Molecular physiology of proton transduction in nociceptors

Current Opinion in Pharmacology

Volumn 1, Issue 1, 2001, Pages 45-51

  Reeh, Peter W ^a   Kress, Michaela ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Acid sensing; Capsaicin; Inflammation; Nociception; Peripheral; Protons; Sensory; Transduction

Indexed keywords

CAPSAICIN; DRUG RECEPTOR; ION CHANNEL; POTASSIUM CHANNEL; PROTON;

ANIMAL; CHANNEL GATING; CHEMISTRY; DRUG EFFECT; HUMAN; MOUSE; MOUSE MUTANT; NOCICEPTIVE RECEPTOR; PH; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CAPSAICIN; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; ION CHANNELS; MICE; MICE, KNOCKOUT; NOCICEPTORS; POTASSIUM CHANNELS; PROTONS; RECEPTORS, DRUG; SIGNAL TRANSDUCTION;

EID: 0035261565     PISSN: 14714892     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1471-4892(01)00014-5     Document Type: Review

References (59)

1. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature. 386:1997;173-177.
2. Chen C-C, England S, Akopian AN, Wood JN. A sensory neuron-specific, proton-gated ion channel. Proc Natl Acad Sci USA. 95:1998;10240-10245.
3. + channel. J Biol Chem. 271:1996;7879-7882.
4. Lingueglia E, deWeille JR, Bassilana F, Heurteaux C, Sakai K, Waldmann R, Lazdunski M. A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglion cells. J Biol Chem. 272:1997;29779-29783.
5. + channel specific for sensory neurons. J Biol Chem. 272:1997;20975-20978.
6. Gründer S, Geissler H-S, Bassler E-L, Ruppersberg JP. A new member of acid-sensing ion channels from pituitary gland. Neuroreport. 11:2000;1607-1611.
7. +-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol. 8:1998;418-424.
8. Coscoy S, deWeille JR, Lingueglia E, Lazdunski M. The pre-transmembrane 1 domain of acid-sensing ion channels participates in the ion pore. J Biol Chem. 274:1999;10129-10132.
9. + channel 1 by inducing a conformational change that exposes a residue associated with neurodegeneration. J Biol Chem. 273:1998;30204-30207.
10. Price MP, Lewin GR, McIlwrath SL, Cheung C, Xie J, Heppenstall PA, Stucky CL, Mannsfeldt AG, Brennan TJ, Drummond HA, et al. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature. 407:2000;1007-1011.
11. + channel with novel properties. J Biol Chem. 272:1997;28819-28822.
12. 3+. J Biol Chem. 275:2000;28519-28525.
13. +-channels. J Biol Chem. 275:2000;25116-25121. This paper presents for the first time a blocker psalmotoxin 1 (PcTX-1) from the American tarantula Psalmopoeus cambridgei that selectively inhibits ASIC1a. The purification and characterization of the toxin is reported together with functional studies on expressed ASIC1a and native currents of sensory neurons.
14. 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. 389:1997;816-824.
15. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann B, Basbaum AI, Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 21:1998;531-543.
16. Hayes P, Meadows HJ, Gunthorpe MJ, Harries MH, Duckworth DM, Cairns W, Harrison DC, Clarke CE, Ellington K, Prinjha RK, et al. Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain. 88:2000;205-215. The human VR1 gene encodes a protein with 92% homology to rat VR1 and identical functions. The cDNA of hVR1 allows for stable transfection of HEK293 cells.
17. Bevan S, Geppetti P. Protons: small stimulants of capsaicin-sensitive sensory nerves. Trends Neurosci. 17:1994;509-512.
18. Szallasi A, Blumberg PM. Vanilloid (capsaicin) receptors and mechanisms. Pharm Rev. 51:1999;159-211. An excellent and extensive actual review providing good overview but also going into the depth, for example, of structure-activity relations for vanilloids, mechanisms of desensitization, and so on.
