International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Molecular Characterization of $Ca_v2.3$ in Rat Trigeminal Ganglion Neurons

  • Fang, Zhi (Department of Physiology and Program in Molecular and Cellular Neuroscience, College of Dentistry and Dental Research Institute, Seoul National University) ;
  • Kim, Joong-Soo (Department of Physiology and Program in Molecular and Cellular Neuroscience, College of Dentistry and Dental Research Institute, Seoul National University) ;
  • Oh, Seog-Bae (Department of Physiology and Program in Molecular and Cellular Neuroscience, College of Dentistry and Dental Research Institute, Seoul National University)
  • Published : 2006.06.30
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Abstract

R-type($Ca_v2.3$) calcium channel contributes to pain sensation in peripheral sensory neurons. Six isoforms of $Ca_v2.3$ that result from combinations of presence or deletion of three inserts(insert I and insert in the II-III loop, and insert III in N-terminal regions) have been demonstrated to be present in different mammalian tissues. However, the molecular basis of $Ca_v2.3$ in trigeminal ganglion(TG) neurons is not known. In the present study, we determined which isoforms of $Ca_v2.3$ are expressed in rat TG neurons using the RT-PCR analysis. Whole tissue RT-PCR analyses revealed that only two isoforms, $Ca_v2.3a$ and $Ca_v2.3e$, were present in TG neurons. From single-cell RT-PCR, we found that $Ca_v2.3e$ rather than $Ca_v2.3a$ was the major isoform expressed in TG neurons, and $Ca_v2.3e$ was preferentially detected in small-sized neurons that express nociceptive marker, transient receptor potential vanilloid 1(TRPV1). Our results suggest that $Ca_v2.3e$ in trigeminal neurons may be a potential target for the pain treatment.

