Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals

Journal of Neuroscience

Volumn 26, Issue 48, 2006, Pages 12512-12525

  Madrid, Rodolfo ^a   Donovan Rodríguez, Tansy ^a   Meseguer, Victor ^a   Acosta, Mari Carmen ^a   Belmonte, Carlos ^a   Viana, Félix ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

BCTC; Cornea; Nociceptor; SKF96365; Somatosensory; Trigeminal ganglion

Indexed keywords

[1 (2 (4 METHOXYPHENYL) 2 (3 (4 METHOXYPHENYL)PROPOXY)ETHYL 1H IMIDAZOLE HYDROCHLORIDE; [N (4 TERT BUTYLPHENYL) 4 (3 CHLOROPYRIDIN 2 YL)PIPERAZINE 1 CARBOXAMIDE]; AMIDE; IMIDAZOLE DERIVATIVE; MENTHOL; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL MELASTATIN 8; VANILLOID RECEPTOR 1;

ARTICLE; COLD EXPOSURE; CONTROLLED STUDY; CORNEA; EVOKED SOMATOSENSORY RESPONSE; GUINEA PIG; HUMAN; HUMAN CELL; NERVE CELL; NERVE ENDING; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TEMPERATURE SENSITIVITY; THERMORECEPTOR;

ANIMALS; CELL LINE; COLD; GUINEA PIGS; HUMANS; MICE; NEURONS, AFFERENT; PERIPHERAL NERVES; PRESYNAPTIC TERMINALS; PYRAZINES; PYRIDINES; RATS; TEMPERATURE SENSE; THERMORECEPTORS; TRIGEMINAL GANGLION; TRPM CATION CHANNELS;

EID: 33845261834     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3752-06.2006     Document Type: Article

References (64)

