Transient receptor potential channels as targets for phytochemicals

ACS Chemical Neuroscience

Volumn 5, Issue 11, 2014, Pages 1117-1130

  Premkumar, Louis S ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Botanical; Neuropeptide; Phytochemical; TRP channel

Indexed keywords

ALLICIN; ALLYL ISOTHIOCYANATE; ALPHA SANSHOOL; CANNABICHROMENE; CANNABIDIVARIN; CANNABIGEROL; CAPSAICIN; CINEOLE; CINNAMALDEHYDE; CURCUMIN; DEHYDROLIGUSTILIDE; DIALLYLDISULFIDE; DICENTRINE; EUGENOL; HYPERFORIN; LIGUSTILIDE; LINALOOL; MENTHOL; NABIXIMOLS; NICOTINE; PACLITAXEL; PARADOL; PIPERINE; PLANT MEDICINAL PRODUCT; SHOGAOL; TETRAHYDROCANNABIVARIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRIPTOLIDE; UMBELLULINE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

CELL MEMBRANE PERMEABILITY; DRUG BIOAVAILABILITY; DRUG EFFECT; DRUG EXCRETION; DRUG METABOLISM; DRUG SYNTHESIS; DRUG TARGETING; RECEPTOR POTENTIAL; REVIEW; SEQUENCE HOMOLOGY; ANIMAL; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM;

ANIMALS; HUMANS; PHYTOCHEMICALS; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84912532627     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn500094a     Document Type: Review

References (159)

1. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D. (1997) The capsaicin receptor: a heata-ctivated ion channel in the pain pathway. Nature 389, 816-824.
2. Cosens, D. J., and Manning, A. (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224, 285-287.
3. Montell, C., and Rubin, G. M. (1989) Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2, 1313-1323.
4. Montell, C. (2005) The TRP superfamily of cation channels. Sci. STKE, re3.
5. 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., McIntyre, P., Jegla, T., Bevan, S., and Patapoutian, A. (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819-829.
6. Jordt, S. E., Bautista, D. M., Chuang, H. H., McKemy, D. D., Zygmunt, P. M., Hogestatt, E. D., Meng, I. D., and Julius, D. (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265.
7. 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., and Patapoutian, A. (2002) A TRP channel that senses cold stimuli and menthol. Cell 108, 705-715.
8. McKemy, D. D., Neuhausser, W. M., and Julius, D. (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416, 52-58.
9. Cao, E., Liao, M., Cheng, Y., and Julius, D. (2013) TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504, 113-118.
10. Liao, M., Cao, E., Julius, D., and Cheng, Y. (2013) Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504, 107-112.
11. Bikman, B. T., Zheng, D., Pories, W. J., Chapman, W., Pender, J. R., Bowden, R. C., Reed, M. A., Cortright, R. N., Tapscott, E. B., Houmard, J. A., Tanner, C. J., Lee, J., and Dohm, G. L. (2008) Mechanism for improved insulin sensitivity after gastric bypass surgery. J. Clin. Endocrinol. Metab. 93, 4656-4663.
12. Corey, D. P., Garcia-Anoveros, J., Holt, J. R., Kwan, K. Y., Lin, S. Y., Vollrath, M. A., Amalfitano, A., Cheung, E. L., Derfler, B. H., Duggan, A., Geleoc, G. S., Gray, P. A., Hoffman, M. P., Rehm, H. L., Tamasauskas, D., and Zhang, D. S. (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432, 723-730.
13. Bandell, M., Story, G. M., Hwang, S. W., Viswanath, V., Eid, S. R., Petrus, M. J., Earley, T. J., Patapoutian, A., Bautista, D. M., Movahed, P., Hinman, A., Axelsson, H. E., Sterner, O., Hogestatt, E. D., Julius, D., Jordt, S. E., and Zygmunt, P. M. (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41, 849-857.
14. Bautista, D. M., Movahed, P., Hinman, A., Axelsson, H. E., Sterner, O., Hogestatt, E. D., Julius, D., Jordt, S. E., and Zygmunt, P. M. (2005) Pungent products from garlic activate the sensory ion channel TRPA1. Proc. Natl. Acad. Sci. U.S.A. 102, 12248-12252.
15. Macpherson, L. J., Geierstanger, B. H., Viswanath, V., Bandell, M., Eid, S. R., Hwang, S., and Patapoutian, A. (2005) The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr. Biol. 15, 929-934.
16. Kwan, K. Y., Allchorne, A. J., Vollrath, M. A., Christensen, A. P., Zhang, D. S., Woolf, C. J., and Corey, D. P. (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50, 277-289.
17. Andersson, D. A., Gentry, C., Moss, S., and Bevan, S. (2008) Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J. Neurosci. 28, 2485-2494.
18. Bessac, B. F., Sivula, M., von Hehn, C. A., Escalera, J., Cohn, L., and Jordt, S. E. (2008) TRPA1 is a major oxidant sensor in murine airway sensory neurons. J. Clin. Invest. 118, 1899-1910.
