Voltage-and temperature-dependent activation of TRPV3 channels is potentiated by receptor-mediated PI(4,5)P2 hydrolysis

Journal of General Physiology

Volumn 137, Issue 3, 2011, Pages 271-288

  Doerner, Julia F ^a,c,d   Hatt, Hanns ^a   Ramsey, I Scott ^b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHRM1 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MUSCARINIC RECEPTOR; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLINOSITOL KINASE; PHOSPHOLIPASE C BETA; PURINERGIC RECEPTOR; TRPV3 PROTEIN, HUMAN; VANILLOID RECEPTOR;

ARTICLE; BINDING SITE; CELL MEMBRANE POTENTIAL; CELL STRAIN HEK293; CHANNEL GATING; CHEMISTRY; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; HUMAN; HYDROLYSIS; KERATINOCYTE; KINETICS; METABOLISM; MUTATION; PATCH CLAMP; PROTEIN MOTIF; SECOND MESSENGER; TEMPERATURE;

1-PHOSPHATIDYLINOSITOL 4-KINASE; AMINO ACID MOTIFS; BINDING SITES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HEK293 CELLS; HUMANS; HYDROLYSIS; ION CHANNEL GATING; KERATINOCYTES; KINETICS; MEMBRANE POTENTIALS; MUTATION; PATCH-CLAMP TECHNIQUES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOLIPASE C BETA; RECEPTORS, MUSCARINIC; RECEPTORS, PURINERGIC; SECOND MESSENGER SYSTEMS; TEMPERATURE; TRANSFECTION; TRPV CATION CHANNELS;

EID: 79952148112     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200910388     Document Type: Article

References (91)

1. Albert, A. P., S. N. Saleh, and W. A. Large. 2008. Inhibition of native TRPC6 channel activity by phosphatidylinositol 4, 5-bisphosphate in mesenteric artery myocytes. J. Physiol. 586:3087-3095. doi:10.1113/jphysiol.2008.153676 (Pubitemid 351984692)
2. Anand, U., W. R. Otto, P. Facer, N. Zebda, I. Selmer, M. J. Gunthorpe, I. P. Chessell, M. Sinisi, R. Birch, and P. Anand. 2008. TRPA1 receptor localisation in the human peripheral nervous system and functional studies in cultured human and rat sensory neurons. Neurosci. Lett. 438:221-227. doi:10.1016/j.neulet.2008.04.007
3. Asakawa, M., T. Yoshioka, T. Matsutani, I. Hikita, M. Suzuki, I. Oshima, K. Tsukahara, A. Arimura, T. Horikawa, T. Hirasawa, and T. Sakata. 2006. Association of a mutation in TRPV3 with defective hair growth in rodents. J. Invest. Dermatol. 126:2664-2672. doi:10.1038/sj.jid.5700468 (Pubitemid 44764051)
4. Bang, S., K. Y. Kim, S. Yoo, S. H. Lee, and S. W. Hwang. 2007. Transient receptor potential V2 expressed in sensory neurons is activated by probenecid. Neurosci. Lett. 425:120-125. doi:10.1016/j.neulet.2007.08.035 (Pubitemid 47410367)
5. Bezanilla, F. 2008. Ion channels: from conductance to structure. Neuron. 60:456-468. doi:10.1016/j.neuron. 2008.10.035
6. 2 activation and thermosensation in TRP channels. Proc. Natl. Acad. Sci. USA. 104:10246-10251. doi:10.1073/pnas.0703420104 (Pubitemid 47175294)
7. Braun, M., K. Lelieur, and M. Kietzmann. 2006. Purinergic substances promote murine keratinocyte proliferation and enhance impaired wound healing in mice. Wound Repair Regen. 14:152-161. doi:10.1111/j.1743-6109.2006.00105.x
8. Chen, J., D. Kim, B. R. Bianchi, E. J. Cavanaugh, C. R. Faltynek, P. R. Kym, and R. M. Reilly. 2009. Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol. Pain. 5:3. doi:10.1186/1744-8069-5-3
9. Cheng, X., J. Jin, L. Hu, D. Shen, X. P. Dong, M. A. Samie, J. Knoff, B. Eisinger, M. L. Liu, S. M. Huang, et al. 2010. TRP channel regulates EGFR signaling in hair morphogenesis and skin barrier formation. Cell. 141:331-343. doi:10.1016/j.cell.2010.03.013
