International Journal of Oral Biology

  • 제40권4호
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  • Pages.211-216
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  • 2015
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  • 1226-7155(pISSN)
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  • 2287-6618(eISSN)
대한구강생물학회 (The Korean Academy of Oral Biology)
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Ryanodine Receptor-mediated Calcium Release Regulates Neuronal Excitability in Rat Spinal Substantia Gelatinosa Neurons

  • Park, Areum (Department of Oral Physiology, College of Dentistry, Institute of Wonkwang Biomaterial and Implant, Wonkwang University) ;
  • Chun, Sang Woo (Department of Oral Physiology, College of Dentistry, Institute of Wonkwang Biomaterial and Implant, Wonkwang University)
  • 투고 : 2015.12.01
  • 심사 : 2015.12.15
  • 발행 : 2015.12.31
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초록

Nitric Oxide (NO) is an important signaling molecule in the nociceptive process. Our previous study suggested that high concentrations of sodium nitroprusside (SNP), a NO donor, induce a membrane hyperpolarization and outward current through large conductances calcium-activated potassium ($BK_{ca}$) channels in substantia gelatinosa (SG) neurons. In this study, patch clamp recording in spinal slices was used to investigate the sources of $Ca^{2+}$ that induces $Ca^{2+}$-activated potassium currents. Application of SNP induced a membrane hyperpolarization, which was significantly inhibited by hemoglobin and 2-(4-carboxyphenyl) -4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (c-PTIO), NO scavengers. SNP-induced hyperpolarization was decreased in the presence of charybdotoxin, a selective $BK_{Ca}$ channel blocker. In addition, SNP-induced response was significantly blocked by pretreatment of thapsigargin which can remove $Ca^{2+}$ in endoplasmic reticulum, and decreased by pretreatment of dentrolene, a ryanodine receptors (RyR) blocker. These data suggested that NO induces a membrane hyperpolarization through $BK_{ca}$ channels, which are activated by intracellular $Ca^{2+}$ increase via activation of RyR of $Ca^{2+}$ stores.