19. Cao, D. S., Zhong, L., Hsieh, T. H., Abooj, M., Bishnoi, M., Hughes, L., and Premkumar, L. S. (2012) Expression of transient receptor potential ankyrin 1 (TRPA1) and its role in insulin release from rat pancreatic beta cells. PloS One 7, e38005.
20. Brownlee, M. (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813-820.
21. Nagata, K., Duggan, A., Kumar, G., and Garcia-Anoveros, J. (2005) Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J. Neurosci. 25, 4052-4061.
22. Obata, K., Katsura, H., Mizushima, T., Yamanaka, H., Kobayashi, K., Dai, Y., Fukuoka, T., Tokunaga, A., Tominaga, M., and Noguchi, K. (2005) TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J. Clin. Invest. 115, 2393-2401.
23. Hinman, A., Chuang, H. H., Bautista, D. M., and Julius, D. (2006) TRP channel activation by reversible covalent modification. Proc. Natl. Acad. Sci. U.S.A. 103, 19564-19568.
24. Raisinghani, M., Zhong, L., Jeffry, J. A., Bishnoi, M., Pabbidi, R. M., Pimentel, F., Cao, D. S., Evans, M. S., and Premkumar, L. S. (2011) Activation characteristics of transient receptor potential ankyrin 1 and its role in nociception. Am. J. Physiol.: Cell Physiol. 301, C587-600.
25. Premkumar, L. S., and Raisinghani, M. (2006) Nociceptors in cardiovascular functions: complex interplay as a result of cyclo-oxygenase inhibition. Mol. Pain 2, 26.
26. Khan, A., Safdar, M., Ali Khan, M. M., Khattak, K. N., and Anderson, R. A. (2003) Cinnamon improves glucose and lipids of people with type 2 diabetes. Diabetes Care 26, 3215-3218.
27. Hlebowicz, J., Darwiche, G., Bjorgell, O., and Almer, L. O. (2007) Effect of cinnamon on postprandial blood glucose, gastric emptying, and satiety in healthy subjects. Am. J. Clin. Nutr. 85, 1552-1556.
28. Lissiman, E., Bhasale, A. L., and Cohen, M. (2009) Garlic for the common cold. Cochrane Database Syst. Rev. 3, CD006206.
29. Lissiman, E., Bhasale, A. L., and Cohen, M. (2012) Garlic for the common cold. Cochrane Database Syst. Rev. 14, CD006206.
30. Cutler, R. R., Odent, M., Hajj-Ahmad, H., Maharjan, S., Bennett, N. J., Josling, P. D., Ball, V., Hatton, P., and Dall'Antonia, M. (2009) In vitro activity of an aqueous allicin extract and a novel allicin topical gel formulation against Lancefield group B streptococci. J. Antimicrob. Chemother. 63, 151-154.
31. Khanum, F., Anilakumar, K. R., and Viswanathan, K. R. (2004) Anticarcinogenic properties of garlic: a review. Crit. Rev. Food. Sci. Nutr. 44, 479-488.
32. Shenoy, N. R., and Choughuley, A. S. (1992) Inhibitory effect of diet related sulphydryl compounds on the formation of carcinogenic nitrosamines. Cancer Lett. 65, 227-232.
33. Koizumi, K., Iwasaki, Y., Narukawa, M., Iitsuka, Y., Fukao, T., Seki, T., Ariga, T., and Watanabe, T. (2009) Diallyl sulfides in garlic activate both TRPA1 and TRPV1. Biochem. Biophys. Res. Commun. 382, 545-548.
34. Leamy, A. W., Shukla, P., McAlexander, M. A., Carr, M. J., and Ghatta, S. (2011) Curcumin (( E,E)-1,7-bis(4-hydroxy-3-methoxy-phenyl)-1,6-heptadiene-3,5-dione) activates and desensitizes the nociceptor ion channel TRPA1. Neurosci. Lett. 503, 157-162.
35. Gupta, S. C., Patchva, S., and Aggarwal, B. B. (2013) Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J. 15, 195-218.
36. Song, Y., Sonawane, N. D., Salinas, D., Qian, L., Pedemonte, N., Galietta, L. J., and Verkman, A. S. (2004) Evidence against the rescue of defective DeltaF508-CFTR cellular processing by curcumin in cell culture and mouse models. J. Biol. Chem. 279, 40629-40633.
37. Gao, J., Zhou, H., Lei, T., Zhou, L., Li, W., Li, X., and Yang, B. (2011) Curcumin inhibits renal cyst formation and enlargement in vitro by regulating intracellular signaling pathways. Eur. J. Pharmacol. 654, 92-99.
38. Sohma, Y., Yu, Y. C., and Hwang, T. C. (2013) Curcumin and genistein: the combined effects on disease-associated CFTR mutants and their clinical implications. Curr. Pharm. Des. 19, 3521-3528.
39. Nassini, R., Materazzi, S., Vriens, J., Prenen, J., Benemei, S., De Siena, G., la Marca, G., Andre, E., Preti, D., Avonto, C., Sadofsky, L., Di Marzo, V., De Petrocellis, L., Dussor, G., Porreca, F., Taglialatela-Scafati, O., Appendino, G., Nilius, B., and Geppetti, P. (2012) The 'headache tree' via umbellulone and TRPA1 activates the trigeminovascular system. Brain 135, 376-390.
