1,8-cineole, a TRPM8 agonist, is a novel natural antagonist of human TRPA1

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Takaishi, Masayuki ^a,b   Fujita, Fumitaka ^a,b   Uchida, Kunitoshi ^a,c   Yamamoto, Satoshi ^b   Shimizu, Maki Sawada ^b   Uotsu, Chihiro Hatai ^b   Shimizu, Mayumi ^b   Tominaga, Makoto ^a,c  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b C   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

1,8 cineole; Pain relief; TRP channels; TRPA1

Indexed keywords

1,4 CINEOLE; ALLYL ISOTHIOCYANATE; CINEOLE; EUCALYPTUS OIL; MENTHOL; OCTANOL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; UNCLASSIFIED DRUG;

ADULT; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG MECHANISM; DRUG SCREENING; ELECTROPHYSIOLOGY; HUMAN; HUMAN EXPERIMENT; IN VIVO STUDY; INHIBITION KINETICS; MALE; MOLECULAR CLONING; MOUSE; NONHUMAN; NORMAL HUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY IRRITATION TEST; SENSORY NERVE CELL; SENSORY SYSTEM EXAMINATION; SPINAL GANGLION;

CALCIUM CHANNELS; CELL LINE; GANGLIA, SPINAL; HUMANS; ISOTHIOCYANATES; MENTHOL; MONOTERPENES; NERVE TISSUE PROTEINS; OCTANOLS; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPM CATION CHANNELS;

EID: 84870063505     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-86     Document Type: Article

References (56)

