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The Journal of Neuroscience, May 11, 2005, 25(19):4868-4878; doi:10.1523/JNEUROSCI.0249-05.2005

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Cellular/Molecular
trkA Is Expressed in Nociceptive Neurons and Influences Electrophysiological Properties via Nav1.8 Expression in Rapidly Conducting Nociceptors

Xin Fang,¹ Laiche Djouhri,¹ Simon McMullan,² Carol Berry,¹ Kenji Okuse,³ Stephen G. Waxman,⁴ and Sally N. Lawson¹

¹Department of Physiology, Medical School, University of Bristol, Bristol BS8 1TD, United Kingdom, ²Hypertension and Stroke Research Laboratory, University of Sydney, Sydney 2065, Australia, ³Department of Biology, University College London, London WC1E 6BT, United Kingdom, and ⁴Department of Neurology, Yale University School of Medicine, New Haven, Connecticut 06510

To test the hypothesis that trkA (the high-affinity NGF receptor) is selectively expressed in nociceptive dorsal root ganglion (DRG) neurons, we examined the intensity of trkA immunoreactivity in single dye-injected rat DRG neurons, the sensory receptor properties of which were identified in vivo with mechanical and thermal stimuli. We provide the first evidence in single identified neurons that strong trkA expression in DRGs is restricted to nociceptive neurons, probably accounting for the profound influence of NGF on these neurons. Furthermore, we demonstrate that trkA expression is as high in rapidly conducting (A/) as in more slowly conducting (A and C) nociceptors. All A/ low-threshold mechanoreceptors (LTMs) are trkA negative, although weak but detectable trkA is present in some C and A LTMs.

NGF can influence electrophysiological properties of DRG neurons, probably by binding to trkA. We found positive correlations for single identified A/ (but not C or A) nociceptors between trkA immunocytochemical intensity and electrophysiological properties typical of nociceptors, namely long action potential and afterhyperpolarization durations and large action potential amplitudes. Furthermore, for A/ (notCorA) nociceptors, trkA intensity is inversely correlated with conduction velocity. Similar relationships, again only in A/ nociceptors, between electrophysiological properties and trkA expression exist for sodium channel Nav1.8 but not Nav1.9 immunoreactivities. These findings suggest that in A/ nociceptors, influences of NGF on expression levels of Nav1.8 are related to, and perhaps limited by, expression levels of trkA. This view is supported by a positive correlation between immuno-intensities of trkA and Nav1.8 in A-fiber, but not C-fiber, nociceptors.

Key words: NGF; pain; dorsal root ganglion (DRG); conduction velocity; action potential; sodium channel

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Received Jan 18, 2005; revised April 1, 2005; accepted April 4, 2005.

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