40. Zhong, J., Pollastro, F., Prenen, J., Zhu, Z., Appendino, G., and Nilius, B. (2011) Ligustilide: a novel TRPA1 modulator. Pfluegers Arch. 462, 841-849.
41. Materazzi, S., Fusi, C., Benemei, S., Pedretti, P., Patacchini, R., Nilius, B., Prenen, J., Creminon, C., Geppetti, P., and Nassini, R. (2012) TRPA1 and TRPV4 mediate paclitaxel-induced peripheral neuropathy in mice via a glutathione-sensitive mechanism. Pfluegers Arch. 463, 561-569.
42. De Petrocellis, L., Vellani, V., Schiano-Moriello, A., Marini, P., Magherini, P. C., Orlando, P., and Di Marzo, V. (2008) Plant-derived cannabinoids modulate the activity of transient receptor potential channels of ankyrin type-1 and melastatin type-8. J. Pharmacol. Exp. Ther. 325, 1007-1015.
43. Montrucchio, D. P., Cordova, M. M., and Santos, A. R. (2013) Plant derived aporphinic alkaloid S-(+)-dicentrine induces antinociceptive effect in both acute and chronic inflammatory pain models: evidence for a role of TRPA1 channels. PloS One 8, e67730.
44. Talavera, K., Gees, M., Karashima, Y., Meseguer, V. M., Vanoirbeek, J. A., Damann, N., Everaerts, W., Benoit, M., Janssens, A., Vennekens, R., Viana, F., Nemery, B., Nilius, B., and Voets, T. (2009) Nicotine activates the chemosensory cation channel TRPA1. Nat. Neurosci. 12, 1293-1299.
45. Riera, C. E., Menozzi-Smarrito, C., Affolter, M., Michlig, S., Munari, C., Robert, F., Vogel, H., Simon, S. A., and Le Coutre, J. (2009) Compounds from Sichuan and Melegueta peppers activate, covalently and non-covalently, TRPA1 and TRPV1 channels. Br. J. Pharmacol. 157, 1398-1409.
46. Vazquez, G., Wedel, B. J., Aziz, O., Trebak, M., and Putney, J. W., Jr. (2004) The mammalian TRPC cation channels. Biochim. Biophys. Acta 1742, 21-36.
47. Birnbaumer, L. (2009) The TRPC class of ion channels: a critical review of their roles in slow, sustained increases in intracellular Ca(2+) concentrations. Annu. Rev. Pharmacol. Toxicol. 49, 395-426.
48. Leuner, K., Kazanski, V., Muller, M., Essin, K., Henke, B., Gollasch, M., Harteneck, C., and Muller, W. E. (2007) Hyperforin-a key constituent of St. John's wort specifically activates TRPC6 channels. FASEB J. 21, 4101-4111.
49. Sikand, P., and Premkumar, L. S. (2007) Potentiation of glutamatergic synaptic transmission by protein kinase C-mediated sensitization of TRPV1 at the first sensory synapse. J. Physiol. 581, 631-647.
50. Cao, D. S., Yu, S. Q., and Premkumar, L. S. (2009) Modulation of transient receptor potential Vanilloid 4-mediated membrane currents and synaptic transmission by protein kinase C. Mol. Pain 5, 5.
51. Jeffry, J. A., Yu, S. Q., Sikand, P., Parihar, A., Evans, M. S., and Premkumar, L. S. (2009) Selective targeting of TRPV1 expressing sensory nerve terminals in the spinal cord for long lasting analgesia. PloS One 4, e7021.
52. Evans, M. S., Cheng, X., Jeffry, J. A., Disney, K. E., and Premkumar, L. S. (2012) Sumatriptan inhibits TRPV1 channels in trigeminal neurons. Headache 52, 773-784.
53. Zhou, J., Du, W., Zhou, K., Tai, Y., Yao, H., Jia, Y., and Ding, Y. (2008) Critical role of TRPC6 channels in the formation of excitatory synapses. Nat. Neurosci. 11, 741-743.
54. Nilius, B., and Owsianik, G. (2011) The transient receptor potential family of ion channels. Genome Biol. 12, 218.
55. Carakostas, M. C., Curry, L. L., Boileau, A. C., and Brusick, D. J. (2008) Overview: the history, technical function and safety of rebaudioside A, a naturally occurring steviol glycoside, for use in food and beverages. Food Chem. Toxicol. 46 (Suppl 7), S1-S10.
56. Medler, K. F. (2011) Multiple roles for TRPs in the taste system: not your typical TRPs. Adv. Exp. Med. Biol. 704, 831-846.
57. Sprous, D., and Palmer, K. R. (2010) The T1R2/T1R3 sweet receptor and TRPM5 ion channel taste targets with therapeutic potential. Prog. Mol. Biol. Transl. Sci. 91, 151-208.
58. Palmer, R. K. (2007) The pharmacology and signaling of bitter, sweet, and umami taste sensing. Mol. Interv. 7, 87-98.
