The Korean Journal of Physiology and Pharmacology

  • 제16권3호
  • /
  • Pages.211-217
  • /
  • 2012
  • /
  • 1226-4512(pISSN)
  • /
  • 2093-3827(eISSN)
대한약리학회 (The Korean Society of Pharmacology)
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Activation of the cGMP/Protein Kinase G Pathway by Nitric Oxide Can Decrease TRPV1 Activity in Cultured Rat Dorsal Root Ganglion Neurons

  • Jin, Yun-Ju (Department of Physiology, Seoul National University College of Medicine) ;
  • Kim, Jun (Department of Physiology, Seoul National University College of Medicine) ;
  • Kwak, Ji-Yeon (Department of Physiology and Biophysics, Inha University College of Medicine)
  • 투고 : 2012.04.10
  • 심사 : 2012.06.12
  • 발행 : 2012.06.30
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초록

Recent studies have demonstrated that nitric oxide (NO) activates transient receptor potential vanilloid subtype 1 (TRPV1) via S-nitrosylation of the channel protein. NO also modulates various cellular functions via activation of the soluble guanylyl cyclase (sGC)/protein kinase G (PKG) pathway and the direct modification of proteins. Thus, in the present study, we investigated whether NO could indirectly modulate the activity of TRPV1 via a cGMP/PKG-dependent pathway in cultured rat dorsal root ganglion (DRG) neurons. NO donors, sodium nitroprusside (SNP) and S-nitro-N-acetylpenicillamine (SNAP), decreased capsaicin-evoked currents ($I_{cap}$). NO scavengers, hemoglobin and 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (CPTIO), prevented the inhibitory effect of SNP on $I_{cap}$. Membrane-permeable cGMP analogs, 8-bromoguanosine 3', 5'-cyclic monophosphate (8bromo-cGMP) and 8-(4chlorophenylthio)-guanosine 3',5'-cyclic monophosphate (8-pCPT-cGMP), and the guanylyl cyclase stimulator YC-1 mimicked the effect of SNP on $I_{cap}$. The PKG inhibitor KT5823 prevented the inhibition of $I_{cap}$ by SNP. These results suggest that NO can downregulate the function of TRPV1 through activation of the cGMP/PKG pathway in peripheral sensory neurons.

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참고문헌

  1. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997;389:816-824. https://doi.org/10.1038/39807
  2. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 1998;21:531-543. https://doi.org/10.1016/S0896-6273(00)80564-4
  3. Oh U, Hwang SW, Kim D. Capsaicin activates a nonselective cation channel in cultured neonatal rat dorsal root ganglion neurons. J Neurosci. 1996;16:1659-1667.
  4. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000;288:306-313. https://doi.org/10.1126/science.288.5464.306
  5. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature. 2000;405:183-187. https://doi.org/10.1038/35012076
  6. Shin J, Cho H, Hwang SW, Jung J, Shin CY, Lee SY, Kim SH, Lee MG, Choi YH, Kim J, Haber NA, Reichling DB, Khasar S, Levine JD, Oh U. Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc Natl Acad Sci USA. 2002;99:10150-10155. https://doi.org/10.1073/pnas.152002699
  7. Shim WS, Tak MH, Lee MH, Kim M, Kim M, Koo JY, Lee CH, Kim M, Oh U. TRPV1 mediates histamine-induced itching via the activation of phospholipase $A_2$ and 12-lipoxygenase. J Neurosci. 2007;27:2331-2337. https://doi.org/10.1523/JNEUROSCI.4643-06.2007
