From chills to chilis: mechanisms for thermosensation and chemesthesis via thermoTRPs

Current Opinion in Neurobiology

Volumn 17, Issue 4, 2007, Pages 490-497

  Bandell, Michael ^a,b   Macpherson, Lindsey J ^a   Patapoutian, Ardem ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL AGENT; ENVIRONMENTAL CHEMICAL; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VANILLOID RECEPTOR;

COLD EXPOSURE; DESENSITIZATION; HEAT SENSITIVITY; HUMAN; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; SENSITIZATION; SENSORY NERVE CELL; SKIN NERVE; SPINAL GANGLION; TEMPERATURE SENSITIVITY; THERMAL EXPOSURE; THERMOMETER; THERMOSTABILITY;

ANIMALS; CHEMORECEPTORS; HUMANS; MODELS, MOLECULAR; TEMPERATURE SENSE; THERMORECEPTORS; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 34948851846     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2007.07.014     Document Type: Review

References (78)

1. Dhaka A., Viswanath V., and Patapoutian A. TRP ion channels and temperature sensation. Annu Rev Neurosci 29 (2006) 135-161
2. Lumpkin E.A., and Caterina M.J. Mechanisms of sensory transduction in the skin. Nature 445 (2007) 858-865
3. Moqrich A., Hwang S.W., Earley T.J., Petrus M.J., Murray A.N., Spencer K.S., Andahazy M., Story G.M., and Patapoutian A. Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307 (2005) 1468-1472
4. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., and Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000) 306-313
5. Kwan K.Y., Allchorne A.J., Vollrath M.A., Christensen A., Zhang D.S., Woolf C.J., and Corey D.P. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50 (2006) 277-289
6. Lee H., Iida T., Mizuno A., Suzuki M., and Caterina M.J. Altered thermal selection behavior in mice lacking transient receptor potential vanilloid 4. J Neurosci 25 (2005) 1304-1310
7. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., Harries M.H., Latcham J., Clapham C., Atkinson K., et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (2000) 183-187
8. Dhaka A., Murray A.N., Mathur J., Earley T., Petrus M., and Patapoutian A. TRPM8 is required for cold sensation in mice. Neuron 54 (2007) 371-378
9. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
10. Clapham D.E., Julius D., Montell C., and Schultz G. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol Rev 57 (2005) 427-450
11. Montell C. The TRP superfamily of cation channels. Sci STKE 2005 (2005) re3
12. Yu F.H., and Catterall W.A. The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE 2004 (2004) re15
13. Tombola F., Pathak M.M., and Isacoff E.Y. How does voltage open an ion channel?. Annu Rev Cell Dev Biol 22 (2006) 23-52
14. Voets T., Owsianik G., Janssens A., Talavera K., and Nilius B. TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat Chem Biol 3 (2007) 174-182. This study suggests that charged residues in the S4 and S4-S5 linker of TRPM8 form the voltage sensor. Mutations in this region also affected menthol affinity. Mutation-induced changes in voltage sensitivity were paralleled by changes in thermal sensitivity in agreement with the proposed model in which thermal and voltage activation act on the same gating step.
15. Bandell M., Dubin A.E., Petrus M.J., Orth A., Mathur J., Hwang S.W., and Patapoutian A. High-throughput random mutagenesis screen reveals TRPM8 residues specifically required for activation by menthol. Nat Neurosci 9 (2006) 493-500. The authors take a novel high-throughput approach to identify structural elements involved in TRPM8 activation by menthol. The study identifies two distinct sites on the channel required for menthol sensitivity. They propose that the S2 region is involved in menthol binding while the C-terminal TRP domain is required to couple menthol binding to channel opening. This study suggests a common mechanism of activation for structurally diverse compounds such as capsaicin and menthol.