59. Depoortere, I. (2014) Taste receptors of the gut: emerging roles in health and disease. Gut 63, 179-190.
60. Kaji, I., Karaki, S. I., and Kuwahara, A. (2014) Taste Sensing in the Colon. Curr. Pharm. Des. 20, 2766-2774.
61. Premkumar, L. S., Raisinghani, M., Pingle, S. C., Long, C., and Pimentel, F. (2005) Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. J. Neurosci. 25, 11322-11329.
62. Tsuzuki, K., Xing, H., Ling, J., and Gu, J. G. (2004) Mentholinduced Ca2+ release from presynaptic Ca2+ stores potentiates sensory synaptic transmission. J. Neurosci. 24, 762-771.
63. Tsavaler, L., Shapero, M. H., Morkowski, S., and Laus, R. (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res. 61, 3760-3769.
64. Uhl, G. R., Walther, D., Behm, F. M., and Rose, J. E. (2011) Menthol preference among smokers: association with TRPA1 variants. Nicotine Tob. Res. 13, 1311-1315.
65. Hans, M., Wilhelm, M., and Swandulla, D. (2012) Menthol suppresses nicotinic acetylcholine receptor functioning in sensory neurons via allosteric modulation. Chem. Senses 37, 463-469.
66. Willis, D. N., Liu, B., Ha, M. A., Jordt, S. E., and Morris, J. B. (2011) Menthol attenuates respiratory irritation responses to multiple cigarette smoke irritants. FASEB J. 25, 4434-4444.
67. Leuenroth, S. J., Okuhara, D., Shotwell, J. D., Markowitz, G. S., Yu, Z., Somlo, S., and Crews, C. M. (2007) Triptolide is a traditional Chinese medicine-derived inhibitor of polycystic kidney disease. Proc. Natl. Acad. Sci. U.S.A. 104, 4389-4394.
68. Szallasi, A., and Blumberg, P. M. (1999) Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol. Rev. 51, 159-212.
69. Vennekens, R., Owsianik, G., and Nilius, B. (2008) Vanilloid transient receptor potential cation channels: an overview. Curr. Pharm. Des. 14, 18-31.
70. Vriens, J., Nilius, B., and Vennekens, R. (2008) Herbal compounds and toxins modulating TRP channels. Curr. Neuropharmacol. 6, 79-96.
71. Hellwig, N., Albrecht, N., Harteneck, C., Schultz, G., and Schaefer, M. (2005) Homo- and heteromeric assembly of TRPV channel subunits. J. Cell Sci. 118, 917-928.
72. Tominaga, M., Caterina, M. J., Malmberg, A. B., Rosen, T. A., Gilbert, H., Skinner, K., Raumann, B. E., Basbaum, A. I., and Julius, D. (1998) The cloned capsaicin receptor integrates multiple painproducing stimuli. Neuron 21, 531-543.
73. Nakatsuka, T., Furue, H., Yoshimura, M., and Gu, J. G. (2002) Activation of central terminal vanilloid receptor-1 receptors and alpha beta-methylene-ATP-sensitive P2X receptors reveals a converged synaptic activity onto the deep dorsal horn neurons of the spinal cord. J. Neurosci. 22, 1228-1237.
74. Baccei, M. L., Bardoni, R., and Fitzgerald, M. (2003) Development of nociceptive synaptic inputs to the neonatal rat dorsal horn: glutamate release by capsaicin and menthol. J. Physiol. 549, 231-242.
75. Kim, Y. H., Back, S. K., Davies, A. J., Jeong, H., Jo, H. J., Chung, G., Na, H. S., Bae, Y. C., Kim, S. J., Kim, J. S., Jung, S. J., and Oh, S. B. (2012) TRPV1 in GABAergic interneurons mediates neuropathic mechanical allodynia and disinhibition of the nociceptive circuitry in the spinal cord. Neuron 74, 640-647.
76. Doyle, M. W., Bailey, T. W., Jin, Y. H., and Andresen, M. C. (2002) Vanilloid receptors presynaptically modulate cranial visceral afferent synaptic transmission in nucleus tractus solitarius. J. Neurosci. 22, 8222-8229.
77. Marinelli, S., Di Marzo, V., Berretta, N., Matias, I., Maccarrone, M., Bernardi, G., and Mercuri, N. B. (2003) Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J. Neurosci. 23, 3136-3144.
78. Marinelli, S., Vaughan, C. W., Christie, M. J., and Connor, M. (2002) Capsaicin activation of glutamatergic synaptic transmission in the rat locus coeruleus in vitro. J. Physiol. 543, 531-540.
79. Gibson, H. E., Edwards, J. G., Page, R. S., Van Hook, M. J., and Kauer, J. A. (2008) TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 57, 746-759.
80. Grueter, B. A., Brasnjo, G., and Malenka, R. C. (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat. Neurosci. 13, 1519-1525.
81. Premkumar, L. S., and Ahern, G. P. (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408, 985-990.
82. Caterina, M. J., and Julius, D. (2001) The vanilloid receptor: a molecular gateway to the pain pathway. Annu. Rev. Neurosci. 24, 487-517.
