Inflammatory mediators release calcitonin gene-related peptide from dorsal root ganglion neurons of the rat

Neuroscience

Volumn 98, Issue 1, 2000, Pages 135-140

  Averbeck, B ^a   Izydorczyk, I ^b   Kress, M ^b  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Acidosis; Bradykinin; Capsazepine; Inflammation; Neuropeptides; Serotonin

Indexed keywords

BRADYKININ; BRADYKININ DERIVATIVE; BRADYKININ RECEPTOR; CALCITONIN GENE RELATED PEPTIDE; CALCIUM; CAPSAICIN RECEPTOR ANTAGONIST; CAPSAZEPINE; ICATIBANT; PROSTAGLANDIN E2; RECEPTOR SUBTYPE; SEROTONIN; UNCLASSIFIED DRUG;

ACIDITY; ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG POTENTIATION; ENZYME IMMUNOASSAY; FEMALE; INFLAMMATION; MALE; MEDIATOR; NERVE CELL CULTURE; NEUROTRANSMITTER RELEASE; NONHUMAN; PH; PRIORITY JOURNAL; RAT; SPINAL GANGLION;

ACIDS; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM; CAPSAICIN; CELLS, CULTURED; DINOPROSTONE; FEMALE; FREE RADICAL SCAVENGERS; GANGLIA, SPINAL; HYDROGEN-ION CONCENTRATION; INFLAMMATION MEDIATORS; KALLIDIN; MALE; NEURONS; RATS; RATS, WISTAR; RECEPTORS, DRUG; SEROTONIN; STIMULATION, CHEMICAL;

EID: 0034091199     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00095-6     Document Type: Article

References (58)

