Modulation of IA currents by capsaicin in rat trigeminal ganglion neurons

Journal of Neurophysiology

Volumn 89, Issue 3, 2003, Pages 1387-1401

  Liu, L ^a   Simon, S A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; CYCLIC AMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYTIDINE TRIPHOSPHATE; KT 5823; N (6 AMINOHEXYL) 1 NAPHTHALENESULFONAMIDE; PHORBOL DIBUTYRATE; VANILLOID RECEPTOR; ALKALOID; BENZYLAMINE DERIVATIVE; CALMODULIN; CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN-DEPENDENT PROTEIN KINASE II; CARBAZOLE DERIVATIVE; CARCINOGEN; CYCLIC GMP; DRUG RECEPTOR; ENZYME INHIBITOR; INDOLE DERIVATIVE; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; POTASSIUM; PROTEIN KINASE (CALCIUM,CALMODULIN); SULFONAMIDE; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; MEMBRANE CURRENT; MOUSE; NEUROMODULATION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TRIGEMINUS GANGLION; ANIMAL; CELL MEMBRANE POTENTIAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ELECTROSTIMULATION; GENETICS; METABOLISM; MOUSE MUTANT; NERVE CELL INHIBITION; NOCICEPTIVE RECEPTOR; PATCH CLAMP; PHYSIOLOGY; SENSORY NERVE CELL; SPRAGUE DAWLEY RAT;

ALKALOIDS; ANIMALS; BENZYLAMINES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALMODULIN; CAPSAICIN; CARBAZOLES; CARCINOGENS; CYCLIC AMP; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; CYTIDINE TRIPHOSPHATE; ELECTRIC STIMULATION; ENZYME INHIBITORS; INDOLES; MEMBRANE POTENTIALS; MICE; MICE, MUTANT STRAINS; NEURAL INHIBITION; NEURONS, AFFERENT; NOCICEPTORS; PATCH-CLAMP TECHNIQUES; PHORBOL 12,13-DIBUTYRATE; POTASSIUM; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DRUG; SULFONAMIDES; TRIGEMINAL GANGLION;

EID: 0037342245     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00210.2002     Document Type: Article

References (58)

