Capsaicin, acid and heat-evoked currents in rat trigeminal ganglion neurons: Relationship to functional VR1 receptors

Physiology and Behavior

Volumn 69, Issue 3, 2000, Pages 363-378

  Liu, L ^a   Simon, S A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Acid; Pain; Taste; Trigeminal; Vanilloid

Indexed keywords

ACID; AMILORIDE; CAPSAICIN; CAPSAZEPINE; CARRIER PROTEIN; ION CHANNEL; PROTON; RECEPTOR SUBTYPE; VANILLOID RECEPTOR;

ACIDITY; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; EVOKED SOMATOSENSORY RESPONSE; FEMALE; HEAT; MALE; NERVE CELL CULTURE; NERVE CONDUCTION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY STIMULATION; TASTE; TEMPERATURE SENSITIVITY; THERMAL STIMULATION; TRIGEMINUS GANGLION;

EID: 0034044221     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0031-9384(00)00209-2     Document Type: Article

References (79)

1. Akaike N., Krishtal O.A., Maruama T. Proton-induced sodium current in frog isolated dorsal root ganglion cells. J Neurophysiol. 63:1990;805-813.
2. Akaike N., Ueno S. Proton-induced currents in neuronal cells. Prog Neurobiol. 43:1994;73-83.
3. Akopian A.N., Sivilotti L., Wood J.N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature. 379:1996;257-262.
4. + channel with novel properties. J Biol Chem. 272:1997;28819-28822.
5. Baumann T.K., Burchiel K.J., Ingram S.L., Martensen M.E. Responses of adult dorsal root ganglion neurons in culture to capsaicin and low pH. Pain. 65:1998;31-38.
6. Belmonte C., Gallar J., Pozo M.A., Rebollo I. Excitation by irritant chemical substances of sensory afferent units in the cat's cornea. J Physiol (Lond). 427:1991;709-725.
7. Belmonte C., Garcia-Hirschfeld J., Gallar J. Neurobiology of ocular pain. Prog Retinal Eye Res. 16:1998;117-156.
8. Bevan S., Geppetti P. Protons. small stimulants of capsaicin sensitive sensory nerves Trends Neurosci. 17:1994;509-512.
9. Bevan S., Hothi S., Hughes G., James I.F., Rang H.P., Shah K., Walpole C.S.J., Yeats J.C. Capsazepine. a competitive antagonist of the sensory neurone excitant capsaicin Br J Pharmacol. 107:1992;544-552.
10. Bevan S., Rang H.P., Shah K. Capsazepine does not block the proton-induced activation of rat sensory neurons. Br J Physiol. 107:1992;235.
11. Bevan S., Winter J. Nerve growth factor differentially regulates the chemosensitivity of adult rat cultured sensory neurones. J Neurosci. 15:1995;4918-4926.
12. Bevan S., Yeats J. Protons activate a cation conductance in a subpopulation of rat dorsal root ganglion neurones. J Physiol (Lond). 433:1991;145-161.
13. Bryant B.P., Moore P.A. Factors affecting the sensitivity of the lingual trigeminal nerve to acids. Am J Physiol. 268(Pt 2):1995;R58-R65.
14. Carstens E., Kuenzler N., Handwerker H.O. Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to the oral or ocular mucosa. J Neurophysiol. 80:1998;465-492.
15. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., Julius D. A capsaicin-receptor analogue with a high threshold for noxious heat. Nature. 398:1999;436-441.
16. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor. a heat-activated ion channel in the pain pathway Nature. 389:1997;816-824.
17. Cesare P., McNaughton P. A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin. Proc Natl Acad Sci USA. 93:1996;15435-15439.
18. Cesare P., Moriondo A., Vellani V., McNaughton P.A. Ion channels gated by heat. Proc Natl Acad Sci USA. 96:1999;7658-7663.
19. Chen C-.C., England S., Akopian A.N., Wood J.N. A sensory neuron-specific, proton-gated ion channel. Proc Natl Acad Sci USA. 95:1998;10240-10245.
20. Chen X., Belmonte C., Rang H.P. Capsaicin and carbon dioxide act by distinct mechanisms on sensory nerve terminals in the cat cornea. Pain. 70:1997;23-29.
21. Davies N.W., Lux H.D., Morad M. Site and mechanism of activation of proton-induced sodium current in chick dorsal root ganglion neurons. J Physiol (Lond). 399:1988;195-225.
22. DeCoursey T.E. Four varieties of voltage gated-proton channels. Front Biosci. 3:1998;477-483.
23. Fox A.J., Urban L., Barnes P.J., Dray A. Effects of capsazepine against capsaicin- and proton-evoked excitation of single airway C-fibers and vagus nerve from the guinea pig. Neuroscience. 67:1995;741-752.
