Topical application of l-menthol induces heat analgesia, mechanical allodynia, and a biphasic effect on cold sensitivity in rats

Behavioural Brain Research

Volumn 212, Issue 2, 2010, Pages 179-186

  Klein, Amanda H ^a   Sawyer, Carolyn M ^a   Carstens, Mirela Iodi ^a   Tsagareli, Merab G ^b   Tsiklauri, Nana ^b   Carstens, E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Tbilisi St Andrew the First Called Georgian University of Georgian Patriarchate   (Georgia)

Author keywords

Cold pain; Hyperalgesia; Hypoalgesia; Mechanical allodynia; Menthol; Pain; Thermal preference

Indexed keywords

MENTHOL; ANTIPRURITIC AGENT;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; COLD SENSITIVITY; CONTROLLED STUDY; HEAT; HYPERSENSITIVITY; HYPOALGESIA; LATENT PERIOD; MALE; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; TEMPERATURE; WITHDRAWAL REFLEX; AGING; ANIMAL; COLD; DOSE RESPONSE; DRUG EFFECTS; HINDLIMB; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; SPRAGUE DAWLEY RAT; STIMULATION; TEMPERATURE SENSE; TIME; TOPICAL DRUG ADMINISTRATION;

ADMINISTRATION, TOPICAL; AGING; ANIMALS; ANTIPRURITICS; COLD TEMPERATURE; DOSE-RESPONSE RELATIONSHIP, DRUG; HINDLIMB; HOT TEMPERATURE; MALE; MENTHOL; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; TEMPERATURE SENSE; TIME FACTORS; THERMOSENSING;

EID: 77953022788     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.04.015     Document Type: Article

References (69)