83. Minke, B., and Cook, B. (2002) TRP channel proteins and signal transduction. Physiol. Rev. 82, 429-472.
84. Clapham, D. E. (2003) TRP channels as cellular sensors. Nature 426, 517-524.
85. Premkumar, L. S., and Bishnoi, M. (2011) Disease-related changes in TRPV1 expression and its implications for drug development. Curr. Top. Med. Chem. 11, 2192-2209.
86. Julius, D. (2013) TRP channels and pain. Annu. Rev. Cell Dev. Biol. 29, 355-384.
87. Mezey, E., Toth, Z. E., Cortright, D. N., Arzubi, M. K., Krause, J. E., Elde, R., Guo, A., Blumberg, P. M., and Szallasi, A. (2000) 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. U.S.A. 97, 3655-3660.
88. Huang, S. M., Bisogno, T., Trevisani, M., Al-Hayani, A., De Petrocellis, L., Fezza, F., Tognetto, M., Petros, T. J., Krey, J. F., Chu, C. J., Miller, J. D., Davies, S. N., Geppetti, P., Walker, J. M., and Di Marzo, V. (2002) An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc. Natl. Acad. Sci. U.S.A. 99, 8400-8405.
89. Mishra, S. K., Tisel, S. M., Orestes, P., Bhangoo, S. K., and Hoon, M. A. (2011) TRPV1-lineage neurons are required for thermal sensation. EMBO J. 30, 582-593.
90. Cavanaugh, D. J., Chesler, A. T., Braz, J. M., Shah, N. M., Julius, D., and Basbaum, A. I. (2011) Restriction of transient receptor potential vanilloid-1 to the peptidergic subset of primary afferent neurons follows its developmental downregulation in nonpeptidergic neurons. J. Neurosci. 31, 10119-10127.
91. Lundberg, J. M., Martling, C. R., and Saria, A. (1983) Substance P and capsaicin-induced contraction of human bronchi. Acta Physiol. Scand. 119, 49-53.
92. Mitchell, J. A., Williams, F. M., Williams, T. J., and Larkin, S. W. (1997) Role of nitric oxide in the dilator actions of capsaicin-sensitive nerves in the rabbit coronary circulation. Neuropeptides 31, 333-338.
93. Zygmunt, P. M., Petersson, J., Andersson, D. A., Chuang, H., Sorgard, M., Di Marzo, V., Julius, D., Hogestatt, E. D., and Wang, Y. (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400, 452-457.
94. Birder, L. A., Nakamura, Y., Kiss, S., Nealen, M. L., Barrick, S., Kanai, A. J., Wang, E., Ruiz, G., De Groat, W. C., Apodaca, G., Watkins, S., and Caterina, M. J. (2002) Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat. Neurosci. 5, 856-860.
95. Cruz, F., and Dinis, P. (2007) Resiniferatoxin and botulinum toxin type A for treatment of lower urinary tract symptoms. Neurourol. Urodyn. 26, 920-927.
96. Varga, A., Nemeth, J., Szabo, A., McDougall, J. J., Zhang, C., Elekes, K., Pinter, E., Szolcsanyi, J., and Helyes, Z. (2005) Effects of the novel TRPV1 receptor antagonist SB366791 in vitro and in vivo in the rat. Neurosci. Lett. 385, 137-142.
97. Gavva, N. R. (2008) Body-temperature maintenance as the predominant function of the vanilloid receptor TRPV1. Trends Pharmacol. Sci. 29, 550-557.
98. Lehto, S. G., Tamir, R., Deng, H., Klionsky, L., Kuang, R., Le, A., Lee, D., Louis, J. C., Magal, E., Manning, B. H., Rubino, J., Surapaneni, S., Tamayo, N., Wang, T., Wang, J., Wang, J., Wang, W., Youngblood, B., Zhang, M., Zhu, D., Norman, M. H., and Gavva, N. R. (2008) Antihyperalgesic effects of (R, E)-N-(2-hydroxy-2,3-dihydro-1 H-inden-4-yl)-3-(2-(piperidin-1-yl)-4-(trifluorom ethyl)phenyl)-acrylamide (AMG8562), a novel transient receptor potential vanilloid type 1 modulator that does not cause hyperthermia in rats. J. Pharmacol. Exp. Ther. 326, 218-229.
99. Pabbidi, R. M., Yu, S. Q., Peng, S., Khardori, R., Pauza, M. E., and Premkumar, L. S. (2008) Influence of TRPV1 on diabetes-induced alterations in thermal pain sensitivity. Mol. Pain 4, 9.
100. Van Buren, J. J., Bhat, S., Rotello, R., Pauza, M. E., and Premkumar, L. S. (2005) Sensitization and translocation of TRPV1 by insulin and IGF-I. Mol. Pain 1, 17.
101. Bishnoi, M., Bosgraaf, C. A., Abooj, M., Zhong, L., and Premkumar, L. S. (2011) Streptozotocin-induced early thermal hyperalgesia is independent of glycemic state of rats: role of transient receptor potential vanilloid 1(TRPV1) and inflammatory mediators. Mol. Pain 7, 52.