24. Franco-Cereceda A., Lundberg J.M. Capsazepine inhibits low pH- and lactic acid-evoked release of calcitonin gene-related peptide from sensory nerves in guinea-pig heart. Eur J Pharm. 221:1992;183-184.
25. Gilmore M.M., Green B.G. Sensory irritation and taste produced by NaCl and citric acid. effects of capsaicin desensitization Chem Senses. 18:1993;257-272.
26. 3 purinoreceptor and IB4 binding sites Eur J Neurosci. 11:1999;946-958.
27. Jung J., Hwang S.W., Kwak J., Lee S., Kang C., Kim W.B., Kim D., Oh U. Capsaicin binds to the intracellular domain of the capsaicin-activated ion channel. J Neurosci. 19:1999;529-538.
28. Kanzaki M., Zhang Y.Q., Mashima H., Li L., Shibata M., Kojima I. Translocation of a calcium-permeable cation channel by insulin-like growth factor-1. Nat Cell Biol. 1:1999;165-170.
29. Karrer T., Bartoshuck L. Capsaicin desensitization and recovery on the human tongue. Physiol Behav. 49:1991;757-764.
30. Katz D.B., Nicolelis M.A.L., Simon S.A. There is more to taste than meets the tongue. Am J Physiol. 278:2000;66-69.
31. Kirschstein, T, Busselberg D, Treede R-D. Coexpression of heat-evoked and capsaicin-evoked inward currents in acutely dissociated rat dorsal root ganglion neurons. Neurosci Lett 1997;33-6.
32. Kirschstein T., Greffrath W., Busselberg D., Treede R-D Inhibition of rapid heat responses in nociceptive primary sensory neurons by vanilloid receptor antagonists. J Neurophysiol. 2000()):in press.
33. Konietzny F., Hensel H. The effect of capsaicin on the response characteristic of human C-polymodal nociceptors. J Ther Biol. 8:1983;213-215.
34. Konnerth A., Lux H.D., Morad M. Proton-induced transformation of calcium channel in chick dorsal root ganglion cells. J Physiol. 386:1987;603-633.
35. Kress M., Reeh P.W. Chemical excitation and sensitization in nociceptors. Belmonte C., Cervero F. Neurobiology of Nociceptors. 1996;262-297 Oxford University Press, Oxford, UK.
36. Kress M., Zeilhofer M.U. Capsaicin, protons and heat. new excitement about nociceptors TIPS. 20:1999;112-118.
37. Krishtal O.A., Pidoplichko V.I. A receptor for protons in the nerve cell membrane. Neuroscience. 5:1980;2325-2327.
38. Lindhal O. Pain. a chemical explanation Acta Rheum Scand. 8:1962;161-169.
39. Lingueglia E., de Welle J., Bassilana F., Heurteaux C., Sakai H., Waldmann R. Lazdunski M. A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglion cells. J Biol Chem. 272:1998;29778-29783.
40. Liu L., Simon S.A. A rapid capsaicin-activated current in rat trigeminal ganglion neurons. Proc Natl Acad Sci USA. 91:1994;738-741.
41. Liu L., Simon S.A. Capsaicin-induced currents with distinct desensitization and Ca++ dependence in rat trigeminal ganglion cells. J Neurophysiol. 75:1996;1503-1514.
42. Liu L., Simon S.A. The responses of rat trigeminal ganglion neurons to capsaicin and two non pungent vanilloid receptor agonists. olvanil and glyceryl nonamide J Neurosci. 17:1997;4101-4111.
43. 2+ in the tachyphylaxis response to capsaicin, zingerone and olvanil in rat trigeminal ganglion neurons. Brain Res. 809:1998;246-252.
44. Lou Y., Lundberg J.M. Inhibition of low pH evoked activation of airway sensory nerves by capsazepine. Biochem Biophys Res Comm. 189:1992;537-544.
45. Lynn B. The heat sensitization of polymodal nociceptors in the rabbit and its independence of the local blood flow. J Physiol. 287:1979;493-507.
46. Martensen M.E., Arguelles J.H., Baumann T.K. Enhancement of rat trigeminal ganglion responses to piperine in a low-pH environment and block by capsazepine. Brain Res. 761:1997;71-76.
47. Martenson M.E., Ingram S.L., Baumann T.K. Potentiation of rabbit trigeminal responses to capsaicin in a low pH environment. Brain Res. 651:1994;143-147.
48. Micheal G.J., Priestly J.V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci. 19:1999;1844-1854.
49. Nagy I., Rang H.P. Similarities and differences between the responses of rat sensory neurons to noxious heat and capsaicin. J Neurosci. 19:1999;10647-10655.
50. Oh U., Hwang S.W., Kim D. Capsaicin activates a nonselective cation channel in cultured neonatal dorsal root ganglion neurons. J Neurosci. 16:1996;1659-1667.
51. Perkins M., Dray A. Novel pharmacological strategies for analgesia. Ann Rheum Dis. 55:1996;715-722.
