Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2014, Article ID 938235, 12 pages
http://dx.doi.org/10.1155/2014/938235
Research Article

Nociceptive Neurons Differentially Express Fast and Slow T-Type Ca2+ Currents in Different Types of Diabetic Neuropathy

1International Center of Molecular Physiology of National Academy of Sciences of Ukraine, 4 Bogomoletz Street., Kyiv 01024, Ukraine
2State Key Laboratory of Molecular and Cellular Biology, Bogomoletz Institute of Physiology of National Academy of Sciences of Ukraine, 4 Bogomoletz Street, Kyiv 01024, Ukraine

Received 3 November 2013; Revised 24 December 2013; Accepted 30 December 2013; Published 18 February 2014

Academic Editor: Dong-ho Youn

Copyright © 2014 Eugen V. Khomula et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Gooch and D. Podwall, “The diabetic neuropathies,” Neurologist, vol. 10, no. 6, pp. 311–322, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. N. A. Calcutt, J. D. Freshwater, and A. P. Mizisin, “Prevention of sensory disorders in diabetic Sprague-Dawley rats by aldose reductase inhibition or treatment with ciliary neurotrophic factor,” Diabetologia, vol. 47, no. 4, pp. 718–724, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. K. K. Beiswenger, N. A. Calcutt, and A. P. Mizisin, “Dissociation of thermal hypoalgesia and epidermal denervation in streptozotocin-diabetic mice,” Neuroscience Letters, vol. 442, no. 3, pp. 267–272, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. I. G. Obrosova, “Diabetic painful and insensate neuropathy: pathogenesis and potential treatments,” Neurotherapeutics, vol. 6, no. 4, pp. 638–647, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Dobretsov, M. M. Backonja, D. Romanovsky, and J. R. Stimers, “Animal models of diabetic neuropathic pain,” Neuromethods, vol. 49, pp. 147–169, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. T.-J. Huang, N. M. Sayers, P. Fernyhough, and A. Verkhratsky, “Diabetes-induced alterations in calcium homeostasis in sensory neurones of streptozotocin-diabetic rats are restricted to lumbar ganglia and are prevented by neurotrophin-3,” Diabetologia, vol. 45, no. 4, pp. 560–570, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Kostyuk, N. Voitenko, I. Kruglikov et al., “Diabetes-induced changes in calcium homeostasis and the effects of calcium channel blockers in rat and mice nociceptive neurons,” Diabetologia, vol. 44, no. 10, pp. 1302–1309, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. I. Kruglikov, O. Gryshchenko, L. Shutov, E. Kostyuk, P. Kostyuk, and N. Voitenko, “Diabetes-induced abnormalities in ER calcium mobilization in primary and secondary nociceptive neurons,” Pflugers Archiv European Journal of Physiology, vol. 448, no. 4, pp. 395–401, 2004. View at Google Scholar · View at Scopus
  9. L. Shutov, I. Kruglikov, O. Gryshchenko et al., “The effect of nimodipine on calcium homeostasis and pain sensitivity in diabetic rats,” Cellular and Molecular Neurobiology, vol. 26, no. 7-8, pp. 1541–1557, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. J. N. Campbell and R. A. Meyer, “Mechanisms of neuropathic pain,” Neuron, vol. 52, no. 1, pp. 77–92, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Veves, M. Backonja, and R. A. Malik, “Painful diabetic neuropathy: epidemiology, natural history, early diagnosis, and treatment options,” Pain Medicine, vol. 9, no. 6, pp. 660–674, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. A. I. Basbaum, D. M. Bautista, G. Scherrer, and D. Julius, “Cellular and molecular mechanisms of pain,” Cell, vol. 139, no. 2, pp. 267–284, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Perez-Reyes, “Molecular physiology of low-voltage-activated T-type calcium channels,” Physiological Reviews, vol. 83, no. 1, pp. 117–161, 2003. View at Google Scholar · View at Scopus