1. Baccaglini P.J., Hogan P.G. Some rat sensory neurons in culture express characteristics of differential pain sensory cells. Proc. natn. Acad. Sci. U.S.A. 80:1983;594-598.
2. Bevan S., Yeats J. Protons activate a cation conductance in a subpopulation of rat dorsal root ganglion neurons. J. Physiol., Lond. 433:1991;145-161.
3. Bevan S., Hothi S., Hughes G., James I.F., Rang H.P., Shah K., Walpole C.S., Yeats J.C. Capsazepine: a competitive antagonist of the sensory neurone excitant capsaicin. Br. J. Pharmac. 107:1992;544-552.
4. Billiard J., Koh D.-S., Babcock D.F., Hille B. Protein kinase C as a signal for exocytosis. Proc. natn. Acad. Sci. U.S.A. 94:1997;12,192-12,197.
5. Brimijoin S., Lundberg J.M., Brodin E., Hokfelt T., Nilsson G. Axonal transport of substance P in the vagus and sciatic nerves of the guinea pig. Surg. Neurol. 191:1980;443-457.
6. Brown D.A., Higashida H. Inositol 1,4,5-trisphosphate and diacylglycerol mimic bradykinin effects on mouse neuroblastoma×rat glioma hybrid cells. J. Physiol., Lond. 397:1988;185-207.
7. Burgress G.M., Mullaney I., McNeil M., Dunn P.M., Rang H.P. Second messenger involved in the mechanism of action of bradykinin in sensory neurons in culture. J. Neurosci. 9:1989;3314-3325.
8. Catarina 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.
9. Cui M., Nicol G.D. Cyclic AMP mediates the prostaglandin E2-induced potentiation of bradykinin excitation in rat sensory neurons. Neuroscience. 66:1995;459-466.
10. Davis C.L., Naeem S., Phagoo S.B., Campbell E.A., Urban L., Burgess G.M. B1 bradykinin receptors and sensory neurones. Br. J. Pharmac. 118:1996;1469-1476.
11. Derkach V., Surprenant A.M., North R.A. 5-HT3 receptors are membrane ion channels. Nature. 339:1989;706-709.
12. Docherty R.J., Yeats J.C., Piper A.S. Capsazepine block of voltage-activated calcium channels in adult rat dorsal root ganglion neurones in culture. Br. J. Pharmac. 121:1997;1461-1467.
13. Dray A., Patel I.A., Perkins M.N., Rueff A. Bradykinin-induced activation of nociceptors: receptor and mechanistic studies on the neonatal rat spinal cord-tail preparation in vitro. Br. J. Pharmac. 107:1992;1129-1134.
14. Fitzgerald E.M., Okuse K., Wood J.N., Dolphin A.C., Moss S.J. cAMP-dependent phosphorylation of the tetrodotoxin-resistant voltage-dependent sodium channel SNS. J. Physiol., Lond. 516:1999;433-446.
15. Fox A.J., Barnes P.J., Urban L., Dray A. An in vitro study of the properties of single vagal afferents innervating guinea-pig airways. J. Physiol., Lond. 469:1993;21-35.
16. Franco Cereceda A., Kallner G., Lundberg J.M. Capsazepine-sensitive release of calcitonin gene-related peptide from C-fibre afferents in the guinea-pig heart by low pH and lactic acid. Eur. J. Pharmac. 238:1993;311-316.
17. Franco Cereceda A., Saria A., Lundberg J.M. Differential release of calcitonin gene-related peptide and neuropeptide Y from the isolated heart by capsaicin, ischaemia, nicotine, bradykinin and ouabain. Acta physiol. scand. 135:1989;173-187.
18. Geppetti P., Del Bianco E., Patacchini R., Santicioli P., Maggi C.A., Tramontana M. Low pH-induced release of calcitonin gene-related peptide from capsaicin-sensitive sensory nerves: mechanism of action and biological response. Neuroscience. 41:1991;295-301.
19. Geppetti P., Del Bianco E., Tramontana M., Vigano T., Folco G.C., Maggi C.A., Manzini S, Fanciullacci M. Arachidonic acid and bradykinin share a common pathway to release neuropeptide from capsaicin-sensitive sensory nerve fibers of the guinea pig heart. J. Pharmac. exp. Ther. 259:1991;759-765.
20. Gold M.S., Levine J.D., Correa A.M. Modulation of TTX-R INa by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro. J. Neurosci. 18:1998;10,345-10,355.
21. Griesbacher T., Lembeck F. Effect of bradykinin antagonists on bradykinin-induced plasma extravasation, venoconstriction, prostaglandin E2 release, nociceptor stimulation and contraction of the iris sphincter muscle in the rabbit. Br. J. Pharmac. 92:1987;333-340.
22. Haley J.E., Dickenson A.H., Schachter M. Electrophysiological evidence for a role of bradykinin in chemical nociception in the rat. Neurosci. Lett. 97:1989;198-202.
23. Handwerker H. O., Reeh P. W. and Steen K. H. (1990) Effects of 5HT on nociceptors. In Serotonin and Pain (ed. Besson J. M.). Elsevier Science, Amsterdam.
24. Hingtgen C.M., Vasko M.R. Prostacyclin enhances the evoked-release of substance P and calcitonin gene-related peptide from rat sensory neurons. Brain Res. 655:1994;51-60.
25. Hingtgen C.M., Waite K.J., Vasko M.R. Prostaglandins facilitate peptide release from rat sensory neurons by activating the adenosine 3′,5′-cyclic monophosphate transduction cascade. J. Neurosci. 15:1995;5411-5419.
26. Hua X.Y., Yaksh T.L. Pharmacology of the effects of bradykinin, serotonin, and histamine on the release of calcitonin gene-related peptide from C-fiber terminals in the rat trachea. J. Neurosci. 13:1993;1947-1953.
27. 2+-dependent exocytosis in the somata of dorsal root ganglion neurons. Neuron. 17:1996;135-145.
28. Keen P., Harmar A.J., Spears F., Winter E. Biosynthesis axonal transport and turnover of neuronal substance P. Ciba. Found. Symp. 1982;145-164.
29. Kress M., Guthmann C., Averbeck B., Reeh P.W. Calcitonin gene-related peptide, substance P and prostaglandin E2 release from rat skin induced by antidromic nerve stimulation in vitro. Neuroscience. 89:1999;303-310.
