Modulation of temperature-sensitive TRP channels

Seminars in Cell and Developmental Biology

Volumn 17, Issue 6, 2006, Pages 638-645

  Huang, Jiehong ^a   Zhang, Xuming ^a   McNaughton, Peter A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Intracellular signalling; Protein kinase; Sensory transduction; Thermal sensation

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ENZYME PHOSPHORYLATION; HEART CONTRACTION; HEAT SENSITIVITY; HUMAN; ION TRANSPORT; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; TEMPERATURE MEASUREMENT;

ANIMALIA;

EID: 33846366006     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2006.11.002     Document Type: Review

References (114)

1. Cosens D.J., and Manning A. Abnormal electroretinogram from a Drosophila mutant. Nature 224 (1969) 285-287
2. Montell C., and Rubin G.M. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2 (1989) 1313-1323
3. 2+ channel in Drosophila photoreceptors. Neuron 8 (1992) 643-651
4. Ramsey I.S., Delling M., and Clapham D.E. An introduction to trp channels. Annu Rev Physiol 68 (2006) 619-647
5. Clapham D.E. TRP channels as cellular sensors. Nature 426 (2003) 517-524
6. Mosavi L.K., Cammett T.J., Desrosiers D.C., and Peng Z.Y. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13 (2004) 1435-1448
7. 2+/calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol 123 (2004) 53-62
8. Voets T., and Nilius B. TRPs make sense. J Membr Biol 192 (2003) 1-8
9. Garcia-Sanz N., Fernandez-Carvajal A., Morenilla-Palao C., Planells-Cases R., Fajardo-Sanchez E., Fernandez-Ballester G., et al. Identification of a tetramerization domain in the C terminus of the vanilloid receptor. J Neurosci 24 (2004) 5307-5314
10. Hille B. Ionic channels of excitable membranes (2001), Sinauer Associates, Sunderland, MA
11. 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
12. Guler A.D., Lee H., Iida T., Shimizu I., Tominaga M., and Caterina M. Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22 (2002) 6408-6414
13. Peier A.M., Reeve A.J., Andersson D.A., Moqrich A., Earley T.J., Hergarden A.C., et al. A heat-sensitive TRP channel expressed in keratinocytes. Science 296 (2002) 2046-2049
14. Smith G.D., Gunthorpe M.J., Kelsell R.E., Hayes P.D., Reilly P., Facer P., et al. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418 (2002) 186-190
15. 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
16. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., and Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398 (1999) 436-441
17. 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
18. 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 108 (2002) 705-715
19. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112 (2003) 819-829
20. Bautista D.M., Movahed P., Hinman A., Axelsson H.E., Sterner O., Hogestatt E.D., et al. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 102 (2005) 12248-12252
21. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124 (2006) 1269-1282
22. Talavera K., Yasumatsu K., Voets T., Droogmans G., Shigemura N., Ninomiya Y., et al. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438 (2005) 1022-1025
23. Togashi K., Hara Y., Tominaga T., Higashi T., Konishi Y., Mori Y., et al. TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25 (2006) 1804-1815
24. Cesare P., and McNaughton P.A. A novel heat-activated current in nociceptive neurons, and its sensitization by bradykinin. Proc Natl Acad Sci USA 93 (1996) 15435-15439
25. Mezey E., Toth Z.E., Cortright D.N., Arzubi M.K., Krause J.E., Elde R., et al. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc Natl Acad Sci USA 97 (2000) 3655-3660
26. Roberts J.C., Davis J.B., and Benham C.D. [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res 995 (2004) 176-183
27. Southall M.D., Li T., Gharibova L.S., Pei Y., Nicol G.D., and Travers J.B. Activation of epidermal vanilloid receptor-1 induces release of proinflammatory mediators in human keratinocytes. J Pharmacol Exp Ther 304 (2003) 217-222
28. Kato S., Aihara E., Nakamura A., Xin H., Matsui H., Kohama K., et al. Expression of vanilloid receptors in rat gastric epithelial cells: role in cellular protection. Biochem Pharmacol 66 (2003) 1115-1121