1. Peana AT, D'Aquila PS, Chessa ML, Moretti MD, Serra G, Pippia P. (-)-Linalool produces antinociception in two experimental models of pain. Eur J Pharmacol 2003, 460:37-41. 10.1016/S0014-2999(02)02856-X, 12535857.
2. Christensen AP, Corey DP. TRP channels in mechanosensation: direct or indirect activation?. Nat Rev Neurosci 2007, 8:510-521. 10.1038/nrn2149, 17585304.
3. Minke B, Cook B. TRP channel proteins and signal transduction. Physiol Rev 2002, 82:429-472.
4. Zhang XF, Chen J, Faltynek CR, Moreland RB, Neelands TR. Transient receptor potential A1 mediates an osmotically activated ion channel. Eur J Neurosci 2008, 27:605-611. 10.1111/j.1460-9568.2008.06030.x, 18279313.
5. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 2004, 427:260-265. 10.1038/nature02282, 14712238.
6. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 2006, 50:277-289. 10.1016/j.neuron.2006.03.042, 16630838.
7. Obata K, Katsura H, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Tominaga M, Noguchi K. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 2005, 115:2393-2401. 10.1172/JCI25437, 1187934, 16110328.
8. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 2003, 112:819-829. 10.1016/S0092-8674(03)00158-2, 12654248.
9. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 2004, 41:849-857. 10.1016/S0896-6273(04)00150-3, 15046718.
10. Petrus M, Peier AM, Bandell M, Hwang SW, Huynh T, Olney N, Jegla T, Patapoutian A. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol Pain 2007, 3:40. 10.1186/1744-8069-3-40, 2222610, 18086313.
11. Fujita F, Moriyama T, Higashi T, Shima A, Tominaga M. Methyl p-hydroxybenzoate causes pain sensation through activation of TRPA1 channels. Br J Pharmacol 2007, 151:153-160. 2012982, 17351650.
12. Fujita F, Uchida K, Moriyama T, Shima A, Shibasaki K, Inada H, Sokabe T, Tominaga M. Intracellular alkalization causes pain sensation through activation of TRPA1 in mice. J Clin Invest 2008, 118:4049-4057. 10.1172/JCI35957, 2582441, 19033673.
13. Andersson DA, Gentry C, Moss S, Bevan S. Clioquinol and pyrithione activate TRPA1 by increasing intracellular Zn2+. Proc Natl Acad Sci USA 2009, 106:8374-8379. 10.1073/pnas.0812675106, 2688854, 19416844.
14. Doerner JF, Gisselmann G, Hatt H, Wetzel CH. Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 2007, 282:13180-13189. 10.1074/jbc.M607849200, 17353192.
15. Hu H, Bandell M, Petrus MJ, Zhu MX, Patapoutian A. Zinc activates damage-sensing TRPA1 ion channels. Nat Chem Biol 2009, 5:183-190. 10.1038/nchembio.146, 2677965, 19202543.
16. Wang YY, Chang RB, Waters HN, McKemy DD, Liman ER. The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions. J Biol Chem 2008, 283:32691-32703. 10.1074/jbc.M803568200, 2583289, 18775987.
17. Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA. Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci 2007, 10:277-279. 10.1038/nn1843, 17259981.
18. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Hogestatt ED, Julius D, Jordt SE, Zygmunt PM. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 2005, 102:12248-12252. 10.1073/pnas.0505356102, 1189336, 16103371.
19. Hinman A, Chuang HH, Bautista DM, Julius D. TRP channel activation by reversible covalent modification. Proc Natl Acad Sci USA 2006, 103:19564-19568. 10.1073/pnas.0609598103, 1748265, 17164327.
20. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF, Patapoutian A. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 2007, 445:541-545. 10.1038/nature05544, 17237762.
21. Hu H, Tian J, Zhu Y, Wang C, Xiao R, Herz JM, Wood JD, Zhu MX. Activation of TRPA1 channels by fenamate nonsteroidal anti-inflammatory drugs. Pflugers Arch 2010, 459:579-592. 10.1007/s00424-009-0749-9, 2828537, 19888597.
22. Xiao B, Dubin AE, Bursulaya B, Viswanath V, Jegla TJ, Patapoutian A. Identification of transmembrane domain 5 as a critical molecular determinant of menthol sensitivity in mammalian TRPA1 channels. J Neurosci 2008, 28:9640-9651. 10.1523/JNEUROSCI.2772-08.2008, 2678945, 18815250.
23. Karashima Y, Damann N, Prenen J, Talavera K, Segal A, Voets T, Nilius B. Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 2007, 27:9874-9884. 10.1523/JNEUROSCI.2221-07.2007, 17855602.
24. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006, 124:1269-1282. 10.1016/j.cell.2006.02.023, 16564016.
25. Caceres AI, Brackmann M, Elia MD, Bessac BF, del Camino D, D'Amours M, Witek JS, Fanger CM, Chong JA, Hayward NJ, et al. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc Natl Acad Sci USA 2009, 106:9099-9104. 2684498, 19458046.
26. Chen J, Joshi SK, DiDomenico S, Perner RJ, Mikusa JP, Gauvin DM, Segreti JA, Han P, Zhang XF, Niforatos W, et al. Selective blockade of TRPA1 channel attenuates pathological pain without altering noxious cold sensation or body temperature regulation. Pain 2011, 152:1165-1172. 10.1016/j.pain.2011.01.049, 21402443.
27. Eid SR, Crown ED, Moore EL, Liang HA, Choong KC, Dima S, Henze DA, Kane SA, Urban MO. HC-030031, a TRPA1 selective antagonist, attenuates inflammatory- and neuropathy-induced mechanical hypersensitivity. Mol Pain 2008, 4:48. 10.1186/1744-8069-4-48, 2584039, 18954467.
28. Klionsky L, Tamir R, Gao B, Wang W, Immke DC, Nishimura N, Gavva NR. Species-specific pharmacology of Trichloro(sulfanyl)ethyl benzamides as transient receptor potential ankyrin 1 (TRPA1) antagonists. Mol Pain 2007, 3:39. 10.1186/1744-8069-3-39, 2222611, 18086308.
