Cannabinoids desensitize capsaicin and mustard oil responses in sensory neurons via TRPA1 activation

Journal of Neuroscience

Volumn 28, Issue 5, 2008, Pages 1064-1075

  Akopian, Armen N ^a   Ruparel, Nikita B ^a   Patwardhan, Amol ^a   Hargreaves, Kenneth M ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Cannabinoid; Nociceptor; Pain; Trigeminal; TRPA1; TRPV1

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 3 (2 IODO 5 NITROBENZOYL) 1 (1 METHYL 2 PIPERIDINYLMETHYL)INDOLE; ALLYL ISOTHIOCYANATE; CALCIUM CHANNEL; CANNABINOID; CAPSAICIN; SMALL INTERFERING RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENUATION; CELL ACTIVATION; CHO CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DESENSITIZATION; DRUG EFFECT; DRUG INHIBITION; DRUG MECHANISM; DRUG RESPONSE; FEMALE; MALE; MODULATION; MOUSE; MOUSE MUTANT; NOCICEPTION; NOCICEPTIVE RECEPTOR; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE CELL;

ANIMALS; CANNABINOIDS; CAPSAICIN; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSTARD PLANT; NEURONS, AFFERENT; PAIN; PAIN MEASUREMENT; PLANT OILS; RATS; RATS, SPRAGUE-DAWLEY; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 38749149923     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1565-06.2008     Document Type: Article

References (83)

1. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, Rubino T, Michalski CW, Marsicano G, Monory K, Mackie K, Marian C, Batkai S, Parolaro D, Fischer MJ, Reeh P, Kunos G, Kress M, Lutz B, Woolf CJ, et al. (2007) Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 10:870-879.
2. Ahluwalia J, Urban L, Capogna M, Bevan S, Nagy I (2000) Cannabinoid 1 receptors are expressed in nociceptive primary sensory neurons. Neuroscience 100:685-688.
3. Akopian AN, Ruparel NB, Jeske NA, Hargreaves KM (2007) Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization. J Physiol (Lond) 583:175-193.
4. Amaya F, Shimosato G, Kawasaki Y, Hashimoto S, Tanaka Y, Ji RR, Tanaka M (2006) Induction of CB1 cannabinoid receptor by inflammation in primary afferent neurons facilitates antihyperalgesic effect of peripheral CB1 agonist. Pain 124:175-183.
5. 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.
6. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D (2006) TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269-1282.
7. Binzen U, Greffrath W, Hennessy S, Bausen M, Saaler-Reinhardt S, Treede RD (2006) Co-expression of the voltage-gated potassium channel Kv1.4 with transient receptor potential channels (TRPV1 and TRPV2) and the cannabinoid receptor CB1 in rat dorsal root ganglion neurons. Neuroscience 142:527-539.
8. Bolcskei K, Helyes Z, Szabo A, Sandor K, Elekes K, Nemeth J, Almasi R, Pinter E, Petho G, Szolcsanyi J (2005) Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Pain 117:368-376.
9. Brand G, Jacquot L (2002) Sensitization and desensitization to allyl isothiocyanate (mustard oil) in the nasal cavity. Chem Senses 27:593-598.
10. Bridges D, Rice AS, Egertova M, Elphick MR, Winter J, Michael GJ (2003) Localisation of cannabinoid receptor 1 in rat dorsal root ganglion using in situ hybridisation and immunohistochemistry. Neuroscience 119:803-812.
11. Calignano A, La Rana G, Giuffrida A, Piomelli D (1998) Control of pain initiation by endogenous cannabinoids. Nature 394:277-281.
12. Calignano A, La Rana G, Piomelli D (2001) Antinociceptive activity of the endogenous fatty acid amide, palmitylethanolamide. Eur J Pharmacol 419:191-198.
13. 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.
14. 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.
15. Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517-524.
16. Corey DP, Garcia-Anoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Geleoc GS, Gray PA, Hoffman MP, Rehm HL, Tamasauskas D, Zhang DS (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723-730.
17. Croxford JL (2003) Therapeutic potential of cannabinoids in CNS disease. CNS Drugs 17:179-202.
18. Diogenes A, Akopian AN, Hargreaves KM (2007) NGF up-regulates TRPA1: implications for orofacial pain. J Dent Res 86:550-555.
19. 2+-induced potentiation of heat-activated ionic currents requires cAMP/PKA signaling and functional AKAP anchoring. J Neurophysiol 89:2499-2505.
20. Docherty RJ, Yeats JC, Bevan S, Boddeke HW (1996) Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflügers Arch 431:828-837.
21. Dogrul A, Gul H, Akar A, Yildiz O, Bilgin F, Guzeldemir E (2003) Topical cannabinoid antinociception: synergy with spinal sites. Pain 105:11-16.
22. Duncan M, Kendall DA, Ralevic V (2004) Characterization of cannabinoid modulation of sensory neurotransmission in the rat isolated mesenteric arterial bed. J Pharmacol Exp Ther 311:411-419.
23. Ellington HC, Cotter MA, Cameron NE, Ross RA (2002) The effect of cannabinoids on capsaicin-evoked calcitonin gene-related peptide (CGRP) release from the isolated paw skin of diabetic and non-diabetic rats. Neuropharmacology 42:966-975.
24. Fox A, Kesingland A, Gentry C, McNair K, Patel S, Urban L, James I (2001) The role of central and peripheral cannabinoid 1 receptors in the antihyperalgesic activity of cannabinoids in a model of neuropathic pain. Pain 92:91-100.
25. + channels. J Gen Physiol 122:17-31.
26. Hannon GJ, Rossi JJ (2004) Unlocking the potential of the human genome with RNA interference. Nature 431:371-378.
27. Hohmann AG, Herkenham M (1999) Cannabinoid receptors undergo axonal flow in sensory nerves. Neuroscience 92:1171-1175.
28. Hohmann AG, Farthing JN, Zvonok AM, Makriyannis A (2004) Selective activation of cannabinoid CB2 receptors suppresses hyperalgesia evoked by intradermal capsaicin. J Pharmacol Exp Ther 308:446-453.
29. Hu HZ, Gu Q, Wang C, Colton CK, Tang J, Kinoshita-Kawada M, Lee LY, Wood JD, Zhu MX (2004) 2-Aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279:35741-35748.