102. Akiba, Y., Kato, S., Katsube, K., Nakamura, M., Takeuchi, K., Ishii, H., and Hibi, T. (2004) Transient receptor potential vanilloid subfamily 1 expressed in pancreatic islet beta cells modulates insulin secretion in rats. Biochem. Biophys. Res. Commun. 321, 219-225.
103. Razavi, R., Chan, Y., Afifiyan, F. N., Liu, X. J., Wan, X., Yantha, J., Tsui, H., Tang, L., Tsai, S., Santamaria, P., Driver, J. P., Serreze, D., Salter, M. W., and Dosch, H. M. (2006) TRPV1+ sensory neurons control beta cell stress and islet inflammation in autoimmune diabetes. Cell 127, 1123-1135.
104. Wang, X., Miyares, R. L., and Ahern, G. P. (2005) Oleoylethanolamide excites vagal sensory neurones, induces visceral pain and reduces short-term food intake in mice via capsaicin receptor TRPV1. J. Physiol. 564, 541-547.
105. Ahern, G. P. (2013) Transient receptor potential channels and energy homeostasis. Trends Endocrinol. Metab. 24, 554-560.
106. Kindt, S., Vos, R., Blondeau, K., and Tack, J. (2009) Influence of intra-oesophageal capsaicin instillation on heartburn induction and oesophageal sensitivity in man. Neurogastroenterol. Motil. 21, 1032-e1082.
107. Okumi, H., Tashima, K., Matsumoto, K., Namiki, T., Terasawa, K., and Horie, S. (2012) Dietary agonists of TRPV1 inhibit gastric acid secretion in mice. Planta Med. 78, 1801-1806.
108. Raisinghani, M., Pabbidi, R. M., and Premkumar, L. S. (2005) Activation of transient receptor potential vanilloid 1 (TRPV1) by resiniferatoxin. J. Physiol. 567, 771-786.
109. Roberts, J. C., Davis, J. B., and Benham, C. D. (2004) [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res. 995, 176-183.
110. Chou, M. Z., Mtui, T., Gao, Y. D., Kohler, M., and Middleton, R. E. (2004) Resiniferatoxin binds to the capsaicin receptor (TRPV1) near the extracellular side of the S4 transmembrane domain. Biochemistry 43, 2501-2511.
111. Jung, J., Lee, S. Y., Hwang, S. W., Cho, H., Shin, J., Kang, Y. S., Kim, S., and Oh, U. (2002) Agonist recognition sites in the cytosolic tails of vanilloid receptor 1. J. Biol. Chem. 277, 44448-44454.
112. Gavva, N. R., Klionsky, L., Qu, Y., Shi, L., Tamir, R., Edenson, S., Zhang, T. J., Viswanadhan, V. N., Toth, A., Pearce, L. V., Vanderah, T. W., Porreca, F., Blumberg, P. M., Lile, J., Sun, Y., Wild, K., Louis, J. C., and Treanor, J. J. (2004) Molecular determinants of vanilloid sensitivity in TRPV1. J. Biol. Chem. 279, 20283-20295.
113. Brown, D. C., Iadarola, M. J., Perkowski, S. Z., Erin, H., Shofer, F., Laszlo, K. J., Olah, Z., and Mannes, A. J. (2005) Physiologic and antinociceptive effects of intrathecal resiniferatoxin in a canine bone cancer model. Anesthesiology 103, 1052-1059.
114. Iadarola, M. J., and Mannes, A. J. (2011) The vanilloid agonist resiniferatoxin for interventional-based pain control. Curr. Top. Med. Chem. 11, 2171-2179.
115. Yang, B. H., Piao, Z. G., Kim, Y. B., Lee, C. H., Lee, J. K., Park, K., Kim, J. S., and Oh, S. B. (2003) (2003) Activation of vanilloid receptor 1 (VR1) by eugenol. J. Dent. Res. 82, 781-785.
116. Behrendt, H. J., Germann, T., Gillen, C., Hatt, H., and Jostock, R. (2004) 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, 737-45.
117. McNamara, F. N., Randall, A., and Gunthorpe, M. J. (2005) Effects of piperine, the pungent component of black pepper, at the human vanilloid receptor (TRPV1). Br. J. Pharmacol. 144, 781-790.
118. Bhardwaj, R. K., Glaeser, H., Becquemont, L., Klotz, U., Gupta, S. K., and Fromm, M. F. (2002) Piperine, a major constituent of black pepper, inhibits human P-glycoprotein and CYP3A4. J. Pharmacol. Exp. Ther. 302, 645-650.
119. Bisogno, T., Hanus, L., De Petrocellis, L., Tchilibon, S., Ponde, D. E., Brandi, I., Moriello, A. S., Davis, J. B., Mechoulam, R., and Di Marzo, V. (2001) Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br. J. Pharmacol. 134, 845-852.
120. Xu, H., Blair, N. T., and Clapham, D. E. (2005) Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J. Neurosci. 25, 8924-8937.
121. Pearce, L. V., Petukhov, P. A., Szabo, T., Kedei, N., Bizik, F., Kozikowski, A. P., and Blumberg, P. M. (2004) Evodiamine functions as an agonist for the vanilloid receptor TRPV1. Org. Biomol. Chem. 2, 2281-2286.