10. 2-mediated inhibition. Nature. 411:957-962. doi:10.1038/35082088 (Pubitemid 32601493)
11. Chung, M. K., H. Lee, and M. J. Caterina. 2003. Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J. Biol. Chem. 278:32037-32046. doi:10.1074/jbc. M303251200 (Pubitemid 37048392)
12. Chung, M. K., H. Lee, A. Mizuno, M. Suzuki, and M. J. Caterina. 2004a. 2-aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J. Neurosci. 24:5177-5182. doi:10.1523/JNEUROSCI.0934-04.2004 (Pubitemid 38725400)
13. Chung, M. K., H. Lee, A. Mizuno, M. Suzuki, and M. J. Caterina. 2004b. TRPV3 and TRPV4 mediate warmth-evoked currents in primary mouse keratinocytes. J. Biol. Chem. 279:21569-21575. doi:10.1074/jbc. M401872200 (Pubitemid 38656568)
14. Chung, M. K., A. D. Güler, and M. J. Caterina. 2005. Biphasic currents evoked by chemical or thermal activation of the heat-gated ion channel, TRPV3. J. Biol. Chem. 280:15928-15941. doi:10.1074/jbc. M500596200 (Pubitemid 40616716)
15. Chung, M. K., A. D. Güler, and M. J. Caterina. 2008. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat. Neurosci. 11:555-564. doi:10.1038/nn. 2102 (Pubitemid 351595196)
16. Clapham, D. E. 2003. TRP channels as cellular sensors. Nature. 426:517-524. doi:10.1038/nature02196 (Pubitemid 37522633)
17. Corsini, E., A. Primavera, M. Marinovich, and C. L. Galli. 1998. Selective induction of cell-associated interleukin-1α in murine keratinocytes by chemical allergens. Toxicology. 129:193-200. doi:10.1016/S0300-483X (98) 00088-2 (Pubitemid 29023147)
18. Estacion, M., W. G. Sinkins, and W. P. Schilling. 2001. Regulation of Drosophila transient receptor potential-like (TrpL) channels by phospholipase C-dependent mechanisms. J. Physiol. 530:1-19. doi:10.1111/j.1469-7793.2001. 0001m.x (Pubitemid 32998882)
19. Facer, P., M. A. Casula, G. D. Smith, C. D. Benham, I. P. Chessell, C. Bountra, M. Sinisi, R. Birch, and P. Anand. 2007. Differential expression of the capsaicin receptor TRPV1 and related novel receptors TRPV3, TRPV4 and TRPM8 in normal human tissues and changes in traumatic and diabetic neuropathy. BMC Neurol. 7:11. doi:10.1186/1471-2377-7-11 (Pubitemid 46979373)
20. Gamper, N., and M. S. Shapiro. 2007. Regulation of ion transport proteins by membrane phosphoinositides. Nat. Rev. Neurosci. 8:921-934. doi:10.1038/nrn2257 (Pubitemid 350146933)
21. Giustizieri, M. L., C. Albanesi, J. Fluhr, P. Gisondi, J. Norgauer, and G Girolomoni. 2004. H1 histamine receptor mediates inflammatory responses in human keratinocytes. J. Allergy Clin. Immunol. 114:1176-1182. doi:10.1016/j.jaci.2004.07.054 (Pubitemid 39469162)
22. Grandl, J., H. Hu, M. Bandell, B. Bursulaya, M. Schmidt, M. Petrus, and A. Patapoutian. 2008. Pore region of TRPV3 ion channel is specifically required for heat activation. Nat. Neurosci. 11:1007-1013. doi:10.1038/nn. 2169
23. Greig, A. V., C. Linge, and G Burnstock. 2008. Purinergic receptors are part of a signalling system for proliferation and differentiation in distinct cell lineages in human anagen hair follicles. Purinergic Signal. 4:331-338. doi:10.1007/s11302-008-9108-0
24. Gudermann, T., T. Hofmann, M. Mederos y Schnitzler, and A. Dietrich. 2004. Activation, subunit composition and physiological relevance of DAG-sensitive TRPC proteins. Novartis Found. Symp. 258:103-118. doi:10.1002/0470862580.ch8
25. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77:51-59. doi:10.1016/0378-1119 (89) 90358-2 (Pubitemid 19125653)
26. Hofmann, T., A. G. Obukhov, M. Schaefer, C. Harteneck, T. Gudermann, and G Schultz. 1999. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature. 397:259-263. doi:10.1038/16711 (Pubitemid 29051175)
27. 2+ requirement, and regulation of M current. J. Gen. Physiol. 126:243-262. doi:10.1085/jgp. 200509309 (Pubitemid 41252785)
28. 2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:267-305. doi:10.1085/jgp. 20028605 (Pubitemid 35014730)
29. Hu, H. Z., Q. Gu, C. Wang, C. K. Colton, J. Tang, M. Kinoshita-Kawada, L. Y. Lee, J. D. Wood, and M. X. Zhu. 2004. 2-aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J. Biol. Chem. 279:35741-35748. doi:10.1074/jbc. M404164200 (Pubitemid 39100579)
30. Hu, H. Z., R. Xiao, C. Wang, N. Gao, C. K. Colton, J. D. Wood, and M. X. Zhu. 2006. Potentiation of TRPV3 channel function by unsaturated fatty acids. J. Cell. Physiol. 208:201-212. doi:10.1002/jcp. 20648 (Pubitemid 43849006)
31. 2 and its stabilization by Gbetagamma. Nature. 391:803-806. doi:10.1038/35882 (Pubitemid 28099680)
32. 2. J. Neurosci. 28:13727-13737. doi:10.1523/JNEUROSCI.5741-07.2008
33. Imura, K., T. Yoshioka, T. Hirasawa, and T. Sakata. 2009. Role of TRPV3 in immune response to development of dermatitis. J. Inflamm. (Lond.). 6:17. doi:10.1186/1476-9255-6-17
34. Inoue, K., J. Hosoi, and M. Denda. 2007. Extracellular ATP has stimulatory effects on the expression and release of IL-6 via purinergic receptors in normal human epidermal keratinocytes. J. Invest. Dermatol. 127:362-371. doi:10.1038/sj.jid.5700526 (Pubitemid 46106915)
35. Jacobsen, F., D. Mittler, T. Hirsch, A. Gerhards, M. Lehnhardt, B. Voss, H. U. Steinau, and L. Steinstraesser. 2005. Transient cutaneous adenoviral gene therapy with human host defense peptide hCAP-18/LL-37 is effective for the treatment of burn wound infections. Gene Ther. 12:1494-1502. doi:10.1038/sj.gt.3302568 (Pubitemid 41508674)
36. Jin, H. W., H. Ichikawa, M. Fujita, T. Yamaai, K. Mukae, K. Nomura, and T. Sugimoto. 2005. Involvement of caspase cascade in capsaicin-induced apoptosis of dorsal root ganglion neurons. Brain Res. 1056:139-144. doi:10.1016/j. brainres.2005.07.025 (Pubitemid 41557701)
37. Karashima, Y., J. Prenen, V. Meseguer, G. Owsianik, T. Voets, and B. Nilius. 2008. Modulation of the transient receptor potential channel TRPA1 by phosphatidylinositol 4, 5-biphosphate manipulators. Pflugers Arch. 457:77-89. doi:10.1007/s00424-008-0493-6
38. +-current desensitization. Nat. Cell Biol. 2:507-514. doi:10.1038/35019544
39. 2+ waves in keratinocytes are transmitted to sensory neurons: the involvement of extracellular ATP and P2Y2 receptor activation. Biochem. J. 380:329-338. doi:10.1042/BJ20031089 (Pubitemid 38788103)
40. Lee, H., and M. J. Caterina. 2005. TRPV channels as thermosensory receptors in epithelial cells. Pflugers Arch. 451:160-167. doi:10.1007/s00424- 005-1438-y (Pubitemid 41424919)
41. Lee, W. K., S. W. Choi, H. R. Lee, E. J. Lee, K. H. Lee, and H. O. Kim. 2001. Purinoceptor-mediated calcium mobilization and proliferation in HaCaT keratinocytes. J. Dermatol. Sci. 25:97-105. doi:10.1016/S0923-1811 (00) 00117-1 (Pubitemid 32062990)
42. 2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc. Natl. Acad. Sci. USA. 100:15160-15165. doi:10.1073/pnas.2334159100 (Pubitemid 37518033)