30. Huang SM, Bisogno T, Trevisani M, Al-Hayani A, De Petrocellis L, Fezza F, Tognetto M, Petros TJ, Krey JF, Chu CJ, Miller JD, Davies SN, Geppetti P, Walker JM, Di Marzo V (2002) An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc Natl Acad Sci USA 99:8400-8405.
31. Ibrahim MM, Deng H, Zvonok A, Cockayne DA, Kwan J, Mata HP, Vanderah TW, Lai J, Porreca F, Makriyannis A, Malan Jr TP (2003) Activation of CB2 cannabinoid receptors by AM1241 inhibits experimental neuropathic pain: pain inhibition by receptors not present in the CNS. Proc Natl Acad Sci USA 100:10529-10533.
32. Ibrahim MM, Porreca F, Lai J, Albrecht PJ, Rice FL, Khodorova A, Davar G, Makriyannis A, Vanderah TW, Mata HP, Malan Jr TP (2005) CB2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc Natl Acad Sci USA 102:3093-3098.
33. Ibrahim MM, Rude ML, Stagg NJ, Mata HP, Lai J, Vanderah TW, Porreca F, Buckley NE, Makriyannis A, Malan Jr TP (2006) CB(2) cannabinoid receptor mediation of antinociception. Pain 122:36-42.
34. Jacquot L, Monnin J, Lucarz A, Brand G (2005) Trigeminal sensitization and desensitization in the nasal cavity: a study of cross interactions. Rhinology 43:93-98.
35. Jaggar SI, Hasnie FS, Sellaturay S, Rice AS (1998) The anti-hyperalgesic actions of the cannabinoid anandamide and the putative CB2 receptor agonist palmitoylethanolamide in visceral and somatic inflammatory pain. Pain 76:189-199.
36. Jeske NA, Patwardhan AM, Gamper N, Price TJ, Akopian AN, Hargreaves KM (2006) Cannabinoid WIN 55,212-2 regulates TRPV1 phosphorylation in sensory neurons. J Biol Chem 281:32879-32890.
37. Johanek LM, Simone DA (2004) Activation of peripheral cannabinoid receptors attenuates cutaneous hyperalgesia produced by a heat injury. Pain 109:432-442.
38. Johanek LM, Heitmiller DR, Turner M, Nader N, Hodges J, Simone DA (2001) Cannabinoids attenuate capsaicin-evoked hyperalgesia through spinal and peripheral mechanisms. Pain 93:303-315.
39. 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.
40. Juliano RL, Dixit VR, Kang H, Kim TY, Miyamoto Y, Xu D (2005) Epigenetic manipulation of gene expression: a toolkit for cell biologists. J Cell Biol 169:847-857.
41. 2+/calmodulin-dependent kinase II regulates its vanilloid binding. J Biol Chem 279:7048-7054.
42. Katsura H, Obata K, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Sakagami M, Noguchi K (2006) Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats. Exp Neurol 200:112-123.
43. 2+ influx in intermediate-size primary afferent neurons of adult rats. Neuroscience 115:613-625.
44. 1 and opioid agonists on two populations of adult rat dorsal root ganglion neurons. J Neurosci 24:1744-1753.
45. Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, Noguchi K (2005) Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J Comp Neurol 493:596-606.
46. Koplas PA, Rosenberg RL, Oxford GS (1997) The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17:3525-3537.
47. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-289.
48. Lauckner JE, Hille B, Mackie K (2005) The cannabinoid agonist WIN55,212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc Natl Acad Sci USA 102:19144-19149.
49. 2+ in the desensitization responses to capsaicin, zingerone and olvanil in rat trigeminal ganglion neurons. Brain Res 809:246-252.
50. Liu L, Lo Y, Chen I, Simon SA (1997) The responses of rat trigeminal ganglion neurons to capsaicin and two nonpungent vanilloid receptor agonists, olvanil and glyceryl nonamide. J Neurosci 17:4101-4111.
51. Maccarrone M, Di Rienzo M, Battista N, Gasperi V, Guerrieri P, Rossi A, Finazzi-Agro A (2003) The endocannabinoid system in human keratinocytes. Evidence that anandamide inhibits epidermal differentiation through CB1 receptor-dependent inhibition of protein kinase C, activation protein-1, and transglutaminase. J Biol Chem 278:33896-33903.
52. Malan Jr TP, Ibrahim MM, Deng H, Liu Q, Mata HP, Vanderah T, Porreca F, Makriyannis A (2001) CB2 cannabinoid receptor-mediated peripheral antinociception. Pain 93:239-245.
53. Malan Jr TP, Ibrahim MM, Lai J, Vanderah TW, Makriyannis A, Porreca F (2003) CB2 cannabinoid receptor agonists: pain relief without psychoactive effects? Curr Opin Pharmacol 3:62-67.
54. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561-564.
55. 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.
56. McMahon SB, Wood JN (2006) Increasingly irritable and close to tears: TRPA1 in inflammatory pain. Cell 124:1123-1125.
57. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61-65.