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References

  1. Brown, S.P., Safo, P.K., and Regehr, W.G. Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24:5623-5631, 2004 https://doi.org/10.1523/JNEUROSCI.0918-04.2004
  2. Catterall, W.A. Structure and regulation of voltage-gated $Ca^{2+}$ channels. Annu Rev Cell Dev Biol 16:521-555, 2000 https://doi.org/10.1146/annurev.cellbio.16.1.521
  3. Dietrich, D., Kirschstein, T., Kukley, M., and Pereverzev, A., von der Brelie, C., Schneider, T., and Beck, H. Functional specialization of presynaptic Cav2.3 $Ca^{2+}$ channels. Neuron 39:483-496, 2003 https://doi.org/10.1016/S0896-6273(03)00430-6
  4. Dredge, B.K., Polydorides, A.D., and Darnell, R.B. The splice of life: alternative splicing and neurological disease. Nat Rev Neurosci 2:43-50, 2001 https://doi.org/10.1038/35049061
  5. Dunlap, K., Luebke, J.I., and Turner, T.J. Identification of calcium channels that control neurosecretion. Science 266:828-831,1994 https://doi.org/10.1126/science.226.4676.828
  6. Foehring, R.C., Mermelstein, P.G., Song, W.J., Ulrich, S., and Surmeier, D.J. Unique properties of R-type, calcium currents in neocortical and neostriatal neurons. J Neurophysiol 84:2225-2236, 2000 https://doi.org/10.1152/jn.2000.84.5.2225
  7. Graveley, B.R. Alternative splicing: increasing diversity in the proteomic world. Trends Genet 17:100-107, 2001 https://doi.org/10.1016/S0168-9525(00)02176-4
  8. Hokfelt, T., Zhang, X., and Wiesenfeld-Hallin, Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17:22-30, 1994 https://doi.org/10.1016/0166-2236(94)90031-0
  9. Hunt, S.P. and Mantyh, P.W. The molecular dynamics of pain control. Nat Rev Neurosci 2:83-91, 2001
  10. Ikeda, M. and Matsumoto, S. Classification of voltagedependent $Ca^{2+}$ channels in trigeminal ganglion neurons from neonatal rats. Life Sci 73:1175-1187, 2003 https://doi.org/10.1016/S0024-3205(03)00414-4
  11. Ishibashi, H., Rhee, J.S., and Akaike, N. Regional difference of high voltage-activated $Ca^{2+}$ channels in rat CNS neurones. Neuroreport 6:1621-1624, 1995 https://doi.org/10.1097/00001756-199508000-00008
  12. Keegan, L.P., Gallo, A., and O'Connell, M.A. The many roles of an RNA editor. Nat Rev Genet 2:869-878, 2001
  13. Lee, S.C., Choi, S., Lee, T., Kim, H.L., Chin, H., and Shin, H.S. Molecular basis of R-type calcium channels in central amygdala neurons of the mouse. Proc Natl Acad Sci U S A 99:3276-3281, 2002
  14. Murakami, M., Suzuki, T., Nakagawasai, O., Murakami, H., Murakami, S., Esashi, A., Taniguchi, R., Yanagisawa, T., Tan-No, K., Miyoshi, I., Sasano, and H., Tadano, T. Distribution of various calcium channel alpha(1) subunits in murine DRG neurons and antinociceptive effect of omegaconotoxin SVIB in mice. Brain Res 903:231-236, 2001 https://doi.org/10.1016/S0006-8993(01)02427-1
  15. Murray, S.S. and Cheema, S.S. Constitutive expression of the low-affinity neurotrophin receptor and changes during axotomy-induced death of sensory neurones in the neonatal rat dorsal root ganglion. J Anat 202:227-238, 2003 https://doi.org/10.1046/j.1469-7580.2003.00151.x
  16. Niidome, T., Kim, M.S., Friedrich, and T., Mori, Y. Molecular cloning and characterization of a novel calcium channel from rabbit brain. FEBS Lett 308:7-13, 1992 https://doi.org/10.1016/0014-5793(92)81038-N
  17. Pereverzev, A., Leroy, J., Krieger, A., Malecot, C.O., Hescheler, J., Pfitzer, G, Klockner, U., and Schneider, T. Alternate splicing in the cytosolic II-III loop and the carboxy terminus of human E-type voltage-gated Ca(2+) channels: electrophysiological characterization of isoforms. Mol Cell Neurosci 21:352-365, 2002 https://doi.org/10.1006/mcne.2002.1179
  18. Saegusa, H., Kurihara, T., Zong, S., Minowa, O., Kazuno, A., Han, W., Matsuda, Y., Yamanaka, H., Osanai, M., Noda, T., and Tanabe, T. Altered pain responses in mice lacking alpha 1E subunit of the voltage-dependent $Ca^{2+}$ channel. Proc Nat! Acad Sci U S A 97:6132-6137, 2000
  19. Schneider, T., Wei, X., Olcese, R., Costantin, J.L., Neely, A., Palade, P., Perez-Reyes, E., Qin, N., Zhou, J., Crawford, G.D., et al. Molecular analysis and functional expression of the human type E neuronal $Ca^{2+}$ channel alpha 1 subunit. Receptors Channels 2:255-270,1994
  20. Schramm, M., Vajna, R., Pereverzev, A., Tottene, A., Klockner, D., Pietrobon, D., Hesche1er, J., and Schneider, T. Isoforms of alpha1E voltage-gated calcium channels in rat cerebellar granule cells--detection of major calcium channel alpha1transcripts by reverse transcription-polymerase chain reaction. Neuroscience 92:565-575, 1999 https://doi.org/10.1016/S0306-4522(99)00013-5
  21. Sessle, B.J. Recent insights intobrainstem mechanisms underlying craniofacial pain. J Dent Educ 66: 108-112,2002
  22. Silbert, S.C., Beacham, D.W., and McCleskey, E.W. Quantitative single-cell differences in mu-opioid receptor mRNA distinguish myelinated and unmyelinated nociceptors. J Neurosci 23:34-42, 2003 https://doi.org/10.1523/JNEUROSCI.23-01-00034.2003
  23. Szallasi, A. and Blumberg, P.M. Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol Rev 51:159-212,1999
  24. Vajna, R., Schramm, M., Pereverzev, A., Arnhold, S., Grabsch, H., Klockner, U., Perez-Reyes, E., Hescheler, and J., Schneider, T. New isoform of the neuronal $Ca^{2+}$ channel alphalE subunit in islets of Langerhans and kidneydistribution of voltage-gated $Ca^{2+}$ channel alpha1 subunits in cell lines and tissues. Eur J Biochem 257:274-285, 1998 https://doi.org/10.1046/j.1432-1327.1998.2570274.x
  25. Vanegas, H. and Schaible, H. Effects of antagonists to highthreshold calcium channels upon spinal mechanisms of pain, hyperalgesia and allodynia. Pain 85:9-18, 2000 https://doi.org/10.1016/S0304-3959(99)00241-9
  26. Williams, M.E., Marubio, L.M., Deal, C.R., Hans, M., Brust, P.F., Philipson, L.H., Miller, R.J., Johnson, E.C., Harpold, M.M., and Ellis, S.B. Structure and functional characterization of neuronal alpha 1E calcium channel subtypes. J Biol Chem 269: 22347-22357,1994
  27. Wilson, S.M., Toth, P.T., Oh, S.B., Gillard, S.E., Volsen, S., Ren, D., Philipson, L.H., Lee, E.C., Fletcher, C.F., Tessarollo, L., Copeland, N.G., Jenkins, N.A., and Miller, R.J. The status of voltage-dependent calcium channels in alpha IE knock-out mice. J Neurosci 20:8566-8571, 2000 https://doi.org/10.1523/JNEUROSCI.20-23-08566.2000
  28. Yang, B.H., Piao, Z.G., Kim, Y.B., Lee, C.H., Lee, J.K., Park, K., Kim, J.S., and Oh, S.B. Activation ofvanilloid receptor 1 (VR1) by eugenol. J Dent Res 82:781-785, 2003 https://doi.org/10.1177/154405910308201004
  29. Yusaf, S.P., Goodman, J., Pinnock, R.D., Dixon, A.K., and Lee, K. Expression of voltage-gated calcium channel subunits in rat dorsal root ganglion neurons. Neurosci Lett 311:137-141, 2001 https://doi.org/10.1016/S0304-3940(01)02038-9