43. Liu, B., and F. Qin. 2005. Functional control of cold-and mentholsensitive TRPM8 ion channels by phosphatidylinositol 4, 5-bisphosphate. J. Neurosci. 25:1674-1681. doi:10.1523/JNEUROSCI.3632-04.2005 (Pubitemid 40279272)
44. + channel in a lipid membranelike environment. Nature. 450:376-382. doi:10.1038/nature06265 (Pubitemid 350126743)
45. Lukacs, V., B. Thyagarajan, P. Varnai, A. Balla, T. Balla, and T. Rohács. 2007. Dual regulation of TRPV1 by phosphoinositides. J. Neurosci. 27:7070-7080. doi:10.1523/JNEUROSCI.1866-07.2007 (Pubitemid 47015892)
46. Lumpkin, E. A., and M. J. Caterina. 2007. Mechanisms of sensory transduction in the skin. Nature. 445:858-865. doi:10.1038/nature05662
47. Magleby, K. L. 2001. Kinetic gating mechanisms for BK channels: when complexity leads to simplicity. J. Gen. Physiol. 118:583-587. doi:10.1085/jgp. 118.5.583 (Pubitemid 33064293)
48. Mandadi, S., T. Sokabe, K. Shibasaki, K. Katanosaka, A. Mizuno, A. Moqrich, A. Patapoutian, T. Fukumi-Tominaga, K. Mizumura, and M. Tominaga. 2009. TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pflugers Arch. 458:1093-1102. doi:10.1007/s00424-009-0703-x
49. Matta, J. A., and G. P. Ahern. 2007. Voltage is a partial activator of rat thermosensitive TRP channels. J. Physiol. 585:469-482. doi:10.1113/jphysiol. 2007.144287 (Pubitemid 350193918)
50. Maurer, M., M. Opitz, B. M. Henz, and R. Paus. 1997. The mast cell products histamine and serotonin stimulate and TNF-alpha inhibits the proliferation of murine epidermal keratinocytes in situ. J. Dermatol. Sci. 16:79-84. doi:10.1016/S0923-1811 (97) 00043-1 (Pubitemid 28004778)
51. 2+-dependent desensitization of TRPV2 channels is mediated by hydrolysis of phosphatidylinositol 4, 5-bisphosphate. J. Neurosci. 30:13338-13347. doi:10.1523/JNEUROSCI.2108-10.2010
52. Montell, C. 2001. Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Sci. STKE. 2001: re1. doi:10.1126/stke.2001.90. re1
53. Moqrich, A., S. W. Hwang, T. J. Earley, M. J. Petrus, A. N. Murray, K. S. Spencer, M. Andahazy, G. M. Story, and A. Patapoutian. 2005. Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science. 307:1468-1472. doi:10.1126/science.1108609 (Pubitemid 40321945)
54. Musset, B., V. V. Cherny, D. Morgan, Y. Okamura, I. S. Ramsey, D. E. Clapham, and T. E. DeCoursey. 2008. Detailed comparison of expressed and native voltage-gated proton channel currents. J. Physiol. 586:2477-2486. doi:10.1113/jphysiol.2007.149427 (Pubitemid 351689806)
55. Nakanishi, S., K. J. Catt, and T. Balla. 1995. A wortmanninsensitive phosphatidylinositol 4-kinase that regulates hormonesensitive pools of inositolphospholipids. Proc. Natl. Acad. Sci. USA. 92:5317-5321. doi:10.1073/pnas.92.12.5317
56. Nilius, B. 2007. TRP channels in disease. Biochim. Biophys. Acta. 1772:805-812. (Pubitemid 47179880)
57. 2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4, 5-biphosphate. EMBO J. 25:467-478. doi:10.1038/sj.emboj.7600963 (Pubitemid 43237654)
58. Nilius, B., F. Mahieu, Y. Karashima, and T. Voets. 2007. Regulation of TRP channels: a voltage-lipid connection. Biochem. Soc. Trans. 35:105-108. doi:10.1042/BST0350105
59. Nilius, B., G. Owsianik, and T. Voets. 2008. Transient receptor potential channels meet phosphoinositides. EMBO J. 27:2809-2816. doi:10.1038/emboj.2008. 217
60. Otsuguro, K., J. Tang, Y. Tang, R. Xiao, M. Freichel, V. Tsvilovskyy, S. Ito, V. Flockerzi, M. X. Zhu, and A. V. Zholos. 2008. Isoformspecific inhibition of TRPC4 channel by phosphatidylinositol 4, 5-bisphosphate. J. Biol. Chem. 283:10026-10036. doi:10.1074/jbc. M707306200