29. Birder L.A., Kanai A.J., de Groat W.C., Kiss S., Nealen M.L., Burke N.E., et al. Vanilloid receptor expression suggests a sensory role for urinary bladder epithelial cells. Proc Natl Acad Sci USA 98 (2001) 13396-13401
30. Welch J.M., Simon S.A., and Reinhart P.H. The activation mechanism of rat vanilloid receptor 1 by capsaicin involves the pore domain and differs from the activation by either acid or heat. Proc Natl Acad Sci USA 97 (2000) 13889-13894
31. Vlachova V., Teisinger J., Susankova K., Lyfenko A., Ettrich R., and Vyklicky L. Functional role of C-terminal cytoplasmic tail of rat vanilloid receptor 1. J Neurosci 23 (2003) 1340-1350
32. Liu B., Hui K., and Qin F. Thermodynamics of heat activation of single capsaicin ion channels VR1. Biophys J 85 (2003) 2988-3006
33. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21 (1998) 531-543
34. Caterina M.J., and Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24 (2001) 487-517
35. Vellani V., Mapplebeck S., Moriondo A., Davis J.B., and McNaughton P.A. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534 (2001) 813-825
36. Trevisani M., Smart D., Gunthorpe M.J., Tognetto M., Barbieri M., Campi B., et al. Ethanol elicits and potentiates nociceptor responses via the vanilloid receptor-1. Nat Neurosci 5 (2002) 546-551
37. Ross R.A. Anandamide and vanilloid TRPV1 receptors. Br J Pharmacol 140 (2003) 790-801
38. Hwang S.W., Cho H., Kwak J., Lee S.Y., Kang C.J., Jung J., et al. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97 (2000) 6155-6160
39. Ma Q.P. Vanilloid receptor homologue, VRL1, is expressed by both A- and C-fiber sensory neurons. Neuroreport 12 (2001) 3693-3695
40. Hellwig N., Albrecht N., Harteneck C., Schultz G., and Schaefer M. Homo- and heteromeric assembly of TRPV channel subunits. J Cell Sci 118 (2005) 917-928
41. Liapi A., and Wood J.N. Extensive co-localization and heteromultimer formation of the vanilloid receptor-like protein TRPV2 and the capsaicin receptor TRPV1 in the adult rat cerebral cortex. Eur J Neurosci 22 (2005) 825-834
42. Rutter A.R., Ma Q.P., Leveridge M., and Bonnert T.P. Heteromerization and colocalization of TrpV1 and TrpV2 in mammalian cell lines and rat dorsal root ganglia. Neuroreport 16 (2005) 1735-1739
43. Kashiba H., Uchida Y., Takeda D., Nishigori A., Ueda Y., Kuribayashi K., et al. TRPV2-immunoreactive intrinsic neurons in the rat intestine. Neurosci Lett 366 (2004) 193-196
44. Wainwright A., Rutter A.R., Seabrook G.R., Reilly K., and Oliver K.R. Discrete expression of TRPV2 within the hypothalamo-neurohypophysial system: Implications for regulatory activity within the hypothalamic-pituitary-adrenal axis. J Comp Neurol 474 (2004) 24-42
45. Muraki K., Iwata Y., Katanosaka Y., Ito T., Ohya S., Shigekawa M., et al. TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93 (2003) 829-838
46. Xu H., Ramsey I.S., Kotecha S.A., Moran M.M., Chong J.A., Lawson D., et al. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418 (2002) 181-186
47. Moqrich A., Hwang S.W., Earley T.J., Petrus M.J., Murray A.N., Spencer K.S., et al. Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307 (2005) 1468-1472
48. Strotmann R., Harteneck C., Nunnenmacher K., Schultz G., and Plant T.D. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2 (2000) 695-702
49. Liedtke W., Choe Y., Marti-Renom M.A., Bell A.M., Denis C.S., Sali A., et al. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103 (2000) 525-535
50. 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
51. Suzuki M., Mizuno A., Kodaira K., and Imai M. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278 (2003) 22664-22668
52. Voets T., Prenen J., Vriens J., Watanabe H., Janssens A., Wissenbach U., et al. Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem 277 (2002) 33704-33710
53. 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
54. Reid G. ThermoTRP channels and cold sensing: what are they really up to?. Pflugers Arch 451 (2005) 250-263
55. 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
56. Weil A., Moore S.E., Waite N.J., Randall A., and Gunthorpe M.J. Conservation of functional and pharmacological properties in the distantly related temperature sensors TRVP1 and TRPM8. Mol Pharmacol 68 (2005) 518-527
57. Reid G., Babes A., and Pluteanu F. A cold- and menthol-activated current in rat dorsal root ganglion neurones: properties and role in cold transduction. J Physiol 545 (2002) 595-614