1. 2+-dependent PKC activation mediates menthol-induced desensitization of transient receptor potential M8. Neurosci Lett 2006, 397:140-144.
2. Albin K.C., Carstens M.I., Carstens E. Modulation of oral heat and cold pain by irritant chemicals. Chem Senses 2008, 33:3-15.
3. Allchorne A., Broom D., Woolf C. Detection of cold pain, cold allodynia and cold hyperalgesia in freely behaving rats. Mol Pain 2005, 1:1-36.
4. Bautista D.M., Siemens J., Glazer J.M., Tsuruda P.R., Basbaum A.I., Stucky C.L., et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 2007, 448:204-208.
5. Behrendt H.J., 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.
6. Belmonte C., Brock J., Viana F. Converting cold into pain. Exp Brain Res 2009, 196:13-30.
7. Cal K. How does the type of vehicle influence the in vitro skin absorption and elmination kinetics of terpenes?. Arch Dermatol Res 2006, 297:311-315.
8. Cal K. Skin disposition of d-camphor and l-menthol alone and together. Methods Find Exp Clin Pharmacol 2009, 31:237-240.
9. Carstens E., Anderson K.A., Simons C.T., Carstens M.I., Jinks S.L. Analgesia induced by chronic nicotine infusion in rats-differences by gender and pain test. Psychopharmacology 2001, 157:40-45.
10. Cliff M.A., Green B.G. Sensitization and desensitization to capsaicin and menthol in the oral cavity: interactions and individual differences. Physiol Behav 1996, 59:487-494.
11. Cliff M.A., Green B.G. Sensory irritation and coolness produced by menthol: evidence for selective desensitization of irritation. Physiol Behav 1994, 56:1021-1029.
12. Colburn R.W., Lubin M.L., Stone D.J., Wang Y., Lawrence D., D'Andrea M.R., et al. Attenuated cold sensitivity in TRPM8 null mice. Neuron 2007, 54:379-386.
13. Craig A.D., Dostrovsky J.O. Differential projections of thermoreceptive and nociceptive lamina I trigeminothalamic and spinothalamic neurons in the cat. J Neurophysiol 2001, 86:856-870.
14. Dessirier J.M., O'Mahony M., Carstens E. Oral irritant properties of menthol: sensitizing and desensitizing effects of repeated application and cross-desensitization to nicotine. Physiol Behav 2001, 73:25-36.
15. Dhaka A., Earley T.J., Watson J., Patapoutian A. Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J Neurosci 2008, 28:566-575.
16. Dhaka A., Murray A.N., Mathur J., Earley T.J., Petrus M.J., Patapoutian A. TRPM8 is required for cold sensation in mice. Neuron 2007, 54:371-378.
17. Eccles R. Menthol and related cooling compounds. J Pharm Pharmacol 1994, 46:618-630.
18. Galeotti N., Di Cesare Mannelli L., Mazzanti G., Bartolini A., Ghelardini C. Menthol: a natural analgesic compound. Neurosci Lett 2002, 322:145-148.
19. Galeotti N., Ghelardini C., Di Cesare Mannelli L., Mazzanti G., Baghiroli L., Bartolini A. Local anaesthetic activity of (+) and (-)-menthol. Planta Med 2001, 67:174-176.
20. Gilchrist H.D., Allard B.L., Simone D.A. Enhanced withdrawal responses to heat and mechanical stimuli following intraplantar injection of capsaicin in rats. Pain 1996, 67:179-188.
21. Green B.G. Interactions between chemical and thermal cutaneous stimuli-inhibition (counterirritation) and integration. Somatosens Mot Res 1991, 8:301-312.
22. Green B.G. Lingual heat and cold sensitivity following exposure to capsaicin or menthol. Chem Senses 2005, 30:201-202.
23. Green B.G. Menthol inhbits the perception of warmth. Physiol Behav 1986, 38:833-838.
24. Green B.G. The sensory effects of l-menthol on human skin. Somatosens Mot Res 1992, 9:235-244.
25. Green B.G., McAuliffe B.L. Menthol desensitization of capsaicin irritation: evidence of a short-term anti-nociceptive effect. Physiol Behav 2000, 68:631-639.
26. Green B.G., Pope J.V. Innocuous cooling can produce nociceptive sensations that are inhibited during dynamic mechanical contact. Exp Brain Res 2003, 148:290-299.
27. Green B.G., Schoen K.L. Thermal and nociceptive sensations from menthol and their suppression by dynamic contact. Behav Brain Res 2007, 176:284-291.
28. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
29. Hatem S., Attal N., Willer J.-C., Bouhassira D. Psychophysical study of the effects of topical application of menthol in healthy volunteers. Pain 2006, 122:190-196.
30. Hensel H., Zotterman Y. The effect of menthol on the thermoreceptors. Acta Physiol Scand 1951, 24:27-34.
31. Jasmin L., Kohan L., Franssen M., Janni G., Goff J.R. The cold plate as a test of nociceptive behaviors: description and application to the study of chronic neuropathic and inflammatory pain models. Pain 1998, 75:367-382.
32. Jordt S.E., McKemy D.D., Julius D. Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 2003, 13:487-492.
33. Kalantzis A., Robinson P.P., Loescher A.R. Effects of capsaicin and menthol on oral thermal sensory thresholds. Arch Oral Biol 2007, 52:149-153.
34. + channels TREK-2 and TRAAK. J Physiol 2005, 564:103-116.
35. Karashima Y., Damann N., Prenen J., Talavera K., Segal A., Voets T., et al. Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 2007, 27:9874-9884.
36. Klein A.H., Sawyer C.M., Carstens M.I., Tsagareli M., Tskilauri N., Carstens E. Effects of TRPM8 agonist menthol on thermal and mechanical sensitvity in rats. Neuroscience meeting planner 2009, Society for Neuroscience, Chicago, IL.
37. Macpherson L.J., Hwang S.W., Miyamoto T., Dubin A.E., Patapoutian A., Story G.M. More than cool: promiscuous relationships of menthol and other sensory compounds. Mol Cell Neurosci 2006, 32:335-343.