58. Nackley AG, Makriyannis A, Hohmann AG (2003) Selective activation of cannabinoid CB(2) receptors suppresses spinal fos protein expression and pain behavior in a rat model of inflammation. Neuroscience 119:747-757.
59. Numazaki M, Tominaga T, Takeuchi K, Murayama N, Toyooka H, Tominaga M (2003) Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc Natl Acad Sci USA 100:8002-8006.
60. Obata K, Katsura H, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Tominaga M, Noguchi K (2005) TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 115:2393-2401.
61. Patwardhan AM, Jeske NA, Price TJ, Gamper N, Akopian AN, Hargreaves KM (2006a) The cannabinoid WIN 55,212-2 inhibits transient receptor potential vanilloid 1 (TRPV1) and evokes peripheral antihyperalgesia via calcineurin. Proc Natl Acad Sci USA 103:11393-11398.
62. Patwardhan AM, Diogenes A, Berg KA, Fehrenbacher JC, Clarke WP, Akopian AN, Hargreaves KM (2006b) PAR-2 agonists activate trigeminal nociceptors and induce functional competence in the delta opioid receptor. Pain 125:114-124.
63. Perkins NM, Tracey DJ (2000) Hyperalgesia due to nerve injury: role of neutrophils. Neuroscience 101:745-757.
64. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873-884.
65. Piper AS, Yeats JC, Bevan S, Docherty RJ (1999) A study of the voltage dependence of capsaicin-activated membrane currents in rat sensory neurones before and after acute desensitization. J Physiol (Lond) 518:721-733.
66. Price TJ, Helesic G, Parghi D, Hargreaves KM, Flores CM (2003) The neuronal distribution of cannabinoid receptor type 1 in the trigeminal ganglion of the rat. Neuroscience 120:155-162.
67. Price TJ, Patwardhan A, Akopian AN, Hargreaves KM, Flores CM (2004a) Modulation of trigeminal sensory neuron activity by the dual cannabinoid-vanilloid agonists anandamide, N-arachidonoyl-dopamine and arachidonyl-2-chloroethylamide. Br J Pharmacol 141:1118-1130.
68. Price TJ, Patwardhan A, Akopian AN, Hargreaves KM, Flores CM (2004b) Cannabinoid receptor-independent actions of the aminoalkylindole WIN 55,212-2 on trigeminal sensory neurons. Br J Pharmacol 142:257-266.
69. Quartilho A, Mata HP, Ibrahim MM, Vanderah TW, Porreca F, Makriyannis A, Malan TP, Jr (2003) Inhibition of inflammatory hyperalgesia by activation of peripheral CB2 cannabinoid receptors. Anesthesiology 99:955-960.
70. Ralevic V, Kendall DA (2001) Cannabinoid inhibition of capsaicin-sensitive sensory neurotransmission in the rat mesenteric arterial bed. Eur J Pharmacol 418:117-125.
71. Rice AS, Farquhar-Smith WP, Nagy I (2002) Endocannabinoids and pain: spinal and peripheral analgesia in inflammation and neuropathy. Prostaglandins Leukot Essent Fatty Acids 66:243-256.
72. Richardson JD, Kilo S, Hargreaves KM (1998) Cannabinoids reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain 75:111-119.
73. Rosenzweig M, Brennan KM, Tayler TD, Phelps PO, Patapoutian A, Garrity PA (2005) The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419-424.
74. Ross RA, Coutts AA, McFarlane SM, Anavi-Goffer S, Irving AJ, Pertwee RG, MacEwan DJ, Scott RH (2001) Actions of cannabinoid receptor ligands on rat cultured sensory neurones: implications for antinociception. Neuropharmacology 40:221-232.
75. Ruparel NB, Patwardhan AM, Akopian AN, Hargreaves KM (2008) Homologous and heterologous desensitization of capsaicin and mustard oil responses utilize different cellular pathways in nociceptors. Pain, in press.
76. Sagar DR, Smith PA, Millns PJ, Smart D, Kendall DA, Chapman V (2004) TRPV1 and CB(1) receptor-mediated effects of the endovanilloid/endocannabinoid N-arachidonoyl-dopamine on primary afferent fibre and spinal cord neuronal responses in the rat. Eur J Neurosci 20:175-184.
77. Samson MT, Small-Howard A, Shimoda LM, Koblan-Huberson M, Stokes AJ, Turner H (2003) Differential roles of CB1 and CB2 cannabinoid receptors in mast cells. J Immunol 170:4953-4962.
78. 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.
79. Walker JM, Hohmann AG (2005) Cannabinoid mechanisms of pain suppression. Handb Exp Pharmacol 2005:509-554.
80. Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, Vriens J, Cairns W, Wissenbach U, Prenen J, Flockerzi V, Droogmans G, Benham CD, Nilius B (2002) Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277:13569-13577.
81. 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.
82. Woolf CJ, Ma QP, Allchorne A, Poole S (1996) Peripheral cell types contributing to the hyperalgesic action of nerve growth factor in inflammation. J Neurosci 16:2716-2723.
83. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452-457.