61. Peier, A. M., A. J. Reeve, D. A. Andersson, A. Moqrich, T. J. Earley, A. C. Hergarden, G. M. Story, S. Colley, J. B. Hogenesch, P. McIntyre, et al. 2002. A heat-sensitive TRP channel expressed in keratinocytes. Science. 296:2046-2049. doi:10.1126/science.1073140 (Pubitemid 34627531)
62. Peralta, E. G., A. Ashkenazi, J. W. Winslow, J. Ramachandran, and D. J. Capon. 1988. Differential regulation of PI hydrolysis and adenylyl cyclase by muscarinic receptor subtypes. Nature. 334:434-437. doi:10.1038/334434a0
63. Phelps, C. B., R. R. Wang, S. S. Choo, and R. Gaudet. 2010. Differential regulation of TRPV1, TRPV3, and TRPV4 sensitivity through a conserved binding site on the ankyrin repeat domain. J. Biol. Chem. 285:731-740. doi:10.1074/jbc. M109.052548
64. Prescott, E. D., and D. Julius. 2003. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science. 300:1284-1288. doi:10.1126/science.1083646 (Pubitemid 36618238)
65. Ramsey, I. S., M. Delling, and D. E. Clapham. 2006. An introduction to TRP channels. Annu. Rev. Physiol. 68:619-647. doi:10.1146/annurev. physiol.68.040204.100431
66. Rohács, T. 2009. Phosphoinositide regulation of non-canonical transient receptor potential channels. Cell Calcium. 45:554-565. doi:10.1016/j.ceca.2009.03.011
67. 2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat. Neurosci. 8:626-634. doi:10.1038/nn1451 (Pubitemid 40594204)
68. Rosenhouse-Dantsker, A., and D. E. Logothetis. 2007. Molecular characteristics of phosphoinositide binding. Pflugers Arch. 455:45-53. doi:10.1007/s00424-007-0291-6 (Pubitemid 47403985)
69. (2) hydrolysis. Nat. Cell Biol. 4:329-336. (Pubitemid 34521027)
70. Smith, G. D., M. J. Gunthorpe, R. E. Kelsell, P. D. Hayes, P. Reilly, P. Facer, J. E. Wright, J. C. Jerman, J. P. Walhin, L. Ooi, et al. 2002. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature. 418:186-190. doi:10.1038/nature00894 (Pubitemid 34773773)
71. Ständer, S., C. Moormann, M. Schumacher, J. Buddenkotte, M. Artuc, V. Shpacovitch, T. Brzoska, U. Lippert, B. M. Henz, T. A. Luger, et al. 2004. Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp. Dermatol. 13:129-139. doi:10.1111/j.0906-6705.2004.0178.x (Pubitemid 38380276)
72. Stein, A. T., C. A. Ufret-Vincenty, L. Hua, L. F. Santana, and S. E. Gordon. 2006. Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J. Gen. Physiol. 128:509-522. doi:10.1085/jgp. 200609576 (Pubitemid 44664629)
73. Sugimoto, T., C. Xiao, and H. Ichikawa. 1998. Neonatal primary neuronal death induced by capsaicin and axotomy involves an apoptotic mechanism. Brain Res. 807:147-154. doi:10.1016/S0006-8993 (98) 00788-4 (Pubitemid 29005246)
74. Suh, B. C., and B. Hille. 2007. Regulation of KCNQ channels by manipulation of phosphoinositides. J. Physiol. 582:911-916. doi:10.1113/ jphysiol.2007.132647 (Pubitemid 47104327)
75. Suh, B. C., and B. Hille. 2008. PIP2 is a necessary cofactor for ion channel function: how and why? Annu Rev Biophys. 37:175-195. doi:10.1146/annurev. biophys.37.032807.125859
76. + ions depends on the presence of phosphatidylinositol phosphates. Proc. Natl. Acad. Sci. USA. 95:1307-1312. doi:10.1073/pnas.95.3.1307 (Pubitemid 28124954)
77. Ufret-Vincenty, C. A., R. M. Klein, L. Hua, J. Angueyra, and S. E. Gordon. 2011. Localization of the PIP2 sensor of TRPV1 ion channels. J. Biol. Chem. In press.