52. Petersen M., LaMotte R.H. Effect of protons on the inward current evoked by capsaicin in isolated dorsal root ganglion cells. Pain. 54:1993;37-42.
53. Petersen P., LaMotte R.H., Klusch A., Kniffki K.D. Multiple capsaicin-evoked currents in isolated rat sensory neurons. Neuroscience. 75:1996;495-505.
54. Pidoplichko V.I. Ammonia and proton gated channel populations in trigeminal ganglion neurons. Gen Physiol Biophys. 11:1992;39-48.
55. Poulos D.A., Lende R.A. Responses of trigeminal ganglion neurons to thermal stimulation of oral facial regions. I. Steady state responses. J Neurophysiol. 33:1970;508-517.
56. Poulos D.A., Lende R.A. Responses of trigeminal ganglion neurons to thermal stimulation of oral facial regions. II. Temperature change responses. J Neurophysiol. 33:1970;518-526.
57. Prescott J, Allen S, Stephens L. Interactions between oral chemical irritation, taste and temperature. Chem Sens 1999;389-404.
58. Reeh P.W., Steen K.H. Tissue acidosis in nociception and pain. Prog Brain Res. 113:1996;143-151.
59. Reichling D.B., Levine J.D. Heat transduction in rat sensory ganglion neurons by calcium-dependent activation of a cation channel. Proc Natl Acad Sci USA. 94:1997;7006-7011.
60. Robinson P.P. The characteristics and regional distribution of afferent fibers in the chorda tympani of the cat. J Physiol (Lond). 406:1988;345-354.
61. Robinson P.P. The reinnervation of the tongue and salivary glands after lingual nerve injuries in cats. Brain Res. 483:1989;259-271.
62. Rozin P. Getting to like the burn of chili pepper. Chemical Senses.Volume 2. Irritation. 1996.
63. Schiffman S.S., Erickson R.P. The issue of primary tastes versus a taste continuum. Neurosci Biobehav Rev. 4:1980;109-117.
64. Simons C.T., Dressier J.M., Carstens M.I., O'Mahoney M., Carstens E. Neurobiological and psychophysical mechanisms underlying the oral sensation produced by carbonated water. J Neurosci. 15:1999;8134-8144.
65. Szallasi A., Biro T., Szabo T., Modarres S., Petersen M., Klusch A., Blumberg P., Krouse J.E., Sterner O. A non-pungent triprenyl phenol of fungal origin, scutigeral, stimulates rat dorsal root ganglion neurons via interaction at vanilloid receptors. Br J Pharmacol. 126:1999;1351-1358.
66. Szallasi A., Blumberg P.M. Vanilloid (capsaicin) receptors and mechanisms. Pharm Rev. 51:1999;159-211.
67. Szolcsanyi J., Anton F., Reeh P.W., Handwerker H.O. Selective excitation by capsaicin of mechano-heat sensitive nociceptors in rat skin. Brain Res. 446:1998;262-268.
68. 2+ channels. J Physiol (Lond). 493:1996;719-732.
69. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 21:1998;531-543.
70. Treede R-D Meyer R., Raja S.N., Campbell J.N. Evidence for two different heat transduction mechanisms in nociceptive primarily afferents innervating monkey skin. J Physiol. 483:1995;747-758.
71. Vyklicky L., Knotkova-Urbanakova H., Vitaskova Z., Vlachova V., Kress M., Reeh P.W. Inflammatory mediators at acidic pH activate capsaicin receptors in cultured sensory neurons from newborn rats. J Neurosci. 76:1998;670-676.
72. Vyklicky L., Vlachova V., Vitaskova Z., Dittert I., Kabat M., Orkland R.K. Temperature coefficient of membrane currents induced by noxious heat in sensory neurones in the rat. J Physiol. 517:1999;181-192.
73. + sensory channel specific for sensory neurons. J Biol Chem. 272:1997;20975-20978.
74. Waldmann R., Champigny G., Bassilana F., Heurteaux C., Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature. 386:1997;173-177.
75. Waldmann R., Champigny G., Lingueglia E., DeWeille J.R., Heurteaux C., Lazdunski M. H(+)-gated ion channels. Ann NY Acad Sci. 868:1999;67-76.
76. +-gated cation channels-neuronal acid sensors in the ENaC/Deg family of ion channels. Curr Opin Neurobiol. 8:1999;418-424.
77. Wood J.N., Docherty R.J. Chemical activators of sensory neurons. Ann Rev Physiol. 59:1997;457-482.
78. Woolf C.J., Costagin M. Transcriptional and posttranslational plasticity and the generation of inflammatory pain. Proc Natl Acad Sci USA. 96:1999;7723-7730.
79. 2+ permeability of sustained proton-induced cation current in adult dorsal root ganglion neurons. J Neurophysiol. 96:1996;2834-2840.