30. Kress M. and Reeh P. W. (1996) Chemical excitation and sensitization in nociceptors. In Neurobiology of Nociceptors (eds Belmonte C. and Cervero F.). Oxford University Press, Oxford.
31. Kress M., Reeh P.W., Vyklicky L. An interaction of inflammatory mediators and protons in small diameter dorsal root ganglion neurons of the rat. Neurosci. Lett. 224:1997;37-40.
32. Lang E., Novak A., Reeh P.W., Handwerker H.O. Chemosensitivity of fine afferents from rat skin in vitro. J. Neurophysiol. 63:1990;887-901.
33. Lopshire J.C., Nicol G.D. The cAMP transduction cascade mediates the prostaglandin E2 enhancement of the capsaicin-elicited current in rat sensory neurons: whole-cell and single-channel studies. J. Neurosci. 18:1998;6081-6092.
34. Manzini S., Perretti F., De Benedetti L., Pradelles P., Maggi C.A., Geppetti P. A comparison of bradykinin- and capsaicin-induced myocardial and coronary effects in isolated perfused heart of guinea-pig: involvement of substance P and calcitonin gene-related peptide release. Br. J. Pharmac. 97:1989;303-312.
35. Mizumura K., Sato J., Kumazawa T. Effects of prostaglandins and other putative chemical intermediaries on the activity of canine testicular polymodal receptors studied in vitro. Pflügers Arch. 408:1987;565-572.
36. Mizumura K., Minagawa M., Tsujii Y., Kumazawa T. The effects of bradykinin agonists and antagonists on visceral polymodal receptor activities. Pain. 40:1990;221-227.
37. Nakanishi S. Substance P precursor and kininogen: their structures, gene organizations, and regulation. Physiol. Rev. 67:1987;1117-1142.
38. Nicol G.D., Cui M. Enhancement by prostaglandin E2 of bradykinin activation of embryonic rat sensory neurones. J. Physiol., Lond. 480:1994;485-492.
39. Oh U., Hwang S.W., Kim D. Capsaicin activates a nonselective cation channel in cultured neonatal rat dorsal root ganglion neurons. J. Neurosci. 16:1996;1659-1667.
40. Perkins M.N., Campbell E., Dray A. Antinociceptive activity of the bradykinin B1 and B2 receptor antagonists, des-Arg9, [Leu8]-BK and HOE140, in two models of persistent hyperalgesia in the rat. Pain. 53:1993;191-197.
41. Reeh P.W., Steen K.H. Tissue acidosis in nociception and pain. Prog. Brain Res. 113:1996;143-151.
42. Richardson B.P., Engel G. The pharmacology and function of 5-HT3 receptors. Trends Neurosci. September:1986;424-428.
43. Rosenfeld M.G., Mermod J.J., Amara S.G., Swanson L.W., Sawchenko P.E., Rivier J., Vale W.W., Evans R.M. Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Physiol. Rev. 304:1983;129-135.
44. Rueff A., Dray A. Pharmacological characterization of the effects of 5-hydroxytryptamine and different prostaglandins on peripheral sensory neurons in vitro. Agents Actions. 38:1993;C13-C15.
45. Santicioli P., Del Bianco E., Geppetti P., Maggi C.A. Release of calcitonin gene-related peptide-like (CGRP-LI) immunoreactivity from rat isolated soleus muscle by low pH, capsaicin and potassium. Neurosci. Lett. 143:1992;19-22.
46. Santicioli P., Del-Bianco E., Figini M., Bevan S., Maggi C.A. Effect of capsazepine on the release of calcitonin gene-related peptide-like immunoreactivity (CGRP-LI) induced by low pH, capsaicin and potassium in rat soleus muscle. Br. J. Pharmac. 110:1993;609-612.
47. Segond von Banchet G., Petersen M., Heppelmann B. Bradykinin receptors in cultured rat dorsal root ganglion cells: influence of length of time in culture. Neuroscience. 75:1996;1211-1218.
48. Steen K.H., Steen A.E., Kreysel H.W., Reeh P.W. Inflammatory mediators potentiate pain induced by experimental tissue acidosis. Pain. 66:1996;163-170.
49. Steen K.H., Steen A.E., Reeh P.W. A dominant role of acid pH in inflammatory excitation and sensitization of nociceptors in rat skin, in vitro. J. Neurosci. 15:1995;3982-3989.
50. Steranka L.R., Farmer S.G., Burch R.M. Antagonists of B2 bradykinin receptors. Fedn Am. Soc. exp. Biol. J. 3:1989;2019-2025.
51. Steranka L.R., Manning D.C., DeHaas C.J., Ferkany J.W., Borosky S.A., Connor J.R., Vavrek R.J., Stewart J.M., Snyder S.H. Bradykinin as a pain mediator: receptors are localized to sensory neurons, and antagonists have analgesic actions. Proc. natn. Acad. Sci. U.S.A. 85:1988;3245-3249.
52. 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.
53. Vasko M.R., Campbell W.B., Waite K.J. Prostaglandin E2 enhances bradykinin-stimulated release of neuropeptides from rat sensory neurons in culture. J. Neurosci. 14:1994;4987-4997.
54. Vasko M.R., Zirkelbach S.L., Waite K.J. Prostaglandins stimulate the release of substance P from rat spinal cord slices. Prog. Pharmac. clin. Pharmac. 10:1993;69-89.
55. Vyklicky L., Knotkova Urbancova H., Vitaskova Z., Vlachova V., Kress M., Reeh P.W. Inflammatory mediators at acid pH activate capsaicin receptors in cultured sensory neurons from newborn rats. J. Neurophysiol. 79:1998;670-676.
56. Weinreich D., Wonderlin W.F. Inhibition of calcium-dependent spike after-hyperpolarization increases excitability of rabbit visceral sensory neurones. J. Physiol., Lond. 394:1987;415-427.
57. Wood J.N., Winter J., James I.F., Rang H.P., Yeats J., Bevan S. Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J. Neurosci. 8:1988;3208-3220.
58. 2+ currents through capsaicin- and proton-activated ion channels in rat dorsal root ganglion neurones. J. Physiol., Lond. 503:1997;67-78.