78. 3H]inositollabeled phosphoinositide pools. J. Cell Biol. 143:501-510. doi:10.1083/jcb.143.2.501 (Pubitemid 28487866)
79. Voets, T., J. Prenen, J. Vriens, H. Watanabe, A. Janssens, U. Wissenbach, M. Bödding, G. Droogmans, and B. Nilius. 2002. Molecular determinants of permeation through the cation channel TRPV4. J. Biol. Chem. 277:33704-33710. doi:10.1074/jbc. M204828200
80. Voets, T., G. Owsianik, A. Janssens, K. Talavera, and B. Nilius. 2007. TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat. Chem. Biol. 3:174-182. doi:10.1038/nchembio862
81. Wiedemann, C., T. Schäfer, and M. M. Burger. 1996. Chromaffin granule-associated phosphatidylinositol 4-kinase activity is required for stimulated secretion. EMBO J. 15:2094-2101. (Pubitemid 26141126)
82. Xiao, R., J. Tang, C. Wang, C. K. Colton, J. Tian, and M. X. Zhu. 2008a. Calcium plays a central role in the sensitization of TRPV3 channel to repetitive stimulations. J. Biol. Chem. 283:6162-6174. doi:10.1074/jbc. M706535200
83. Xiao, R., J. Tian, J. Tang, and M. X. Zhu. 2008b. The TRPV3 mutation associated with the hairless phenotype in rodents is constitutively active. Cell Calcium. 43:334-343. doi:10.1016/j.ceca.2007.06.004 (Pubitemid 351298569)
84. Xu, H., I. S. Ramsey, S. A. Kotecha, M. M. Moran, J. A. Chong, D. Lawson, P. Ge, J. Lilly, I. Silos-Santiago, Y. Xie, et al. 2002. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature. 418:181-186. doi:10.1038/nature00882 (Pubitemid 34773772)
85. Xu, H., N. T. Blair, and D. E. Clapham. 2005. Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J. Neurosci. 25:8924-8937. doi:10.1523/JNEUROSCI.2574-05.2005 (Pubitemid 41384461)
86. Xu, H., M. Delling, J. C. Jun, and D. E. Clapham. 2006. Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat. Neurosci. 9:628-635. doi:10.1038/nn1692 (Pubitemid 44012260)
87. Yoshioka, T., K. Imura, M. Asakawa, M. Suzuki, I. Oshima, T. Hirasawa, T. Sakata, T. Horikawa, and A. Arimura. 2009. Impact of the Gly573Ser substitution in TRPV3 on the development of allergic and pruritic dermatitis in mice. J. Invest. Dermatol. 129:714-722. doi:10.1038/jid.2008.245
88. (2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron. 37:963-975. doi:10.1016/S0896-6273 (03) 00125-9 (Pubitemid 36398301)
89. Zhang, Z., H. Okawa, Y. Wang, and E. R. Liman. 2005. Phosphatidylinositol 4, 5-bisphosphate rescues TRPM4 channels from desensitization. J. Biol. Chem. 280:39185-39192. doi:10.1074/jbc. M506965200 (Pubitemid 41713870)
90. (2) release from keratinocytes by proteaseactivated receptor-2-activating peptide in ICR mice. Int. Immunopharmacol. 9:1332-1336. doi:10.1016/j.intimp. 2009.08.006
91. Zufall, F., H. Hatt, and S. Firestein. 1993. Rapid application and removal of second messengers to cyclic nucleotide-gated channels from olfactory epithelium. Proc. Natl. Acad. Sci. USA. 90:9335-9339. doi:10.1073/pnas.90.20. 9335 (Pubitemid 23315778)