58. Bandell M., Story G.M., Hwang S.W., Viswanath V., Eid S.R., Petrus M.J., et al. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41 (2004) 849-857
59. Jordt S.E., Bautista D.M., Chuang H.H., McKemy D.D., Zygmunt P.M., Hogestatt E.D., et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427 (2004) 260-265
60. Babes A., Zorzon D., and Reid G. Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur J Neurosci 20 (2004) 2276-2282
61. Kwan K.Y., Allchorne A.J., Vollrath M.A., Christensen A.P., Zhang D.S., Woolf C.J., et al. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50 (2006) 277-289
62. Babes A., Zorzon D., and Reid G. A novel type of cold-sensitive neuron in rat dorsal root ganglia with rapid adaptation to cooling stimuli. Eur J Neurosci 24 (2006) 691-698
63. Obata K., Katsura H., Mizushima T., Yamanaka H., Kobayashi K., Dai Y., et al. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 115 (2005) 2393-2401
64. Katsura H., Obata K., Mizushima T., Yamanaka H., Kobayashi K., Dai Y., et al. Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats. Exp Neurol 200 (2006) 112-123
65. Reid G., and Flonta M.L. Ion channels activated by cold and menthol in cultured rat dorsal root ganglion neurones. Neurosci Lett 324 (2002) 164-168
66. 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
67. Numazaki M., Tominaga T., Toyooka H., and Tominaga M. Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J Biol Chem 277 (2002) 13375-13378
68. Bhave G., Hu H.J., Glauner K.S., Zhu W., Wang H., Brasier D.J., et al. Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 100 (2003) 12480-12485
69. 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
70. 2+-dependent desensitization in the vanilloid receptor TRPV1 by calcineurin and cAMP-dependent protein kinase. J Biol Chem 280 (2005) 13424-13432
71. Jeske N.A., Patwardhan A.M., Gamper N., Price T.J., Akopian A.N., and Hargreaves K.M. Cannabinoid WIN 55,212-2 Regulates TRPV1 Phosphorylation in Sensory Neurons. J Biol Chem 281 (2006) 32879-32890
72. Zhang X., Huang J., and McNaughton P.A. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24 (2005) 4211-4223
73. Bhave G., Karim F., Carlton S.M., and Gereau R.W. Peripheral group I metabotropic glutamate receptors modulate nociception in mice. Nat Neurosci 4 (2001) 417-423
74. Jung J., Shin J.S., Lee S.Y., Hwang S.W., Koo J., Cho H., et al. Phosphorylation of vanilloid receptor 1 by Ca+2/calmodulin-dependent kinase II regulates its vanilloid binding. J Biol Chem (2003)
75. Xu H., Zhao H., Tian W., Yoshida K., Roullet J.B., and Cohen D.M. Regulation of a transient receptor potential (TRP) channel by tyrosine phosphorylation. SRC family kinase-dependent tyrosine phosphorylation of TRPV4 on TYR-253 mediates its response to hypotonic stress. J Biol Chem 278 (2003) 11520-11527
76. 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
77. Gao X., Wu L., and O'Neil R.G. Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278 (2003) 27129-27137
78. 2+ entry in HEK 293 cells transiently expressing human TRPV4. Br J Pharmacol 140 (2003) 413-421
79. Reid G., and Flonta M.L. Cold current in thermoreceptive neurons. Nature 413 (2001) 480
80. Linte R.M., Ciobanu C., Reid G., and Babes A. Desensitization of cold- and menthol-sensitive rat dorsal root ganglion neurones by inflammatory mediators. Exp Brain Res (2006)
81. Premkumar L.S., Raisinghani M., Pingle S.C., Long C., and Pimentel F. Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. J Neurosci 25 (2005) 11322-11329
82. 2+-dependent PKC activation mediates menthol-induced desensitization of transient receptor potential M8. Neurosci Lett 397 (2006) 140-144
83. Stokes A.J., Shimoda L.M., Koblan-Huberson M., Adra C.N., and Turner H. A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells. J Exp Med 200 (2004) 137-147
84. Shin J., Cho H., Hwang S.W., Jung J., Shin C.Y., Lee S.Y., et al. Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc Natl Acad Sci USA 99 (2002) 10150-10155
85. Watanabe H., Vriens J., Prenen J., Droogmans G., Voets T., and Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424 (2003) 434-438
86. Hu H.Z., Xiao R., Wang C., Gao N., Colton C.K., Wood J.D., et al. Potentiation of TRPV3 channel function by unsaturated fatty acids. J Cell Physiol 208 (2006) 201-212
