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The Journal of Neurophysiology Vol. 86 No. 6 December 2001, pp. 2931-2938
Copyright ©2001 by the American Physiological Society
Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook, New York 11794-5230
Shu, X. and
L. M. Mendell.
Acute Sensitization by NGF of the Response of Small-Diameter
Sensory Neurons to Capsaicin. J. Neurophysiol. 86: 2931-2938, 2001. We investigated acute sensitization by
nerve growth factor (NGF) of the response of small-diameter (<30
µm) dissociated dorsal root ganglion (DRG) cells to brief
repeated puffs of capsaicin as a model for thermal hyperalgesia induced
by NGF. We have previously shown that placing NGF in the bath after an
initial puff of capsaicin can completely overcome the tachyphylaxis
normally observed in response to a second puff 10 min later, and this
response is often substantially larger than the first. If tachyphylaxis
is abolished by carrying out the experiment in
Ca2+-free solution, NGF still elicits
potentiation of the second puff. However, the amount of potentiation is
considerably less than that observed when tachyphylaxis also takes
place. Thus it is concluded that NGF has two effects: overcoming
tachyphylaxis and potentiation. With three puffs of capsaicin separated
by 10 min, we have found that the potentiation established after 10 min
exposure to NGF is no longer evident 10 min after removal of NGF. In
Ca2+-free solution the potentiation can last up
to 1 h after removal of NGF. These results suggest that the
initial behavioral sensitization elicited by NGF could result from a
direct effect on the sensory neuron but that its later components most
likely involve other mechanisms. We have also investigated the
contribution of various second-messenger pathways in these actions of
NGF by treating the cells with blockers of MAP kinase (PD98059),
protein kinase A (PKA; PKAI14-22,
H89), and PKC (Bisindolylmaleimide I). Surprisingly, PD98059, which previously has been shown to diminish the
enhancement of capsaicin responses of dissociated neurons when exposed
to NGF for several days, had no effect on the acute response to NGF;
nor did the PKC inhibitor. However, PKA inhibitors reduced the
capsaicin response of the cells to NGF (as determined from the NGF
effect on tachyphylaxis). Consistent with these findings we confirmed
that forskolin, a PKA activator, enhances the effect of NGF on the
capsaicin response. The percentage of small cells sensitized by NGF
under these conditions, as determined by its ability to reduce
tachyphylaxis, was 64%. This suggests that about two-thirds of DRG
cells <30 µm and sensitive to capsaicin express a functional trkA receptor.
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