  14. S. Pathirathna, B. C. Brimelow, M. M. Jagodic et al., “New evidence that both T-type calcium channels and GABAA channels are responsible for the potent peripheral analgesic effects of 5α-reduced neuroactive steroids,” Pain, vol. 114, no. 3, pp. 429–443, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. S. M. Todorovic, V. Jevtovic-Todorovic, A. Meyenburg et al., “Redox modulation of T-Type calcium channels in rat peripheral nociceptors,” Neuron, vol. 31, no. 1, pp. 75–85, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. S. M. Todorovic, A. Meyenburg, and V. Jevtovic-Todorovic, “Mechanical and thermal antinociception in rats following systemic administration of mibefradil, a T-type calcium channel blocker,” Brain Research, vol. 951, no. 2, pp. 336–340, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Bourinet, A. Alloui, A. Monteil et al., “Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception,” The EMBO Journal, vol. 24, no. 2, pp. 315–324, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Choi, H. S. Na, J. Kim et al., “Attenuated pain responses in mice lacking CaV3.2 T-type channels,” Genes, Brain and Behavior, vol. 6, no. 5, pp. 425–431, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. S. M. Todorovic and V. Jevtovic-Todorovic, “T-type voltage-gated calcium channels as targets for the development of novel pain therapies,” British Journal of Pharmacology, vol. 163, no. 3, pp. 484–495, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. R. B. Messinger, A. K. Naik, M. M. Jagodic et al., “In vivo silencing of the CaV3.2 T-type calcium channels in sensory neurons alleviates hyperalgesia in rats with streptozocin-induced diabetic neuropathy,” Pain, vol. 145, no. 1-2, pp. 184–195, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Dogrul, L. R. Gardell, M. H. Ossipov, F. C. Tulunay, J. Lai, and F. Porreca, “Reversal of experimental neuropathic pain by T-type calcium channel blockers,” Pain, vol. 105, no. 1-2, pp. 159–168, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. M. E. Hildebrand and T. P. Snutch, “Contributions of T-type calcium channels to the pathophysiology of pain signaling,” Drug Discovery Today, vol. 3, no. 3, pp. 335–341, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. T. P. Snutch and L. S. David, “T-type calcium channels: an emerging therapeutic target for the treatment of pain,” Drug Development Research, vol. 67, no. 4, pp. 404–415, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. S. M. Todorovic and V. Jevtovic-Todorovic, “Regulation of T-type calcium channels in the peripheral pain pathway,” Channels, vol. 1, no. 4, pp. 238–245, 2007. View at Google Scholar · View at Scopus
  25. M. M. Jagodic, S. Pathirathna, M. T. Nelson et al., “Cell-specific alterations of T-type calcium current in painful diabetic neuropathy enhance excitability of sensory neurons,” Journal of Neuroscience, vol. 27, no. 12, pp. 3305–3316, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. E. M. Talley, L. L. Cribbs, J.-H. Lee, A. Daud, E. Perez-Reyes, and D. A. Bayliss, “Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels,” Journal of Neuroscience, vol. 19, no. 6, pp. 1895–1911, 1999. View at Google Scholar · View at Scopus
  27. E. V. Khomula, V. Y. Viatchenko-Karpinski, A. L. Borisyuk et al., “Specific functioning of Cav3.2 T-type calcium and TRPV1 channels under different types of STZ-diabetic neuropathy,” Biochimica et Biophysica Acta, no. 5, pp. 636–649, 2013. View at Google Scholar
  28. B. Coste, M. Crest, and P. Delmas, “Pharmacological dissection and distribution of NaN/Nav1.9, T-type Ca2+ currents, and mechanically activated cation currents in different populations of DRG neurons,” Journal of General Physiology, vol. 129, no. 1, pp. 57–77, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. C. G. Cardenas, L. P. del Mar, and R. S. Scroggs, “Variation in serotonergic inhibition of calcium channel currents in four types of rat sensory neurons differentiated by membrane properties,” Journal of Neurophysiology, vol. 74, no. 5, pp. 1870–1879, 1995. View at Google Scholar · View at Scopus
  30. R. S. Scroggs and A. P. Fox, “Calcium current variation between acutely isolated adult rat dorsal root ganglion neurons of different size,” Journal of Physiology, vol. 445, pp. 639–658, 1992. View at Google Scholar · View at Scopus
  31. C. L. Stucky and G. R. Lewin, “Isolectin B4-positive and -negative nociceptors are functionally distinct,” Journal of Neuroscience, vol. 19, no. 15, pp. 6497–6505, 1999. View at Google Scholar · View at Scopus
  32. C. J. Woolf and Q. Ma, “Nociceptors-noxious stimulus detectors,” Neuron, vol. 55, no. 3, pp. 353–364, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Vulchanova, T. H. Olson, L. S. Stone, M. S. Riedl, R. Elde, and C. N. Honda, “Cytotoxic targeting of isolectin IB4-binding sensory neurons,” Neuroscience, vol. 108, no. 1, pp. 143–155, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. W. D. Snider and S. B. McMahon, “Tackling pain at the source: new ideas about nociceptors,” Neuron, vol. 20, no. 4, pp. 629–632, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. C.-L. Chen, D. C. Broom, Y. Liu et al., “Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain,” Neuron, vol. 49, no. 3, pp. 365–377, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris, “A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia,” Pain, vol. 32, no. 1, pp. 77–88, 1988. View at Google Scholar · View at Scopus
