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. 2008 Feb 1;23(2):92–100. doi: 10.1007/s12264-007-0013-2

Facial pain induces the alteration of transient receptor potential vanilloid receptor 1 expression in rat trigeminal ganglion

面部炎症痛诱发大鼠三叉神经节神经元中辣椒素受体表达的改变

Lei Pei 1, Chuan-You Lin 1, Jia-Pei Dai 1, Guang-Fu Yin 1,✉
PMCID: PMC5550592  PMID: 17592531

Abstract

Objective

To investigate the involvement of transient receptor potential vanilloid receptor 1 (TRPV1) in the facial inflammatory pain in relation to thermal hyperalgesia and cold pain sensation.

Methods

Facial inflammatory pain model was developed by subcutaneous injection of turpentine oil (TO) into rat facial area. Head withdrawal thermal latency (HWTL) and head withdrawal cold latency (HWCL) were measured once a day for 21 d after TO treatment using thermal and cold measurement apparatus. The immunohistochemical staining, cell-size frequency analysis and the survey of average optical density (OD) value were used to observe the changes of TRPV1 expression in the neurons of the trigeminal ganglion (TG), peripheral nerve fibers in the vibrissal pad, and central projection processes in the trigeminal sensory nuclei caudalis (Vc) on day 3, 5, 7, 14, and 21 after TO injection.

Results

HWTL and HWCL decreased significantly from day 1 to day 14 after TO injection with the lowest value on day 5 and day 3, respectively, and both recovered on day 21. The number of TRPV1-labeled neurons increased remarkably from day 1 to day 14 with a peak on day 7, and returned back to the normal level on day 21. In control rats, only small and medium-sized TG neurons were immunoreactive (IR) to TRPV1, and the TRPV1-IR terminals were abundant in both the vibrissal pad and the Vc. Within 2 weeks of inflammation, the expression of TRPV1 in small and medium-sized TG neurons increased obviously. Also the TRPV1 stained terminals and fibers appeared more frequent and denser in both the vibrissal pad skin and throughout laminae I and the outer zone of laminae II (IIo) of Vc.

Conclusion

Facial inflammatory pain could induce hyperalgesia to noxious heat and cold stimuli, and result in increase of the numbers of TRPV1 positive TG neurons and the peripheral and central terminals of TG. These results suggest that the phenotypic changes of TRPV1 expression in small and medium-sized TG neurons and terminals might play an important role in the development and maintenance of TO-induced inflammatory thermal hyperalgesia and cold pain sensation.