19. 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.
20. Liu L, Simon SA. Capsaicin, acid and heat-evoked currents in rat trigeminal ganglion neurons: relationship to functional VR1 receptors. Physiol Behav. 69:2000;363-378.
21. Steen KH, Reeh PW, Anton F, Handwerker HO. Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci. 12:1992;86-95.
22. McLatchie LM, Bevan S: The effects of pH on the interaction between capsaicin and the vanilloid receptor in rat dorsal root ganglia neurons. Br J Pharmacol 2001, in press.
23. Jordt S-E, Tominaga M, Julius D. Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci USA. 97:2000;8134-8139. Point mutations of VR1 were introduced by using oligonucleotide-directed mutagenesis and the constructs were expressed in HEK293 cells and Xenopus oocytes. There were hypersensitive mutants exhibiting open channels at room temperature and neutral pH, which led to increased death rate of the mammalian cells but not of the oocytes kept at lower temperature (16°C).
24. Baumann TK, Martenson ME. Extracellular protons both increase the activity and reduce the conductance of capsaicin-gated channels. J Neurosci. 20:2000;1-5.
25. 2+ permeability of the sustained proton-induced cation current in adult rat dorsal root ganglion neurons. J Neurophysiol. 76:1996;2834-2840.
26. 2+ currents through capsaicin- and proton-activated ion channels in rat dorsal root ganglion neurones. J Physiol (Lond). 503:1997;67-78.
27. 2+ currents in isolated rat CA1 neurons. J Physiol (Lond). 493:1996;719-732.
28. Hille B. Ionic Channels of Excitable Membranes. 1992;Sinauer Association, Sunderland, MA.
29. Docherty RJ, Yeats JC, Bevan S, Boddeke HWGM. Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflügers Arch - Europ J Physiol. 431:1996;828-837.
30. Wegner H, Reeh PW, Brehm S, Kreysel HW, Steen KH. Diltiazem blocks the pH-induced excitation of rat nociceptors together with their mechanical and electrical excitability, in vitro. J Neurophysiol. 75:1996;1-10.
31. Issberner U, Reeh PW, Steen KH. Pain due to tissue acidosis: a mechanism for inflammatory and ischemic myalgia. Neurosci Lett. 208:1996;191-194.
32. Chen X, Belmonte C, Rang HP. Capsaicin and carbon dioxide act by distinct mechanisms on sensory nerve terminals in the cat cornea. Pain. 70:1997;23-29.
33. Reeh PW, Pethö G. Nociceptor excitation by thermal sensitization - a hypothesis. Sandkühler J, Bromm B, Gebhart GF. Nervous System Plasticity and Chronic Pain. 2000;39-50 Elsevier, Amsterdam.
34. Jung J, Hwang SW, Kwak J, Lee S-Y, Kang CJ, Kim WB, Kim D, Oh U. Capsaicin binds to the intracellular domain of a capsaicin-activated ion channel. J Neurosci. 19:1999;529-538.
35. Schumacher MA, Moff I, Sudanagunta SP, Levine JD. Molecular cloning of an N-terminal splice variant of the capsaicin receptor. J Biol Chem. 275:2000;2756-2762.
36. Kwak J, Wang MH, Hwang SW, Kim T-Y, Lee S-Y, Oh U. Intracellular ATP increases capsaicin-activated channel activity by interacting with nucleotide-binding domains. J Neurosci. 20:2000;8298-8304.
37. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, PetersenZeitz KR, Koltzenburg M, Basbaum AI, Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 288:2000;306-313. The functional consequences of VR1 deletion in mice were extensively studied using behavioural tests, primary afferent nerve and spinal dorsal horn recordings, patch-clamping of sensory neurons, inflammatory (CFA and mustard oil) and neuropathy (Seltzer) models. Hot plate and tail immersion tests showed significantly longer latencies than in wild-type mice only at temperatures of 50-58°C. Nonetheless, the dorsal root ganglion cells of mutant mice exhibited no heat-activated currents at temperatures below 55°C and hardly any sustained proton-induced currents.
38. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature. 405:2000;183-187. With VR1-null mice only a tendency towards longer latency than in wild-type animals was found in the hot-plate test at 52.5°C. Homozygous mutants showed no behavioural hyperalgesia to heating in the carrageenan-inflamed hindpaw, whereas heterozygous animals were as hypersensitive as wild-type ones.
39. Raja SN, Meyer RA, Ringkamp M, Campbell JN. Peripheral neural mechanisms of nociception. Wall PD, Melzack R. Textbook of Pain. 1999;11-57 Churchill Livingston, Edinburgh.
40. Kwak J, Jung JY, Hwang SW, Lee WT, Oh U. A capsaicin-receptor antagonist, capsazepine, reduces inflammation-induced hyperalgesic responses in the rat: evidence for an endogenous capsaicin-like substance. Neuroscience. 86:1998;619-626.
41. Habelt C, Kessler F, Distler C, Kress M, Reeh PW. Interactions of inflammatory mediators and low pH not influenced by capsazepine in rat cutaneous nociceptors. Neuroreport. 11:2000;973-976.
42. Steen KH, Steen AE, Kreysel H-W, Reeh PW. Inflammatory mediators potentiate pain induced by experimental tissue acidosis. Pain. 66:1996;163-170.
43. Vyklicky L, Knotkova-Urbancova H, Vitaskova Z, Vlachova V, Kress M, Reeh PW. Inflammatory mediators at acidic pH activate capsaicin receptors in cultured sensory neurons from newborn rats. J Neurophysiol. 79:1998;670-676.
44. Averbeck B, Izydorczyk I, Kress M. Inflammatory mediators release calcitonin gene-related peptide from dorsal root ganglion neurons of the rat. Neuroscience. 98:2000;135-140.
45. Steen AE, Reeh PW, Geisslinger G, Steen KH. Plasma levels after peroral and topical ibuprofen and effects upon low pH-induced cutaneous and muscle pain. Eur J Pain. 4:2000;195-209.
46. 2 enhancement of the capsaicin-elicited current in rat sensory neurons: whole-cell and single-channel studies. J Neurosci. 18:1998;6081-6092.
47. Vyklicky L, Vlachova V, Vitaskova Z, Dittert I, Kabat M, Orkand RK. Temperature coefficient of membrane currents induced by noxious heat in sensory neurones in the rat. J Physiol (Lond). 517:1999;181-192.
48. i in the ATP-induced heat sensitization process of rat nociceptive neurons. J Neurophysiol. 81:1999;2612-2619.
49. i mediate capsaicin- and proton-induced heat sensitization of rat primary nociceptive neurons. Eur J Neurosci. 11:1999;3143-3150.
50. North RA. Potassium-channel closure taken to TASK. Trends Neurosci. 23:2000;234-235.
51. + channel pharmacology. Soria B, Cena V. Ion Channel Pharmacology. 1998;169-185 Oxford University Press, Oxford.
52. Maingret F, Lauritzen I, Patel A, Heurteaux C, Reyes R, Lesage F, Lazdunski M, Honoré E. TREK-1 is a heat-activated background K+ channel. EMBO J. 19:2000;2483-2491.
53. γS suggest a G-protein-dependent pathway regulating TASK-3 channel activity.
54. Mezey E, Tóth ZE, Cortright DN, Arzubi MK, Krause JE, Elde R, Guo A, Blumberg PM, Szallasi A. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc Natl Acad Sci USA. 97:2000;3655-3660.
55. + channel MDEG1. J Biol Chem. 273:1998;15418-15422.
56. Adams CM, Price MP, Snyder PM, Welsh MJ. Tetraethylammonium block of the BNC1 channel. Biophys J. 76:1999;1377-1383.
57. Gründer S, Geissler H-S, Bassler E-L, Ruppersberg JP. Anew member of acid-sensing ion channels from pituitary gland. Neuroreport. 11:2000;1607-1611.
58. ε in sensitization of the neuronal response to painful heat. Neuron. 23:1999;617-624.
59. +] and is increased under amiloride. Eur J Neurosci. 11:1999;2783-2792.