  37. M. B. Gerke and M. B. Plenderleith, “Binding sites for the plant lectin Bandeiraea simplicifolia I-isolectin B4 are expressed by nociceptive primary sensory neurones,” Brain Research, vol. 911, no. 1, pp. 101–104, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. J.-H. Lee, J. C. Gomora, L. L. Cribbs, and E. Perez-Reyes, “Nickel block of three cloned T-type calcium channels: low concentrations selectively block α1H,” Biophysical Journal, vol. 77, no. 6, pp. 3034–3042, 1999. View at Google Scholar · View at Scopus
  39. A. Tscherter, F. David, T. Ivanova et al., “Minimal alterations in T-type calcium channel gating markedly modify physiological firing dynamics,” Journal of Physiology, vol. 589, no. 7, pp. 1707–1724, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Yue, L. Liu, Z. Liu, B. Shu, and Y. Zhang, “Upregulation of T-type Ca2+ channels in primary sensory neurons in spinal nerve injury,” Spine, vol. 38, no. 6, pp. 463–470, 2013. View at Google Scholar
  41. K. E. Rose, N. Lunardi, A. Boscolo et al., “Immunohistological demonstration of CaV3.2 T-type voltage-gated calcium channel expression in soma of dorsal root ganglion neurons and peripheral axons of rat and mouse,” Neuroscience, vol. 250, pp. 263–274, 2013. View at Google Scholar
  42. X. Zhong, J. R. Liu, J. W. Kyle, D. A. Hanck, and W. S. Agnew, “A profile of alternative RNA splicing and transcript variation of CACNA1H, a human T-channel gene candidate for idiopathic generalized epilepsies,” Human Molecular Genetics, vol. 15, no. 9, pp. 1497–1512, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. K. E. Hall, A. A. F. Anders, and J. W. Wiley, “Voltage-dependent calcium currents are enhanced in dorsal root ganglion neurones from the Bio Bred/Worchester diabetic rat,” Journal of Physiology, vol. 486, no. 2, pp. 313–322, 1995. View at Google Scholar · View at Scopus
  44. K. E. Hall, J. Liu, A. A. F. Sima, and J. W. Wiley, “Impaired inhibitory G-protein function contributes to increased calcium currents in rats with diabetic neuropathy,” Journal of Neurophysiology, vol. 86, no. 2, pp. 760–770, 2001. View at Google Scholar · View at Scopus
  45. J. R. Latham, S. Pathirathna, M. M. Jagodic et al., “Selective T-type calcium channel blockade alleviates hyperalgesia in ob/ob mice,” Diabetes, vol. 58, no. 11, pp. 2656–2665, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. W. Choe, R. B. Messinger, E. Leach et al., “TTA-P2 is a potent and selective blocker of T-type calcium channels in rat sensory neurons and a novel antinociceptive agent,” Molecular Pharmacology, vol. 80, no. 5, pp. 900–910, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. M. M. Jagodic, S. Pathirathna, P. M. Joksovic et al., “Upregulation of the T-type calcium current in small rat sensory neurons after chronic constrictive injury of the sciatic nerve,” Journal of Neurophysiology, vol. 99, no. 6, pp. 3151–3156, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. L. A. Swayne and E. Bourinet, “Voltage-gated calcium channels in chronic pain: emerging role of alternative splicing,” Pflugers Archiv European Journal of Physiology, vol. 456, no. 3, pp. 459–466, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. M. T. Nelson, P. M. Joksovic, E. Perez-Reyes, and S. M. Todorovic, “The endogenous redox agent L-cysteine induces T-type Ca2+ channel-dependent sensitization of a novel subpopulation of rat peripheral nociceptors,” Journal of Neuroscience, vol. 25, no. 38, pp. 8766–8775, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. A. S. Kozlov, F. McKenna, J.-H. Lee et al., “Distinct kinetics of cloned T-type Ca2+ channels lead to differential Ca2+ entry and frequency-dependence during mock action potentials,” European Journal of Neuroscience, vol. 11, no. 12, pp. 4149–4158, 1999. View at Google Scholar · View at Scopus
  51. R. C. H. Warre, N. C. L. McNaughton, and A. D. Randall, “Differential discrimination of fast and slow synaptic waveforms by two low-voltage-activated calcium channels,” Neuroscience, vol. 110, no. 2, pp. 375–388, 2002. View at Publisher · View at Google Scholar · View at Scopus