키워드

참고문헌

  1. Cheng LZ, Lu N, Zhang YQ, Zhao ZQ. Ryanodine receptors contribute to the induction of nociceptive input-evoked long-term potentiation in the rat spinal cord slice. Mol Pain. 2010;6:1-12. doi:http://dx.doi.org/10.1186/1744.8069.6.1.
  2. Ahern GP, Klyachko VA, Jackson MB. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends in Neurosci. 2002;25:510-517. doi:http://dx.doi.org/10.1016/S0166.2236(02)02254.3.
  3. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev. 2007;8:766-775. doi:http://dx.doi.org/10.1038/nrn2214.
  4. Cury Y, Picolo G, Gutierrez VP, Ferreira SH. Pain and analgesia: The dual effect of nitric oxide in the nociceptive system. Nitric Oxide. 2011;25:243-254. doi:http://dx.doi.org/10.1016/ j.niox.2011.06.004.
  5. Guan Y, Yaster M, Raja SN, Tao YX. Genetic knockout and pharmacologic inhibition of neuronal nitric oxide synthase attenuate nerve injury-induced mechanical hypersensitivity in mice. Mol Pain. 2007;3:29-39. doi:http://dx.doi.org/10.1186/1744.8069.3.29.
  6. Tanabe M, Nagatani Y, Saitoh K, Takasu K, Ono H. Pharmacological assessments of nitric oxide synthase isoforms and downstream diversity of NO signaling in the maintenance of thermal and mechanical hypersensitivity after peripheral nerve injury in mice. Neuropharmacol. 2009;56:702-708. doi:http://dx.doi.org/10.1016/j.neuropharm.2008.12.003.
  7. Chu YC, Guan Y, Skinner J, Raja SN, Johns RA, Tao YX. Effect of genetic knockout or pharmacologic inhibition of neuronal nitric oxide synthase on complete Freund's adjuvant-induced persistent pain. Pain. 2005;119:113-123. doi:http://dx.doi.org/10.1016/j.pain.2005.09.024.
  8. Coderre TJ, Yashpal K. Intracellular messengers contributing to persistent nociception and hyperalgesia induced by L-glutamate and substance P in the rat formalin pain model. Eur J Neurosci. 1994;6:1328-1334. doi:http://dx.doi.org/10.1111/j.1460.9568.
  9. Meller ST, Cummings CP, Traub RJ, Gebhart GF. The role of nitric oxide in the development and maintenance of the hyperalgesia produced by intraplantar injection of carrageenan in the rat. Neurosci. 1994;60:367-374. doi:http://dx.doi.org/10.1016/0306.4522.
  10. Chung E, Burke B, Bieber AJ, Doss JC, Ohgami Y, Quock RM. Dynorphin-mediated antinociceptive effects of L-arginine and SIN-1 (an NO donor) in mice. Brain Res Bull. 2006;3:245-250. doi:http://dx.doi.org/10.1016/j.brainresbull.2006.05.008.
  11. Park AR, Lee HI, Semjid D, Kim DK, Chun SW. Dual effect of exogenous nitric oxide on neuronal excitability in rat substantia gelatinosa neurons. Neural Plas. 2014;10:1155-1165. doi:http://dx.doi.org/10.1155/2014.628531.
  12. Wu BN, Chen CF, Hong YR, Howng SL, Lin YL, Chen IJ. Activation of BKCa channels via cyclic AMP- and cyclic GMP-dependent protein kinases by eugenosedin-A in rat basilar artery myocytes. Br J Pharmacol. 2007;152:374-385. doi:http://dx.doi.org/10.1038/sj.bjp.0707406.
  13. Gribkoff VK, Starrett JEJ, Dworetzky SI. Maxi-K potassium channels: form, function, and modulation of a class of endogenous regulators of intracellular calcium. Neuroscientist. 2001;7:166-177. doi:http://dx.doi.org/10.1177/107385840100700211.
  14. Salkoff L, Butler A, Ferreira G. High-conductance potassium channels of the SLO family. Nat Rev Neurosci. 2006;7:921-931. doi:http://dx.doi.org/10.1038/nrn1992.
  15. McManus OB. Calcium-activated potassium channels: regulation by calcium. J Bioenerg Biomembr. 1991;23:537-560. doi:http://dx.doi.org/10.1007/BF00785810.
  16. Lu YF, Hawkins RD. Ryanodine receptors contribute to cGMP-induced late-phase LTP and CREB phosphorylation in the hippocampus. J Neurophysiol. 2002;88:1270-1278. doi:http://dx.doi.org/10.1152/jn.01036.2001.
  17. Galante M, Marty A. Presynaptic ryanodine-sensitive calcium stores contribute to evoked neurotransmitter release at the basket cell-Purkinje cell synapse. J Neurosci. 2003;23:11229-11234. https://doi.org/10.1523/JNEUROSCI.23-35-11229.2003
  18. Verkhratsky A. Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev. 2005;85:201-279. doi:http://dx.doi.org/10.1152/physrev.00004.
  19. Coskun S, Karatas F, Acarturk F, Olmus H, Selvi M, Erbas D. The effect of L-NAME administrations after oral mucosal incision on wound NO level in rabbit. Mol Cellular Biochem. 2005;278:65-69. doi:http://dx.doi.org/10.1007/s11010.005.6628.6.
  20. Sousa AM, Prado WA. The dual effect of a nitric oxided on nociception. Brain Res. 2001;897:9-19. doi:http://dx.doi.org/10.1016/S0006.8993(01)01995.3.
  21. Li K, Qi WX. Effects of multiple intrathecal administration of L-arginine with different doses on formalin-induced nociceptive behavioral responses in rats. Neurosci Bull. 2010;26:211-218. doi:http://dx.doi.org/10.1007/s12264.010.0127.9.
  22. Kawabata A, Manabe S, Manabe Y, Takagi H. Effect of topical administration of L-arginine on formalin-induced nociception in the mouse: a dual role of peripherally formed NO in pain modulation. Br J Pharmacol. 1994;112:547-550. doi:http://dx.doi.org/10.1111/j.1476.5381.
  23. Anggard E. Nitric oxide: mediator, murderer, and medicine. Lancet. 1994;9:1199-206. doi:http://dx.doi.org/10.1016/S0140.6736(94)92405.8.
  24. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitriteinduced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys. 1991;288:481-487. doi:http://dx.doi.org/10.1016/0003.9861(91)90224.7.
  25. Savaria D, Lanoue C, Cadieux A, Rousseau E. Large conducting potassium channel reconstituted from airway smooth muscle. Am J Physiol. 1992;262:327-336.
  26. Lang RJ, Watson MJ. Effects of nitric oxide donors, S-nitroso-L-cysteine and sodium nitroprusside, on the whole-cell and single channel currents in single myocytes of the guinea-pig proximal colon. Br J Pharmacol. 1998; 123:505-517. doi:http://dx.doi.org/10.1038/sj.bjp.0701605.
  27. Ahern GP, Hsu SF, Jackson MB. Direct actions of nitric oxide on rat neurohypophysial $K^+$ channels. J Physiol. 1999; 520:165-176. doi:http://dx.doi.org/10.1111/j.1469.7793.1999.00165.
  28. Forstermann U, Pollock JS, Schmidt HH, Heller M, Muread F. Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc Natl Acad Sci USA. 1991;88:1788-1792. doi:http://dx.doi.org/10.1073/pnas.88.5.1788.
  29. Zhang J, Snyder SH. Nitric oxide in the nervous system. Ann Rev Pharmacol Toxicol. 1995;35:213-233. doi:http://dx.doi.org/10.1146/annurev.pa.35.040195.001241.
  30. Marty A. Ca-dependent $K^+$ channels with large unitary conductance in chromaffin cell membranes. Nature. 1981;291:497-500. doi:http://dx.doi.org/10.1038/291497a0.
  31. Rizzuto R. Intracellular $Ca^{2+}$ pools in neuronal signalling. Curr Opin Neurobiol. 2001;11:306-311. doi:http://dx.doi.org/10.1016/S0959.4388(00)00212.9.
  32. Eu JP, Sun J, Xu L, Stamler JS, Meissner G. The skeletal muscle calcium release channel: coupled $O^2$ sensor and NO signaling functions. Cell. 2002;102:499-509. doi:http://dx.doi.org/10.1016/S0092.8674(00)00054.4.
  33. Pessah IN, Kim KH, Feng W. Redox sensing properties of the ryanodine receptor complex. Front Biosci. 2002;7:72-79. doi:http://dx.doi.org/10.2741/pessah.
  34. Galione A. CyclicADP-ribose, the ADP-ribosyl cyclase pathway and calcium signaling. Mol Cell Endocrinol. 1994;98:125-131. doi:http://dx.doi.org/10.1016/0303.7207(94)90130.9.