  8. Lopshire JC, Nicol GD. Activation and recovery of the $PGE_2$-mediated sensitization of the capsaicin response in rat sensory neurons. J Neurophysiol. 1997;78:3154-3164. https://doi.org/10.1152/jn.1997.78.6.3154
  9. Zhang N, Inan S, Cowan A, Sun R, Wang JM, Rogers TJ, Caterina M, Oppenheim JJ. A proinflammatory chemokine, CCL3, sensitizes the heat- and capsaicin-gated ion channel TRPV1. Proc Natl Acad Sci USA. 2005;102:4536-4541. https://doi.org/10.1073/pnas.0406030102
  10. Levine JD, Alessandri-Haber N. TRP channels: targets for the relief of pain. Biochim Biophys Acta. 2007;1772:989-1003. https://doi.org/10.1016/j.bbadis.2007.01.008
  11. Vyklicky L, Lyfenko A, Susankova K, Teisinger J, Vlachova V. Reducing agent dithiothreitol facilitates activity of the capsaicin receptor VR-1. Neuroscience. 2002;111:435-441. https://doi.org/10.1016/S0306-4522(02)00051-9
  12. Jin Y, Kim DK, Khil LY, Oh U, Kim J, Kwak J. Thimerosal decreases TRPV1 activity by oxidation of extracellular sulfhydryl residues. Neurosci Lett. 2004;369:250-255. https://doi.org/10.1016/j.neulet.2004.07.059
  13. Tousova K, Susankova K, Teisinger J, Vyklicky L, Vlachova V. Oxidizing reagent copper-o-phenanthroline is an open channel blocker of the vanilloid receptor TRPV1. Neuropharmacology. 2004;47:273-285. https://doi.org/10.1016/j.neuropharm.2004.04.001
  14. Blaise GA, Gauvin D, Gangal M, Authier S. Nitric oxide, cell signaling and cell death. Toxicology. 2005;208:177-192. https://doi.org/10.1016/j.tox.2004.11.032
  15. Guzik TJ, Korbut R, Adamek-Guzik T. Nitric oxide and superoxide in inflammation and immune regulation. J Physiol Pharmacol. 2003;54:469-487.
  16. Lee JJ. Nitric oxide modulation of GABAergic synaptic transmission in mechanically isolated rat auditory cortical neurons. Korean J Physiol Pharmacol. 2009;13:461-467. https://doi.org/10.4196/kjpp.2009.13.6.461
  17. Martinez-Ruiz A, Cadenas S, Lamas S. Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic Biol Med. 2011;51:17-29. https://doi.org/10.1016/j.freeradbiomed.2011.04.010
  18. Ahern GP, Hsu SF, Jackson MB. Direct actions of nitric oxide on rat neurohypophysial $K^+$ channels. J Physiol. 1999;520:165-176. https://doi.org/10.1111/j.1469-7793.1999.00165.x
  19. Castel H, Vaudry H. Nitric oxide directly activates GABA(A) receptor function through a cGMP/protein kinase-independent pathway in frog pituitary melanotrophs. J Neuroendocrinol. 2001;13:695-705. https://doi.org/10.1046/j.1365-2826.2001.00683.x
  20. Lang RJ, Harvey JR, McPhee GJ, Klemm MF. Nitric oxide and thiol reagent modulation of $Ca^{2+}$-activated $K^+$ (BKCa) channels in myocytes of the guinea-pig taenia caeci. J Physiol. 2000;525:363-376. https://doi.org/10.1111/j.1469-7793.2000.00363.x
  21. Renganathan M, Cummins TR, Waxman SG. Nitric oxide blocks fast, slow, and persistent $Na^+$ channels in C-type DRG neurons by S-nitrosylation. J Neurophysiol. 2002;87:761-775. https://doi.org/10.1152/jn.00369.2001