122. Morera, E., De Petrocellis, L., Morera, L., Moriello, A. S., Nalli, M., Di Marzo, V., and Ortar, G. (2012) Synthesis and biological evaluation of [6]-gingerol analogues as transient receptor potential channel TRPV1 and TRPA1 modulators. Bioorg. Med. Chem. Lett. 22, 1674-1677.
123. Xu, H., Delling, M., Jun, J. C., and Clapham, D. E. (2006) Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat. Neurosci. 9, 628-635.
124. Andre, E., Campi, B., Trevisani, M., Ferreira, J., Malheiros, A., Yunes, R. A., Calixto, J. B., and Geppetti, P. (2006) Pharmacological characterisation of the plant sesquiterpenes polygodial and drimanial as vanilloid receptor agonists. Biochem. Pharmacol. 71, 1248-1254.
125. Iwasaki, Y., Tanabe, M., Kayama, Y., Abe, M., Kashio, M., Koizumi, K., Okumura, Y., Morimitsu, Y., Tominaga, M., Ozawa, Y., and Watanabe, T. (2009) Miogadial and miogatrial with alpha,beta-unsaturated 1,4-dialdehyde moieties - novel and potent TRPA1 agonists. Life Sci. 85, 60-69.
126. Lübbert, M., Kyereme, J., Schöbel, N., Beltrán, L., Wetzel, C. H., and Hatt, H. (2013) Transient receptor potential channels encode volatile chemicals sensed by rat trigeminal ganglion neurons. PLoS One 8, e77998.
127. Trevisan, G., Rossato, M. F., Walker, C. I., Klafke, J. Z., Rosa, F., Oliveira, S. M., Tonello, R., Guerra, G. P., Boligon, A. A., Zanon, R. B., Athayde, M. L., and Ferreira, J. (2012) Identification of the plant steroid alpha-spinasterol as a novel transient receptor potential vanilloid 1 antagonist with antinociceptive properties. J. Pharmacol. Exp. Ther. 343, 258-269.
128. Birnbaumer, L., Yildirim, E., and Abramowitz, J. (2003) A comparison of the genes coding for canonical TRP channels and their M, V and P relatives. Cell Calcium 33, 419-432.
129. 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., Bevan, S., and Patapoutian, A. (2002) A heat-sensitive TRP channel expressed in keratinocytes. Science 296, 2046-2049.
130. 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. (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307, 1468-1472.
131. 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., DiStefano, P. S., Curtis, R., and Clapham, D. E. (2002) TRPV3 is a calciumpermeable temperature-sensitive cation channel. Nature 418, 181-186.
132. Smith, G. D., Gunthorpe, M. J., Kelsell, R. E., Hayes, P. D., Reilly, P., Facer, P., Wright, J. E., Jerman, J. C., Walhin, J. P., Ooi, L., Egerton, J., Charles, K. J., Smart, D., Randall, A. D., Anand, P., and Davis, J. B. (2002) TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418, 186-190.
133. Gopinath, P., Wan, E., Holdcroft, A., Facer, P., Davis, J. B., Smith, G. D., Bountra, C., and Anand, P. (2005) Increased capsaicin receptor TRPV1 in skin nerve fibres and related vanilloid receptors TRPV3 and TRPV4 in keratinocytes in human breast pain. BMC Women's Health 5, 2.
134. Facer, P., Casula, M. A., Smith, G. D., Benham, C. D., Chessell, I. P., Bountra, C., Sinisi, M., Birch, R., and Anand, P. (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.
135. Huang, S. M., Lee, H., Chung, M. K., Park, U., Yu, Y. Y., Bradshaw, H. B., Coulombe, P. A., Walker, J. M., and Caterina, M. J. (2008) Overexpressed transient receptor potential vanilloid 3 ion channels in skin keratinocytes modulate pain sensitivity via prostaglandin E2. J. Neurosci. 28, 13727-13737.
136. Hammarstrom, S., Hamberg, M., Samuelsson, B., Duell, E. A., Stawiski, M., and Voorhees, J. J. (1975) Increased concentrations of nonesterified arachidonic acid, 12L-hydroxy-5,8,10,14-eicosatetraenoic acid, prostaglandin E2, and prostaglandin F2alpha in epidermis of psoriasis. Proc. Natl. Acad. Sci. U.S.A. 72, 5130-5134.
137. Brash, A. R. (2001) Arachidonic acid as a bioactive molecule. J. Clin. Invest. 107, 1339-1345.
138. Mandadi, S., Sokabe, T., Shibasaki, K., Katanosaka, K., Mizuno, A., Moqrich, A., Patapoutian, A., Fukumi-Tominaga, T., Mizumura, K., and Tominaga, M. (2009) TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pfluegers Arch. 458, 1093-2002.
139. Xiao, R., Tang, J., Wang, C., Colton, C. K., Tian, J., and Zhu, M. X. (2008) Calcium plays a central role in the sensitization of TRPV3 channel to repetitive stimulations. J. Biol. Chem. 283, 6162-6174.
