Activation and recovery of the PGE2-mediated sensitization of the capsaicin response in rat sensory neurons

Journal of Neurophysiology

Volumn 78, Issue 6, 1997, Pages 3154-3164

  Lopshire, J C ^a   Nicol, G D ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CAPSAICIN; GUANOSINE PHOSPHATE; KT 5823; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PROSTAGLANDIN E2; CALCIUM; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; ENZYME INHIBITOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN METABOLISM; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; PATCH CLAMP; PHYSIOLOGY; STIMULATION;

ANIMALS; CALCIUM; CAPSAICIN; CELLS, CULTURED; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DINOPROSTONE; ENZYME INHIBITORS; NEURONS, AFFERENT; NITRIC OXIDE; PATCH-CLAMP TECHNIQUES; RATS; STIMULATION, CHEMICAL;

EID: 0031283176     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1997.78.6.3154     Document Type: Article

References (53)

1. ADLER, E. M., AUGUSTINE, G. J., DUFFY, S. N., AND CHARLTON, M. P. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11: 1496-1507, 1991.
2. BACCAGLINI, P. I. AND HOGAN, P. G. Some rat sensory neurons in culture express characteristics of differentiated pain sensory cells. Proc. Natl. Acad. Sci. USA 80: 594-598, 1983.
3. BEVAN, S. AND FORBES, C. A. Membrane effects of capsaicin on rat dorsal root ganglion neurones in cell culture (Abstract). J. Physiol. (Lond.) 398: 28P, 1988.
4. BEVAN, S. AND SZOLCSANYI, J. Sensory neuron-specific actions of capsaicin: mechanisms and applications. Trends Pharmacol. Sci. 11: 330-333, 1990.
5. BEVAN, S. J., JAMES, I. F., RANG, H. P., WINTER, J., AND WOOD, J. N. The mechanism of action of capsaicin-a sensory neurotoxin. In: Neurotoxins and Their Pharmacological Implications, edited by P. Jenner. New York: Raven, 1987, p. 261-277.
6. BREDT, D. S. AND SYNDER, S. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl. Acad. Sci. USA 86: 9030-9033, 1989.
7. CALDWELL, P. C. Calcium chelation and buffers. In: Calcium and Cell Function, edited by A. W. Cuthbert. New York: St. Martin's Press, 1970. p. 11-16.
8. 2+ channel currents through protein phosphorylation in rat pinealocytes. J. Neurosci. 15: 3104-3109, 1995.
9. CHOLEWINSKI, A., BURGESS, G. M., AND BEVAN, S. The role of calcium in capsaicin-induced desensitization in rat cultured dorsal root ganglion neurons. Neuroscience 55: 1015-1023, 1993.
10. 2-induced potentiation of bradykinin excitation in rat sensory neurons. Neuroscience 66: 459-466, 1995.
11. DAVIS, M. E., AKERA, T., BRODY, T. M., AND WATSON, L. Opiate receptor: Cooperativity of binding observed in brain slices. Proc. Natl Acad. Sci. USA 74: 5764-5766, 1977.
12. DETRE, J. A., NAIRNS, A. C., ASWAD, D. W., AND GREENGARD, P. Localization in mammalian brain of G-substrate, a specific substrate for guanosine 3′,5′-cyclic monophosphate-dependent protein kinase, J. Neurosci. 4: 2843-2849, 1984.
13. DOCHERTY, R. J., YEATS, J. C., BEVAN, S., AND BODDEKE, H.W.G.M. Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflügers Arch. 431: 828-837, 1996.
14. 2+ current through a mechanism independent of cGMP-dependent protein kinase. Neuron 1: 693-699, 1988.