  22. Fukao M, Mason HS, Britton FC, Kenyon JL, Horowitz B, Keef KD. Cyclic GMP-dependent protein kinase activates cloned $BK_{Ca}$ channels expressed in mammalian cells by direct phosphorylation at serine 1072. J Biol Chem. 1999;274:10927-10935. https://doi.org/10.1074/jbc.274.16.10927
  23. Han J, Kim N, Kim E, Ho WK, Earm YE. Modulation of ATP-sensitive potassium channels by cGMP-dependent protein kinase in rabbit ventricular myocytes. J Biol Chem. 2001;276:22140-22147. https://doi.org/10.1074/jbc.M010103200
  24. Herring N, Rigg L, Terrar DA, Paterson DJ. NO-cGMP pathway increases the hyperpolarisation-activated current,$I_f$, and heart rate during adrenergic stimulation. Cardiovasc Res. 2001;52:446-453. https://doi.org/10.1016/S0008-6363(01)00425-4
  25. Yoshimura N, Seki S, de Groat WC. Nitric oxide modulates $Ca^{2+}$ channels in dorsal root ganglion neurons innervating rat urinary bladder. J Neurophysiol. 2001;86:304-311. https://doi.org/10.1152/jn.2001.86.1.304
  26. Zhou XB, Ruth P, Schlossmann J, Hofmann F, Korth M. Protein phosphatase 2A is essential for the activation of $Ca^{2+}$-activated $K^+$ currents by cGMP-dependent protein kinase in tracheal smooth muscle and Chinese hamster ovary cells. J Biol Chem. 1996;271:19760-19767. https://doi.org/10.1074/jbc.271.33.19760
  27. Zsombok A, Schrofner S, Hermann A, Kerschbaum HH. A cGMP-dependent cascade enhances an L-type-like $Ca^{2+}$ current in identified snail neurons. Brain Res. 2005;1032:70-76. https://doi.org/10.1016/j.brainres.2004.11.003
  28. Miyamoto T, Dubin AE, Petrus MJ, Patapoutian A. TRPV1 and TRPA1 mediate peripheral nitric oxide-induced nociception in mice. PLoS One. 2009;4:e7596. https://doi.org/10.1371/journal.pone.0007596
  29. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, Mori Y. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol. 2006;2:596-607. https://doi.org/10.1038/nchembio821
  30. Nunez L, Vaquero M, Gomez R, Caballero R, Mateos-Caceres P, Macaya C, Iriepa I, Galvez E, Lopez-Farre A, Tamargo J, Delpon E. Nitric oxide blocks hKv1.5 channels by S-nitrosylation and by a cyclic GMP-dependent mechanism. Cardiovasc Res. 2006;72:80-89. https://doi.org/10.1016/j.cardiores.2006.06.021
  31. Almanza A, Navarrete F, Vega R, Soto E. Modulation of voltage-gated $Ca^{2+}$ current in vestibular hair cells by nitric oxide. J Neurophysiol. 2007;97:1188-1195. https://doi.org/10.1152/jn.00849.2006
  32. Irwin C, Roberts W, Naseem KM. Nitric oxide inhibits platelet adhesion to collagen through cGMP-dependent and independent mechanisms: the potential role for S-nitrosylation. Platelets. 2009;20:478-486. https://doi.org/10.3109/09537100903159375
  33. Jian K, Chen M, Cao X, Zhu XH, Fung ML, Gao TM. Nitric oxide modulation of voltage-gated calcium current by S-nitrosylation and cGMP pathway in cultured rat hippocampal neurons. Biochem Biophys Res Commun. 2007;359:481-485. https://doi.org/10.1016/j.bbrc.2007.05.113
  34. Koplas PA, Rosenberg RL, Oxford GS. The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci. 1997;17:3525-3537.
  35. Thippeswamy T, McKay JS, Quinn JP, Morris R. Nitric oxide, a biological double-faced janus--is this good or bad? Histol Histopathol. 2006;21:445-458.