Keywords: vanilloid receptors, facial pain, hyperalgesia, trigeminal ganglion

References

  • [1].Caterina M.J., Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci. 2001;24:487–517. doi: 10.1146/annurev.neuro.24.1.487. [DOI] [PubMed] [Google Scholar]
  • [2].Tominaga M., Julins D. Capsaicin receptor in the pain pathway. Jpn J Pharmacol. 2000;83:20–24. doi: 10.1254/jjp.83.20. [DOI] [PubMed] [Google Scholar]
  • [3].Guo A., Vulchanova L., Wang J., Li X., Elde R. Immunocytochemical localization of the vanilloid receptor 1 (VR1): relation to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci. 1999;11:946–958. doi: 10.1046/j.1460-9568.1999.00503.x. [DOI] [PubMed] [Google Scholar]
  • [4].Carlton S.M., Coggeshall R.E. Peripheral capsaicin receptors increase in the inflamed rat hindpaw: a possible mechanism for peripheral sensitization. Neurosci Lett. 2001;310:53–56. doi: 10.1016/S0304-3940(01)02093-6. [DOI] [PubMed] [Google Scholar]
  • [5].Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000;288:306–313. doi: 10.1126/science.288.5464.306. [DOI] [PubMed] [Google Scholar]
  • [6].Amaya F., Oh-hashi K., Naruse Y., Iijima N., Ueda M., Shimosato G., et al. Local inflammation increases vanilloid receptor 1 expression within distinct subgroups of DRG neurons. Brain Res. 2003;963:190–196. doi: 10.1016/S0006-8993(02)03972-0. [DOI] [PubMed] [Google Scholar]
  • [7].Zhou Y., Li G.D., Zhao Z.Q. State-dependent phosphorylation of epsilon-isozyme of protein kinase C in adult rat dorsal root ganglia after inflammation and nerve injury. J Neurochem. 2003;85:571–580. doi: 10.1046/j.1471-4159.2003.01675.x. [DOI] [PubMed] [Google Scholar]
  • [8].Ji R., Samad T., Jin S., Schmoll R., Woolf C. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron. 2002;36:57–68. doi: 10.1016/S0896-6273(02)00908-X. [DOI] [PubMed] [Google Scholar]
  • [9].Tominaga M., Wada M., Masu M. Potentiation of capsaicin receptor activity by metabotropic ATP receptors as a possible mechanism for ATP-evoked pain and hyperalgesia. Proc Natl Acad Sci USA. 2001;98:6951–6956. doi: 10.1073/pnas.111025298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [10].Premkumar L.S., Ahern G.P. Induction of vanilloid receptor channel activity by protein kinase C. Nature. 2000;408:985–990. doi: 10.1038/35050121. [DOI] [PubMed] [Google Scholar]
  • [11].Chuang H.H., Prescott E.D., Kong H., Shields S., Jordt S.E., Basbaum A.I., et al. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature. 2001;411:957–962. doi: 10.1038/35082088. [DOI] [PubMed] [Google Scholar]
  • [12].Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983;16:109–110. doi: 10.1016/0304-3959(83)90201-4. [DOI] [PubMed] [Google Scholar]
  • [13].Jasmin L., Kohan L., Franssen M. The cold plate as a test of nociceptive behaviors: description and application to the study of chronic neuropathic and inflammatory pain models. Pain. 1998;75:367–382. doi: 10.1016/S0304-3959(98)00017-7. [DOI] [PubMed] [Google Scholar]
  • [14].Simone D.A., Kajander K.C. Responses of cutaneous A fiber nociceptors to noxious cold. J Neurophysiol. 1997;77:2049–2060. doi: 10.1152/jn.1997.77.4.2049. [DOI] [PubMed] [Google Scholar]
  • [15].Santos A.R., Calixto J.B. Ruthenium red and capsazepine antinociceptive effect in formalin and capsaicin models of pain in mice. Neurosci Lett. 1997;235:73–76. doi: 10.1016/S0304-3940(97)00722-2. [DOI] [PubMed] [Google Scholar]
  • [16].Kwak J.Y., Jung J.Y., Hwang S.W., Lee W.T., Oh U. A capsaicin-receptor antagonist, capsazepine, reduces inflammation-induced hyperalgesic responses in the rat: evidence for an endogenous capsaicin-like substance. Neuroscience. 1998;86:619–626. doi: 10.1016/S0306-4522(98)00012-8. [DOI] [PubMed] [Google Scholar]
  • [17].Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature. 2000;405:183–187. doi: 10.1038/35012076. [DOI] [PubMed] [Google Scholar]
  • [18].Ichikawa H., Sugimoto T. VR1-immunoreactive primary sensory neurons in the rat trigeminal ganglion. Brain Res. 2001;890:184–188. doi: 10.1016/S0006-8993(00)03253-4. [DOI] [PubMed] [Google Scholar]
  • [19].Guan X.M. Medical Neurobiology. 1. Beijing: The People’s Medical Publishing House; 2002. [Google Scholar]
  • [20].Leem J.W., Willis W.D., Weller S.C., Chung J.M. Differential activation and classification of cutaneous afferents in the rat. J Neurophysiol. 1993;70:2411–2424. doi: 10.1152/jn.1993.70.6.2411. [DOI] [PubMed] [Google Scholar]
  • [21].Beitel R.E., Dubner R. Response of unmyelinated (C) polymodal nociceptors to thermal stimuli applied to monkey’s face. J Neurophysiol. 1976;39:1160–1175. doi: 10.1152/jn.1976.39.6.1160. [DOI] [PubMed] [Google Scholar]
  • [22].Hwang S.J., Valtschanoff J.G. Vanilloid receptor VR1-positive afferents are distributed differently at different levels of the rat lumbar spinal cord. Neurosci Lett. 2003;349:41–44. doi: 10.1016/S0304-3940(03)00750-X. [DOI] [PubMed] [Google Scholar]

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