1. Acosta MC, Belmonte C, Gallar J (2001) Sensory experiences in humans and single-unit activity in cats evoked by polymodal stimulation of the cornea. J Physiol (Lond) 534:511-525.
2. Almasi R, Petho G, Bolcskei K, Szolcsanyi J (2003) Effect of resiniferatoxin on the noxious heat threshold temperature in the rat: a novel heat allodynia model sensitive to analgesics. Br J Pharmacol 139:49-58.
3. Babes A, Zorzon D, Reid G (2004) Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur J Neurosci 20:2276-2282.
4. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-857.
5. Behrendt HJ, Germann T, Gillen C, Hatt H, Jostock R (2004) Characterization of the mouse cold-menthol receptor TRPM8 and vanilloid receptor type-1 VR1 using a fluorometric imaging plate reader (FLIPR) assay. Br J Pharmacol 141:737-745.
6. Brauchi S, Orio P, Latorre R (2004) Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. Proc Natl Acad Sci USA 101:15494-15499.
7. Braun HA, Bade H, Hensel H (1980) Static and dynamic discharge patterns of bursting cold fibers related to hypothetical receptor mechanisms. Pflügers Arch 386:1-9.
8. Brock J, Pianova S, Belmonte C (2001) Differences between nerve terminal impulses of polymodal nociceptors and cold sensory receptors of the guinea-pig cornea. J Physiol (Lond) 533:493-501.
9. Brock JA, McLachlan EM, Belmonte C (1998) Tetrodotoxin-resistant impulses in single nociceptor nerve terminals in guinea-pig cornea. J Physiol 512:211-217.
10. Cabanes C, Viana F, Belmonte C (2003) Differential thermosensitivity of sensory neurons in the guinea pig trigeminal ganglion. J Neurophysiol 90:2219-2231.
11. Carr RW, Pianova S, Fernandez J, Fallon JB, Belmonte C, Brock JA (2003) Effects of heating and cooling on nerve terminal impulses recorded from cold-sensitive receptors in the guinea-pig cornea. J Gen Physiol 121:427-439.
12. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
13. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313.
14. Chen CC, Rainville P, Bushnell MC (1996) Noxious and innocuous cold discrimination in humans: evidence for separate afferent channels. Pain 68:33-43.
15. Clapham DE, Julius D, Montell C, Schultz G (2005) International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol Rev 57:427-450.
16. Cliff MA, Green BG (1994) Sensory irritation and coolness produced by menthol: evidence for selective desensitization of irritation. Physiol Behav 56:1021-1029.
17. Craig AD, Chen K, Bandy D, Reiman EM (2000) Thermosensory activation of insular cortex. Nat Neurosci 3:184-190.
18. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187.
19. de la Pena E, Malkia A, Cabedo H, Belmonte C, Viana F (2005) The contribution of TRPM8 channels to cold sensing in mammalian neurones. J Physiol (Lond) 567:415-426.
20. Edelman GM, Gally JA (2001) Degeneracy and complexity in biological systems. Proc Natl Acad Sci USA 98:13763-13768.
21. Gallar J, Pozo MA, Tuckett RP, Belmonte C (1993) Response of sensory units with unmyelinated fibres to mechanical, thermal and chemical stimulation of the cat's cornea. J Physiol (Lond) 468:609-622.
22. Hensel H (1981) Thermoreception and temperature regulation. Monogr Physiol Soc 38:1-321.
23. Hensel H, Wurster RD (1970) Static properties of cold receptors in nasal area of cats. J Neurophysiol 33:271-275.
24. Hensel H, Zotterman Y (1951) The response of the cold receptors to constant cooling. Acta Physiol Scand 22:96-113.
25. Heppelmann B, Messlinger K, Neiss WF, Schmidt RF (1990) Ultrastructural three-dimensional reconstruction of group III and group IV sensory nerve endings ("free nerve endings") in the knee joint capsule of the cat: evidence for multiple receptive sites. J Comp Neurol 292:103-116.
26. Hill K, McNulty S, Randall AD (2004) Inhibition of TRPM2 channels by the antifungal agents clotrimazole and econazole. Naunyn Schmiedebergs Arch Pharmacol 370:227-237.
27. Hille B (2001) Ion channels of excitable membranes. Sunderland, MA: Sinauer.
28. Jordt SE, McKemy DD, Julius D (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13:487-492.
29. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260-265.
30. + channels TREK-2 and TRAAK. J Physiol (Lond) 564:103-116.
31. LaMotte RH, Thalhammer JG (1982) Response properties of high-threshold cutaneous cold receptors in the primate. Brain Res 244:279-287.
32. Liu BY, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:1674-1681.
33. Lu G, Henderson D, Liu L, Reinhart PH, Simon SA (2005) TRPV1b, a functional human vanilloid receptor splice variant. Mol Pharmacol 67:1119-1127.
34. + channel. EMBO J 19:2483-2491.
35. McKemy DD (2005) How cold is it? TRPM8 and TRPA1 in the molecular logic of cold sensation. Mol Pain 1:16.
36. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58.
37. Namer B, Seifert F, Handwerker HO, Maihofner C (2005) TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. NeuroReport 16:955-959.
38. Nealen ML, Gold MS, Thut PD, Caterina MJ (2003) TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90:515-520.
39. 2+ channel ECaC1. Br J Pharmacol 134:453-462.
40. Okazawa M, Takao K, Hori A, Shiraki T, Matsumura K, Kobayashi S (2002) Ionic basis of cold receptors acting as thermostats. J Neurosci 22:3994-4001.
41. Patapoutian A, Peier AM, Story GM, Viswanath V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4:529-539.
42. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705-715.
43. Premkumar LS, Raisinghani M, Pingle SC, Long C, Pimentel F (2005) Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. J Neurosci 25:11322-11329.
44. Reid G (2005) ThermoTRP channels and cold sensing: what are they really up to? Pflügers Arch 451:250-263.
45. Reid G, Flonta M (2001) Cold transduction by inhibition of a background potassium conductance in rat primary sensory neurones. Neurosci Lett 297:171-174.
46. Reid G, Amuzescu B, Zech E, Flonta M (2001) A system for applying rapid warming or cooling stimuli to cells during patch clamp recording or ion imaging. J Neurosci Methods 111:1-8.
47. Reid G, Babes A, Pluteanu F (2002) A cold- and menthol-activated current in rat dorsal root ganglion neurones: properties and role in cold transduction. J Physiol (Lond) 545:595-614.
48. Rohacs T, Lopes CM, Michailidis I, Logothetis DE (2005) PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8:626-634.
49. Roza C, Belmonte C, Viana F (2006) Cold sensitivity in axotomized fibers of experimental neuromas in mice. Pain 120:24-35.
50. Schafer K, Braun HA, Kurten L (1988) Analysis of cold and warm receptor activity in vampire bats and mice. Pflügers Arch 412:188-194.
51. Simone DA, Kajander KC (1997) Responses of cutaneous A-fiber nociceptors to noxious cold. J Neurophysiol 77:2049-2060.
52. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819-829.
53. Thut PD, Wrigley D, Gold MS (2003) Cold transduction in rat trigeminal ganglia neurons in vitro. Neuroscience 119:1071-1083.
54. Valenzano KJ, Grant ER, Wu G, Hachicha M, Schmid L, Tafesse L, Sun Q, Rotshteyn Y, Francis J, Limberis J, Malik S, Whittemore ER, Hodges D (2003) N-(4-tertiarybutylphenyl)-4-(3-chloropyridin-2-yl)tetrahy dropyrazine -1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties. I. in vitro characterization and pharmacokinetic properties. J Pharmacol Exp Ther 306:377-386.
55. Viana F, de la Pena E, Belmonte C (2002) Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat Neurosci 5:254-260.
56. Viana F, de la Pena E, Pecson B, Schmidt RF, Belmonte C (2001) Swelling-activated calcium signalling in cultured mouse primary sensory neurons. Eur J Neurosci 13:722-734.
57. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748-754.
58. Wang GX, Poo MM (2005) Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434:898-904.
59. Wasner G, Schattschneider J, Binder A, Baron R (2004) Topical menthol - a human model for cold pain by activation and sensitization of C nociceptors. Brain 127:1159-1171.
60. Weil A, Moore SE, Waite NJ, Randall A, Gunthorpe MJ (2005) Conservation of functional and pharmacological properties in the distantly related temperature sensors TRPV1 and TRPM8. Mol Pharmacol 68:518-527.
61. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, Albers KM, Koerber HR, Davis BM (2004) Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci 24:6410-6415.
62. Xing H, Ling J, Chen M, Gu JG (2006) Chemical and cold sensitivity of two distinct populations of TRPM8-expressing somatosensory neurons. J Neurophysiol 95:1221-1230.
63. Yarnitsky D, Ochoa JL (1991) Warm and cold specific somatosensory systems. Psychophysical thresholds, reaction times and peripheral conduction velocities. Brain 114:1819-1826.
64. Zimmermann K, Leffler A, Fischer MM, Messlinger K, Nau C, Reeh PW (2005) The TRPV1/2/3 activator 2-aminoethoxydiphenyl borate sensitizes native nociceptive neurons to heat in wildtype but not TRPV1 deficient mice. Neuroscience 135:1277-1284.