29. McGaraughty S, Chu KL, Perner RJ, Didomenico S, Kort ME, Kym PR. TRPA1 modulation of spontaneous and mechanically evoked firing of spinal neurons in uninjured, osteoarthritic, and inflamed rats. Mol Pain 2010, 6:14. 10.1186/1744-8069-6-14, 2841076, 20205719.
30. Nagata K, Duggan A, Kumar G, Garcia-Anoveros J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 2005, 25:4052-4061. 10.1523/JNEUROSCI.0013-05.2005, 15843607.
31. Xu H, Blair NT, Clapham DE. Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J Neurosci 2005, 25:8924-8937. 10.1523/JNEUROSCI.2574-05.2005, 16192383.
32. McKemy DD, Neuhausser WM, Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 2002, 416:52-58. 10.1038/nature719, 11882888.
33. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A. A TRP channel that senses cold stimuli and menthol. Cell 2002, 108:705-715. 10.1016/S0092-8674(02)00652-9, 11893340.
34. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A. TRPM8 is required for cold sensation in mice. Neuron 2007, 54:371-378. 10.1016/j.neuron.2007.02.024, 17481391.
35. Proudfoot CJ, Garry EM, Cottrell DF, Rosie R, Anderson H, Robertson DC, Fleetwood-Walker SM, Mitchell R. Analgesia Mediated by the TRPM8 Cold Receptor in Chronic Neuropathic Pain. Curr Biol 2006, 16:1591-1605. 10.1016/j.cub.2006.07.061, 16920620.
36. Galeotti N, Di Cesare Mannelli L, Mazzanti G, Bartolini A, Ghelardini C. Menthol: a natural analgesic compound. Neurosci Lett 2002, 322:145-148. 10.1016/S0304-3940(01)02527-7, 11897159.
37. Geen BG. The sensory effects of l-menthol on human skin. Mot Res 1992, 9:235-244.
38. Vogt-Eisele AK, Weber K, Sherkheli MA, Vielhaber G, Panten J, Gisselmann G, Hatt H. Monoterpenoid agonists of TRPV3. Br J Pharmacol 2007, 151:530-540. 2013969, 17420775.
39. Green BG. Sensory characteristics of camphor. J Invest Dermatol 1990, 94:662-666. 10.1111/1523-1747.ep12876242, 2324522.
40. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288:306-313. 10.1126/science.288.5464.306, 10764638.
41. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 1999, 398:436-441. 10.1038/18906, 10201375.
42. 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 1997, 389:816-824. 10.1038/39807, 9349813.
43. Colburn RW, Lubin ML, Stone DJ, Wang Y, Lawrence D, D'Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N. Attenuated cold sensitivity in TRPM8 null mice. Neuron 2007, 54:379-386. 10.1016/j.neuron.2007.04.017, 17481392.
44. Behrendt HJ, Germann T, Gillen C, Hatt H, Jostock R. 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 2004, 141:737-745. 10.1038/sj.bjp.0705652, 1574235, 14757700.
45. Saito S, Fukuta N, Shingai R, Tominaga M. Evolution of vertebrate transient receptor potential vanilloid 3 channels: opposite temperature sensitivity between mammals and western clawed frogs. PLoS Genet 2011, 7:e1002041. 10.1371/journal.pgen.1002041, 3072374, 21490957.
46. Sherkheli MA, Benecke H, Doerner JF, Kletke O, Vogt-Eisele AK, Gisselmann G, Hatt H. Monoterpenoids induce agonist-specific desensitization of transient receptor potential vanilloid-3 (TRPV3) ion channels. J Pharm Pharm Sci 2009, 12:116-128.
47. Santos FA, Rao VS. Antiinflammatory and antinociceptive effects of 1,8-cineole a terpenoid oxide present in many plant essential oils. Phytother Res 2000, 14:240-244. 10.1002/1099-1573(200006)14:4<240::AID-PTR573>3.0.CO;2-X, 10861965.
48. Silva J, Abebe W, Sousa SM, Duarte VG, Machado MI, Matos FJ. Analgesic and anti-inflammatory effects of essential oils of Eucalyptus. J Ethnopharmacol 2003, 89:277-283. 10.1016/j.jep.2003.09.007, 14611892.
49. Komatsu T, Uchida K, Fujita F, Zhou Y, Tominaga M. Primary alcohols activate human TRPA1 channel in a carbon chain length-dependent manner. Pflugers Arch 2012, 463:549-559. 10.1007/s00424-011-1069-4, 22222967.
50. van Thriel C, Kiesswetter E, Blaszkewicz M, Golka K, Seeber A. Neurobehavioral effects during experimental exposure to 1-octanol and isopropanol. Scand J Work Environ Health 2003, 29:143-151. 10.5271/sjweh.716, 12718500.
51. Juergens UR, Dethlefsen U, Steinkamp G, Gillissen A, Repges R, Vetter H. Anti-inflammatory activity of 1.8-cineol (eucalyptol) in bronchial asthma: a double-blind placebo-controlled trial. Respir Med 2003, 97:250-256. 10.1053/rmed.2003.1432, 12645832.
52. Laude EA, Morice AH, Grattan TJ. The antitussive effects of menthol, camphor and cineole in conscious guinea-pigs. Pulm Pharmacol 1994, 7:179-184. 10.1006/pulp.1994.1021, 7827436.
53. Levison KK, Takayama K, Isowa K, Okabe K, Nagai T. Formulation optimization of indomethacin gels containing a combination of three kinds of cyclic monoterpenes as percutaneous penetration enhancers. J Pharm Sci 1994, 83:1367-1372. 10.1002/jps.2600830932, 7830256.
54. Williams AC, Barry BW. Terpenes and the lipid-protein-partitioning theory of skin penetration enhancement. Pharm Res 1991, 8:17-24. 10.1023/A:1015813803205, 2014203.
55. Juergens UR, Engelen T, Racke K, Stober M, Gillissen A, Vetter H. Inhibitory activity of 1,8-cineol (eucalyptol) on cytokine production in cultured human lymphocytes and monocytes. Pulm Pharmacol Ther 2004, 17:281-287. 10.1016/j.pupt.2004.06.002, 15477123.
56. Macpherson LJ, Hwang SW, Miyamoto T, Dubin AE, Patapoutian A, Story GM. More than cool: promiscuous relationships of menthol and other sensory compounds. Mol Cell Neurosci 2006, 32:335-343. 10.1016/j.mcn.2006.05.005, 16829128.