1. An WF, Bowlby MR, Betty M, Cao J, Ling H-P, Mendoza G, Hinson JW, Mattsson KL, Strassle BW, Trimmer JS, and Rhodes KJ. Modulation of A-type potassium channels by a family of calcium sensors. Nature 403: 553-556, 2000.
2. Atkins PT and McCleskey EW. Characterization of potassium channels in adult rat sensory neurons and modulation by opiates and cyclic AMP. Neuroscience 56: 759-769, 1993.
3. + channels in rabbit schwann cells. Proc R Soc Lond B 255: 259-265, 1994.
4. Baumann TK, Simone DA, Shain CN, and LaMotte RH. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J Neurophysiol 66: 212-227, 1991.
5. Bielefeldt K. Differential effects of capsaicin on rat visceral sensory neurons. Neuroscience 101: 727-736, 2000.
6. Cardenas CG, Del Mar LP, and Scroggs RS. Variation in serotonergic inhibition of calcium currents in four types of rat sensory neurons differentiated by membranes properties. J Neurophysiol 74: 1870-1879, 1995.
7. Castle NA. Differential inhibition of potassium currents on rat ventricular myocytes by capsaicin. Cardiovascular Res 26: 1137-1144, 1992.
8. Caterina, MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
9. Caterina M, Rosen TA, Tominaga M, Brake AJ, and Julius D. A capsaicin-receptor analogue with a high threshold for noxious heat. Nature 398: 436-441, 1999.
10. Cholewinski A, Burgess GM, and Bevan S. The role of calcium in capsaicin-induced desensitization in rat cultured dorsal root ganglion neurons. Neuroscience 55: 1015-1023, 1993.
11. Cooper EC, Milroy A, Jan YN, Jan LY, and Lowenstein DH. Presynaptic localization of Kv1.4-containing A-type potassium channels near excitatory synapses in the hippocampus. J Neurosci 18: 965-974, 1998.
12. 2+ channels induced by nitric oxide in human neuroblastoma IMR32 cells. J Neurosci 22: 7485-92, 2002.
13. Dessirier JM, Simons CT, Sudo M, Sudo S, and Carstens E. Sensitization, desensitization and stimulus-induced recovery of trigeminal neuronal responses to oral capsaicin and nicotine. J Neurophysiol 84: 1851-1862, 2000.
14. Djouhri L and Lawson SN. Changes in somatic action potential shape in guinea pig nociceptive primary afferent neurones during inflammation. J Physiol 520.2: 565-576, 1999.
15. + channels. J Bioener Biomembr 28: 231-253, 1996.
16. + channels in the frog node of Ranvier. Brain Res 245: 372-375, 1982.
17. Fazekas A, Matheny JL, Roth GI, and Richardson DR. Effect of nitric oxide inhibition on capsaicin-elicited vasodilation in the rat oral circulation. Res Exp Med (Berl) 194: 357-375, 1994.
18. Gold MS, Dastmalchi S, and Levine JD. Co-expression of nociceptor properties in the dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 71: 265-275, 1996a.
19. + currents in adult rat sensory neurons. J Neurophysiol 75: 2629-2646, 1996b.
20. Green BG. Capsaicin sensitization and desensitization on the tongue produced by brief exposures to a low concentration. Neurosci Lett 107: 173-178, 1989.
21. + channels, Types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol Pharmacol 45: 1227-1234, 1994.
22. Harper AA and Lawson SN. Electrical properties of rat dorsal root ganglion neurones with different peripheral nerve conduction velocities. J Physiol 359: 47-54, 1985.
23. Harvey JS, Davis C, James IF, and Burgess GM. Activation of protein kinase C by the capsaicin analogue resiniferatoxin in sensory neurons. J Neurochem 65: 1309-1317.
24. Heyman I and Rang HP. Depolarizing responses to capsaicin in a subpopulation of rat dorsal root ganglion cells. Neurosci Lett 56: 69-75, 1985.
25. Hille, B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, 1993.
26. Ishikawa K, Tanaka M, Black JA, and Waxman SG. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22: 502-507, 2001.
27. Kagaya A, Kugaya A, Okamoto Y, Takebayashi M, Uchitomi Y, and Yamawaki S. Effect of citalopram on the desensitization of seratonin-2A receptor mediated calcium mobilization in rat glioma cells. Prog Neuropsychopharmacol Biol Psychiatry 20: 157-166, 1966.
28. + currents in melantrophs of rat pituitary. Br J Pharmacol 112: 616-624, 1994.
29. Koplas PA, Rosenberg RL, and Oxford GS. The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17: 3525-3537, 1997.
30. Kostyuk P, Veselovsky NS, Fedulova SA, and Tsyndrenko AY. Ionic currents in the somatic membrane of rat dorsal root ganglion neurons. III. Potassium currents. Neuroscience 6: 2439-2444, 1991.