15. DUARTE, I.D.G., DOS SANTOS, I. R., LORENZETTI, B. B., AND FERREIRA, S. H. Analgesia by direct antagonism of nociceptor sensitization involves the arginine-nitric oxide-cGMP pathway. Eur. J. Pharmacol. 217: 225-227, 1992.
16. DUARTE, I.D.G., LORENZETTI, B. B., AND FERREIRA, S. H. Peripheral analgesia and activation of the nitric oxide-cyclic GMP pathway. Eur. J. Pharmacol. 186: 289-293, 1990.
17. DYMSHITZ, J. AND VASKO, M. R. Nitric oxide and cyclic guanosine 3′,5′-monophosphate do not alter neuropeptide release from rat sensory neurons grown in culture. Neuroscience 62: 1279-1286, 1994.
18. FOREMAN, J. C. Peptides and neurogenic inflammation. Br. Med. Bull. 43: 386-400, 1987.
19. GARTHWAITE, J., CHARLES, S. L., AND CHESS-WILLIAMS, R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests a role as intercellular messenger in the brain. Nature 336: 385-388, 1988.
20. GOLDBERG, N. D., HADDOX, M. K., NICOL, S. E., GLASS, D. B., SANFORD, C. H., KUEHL, F. A., JR., AND ESTENSEN, R. Biologic regulation through opposing influences of cyclic GMP and cyclic AMP: the yin yang hypothesis. Adv. Cyclic Nucleotide Res. 5: 307-330, 1975.
21. HAMILL, O. P., MARTY, A., NEHER, E., SAKMANN, B., AND SIGWORTH, F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391: 85-100, 1981.
22. HANDWERKER, H. O. AND KOBAL, G. Psychophysiology of experimentally induced pain. Physiol. Rev. 73: 639-671, 1993.
23. HANDWERKER, H. O. AND REEH, P. W. Pain and inflammation. In: Proceedings of the VIth World Congress on Pain, edited by M. R. Bond, J. E. Charlton, and C. J. Woolf. Amsterdam: Elsevier, 1991, p. 59-70.
24. HEYMAN, I. AND RANG, H. P. Depolarizing responses to capsaicin in a subpopulation of rat dorsal root ganglion cells. Neurosci. Lett. 56: 69-75, 1985.
25. HIGGS, G. A., MONCADA, S., AND VANE, J. R. Eicosanoids in inflammation. Ann. Clin. Res. 16: 287-299, 1984.
26. HINGTGEN, C. M. AND VASKO, M. R. Prostacyclin enhances the evoked-release of substance P and calcitonin gene-related peptide from rat sensory neurons. Brain Res. 655: 51-60, 1994.
27. HINGTGEN, C. M., WAITE, K. J., AND VASKO, M. R. Prostaglandins facilitate peptide release from rat sensory neurons by activating the adenosine 3′,5′-cyclic monophosphate transduction cascade. J. Neurosci. 15: 5411-5419, 1995.
28. HOLZER, P. Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol. Rev. 43: 143-201, 1991.
29. HORN, R. AND MARTY, A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J. Gen. Physiol. 92: 145-159, 1988.
30. 2+-dependent exocytosis in the somata of dorsal root ganglion neurons. Neuron 17: 135-145, 1996.
31. ITO, M. AND KARACHOT, L. Messengers mediating long-term desensitization in cerebellar Purkinje cells. Neuroreport 1: 129-132, 1990.
32. KASE, H., IWAHASHI, K., NAKANISHI, S., MATSUDA, Y., YAMADA, K., TAKAHASHI, M., MURAKATA, C., SATO, A., AND KANEKO, M. K-252 compounds: novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem. Biophys. Res. Commun. 142: 436-440, 1987.
33. KNOWLES, R. G., PALACOIS, M., PALMER, R.M.J., AND MONCADA, S. Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Natl. Acad. Sci. USA 86: 5159-5162, 1989.
34. LIGHT, D. B., CORBIN, J. D., AND STANTON, B. A. Dual ion-channel regulation by cyclic GMP and cyclic GMP-dependent protein kinase. Nature 344: 336-339, 1990.
