Elsevier

Neuroscience

Volume 130, Issue 1, 2005, Pages 223-228
Neuroscience

TRPV2, a capsaicin receptor homologue, is expressed predominantly in the neurotrophin-3-dependent subpopulation of primary sensory neurons

https://doi.org/10.1016/j.neuroscience.2004.09.021Get rights and content

Abstract

TRPV2, a member of transient receptor potential ion channels, responds to high-threshold noxious heat, but neither to capsaicin nor to proton. Although TRPV2 is expressed in medium- to large-sized dorsal root ganglion (DRG) neurons with myelinated fibers in adult rodents, little is known about the neurotrophin dependence of TRPV2-positive neurons in the developing and adult DRGs of mice. In the present study, using immunohistochemistry, we found that TRPV2 was first expressed in DRG neurons at embryonic day (E) 11.5, when neither TRPV1 nor TRPM8 was detected yet. Double-immunofluorescence staining revealed that tyrosine kinase receptor C (TrkC) was expressed in most of TRPV2-positive DRG neurons at E11.5 and E13.5. In addition, the percentage of TRPV2-positive neurons in the total DRG neurons at E13.5 reached the same as that of adulthood. In adult DRGs, TrkC and Ret were expressed in 68% and 25% of TRPV2-positive neurons, respectively. These results suggest that TRPV2 is expressed predominantly in the NT-3-dependent subpopulation of DRG neurons throughout development and in adult mice.

Section snippets

Preparation of mouse embryos

Pregnant C57BL/6 mice (Nihon SLC, Hamamatsu, Japan) were used in the present study. These mice were kept under a 12-h light/dark cycle with food and water ad libitum. At all times, the experiments were carried out under the control of the Animal Research Control Committee in accordance with The Guidelines for Animal Experiments of Wakayama Medical University, Japanese Government Notification on Feeding and Safekeeping of Animals (No. 6), and the National Institute of Health Guide for the Care

Developmental expression of TRPV2 in DRGs, spinal cord, and skin

TRPV2-positive cells were first observed in the mouse DRGs at E11.5 (Fig. 1A). At this stage, all TRPV2-positive cells expressed NeuN, indicating that these cells were postmitotic neurons (Mullen et al., 1992; data not shown). TRPV2 expression in the DRG neurons was observed up to P56 (Figs. 1B, C, 5). There were no significant changes in the percentage of TRPV2-positive neurons in total neuronal population from 13.4±0.6% (121/858 cells) at E13.5 to 18.7±2.3% (229/1230 cells) at P56 (Fig. 3).

Discussion

TRPV2 is expressed in a subpopulation of medium- to large-sized neurons in adult DRGs (Caterina et al., 1999; Ma, 2001; Lewinter et al., 2004). Large-sized neurons are generated between E9 and E10 in mice, and most of which begin to express TrkC between E10 and E11 (Farinas et al., 1998; Ma et al., 1999). In the present study, we found that DRGs began to express TRPV2 between E9.5 and E11.5. In addition, TRPV2 expression was mainly observed in TrkC-positive DRG neurons at E11.5 and E13.5. NT-3

Acknowledgments

We thank Dr. Makoto Tominaga (Section of Cell Signaling, Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences) for the generous gift of the TRPV2 antiserum. We are also grateful to Dr. Keiichiro Okamoto (Department of Physiology, Wakayama Medical University) for critical advices of the statistical analysis. This work was supported by Grant-in-Aid for Scientific Research (C) from The Ministry of Education, Culture, Sports, Science and Technology (15500264) and

References (29)

  • D.L. Bennett et al.

    Postnatal changes in the expression of the trkA high-affinity NGF receptor in primary sensory neurons

    Eur J Neurosci

    (1996)
  • M.J. Caterina et al.

    The capsaicin receptor: a heat-activated ion channel in the pain pathway

    Nature

    (1997)
  • M.J. Caterina et al.

    A capsaicin-receptor homologue with a high threshold for noxious heat

    Nature

    (1999)
  • A.M. Davies et al.

    Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor

    Nature

    (1987)
  • Cited by (45)

    • Purinergic receptor P2Y1 regulates polymodal C-fiber thermal thresholds and sensory neuron phenotypic switching during peripheral inflammation

      2012, Pain
      Citation Excerpt :

      Peripheral inflammation induces an array of changes in dorsal root ganglia (DRG) neurons and within the targeted area, which may be responsible for sensory neuron sensitization [10,14,15] leading to hyperalgesia [2,15]. The inflamed area is known to produce changes in inflammatory mediators, signaling molecules, calcitonin gene-related peptide (CGRP), bradykinin, prostaglandins, serotonin, histamine, H+, adenosine triphosphate, and neurotrophic factors [10,14,15,18,20,23], while the DRG have been shown to contain enhanced levels of neurotrophic factor receptors, ion channels, and other signaling molecules [23,26,31]. Previous reports have shown that isolectin B4 (IB4) binding, transient receptor potential vanilloid type 1 (TRPV1) lacking, polymodal C fibers (CPMs) have a decreased threshold after injection of complete Freund’s adjuvant (CFA) into the skin as measured by an ex vivo skin/nerve/DRG/spinal cord preparation [14], similar to what has been shown after axotomy and regeneration [10].

    • Characterization of Foxp2-expressing cells in the developing spinal cord

      2009, Neuroscience
      Citation Excerpt :

      All controls revealed no labeling (data not shown). Fluorescently labeled cells were quantified in the developing spinal cords with some modifications as described previously (Tamura et al., 2005). Briefly, brachial parts of the specimens from three embryos in each stage (E11.0, E11.5, E12.0, E12.5, E13.5, E15.5, and E17.5) and three neonatal mice (P0) were pooled and processed for sectioning.

    View all citing articles on Scopus
    View full text