31. Kuasno K and Ganier H. Modulation of voltage-activated calcium currents by pain-producing agents in a dorsal root ganglion neuronal line, F-11. J Neurosci Res 34: 158-169, 1993.
32. Kuenzi FM and Dale N. Effect of capsaicin and analogues on potassium and calcium currents and vanilloid receptors in Xenopus embryo spinal neurons. Br J Pharmacol 119: 81-90, 1996.
33. LaMotte RH, Shain CN, Simone DA, and Tsai RJ. Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J Neurophysiol 66: 190-211, 1991.
34. Liu L, Oortgiesen M, Li L, and Simon SA. Capsaicin inhibits activation of voltage-gated sodium currents in capsaicin-sensitive neurons. J Neurophysiol 85: 745-758, 2001.
35. 2+ dependence in rat trigeminal ganglion cells. J Neurophysiol 75: 1503-1514, 1996.
36. Liu L and Simon SA. Capsaicin, acid and heat evoked currents in rat trigeminal ganglion neurons: evidence for functional VRI receptors. Physiol Behav 69: 363-378, 2000.
37. McCleskey EW and Gold MS. Ion channels of nociception. Annu Rev Physiol 61: 835-856, 1999.
38. + channels in the pathophysiology of spinal cord injury. Modulator 14: 5-8, 2001.
39. Nicol GD, Vasko MR, and Evans AR. Prostaglandans suppress an outward potassium current in embryonic rat sensory neurons. J Neurophysiol 77: 167-176, 1997.
40. Pearce RJ and Duchen MR. Differential expression of membrane currents in dissociated mouse primary sensory neurons. Neuroscience 63: 1041-1056, 1994.
41. Parfenova H, Shibita M, Zuckerman S, Mirro R, and Leffer CW. Cyclic nucleotides and cerebrovascular tone in newborn pigs. Am J Physiol Heart Circ Physiol 265: H1972-H1982, 1993.
42. + currents: a role in shaping the photoreceptor potential. J Neurosci 18: 9153-9162, 2002.
43. Petersen M, Pierau Fr-K, and Weyrich M. The influence of capsaicin on membrane currents in dorsal root neurons of the guinea pig and chicken. Pfluegers 409: 403-410, 1987.
44. Rasband MN, Park EW, Vanderah TW, Lai, J, Porreca F, and Trimmer JS. Distinct potassium channels on pain-sensing neurons. Proc Natl Aacd Sci USA 98: 13373-13378, 2001.
45. Ricco MM, Kummer W, Biglari B, Myers AC, and Undem BC. Intrerganglionic segregation of distinct vagal afferent fiber phenotypes in guinea pig airways. J Physiol 496.2: 521-530, 1996.
46. + channels in neurons of the rat trigeminal ganglion. Mol Brain Res 74: 55-68, 2001.
47. Sheih C.-C, Coghlan M, Sullivan JP, and Gopalakrishan M. Potassium channels: molecular defects, diseases, and therapeutic, opportunities. Pharmacol Rev 52: 557-593, 2000.
48. Stansfeld CE, Marsh, SJ, Halliwell JV, and Brown DA. Aminopyridine and dendrotoxin induce repetitive firing in rat visceral sensory neurons by blocking a slowly inactivating outward current. Neurosci Lett 64: 299-304, 1986.
49. Sterner O and Szallasi A. Novel natural vanilloid receptor agonists: new therapeutic targets for drug development. Trends Pharmacol Sci 20: 459-465, 1999.
50. Szolcsanyi J. A pharmacological approach to the elucidation of the role of different nerve fibers and receptor endings in mediation of pain. J Physiol (Paris) 73: 251-259, 1977.
51. Waddell PJ and Lawson SN. The C-fiber conduction block caused by capsaicin on rat vagus nerve in vitro. Pain 39: 237-242, 1989.
52. Wickman K and Clapham DE. Ion channel regulation by G proteins. Physiol Rev 75: 865-885, 1995.
53. Williams JT and Zieglganberger W. The acute effects of capsaicin on rat primary afferents and spinal neurons. Brain Res 253: 125-131, 1982.
54. Wood JN, Coote PR, Minhas A, McNiel M, Mullany I, and Burgess G. Capsaicin-induced ion fluxes increase cGMP but not cAMP levels in rat sensory neurons in culture. J. Neurosci 53: 1203-1211, 1989.
55. Woolf CJ and Costagin M. Transcriptional and posttranslational plasticity and the generation of inflammatory pain. Proc Natl Acad Sci USA 96: 7723-7730, 1999.
56. + currents in dorsal root ganglion neurones innervating the rat urinary bladder. J Physiol 494: 1-16, 1996.
57. Yost CS. Potassium channels. Anesthesiology 90: 1186-1203, 1999.
58. Zhang Y-H, Kenyon JL, and Nicol GD. Phobol ester-induced inhibition of potassium currents in rat sensory neurons requires voltage-dependent entry of calcium. J Neurophysiol 85: 362-373, 2001.