16. Erler I., Al-Ansary D.M., Wissenbach U., Wagner T.F., Flockerzi V., and Niemeyer B.A. Trafficking and assembly of the cold-sensitive TRPM8 channel. J Biol Chem 281 (2006) 38396-38404
17. Jin X., Touhey J., and Gaudet R. Structure of the N-terminal ankyrin repeat domain of the TRPV2 ion channel. J Biol Chem 281 (2006) 25006-25010
18. Lepage P.K., and Boulay G. Molecular determinants of TRP channel assembly. Biochem Soc Trans 35 (2007) 81-83
19. McCleverty C.J., Koesema E., Patapoutian A., Lesley S.A., and Kreusch A. Crystal structure of the human TRPV2 channel ankyrin repeat domain. Protein Sci 15 (2006) 2201-2206
20. 2-binding sites.
21. Tsuruda P.R., Julius D., and Minor Jr. D.L. Coiled coils direct assembly of a cold-activated TRP channel. Neuron 51 (2006) 201-212
22. Owsianik G., D'Hoedt D., Voets T., and Nilius B. Structure-function relationship of the TRP channel superfamily. Rev Physiol Biochem Pharmacol 156 (2006) 61-90
23. Hille B. Ion Channels of Excitable Membranes. edn 3 (2001), Sinauer, Sunderland, MA
24. Clapham D.E. TRP channels as cellular sensors. Nature 426 (2003) 517-524
25. Watanabe H., Vriens J., Suh S.H., Benham C.D., Droogmans G., and Nilius B. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277 (2002) 47044-47051
26. Voets T., Droogmans G., Wissenbach U., Janssens A., Flockerzi V., and Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430 (2004) 748-754
27. Nilius B., Talavera K., Owsianik G., Prenen J., Droogmans G., and Voets T. Gating of TRP channels: a voltage connection?. J Physiol 567 (2005) 35-44
28. Togashi K., Hara Y., Tominaga T., Higashi T., Konishi Y., Mori Y., and Tominaga M. TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25 (2006) 1804-1815
29. Brauchi S., Orio P., and Latorre R. Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. Proc Natl Acad Sci USA 101 (2004) 15494-15499
30. Vriens J., Watanabe H., Janssens A., Droogmans G., Voets T., and Nilius B. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101 (2004) 396-401
31. Brauchi S., Orta G., Salazar M., Rosenmann E., and Latorre R. A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J Neurosci 26 (2006) 4835-4840. Using domain swap experiments, the authors show that TRPV1 can be converted from a heat-sensing into a cold-sensing channel by replacing the C-terminal domain with that of TRPM8. In the reciprocal experiment, TRPM8 was changed into a heat-activated channel. This data is suggested to support a model for thermal activation in which temperature and voltage affect the channel independently.
32. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., Earley T.J., Hergarden A.C., Andersson D.A., Hwang S.W., et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112 (2003) 819-829
33. Zurborg S., Yurgionas B., Jira J.A., Caspani O., and Heppenstall P.A. Direct activation of the ion channel TRPA1 by Ca(2+). Nat Neurosci 10 (2007) 277-279. This study proposes that cold activation may result from the release of intracellular calcium.
34. Doerner J.F., Gisselmann G., Hatt H., and Wetzel C.H. Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 282 (2007) 13180-13189
35. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., and Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124 (2006) 1269-1282
36. Behrendt H.J., Germann T., Gillen C., Hatt H., and 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 141 (2004) 737-745
37. Bandell M., Story G.M., Hwang S.W., Viswanath V., Eid S.R., Petrus M.J., Earley T.J., and Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41 (2004) 849-857
38. Peier A.M., Moqrich A., Hergarden A.C., Reeve A.J., Andersson D.A., Story G.M., Earley T.J., Dragoni I., McIntyre P., Bevan S., et al. A TRP channel that senses cold stimuli and menthol. Cell 108 (2002) 705-715