87. Cesare P., Dekker L.V., Sardini A., Parker P.J., and McNaughton P.A. Specific involvement of PKC-epsilon in sensitization of the neuronal response to painful heat. Neuron 23 (1999) 617-624
88. Chuang H.H., Prescott E.D., Kong H., Shields S., Jordt S.E., Basbaum A.I., et al. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411 (2001) 957-962
89. Prescott E.D., and Julius D. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300 (2003) 1284-1288
90. Bonnington J.K., and McNaughton P.A. Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. J Physiol 551 (2003) 433-446
91. Zhuang Z.Y., Xu H., Clapham D.E., and Ji R.R. Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 24 (2004) 8300-8309
92. Liu B., Ma W., Ryu S., and Qin F. Inhibitory modulation of distal C-terminal on protein kinase C-dependent phospho-regulation of rat TRPV1 receptors. J Physiol 560 (2004) 627-638
93. Liu B., Zhang C., and Qin F. Functional recovery from desensitization of vanilloid receptor TRPV1 requires resynthesis of phosphatidylinositol 4,5-bisphosphate. J Neurosci 25 (2005) 4835-4843
94. Stein A.T., Ufret-Vincenty C.A., Hua L., Santana L.F., and Gordon S.E. Phosphoinositide 3-Kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the membrane. J Gen Physiol 128 (2006) 509-522
95. 2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J 25 (2006) 467-478
96. Rohacs T., Lopes C.M., Michailidis I., and Logothetis D.E. PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8 (2005) 626-634
97. 2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci USA 100 (2003) 15160-15165
98. Zhang Z., Okawa H., Wang Y., and Liman E.R. Phosphatidylinositol 4,5-bisphosphate rescues TRPM4 channels from desensitization. J Biol Chem 280 (2005) 39185-39192
99. McMahon S.B., and Koltzenburg M. Wall and Melzack's textbook of pain (2005), Churchill Livingston, London
100. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000) 306-313
101. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (2000) 183-187
102. Moriyama T., Higashi T., Togashi K., Iida T., Segi E., Sugimoto Y., et al. Sensitization of TRPV1 by EP1 and IP reveals peripheral nociceptive mechanism of prostaglandins. Mol Pain 1 (2005) 3
103. Van Buren J.J., Bhat S., Rotello R., Pauza M.E., and Premkumar L.S. Sensitization and translocation of TRPV1 by insulin and IGF-I. Mol Pain 1 (2005) 17
104. Morenilla-Palao C., Planells-Cases R., Garcia-Sanz N., and Ferrer-Montiel A. Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J Biol Chem 279 (2004) 25665-25672
105. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
106. Bron R., Klesse L.J., Shah K., Parada L.F., and Winter J. Activation of Ras is necessary and sufficient for upregulation of vanilloid receptor type 1 in sensory neurons by neurotrophic factors. Mol Cell Neurosci 22 (2003) 118-132
107. Puntambekar P., Mukherjea D., Jajoo S., and Ramkumar V. Essential role of Rac1/NADPH oxidase in nerve growth factor induction of TRPV1 expression. J Neurochem 95 (2005) 1689-1703
108. Huang J., Zhang X., and McNaughton P.A. Inflammatory pain: the cellular basis of heat hyperalgesia. Curr Neuropharmacol 4 (2006) 197-206
109. Kanzaki M., Zhang Y.Q., Mashima H., Li L., Shibata H., and Kojima I. Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1 (1999) 165-170
110. Boels K., Glassmeier G., Herrmann D., Riedel I.B., Hampe W., Kojima I., et al. The neuropeptide head activator induces activation and translocation of the growth-factor-regulated Ca(2+)-permeable channel GRC. J Cell Sci 114 (2001) 3599-3606
111. Penna A., Juvin V., Chemin J., Compan V., Monet M., and Rassendren F.A. PI3-kinase promotes TRPV2 activity independently of channel translocation to the plasma membrane. Cell Calcium (2006)
112. Todaka H., Taniguchi J., Satoh J., Mizuno A., and Suzuki M. Warm temperature-sensitive transient receptor potential vanilloid 4 (TRPV4) plays an essential role in thermal hyperalgesia. J Biol Chem 279 (2004) 35133-35138
113. Alessandri-Haber N., Joseph E., Dina O.A., Liedtke W., and Levine J.D. TRPV4 mediates pain-related behavior induced by mild hypertonic stimuli in the presence of inflammatory mediator. Pain 118 (2005) 70-79
114. 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 16 (2006) 1591-1605