  36. Campbell DL, Stamler JS, Strauss HC. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol. 1996;108:277-293. https://doi.org/10.1085/jgp.108.4.277
  37. Ellershaw DC, Greenwood IA, Large WA. Dual modulation of swelling-activated chloride current by NO and NO donors in rabbit portal vein myocytes. J Physiol. 2000;528:15-24. https://doi.org/10.1111/j.1469-7793.2000.00015.x
  38. White RE, Lee AB, Shcherbatko AD, Lincoln TM, Schonbrunn A, Armstrong DL. Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature. 1993;361:263-266. https://doi.org/10.1038/361263a0
  39. Dun NJ, Dun SL, Forstermann U, Tseng LF. Nitric oxide synthase immunoreactivity in rat spinal cord. Neurosci Lett. 1992;147:217-220. https://doi.org/10.1016/0304-3940(92)90599-3
  40. Zhang X, Verge V, Wiesenfeld-Hallin Z, Ju G, Bredt D, Synder SH, Hokfelt T. Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J Comp Neurol. 1993;335:563-575. https://doi.org/10.1002/cne.903350408
  41. Saito S, Kidd GJ, Trapp BD, Dawson TM, Bredt DS, Wilson DA, Traystman RJ, Snyder SH, Hanley DF. Rat spinal cord neurons contain nitric oxide synthase. Neuroscience. 1994;59:447-456. https://doi.org/10.1016/0306-4522(94)90608-4
  42. Haley JE, Dickenson AH, Schachter M. Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat. Neuropharmacology. 1992;31:251-258. https://doi.org/10.1016/0028-3908(92)90175-O
  43. Malmberg AB, Yaksh TL. Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats. Pain. 1993;54:291-300. https://doi.org/10.1016/0304-3959(93)90028-N
  44. Przewlocki R, Machelska H, Przewlocka B. Inhibition of nitric oxide synthase enhances morphine antinociception in the rat spinal cord. Life Sci. 1993;53:PL1-5. https://doi.org/10.1016/0024-3205(93)90615-A
  45. Hao JX, Xu XJ. Treatment of a chronic allodynia-like response in spinally injured rats: effects of systemically administered nitric oxide synthase inhibitors. Pain. 1996;66:313-319. https://doi.org/10.1016/0304-3959(96)03039-4
  46. Roche AK, Cook M, Wilcox GL, Kajander KC. A nitric oxide synthesis inhibitor (L-NAME) reduces licking behavior and Fos-labeling in the spinal cord of rats during formalin-induced inflammation. Pain. 1996;66:331-341. https://doi.org/10.1016/0304-3959(96)03025-4
  47. Machelska H, Labuz D, Przewlocki R, Przewlocka B. Inhibition of nitric oxide synthase enhances antinociception mediated by mu, delta and kappa opioid receptors in acute and prolonged pain in the rat spinal cord. J Pharmacol Exp Ther. 1997;282:977-984.
  48. Aley KO, McCarter G, Levine JD. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci. 1998;18:7008-7014.
  49. Ferreira SH, Duarte ID, Lorenzetti BB. The molecular mechanism of action of peripheral morphine analgesia: stimulation of the cGMP system via nitric oxide release. Eur J Pharmacol. 1991;201:121-122. https://doi.org/10.1016/0014-2999(91)90333-L
  50. Ferreira SH, Lorenzetti BB, Faccioli LH. Blockade of hyperalgesia and neurogenic oedema by topical application of nitroglycerin. Eur J Pharmacol. 1992;217:207-209. https://doi.org/10.1016/0014-2999(92)90871-Z
  51. Harima A, Shimizu H, Takagi H. Analgesic effect of L-arginine in patients with persistent pain. Eur Neuropsychopharmacol. 1991;1:529-533. https://doi.org/10.1016/0924-977X(91)90006-G
  52. Moore PK, Oluyomi AO, Babbedge RC, Wallace P, Hart SL. L-NG-nitro arginine methyl ester exhibits antinociceptive activity in the mouse. Br J Pharmacol. 1991;102:198-202. https://doi.org/10.1111/j.1476-5381.1991.tb12153.x
  53. Kawabata A, Fukuzumi Y, Fukushima Y, Takagi H. Antinociceptive effect of L-arginine on the carrageenin-induced hyperalgesia of the rat: possible involvement of central opioidergic systems. Eur J Pharmacol. 1992;218:153-158. https://doi.org/10.1016/0014-2999(92)90159-2
  54. Lauretti GR, Lima IC, Reis MP, Prado WA, Pereira NL. Oral ketamine and transdermal nitroglycerin as analgesic adjuvants to oral morphine therapy for cancer pain management. Anesthesiology. 1999;90:1528-1533. https://doi.org/10.1097/00000542-199906000-00005
  55. Durate ID, Lorenzetti BB, Ferreira SH. Peripheral analgesia and activation of the nitric oxide-cyclic GMP pathway. Eur J Pharmacol. 1990;186:289-293. https://doi.org/10.1016/0014-2999(90)90446-D

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