35. 2+ dependence in rat trigeminal ganglion cells. J. Neurophysiol. 75: 1503-1514, 1996.
36. MARSH, S. J., STANSFELD, C. E., BROWN, D. A., DAVEY, R., AND MCCARTHY, D. The mechanism of action of capsaicin on sensory C-type neurons and their axons in vitro. Neuroscience 23: 275-289, 1987.
37. MCGEHEE, D. S., GOY, M. F., AND OXFORD, G. S. Involvement of the nitric oxide-cyclic GMP pathway in the desensitization of bradykinin responses of cultured rat sensory neurons. Neuron 9: 315-324, 1992.
38. 2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc. Natl. Acad Sci. USA 88: 1197-1201, 1991.
39. MURTHY, K. S. AND MAKHLOUF, G. M. Interaction of cA-kinase and cG-kinase in mediating relaxation of dispersed smooth muscle cells. Am. J. Physiol. 268 (Cell Physiol. 37): C171-C180, 1995.
40. 2 enhances bradykinin activation of embryonic rat sensory neurones. J. Physiol. (Lond.) 480: 485-492, 1994.
41. OH, U., HWANG, S. W., AND KIM, D. Capsaicin activates a nonselective cation channel in cultured neonatal rat dorsal root ganglion neurons. J. Neurosci. 16: 1659-1667, 1996.
42. QIAN, Y., CHAO, D. S., SANTILLANO, D. R., CORNWELL, T. L., NAIRN, A. C., GREENGARD, P., LINCOLN, T. M., AND BREDT, D. S. cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons. J. Neurosci. 16: 3130-3138, 1996.
43. RAE, J., COOPER, K., GATES, P., AND WATSKY, M. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods 37: 15-26, 1991.
44. SALMON, J. A. AND HIGGS, G. A. Prostaglandins and leukotrienes as inflammatory mediators. Br. Med. Bull. 43: 285-296, 1987.
45. STERN, M. D. Buffering of calcium in the vicinity of a channel pore. Cell Calcium 13: 183-192, 1992.
46. SZALLASI, A., LEWIN, N. A., AND BLUMBERG, P. M. Vanilloid (capsaicin) receptor in the rat: positive cooperativity of resiniferatoxin binding and its modulation by reduction and oxidation. J. Pharmacol. Exp. Ther. 266: 678-683, 1993.
47. 2 enhances bradykinin-stimulated release of neuropeptides from rat sensory neurons in culture. J. Neurosci. 14: 4987-4997, 1994.
48. WAHLER, G. M. AND DOLLINGER, S. J. Nitric oxide donor SIN-1 inhibits mammalian cardiac calcium current through cGMP-dependent protein kinase. Am. J. Physiol. 268 (Cell Physiol. 37): C45-C54, 1995.
49. WHITE, R. E., LEE, A. B., SHCHERBATKO, A. D., LINCOLN, T. M., SCHONBRUNN, A., AND ARMSTRONG, D. L. Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature 361: 263-266, 1993.
50. WOOD, J. N., COOTE, P. R., MINHAS, A., MULLANEY, I., MCNEILL, M., AND BURGESS, G. M. Capsaicin-induced ion fluxes increase cyclic GMP but not cyclic AMP levels in rat sensory neurones in culture. J. Neurochem. 53: 1203-1211, 1989.
51. WOOD, J. N., WINTER, J., JAMES, I. F., RANG, H. P., YEATS, J., AND BEVAN, S. Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J. Neurosci. 8: 3208-3220, 1988.
52. YEATS, J. C., DOCHERTY, R. J., AND BEVAN, S. Calcium-dependent and independent desensitization of capsaicin-evoked responses in voltage-clamped adult rat dorsal root ganglion (DRG) neurones in culture (Ab-stract). J. Physiol. (Lond.) 446: 390P, 1991.
53. + currents by cGMP-dependent protein kinase in tracheal smooth muscle and Chinese hamster ovary cells. J. Biol. Chem. 271: 19760-19767, 1996.