39. McKemy D.D., Neuhausser W.M., and Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416 (2002) 52-58
40. Bautista D.M., Movahed P., Hinman A., Axelsson H.E., Sterner O., Hogestatt E.D., Julius D., Jordt S.E., and Zygmunt P.M. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 102 (2005) 12248-12252
41. Jordt S.E., Bautista D.M., Chuang H.H., McKemy D.D., Zygmunt P.M., Hogestatt E.D., Meng I.D., and Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427 (2004) 260-265
42. Xu H., Blair N.T., and Clapham D.E. Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J Neurosci 25 (2005) 8924-8937
43. Smith P.L., Maloney K.N., Pothen R.G., Clardy J., and Clapham D.E. Bisandrographolide from Andrographis paniculata activates TRPV4 channels. J Biol Chem 281 (2006) 29897-29904
44. Macpherson L.J., Geierstanger B.H., Viswanath V., Bandell M., Eid S.R., Hwang S., and Patapoutian A. The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15 (2005) 929-934
45. Macpherson L.J., Hwang S.W., Miyamoto T., Dubin A.E., Patapoutian A., and Story G.M. More than cool: promiscuous relationships of menthol and other sensory compounds. Mol Cell Neurosci 32 (2006) 335-343
46. Trevisani M., Smart D., Gunthorpe M.J., Tognetto M., Barbieri M., Campi B., Amadesi S., Gray J., Jerman J.C., Brough S.J., et al. Ethanol elicits and potentiates nociceptor responses via the vanilloid receptor-1. Nat Neurosci 5 (2002) 546-551
47. Siemens J., Zhou S., Piskorowski R., Nikai T., Lumpkin E.A., Basbaum A.I., King D., and Julius D. Spider toxins activate the capsaicin receptor to produce inflammatory pain. Nature 444 (2006) 208-212
48. Hill K., and Schaefer M. TRPA1 is differentially modulated by the amphipathic molecules trinitrophenol and chlorpromazine. J Biol Chem 282 (2007) 7145-7153
49. McNamara F.N., Randall A., and Gunthorpe M.J. Effects of piperine, the pungent component of black pepper, at the human vanilloid receptor (TRPV1). Br J Pharmacol 144 (2005) 781-790
50. Chung M.K., Lee H., Mizuno A., Suzuki M., and Caterina M.J. 2-Aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J Neurosci 24 (2004) 5177-5182
51. Hu H.Z., Gu Q., Wang C., Colton C.K., Tang J., Kinoshita-Kawada M., Lee L.Y., Wood J.D., and Zhu M.X. 2-Aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279 (2004) 35741-35748
52. Jordt S.E., and Julius D. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108 (2002) 421-430
53. Chuang H.H., Neuhausser W.M., and Julius D. The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43 (2004) 859-869
54. Hinman A., Chuang H.H., Bautista D.M., and Julius D. TRP channel activation by reversible covalent modification. Proc Natl Acad Sci USA 103 (2006) 19564-19568. This study proposes that TRPA1 is activated by electrophilic compounds covalently binding to cysteine and perhaps lysine residues in the channel. Using site-directed mutagenesis, three cysteine residues and a lysine residue are shown to be important for channel activation by these compounds.
55. Macpherson L.J., Dubin A.E., Evans M.J., Marr F., Schultz P.G., Cravatt B.F., and Patapoutian A. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445 (2007) 541-545. Hypothesizing that covalent binding is a mechanism for TRPA1 activation, the authors demonstrate that cysteine-reactive reagents bind directly to cysteine residues in TRPA1 using click chemistry and mass spectrometry. This group also identifies three cysteine residues that are required for normal channel activation by cysteine-reactive compounds.
56. Jordt S.E., Tominaga M., and Julius D. Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci USA 97 (2000) 8134-8139
57. Yoshida T., Inoue R., Morii T., Takahashi N., Yamamoto S., Hara Y., Tominaga M., Shimizu S., Sato Y., and Mori Y. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2 (2006) 596-607
