have differing effects on the growth of dorsal root axons in developing mammalian spinal cord
L Zhang, RE Schmidt, Q Yan and WD Snider
Department of Neurology, Washington University Medical School, St. Louis, Missouri 63110.
The functions of neurotrophins in relation to axon growth and branching
during development of the nervous system are unknown. In order to address
this question, we have investigated the influences of systemically
administered mouse nerve growth factor (mNGF) and human recombinant
neurotrophin-3 (hrNT-3) on dorsal root axon growth in the spinal cord of
embryonic rats. As anticipated, mNGF has a marked influence on growth of
dorsal root axons. In mNGF-treated animals, dorsal root axons in the
developing dorsal funiculi and axon collaterals in developing gray matter
are substantially longer than those of age-matched controls. Furthermore,
growth cones of some dorsal root axons have more than twice the surface
area of controls. These effects of NGF are highly selective. Dorsal root
axons that occupy a lateral position in white matter and that normally give
off collaterals to superficial dorsal horn are prominently affected. Axons
that run medially in dorsal columns and that give off collaterals to
laminae III and IV and the ventral horn are not demonstrably influenced by
treatment with exogenous mNGF. In contrast to the striking effects of mNGF
on dorsal root axon growth, the influences of hrNT-3 were considerably more
complex. Administration of hrNT-3 increased the mean soma area of DRG
neurons, particularly those at the larger end of the size spectrum,
consistent with its hypothesized role as a growth factor for proprioceptive
sensory neurons. However, in striking contrast to the actions of mNGF,
hrNT-3 consistently inhibited axon collateral growth in gray matter at
early developmental stages. At later stages, we could not discern a
clear-cut influence of hrNT-3 on dorsal root axon growth and branching. We
conclude that the ability of mNGF to stimulate axon growth in both white
and gray matter is consistent with the idea that mNGF regulates the
developing axonal projections of DRG neurons in vivo. In contrast,
systemically administered hrNT-3 inhibits the axon collateralizations of
DRG neurons in gray matter at early developmental stages. We hypothesize
that this inhibitory effect may be related to disruption of a chemotropic
gradient of NT-3, or to the widespread expression of the NT-3 receptor
trkC, on non-neuronal cells.
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