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The Journal of Neuroscience, June 1, 1998, 18(11):4374-4383
Axotomy Upregulates the Anterograde Transport and Expression of
Brain-Derived Neurotrophic Factor by Sensory Neurons
James R.
Tonra,
Rory
Curtis,
Vivien
Wong,
Kenneth D.
Cliffer,
John S.
Park,
Andrew
Timmes,
Trang
Nguyen,
Ronald M.
Lindsay,
Ann
Acheson, and
Peter
S.
DiStefano
Regeneron Pharmaceuticals, Inc., Tarrytown, New York 10591
In addition to the known retrograde transport of neurotrophins, it
is now evident that endogenous brain-derived neurotrophic factor (BDNF)
is transported in the anterograde direction in peripheral and central
neurons. We used a double-ligation procedure that distinguishes between
anterograde and retrograde flow to quantify the anterograde transport
of endogenous neurotrophins and neuropeptides in the peripheral nervous
system before and after axotomy. BDNF accumulation proximal to the
ligation (anterograde transport) was twice that distal to the ligation
(retrograde direction). Anterograde transport of nerve growth factor
and neurotrophin-3 was not evident. Furthermore, BDNF anterograde
transport increased 3.5-fold within 24 hr after sciatic nerve injury or
dorsal rhizotomy. Anterograde transport of substance P and calcitonin
gene-related peptide decreased after peripheral nerve lesion,
demonstrating that there was no generalized increase in anterograde
transport. To determine the source of the anterogradely transported
BDNF, we performed in situ hybridization in a variety of
tissues before and after axotomy. Expression of BDNF mRNA in proximal
nerve segments did not change with treatment, showing that the
increased accumulation of BDNF was not a result of increased local
synthesis. BDNF mRNA and protein were expressed by dorsal root ganglion
sensory neurons but not by motor neurons. BDNF mRNA expression was
increased 1 d after nerve injury, and BDNF protein was also
increased twofold to threefold, suggesting that sensory neurons are the
major contributing source of the increased BDNF traffic in the sciatic
nerve. Our results suggest that increased anterogradely transported
BDNF plays a role in the early neuronal response to peripheral nerve injury at sites distal to the cell body.
Key words:
anterograde transport; retrograde transport; neurotrophin; BDNF; sciatic nerve; dorsal root ganglion
Copyright © 1998 Society for Neuroscience 0270-6474/98/18114374-10$05.00/0
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