58. Massullo P., Sumoza-Toledo A., Bhagat H., and Partida-Sanchez S. TRPM channels, calcium and redox sensors during innate immune responses. Semin Cell Dev Biol 17 (2006) 654-666
59. Poteser M., Graziani A., Rosker C., Eder P., Derler I., Kahr H., Zhu M.X., Romanin C., and Groschner K. TRPC3 and TRPC4 associate to form a redox-sensitive cation channel. Evidence for expression of native TRPC3-TRPC4 heteromeric channels in endothelial cells. J Biol Chem 281 (2006) 13588-13595
60. 2 is an essential requirement for TRPM8 function. See also [20].
61. 2+-dependent PKC activation mediates menthol-induced desensitization of transient receptor potential M8. Neurosci Lett 397 (2006) 140-144
62. Bhave G., Zhu W., Wang H., Brasier D.J., Oxford G.S., and Gereau R.W. cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35 (2002) 721-731
63. Numazaki M., Tominaga T., Takeuchi K., Murayama N., Toyooka H., and Tominaga M. Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc Natl Acad Sci USA 100 (2003) 8002-8006
64. 2, in which it is required for TRPV1 activity rather than inhibition [66,67].
65. 2 [66,67].
66. Chuang H.H., Prescott E.D., Kong H., Shields S., Jordt S.E., Basbaum A.I., Chao M.V., and Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411 (2001) 957-962
67. Prescott E.D., and Julius D. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300 (2003) 1284-1288
68. Zhang X., and McNaughton P.A. Why pain gets worse: the mechanism of heat hyperalgesia. J Gen Physiol 128 (2006) 491-493
69. Nilius B., Owsianik G., Voets T., and Peters J.A. Transient receptor potential cation channels in disease. Physiol Rev 87 (2007) 165-217
70. Peier A.M., Reeve A.J., Andersson D.A., Moqrich A., Earley T.J., Hergarden A.C., Story G.M., Colley S., Hogenesch J.B., McIntyre P., et al. A heat-sensitive TRP channel expressed in keratinocytes. Science 296 (2002) 2046-2049
71. Xu H., Ramsey I.S., Kotecha S.A., Moran M.M., Chong J.A., Lawson D., Ge P., Lilly J., Silos-Santiago I., Xie Y., et al. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418 (2002) 181-186
72. Talavera K., Yasumatsu K., Voets T., Droogmans G., Shigemura N., Ninomiya Y., Margolskee R.F., and Nilius B. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438 (2005) 1022-1025
73. Colburn R.W., Lubin M.L., Stone Jr. D.J., Wang Y., Lawrence D., D'Andrea M.R., Brandt M.R., Liu Y., Flores C.M., and Qin N. Attenuated cold sensitivity in TRPM8 null mice. Neuron 54 (2007) 379-386
74. Bautista D.M., Siemens J., Glazer J.M., Tsuruda P.R., Basbaum A.I., Stucky C.L., Jordt S.E., and Julius D. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448 (2007) 204-208
75. Sawada Y., Hosokawa H., Hori A., Matsumura K., and Kobayashi S. Cold sensitivity of recombinant TRPA1 channels. Brain Res 1160 (2007) 39-46. The authors show that in inside-out membrane patches excised from mTRPA1 expressing HEK293 cells, deep cooling (5-18 °C) and allyl isothiocyanate activate the same channels, which were inhibited by the TRPA1 antagonist camphor. Calcium free bath solutions were used in these experiments. It is also shown that AITC and deep cooling increase intracellular calcium in cultured DRG neurons, with most AITC sensitive neurons responding to cooling.
76. Lishko P.V., Procko E., Jin X., Phelps C.B., and Gaudet R. The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54 (2007) 905-918
77. Lukacs V., Thyagarajan B., Varnai P., Balla A., Balla T., and Rohacs T. Dual regulation of TRPV1 by phosphoinositides. J Neurosci 27 (2007) 7070-7080
78. Neeper M.P., Liu Y., Hutchinson T.L., Wang Y., Flores C.M., and Qin N. Activation properties of heterologously expressed mammalian TRPV2: evidence for species dependence. J Biol Chem 282 (2007) 15894-15902