38. Madrid R., Donovan-Rodriguez T., Meseguer V., Acosta M.C., Belmonte C., Viana F. Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals. J Neurosci 2006, 26:12512-12525.
39. Magnusson B.M., Walters K.A., Roberts M.S. Veterinary drug delivery: potential for skin penetration enhancement. Adv Drug Deliv Rev 2001, 50:205-227.
40. Malkia A., Madrid R., Meseguer V., de la Pena E., Valero M., Belmonte C., et al. Bidirectional shifts of TRPM8 channel gating by temperature and chemical agents modulate the cold sensitivity of mammalian thermoreceptors. J Physiol (Lond) 2007, 581:155-174.
41. McKemy D.D., Neuhausser WM W.M., Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 2002, 416:52-58.
42. Moqrich A., Hwang S.W., Earley T.J., Petrus M.J., Murray A.N., Spencer K.S.R., et al. Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 2005, 307:1468-1472.
43. Munns C., AlQatari M., Koltzenburg M. Many cold sensitive peripheral neurons of the mouse do not express TRPM8 or TRPA1. Cell Calcium 2007, 41:331-342.
44. Namer B., Seifert F., Handwerker H.O., Maihöfner C. TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. NeuroReport 2005, 16:955-959.
45. Nealen M.L., Gold M.S., Thut P.D., Caterina M.J. TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 2003, 90:515-520.
46. Neddermeyer T.J., Flühr K., Lötsch J. Principle components analysis of pain thresholds to thermal, electrical, and mechanical stimuli suggests a predominant common source of variance. Pain 2008, 138:286-291.
47. + channels TRAAK and TREK-1 control both warm and cold perception. EMBO J 2009, 28:1308-1318.
48. Patel T., Ishiuji Y., Yosipovitch G. Menthol: a refreshing look at this ancient compound. J Am Acad Dermatol 2007, 57:873-878.
49. Peier A.M., Moqrich A., Hergarden A.C., Reeve A.J., Andersson D.A., Story G.M., et al. A TRP channel that senses cold stimuli and menthol. Cell 2002, 108:705-715.
50. Proudfoot C.J., Garry E.M., Cottrell D.F., Rosie R., Anderson H., Robertson D.C., et al. Analgesia mediated by the TRPM8 cold receptor in chronic neuropathic pain. Curr Biol 2006, 16:1591-1605.
51. Reid G. ThermoTRP channels and cold sensing: what are they really up to?. Pflugers Arch 2005, 451:250-263.
52. Reid G., Babes A., Pluteanu F. A cold- and menthol-activated current in rat dorsal root ganglion neurones: properties and role in cold transduction. J Physiol (Lond) 2002, 545:595-614.
53. Reid G., Flonta M.L. Cold transduction by inhibition of a background potassium conductance in rat primary sensory neurones. Neurosci Lett 2001, 297:171-174.
54. Reid G., Flonta M.L. Physiology: cold current in thermoreceptive neurons. Nature 2001, 413:480.
55. Rohacs T., Lopes C.M.B., Michailidis I., Logothetis D.E. PI(4,5)P-2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 2005, 8:626-634.
56. Rossi H.L., Vierck C.J., Caudle R.M., Neubert J.K. Characterization of cold sensitivity and thermal preference using an operant orofacial assay. Mol Pain 2006, 2:37.
57. Sugibayashi K., Kobayashi D., Nakagaki E., Hatanaka T., Inoue N., Kusumi S., et al. Differences in enhancing effect of l-menthol, ethanol and their combination between hairless rat and human skin. Int J Pharm 1995, 113:189-197.
58. Tsagareli M.G., Tsiklauri N., Zanotto K.L., Carstens M.I., Klein A.H., Sawyer C.M., et al. Behavioral evidence of thermal hyperalgesia and mechanical allodynia induced by intradermal cinnamaldehyde in rats. Neurosci Lett. 2010, 473(3):233-236. http://www.ncbi.nlm.nih.gov/pubmed/20219630.
59. Tzabazis A., Klyukinov M., Manering N., Nemenov M.I., Shafer S.L., Yeomans D.C. Differential activation of trigeminal C or Aδ nociceptors by infrared diode laser in rats: behavioral evidence. Brain Res 2005, 1037:148-156.
60. Vetter I., Wyse B.D., Roberts-Thomson S.J., Monteith G.R., Cabot P.J. Mechanisms involved in potentiation of transient receptor potential vanilloid 1 responses by ethanol. Eur J Pain 2008, 12:441-454.
61. Viana F., de la Pena E., Belmonte C. Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat Neurosci 2002, 5:254-260.
62. Voets T., Droogmans G., Wissenbach U., Janssens A., Flockerzi V., Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 2004, 430:748-754.
63. Veterinary applications of skin penetration enhancers 1993, Marcel Dekker, New York, p. 345-364. K.A. Walters, M.S. Roberts (Eds.).
64. Wasner G., Naleschinski D., Binder A., Schattschneider J., McLachlan E., Baron R.M. The effect of menthol on cold allodynia in patients with neuropathic pain. Pain Med 2008, 9:354-358.
65. Wasner G., Schattschneider J., Binder A., Baron R. Topical menthol-a human model for cold pain by activation and sensitization of C nociceptors. Brain 2004, 127:1159-1171.
66. Wrigley P.J., Jeong H.-J., Vaughan C.W. Primary afferents with TRPM8 and TRPA1 profiles target distinct populations of rat superficial dorsal horn neurones. Br J Pharmacol 2009, 157:371-380.
67. Yosipovitch G., Szolar C., Hui X., Maibach H. Effect of topically applied menthol on thermal, pain and itch sensations and biophysical properties of the skin. Arch Dermatol Res 1996, 288:245-248.
68. Zanotto K.L., Carstens M.I., Carstens E. Cross-desensitization of responses of rat trigeminal subnucleus caudalis neurons to cinnamaldehyde and menthol. Neurosci Lett 2008, 430:29-33.
69. Zanotto K.L., Merrill A.W., Carstens M.I., Carstens E. Neurons in superficial trigeminal subnucleus caudalis responsive to oral cooling, menthol, and other irritant stimuli. J Neurophysiol 2007, 97:966-978.