140. Imura, K. (2007) Influence of TRPV3 mutation on hair growth cycle in mice. Biochem. Biophys. Res. Commun. 363, 479-483.
141. Asakawa, M., Yoshioka, T., Matsutani, T., Hikita, I., Suzuki, M., Oshima, I., Tsukahara, K., Arimura, A., Horikawa, T., Hirasawa, T., and Sakata, T. (2006) Association of a mutation in TRPV3 with defective hair growth in rodents. J. Invest. Dermatol. 126, 2664-2672.
142. Macpherson, L. J., Hwang, S. W., Miyamoto, T., Dubin, A. E., Patapoutian, A., and Story, G. M. (2006) More than cool: promiscuous relationships of menthol and other sensory compounds. Mol. Cell Neurosci. 32, 335-343.
143. Moussaieff, A., Rimmerman, N., Bregman, T., Straiker, A., Felder, C. C., Shoham, S., Kashman, Y., Huang, S. M., Lee, H., Shohami, E., Mackie, K., Caterina, M. J., Walker, J. M., Fride, E., and Mechoulam, R. (2008) Incensole acetate, an incense component, elicits psychoactivity by activating TRPV3 channels in the brain. FASEB J. 22, 3024-3034.
144. De Petrocellis, L., Orlando, P., Moriello, A. S., Aviello, G., Stott, C., Izzo, A. A., and Di Marzo, V. (2012) Cannabinoid actions at TRPV channels: effects on TRPV3 and TRPV4 and their potential relevance to gastrointestinal inflammation. Acta Physiol. 204, 255-266.
145. Strotmann, R., Harteneck, C., Nunnenmacher, K., Schultz, G., and Plant, T. D. (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat. Cell Biol. 2, 695-702.
146. Watanabe, H., Davis, J. B., Smart, D., Jerman, J. C., Smith, G. D., Hayes, P., Vriens, J., Cairns, W., Wissenbach, U., Prenen, J., Flockerzi, V., Droogmans, G., Benham, C. D., and Nilius, B. (2002) Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J. Biol. Chem. 277, 13569-13577.
147. Suzuki, M., Mizuno, A., Kodaira, K., and Imai, M. (2003) Impaired pressure sensation in mice lacking TRPV4. J. Biol. Chem. 278, 22664-22668.
148. Nilius, B., Droogmans, G., and Wondergem, R. (2003) Transient receptor potential channels in endothelium: solving the calcium entry puzzle? Endothelium 10, 5-15.
149. Kohler, R., Heyken, W. T., Heinau, P., Schubert, R., Si, H., Kacik, M., Busch, C., Grgic, I., Maier, T., and Hoyer, J. (2006) Evidence for a functional role of endothelial transient receptor potential V4 in shear stress-induced vasodilatation. Arterioscler., Thromb., Vasc. Biol. 26, 1495-15502.
150. Watanabe, H., Vriens, J., Suh, S. H., Benham, C. D., Droogmans, G., and Nilius, B. (2002) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J. Biol. Chem. 277, 47044-47051.
151. Watanabe, H., Vriens, J., Prenen, J., Droogmans, G., Voets, T., and Nilius, B. (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424, 434-438.
152. Loukin, S. H., Su, Z., and Kung, C. (2009) Hypotonic shocks activate rat TRPV4 in yeast in the absence of polyunsaturated fatty acids. FEBS Lett. 583, 754-758.
153. Cao, D. S., Yu, S. Q., and Premkumar, L. S. (2009) Modulation of transient receptor potential Vanilloid 4-mediated membrane currents and synaptic transmission by protein kinase C. Mol. Pain 5, 5.
154. Matthews, B. D., Thodeti, C. K., Tytell, J. D., Mammoto, A., Overby, D. R., and Ingber, D. E. (2010) Ultra-rapid activation of TRPV4 ion channels by mechanical forces applied to cell surface beta1 integrins. Integr. Biol. 2, 435-442.
155. Alessandri-Haber, N., Dina, O. A., Joseph, E. K., Reichling, D. B., and Levine, J. D. (2008) Interaction of transient receptor potential vanilloid 4, integrin, and SRC tyrosine kinase in mechanical hyperalgesia. J. Neurosci. 28, 1046-1057.
156. Chen, X., Alessandri-Haber, N., and Levine, J. D. (2007) Marked attenuation of inflammatory mediator-induced C-fiber sensitization for mechanical and hypotonic stimuli in TRPV4-/- mice. Mol. Pain 3, 31.
157. Alessandri-Haber, N., Yeh, J. J., Boyd, A. E., Parada, C. A., Chen, X., Reichling, D. B., and Levine, J. D. (2003) Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39, 497-511.
158. Alessandri-Haber, N., Joseph, E., Dina, O. A., Liedtke, W., and Levine, J. D. (2005) TRPV4 mediates pain-related behavior induced by mild hypertonic stimuli in the presence of inflammatory mediator. Pain 118, 70-79.
159. Smith, P. L., Maloney, K. N., Pothen, R. G., Clardy, J., and Clapham, D. E. (2006) Bisandrographolide from Andrographis paniculata activates TRPV4 channels. J. Biol. Chem. 281, 29897-29904.