TRP channels as sensors and signal integrators of redox status changes

Frontiers in Pharmacology

Volumn OCT, Issue , 2011, Pages

  Takahashi, Nobuaki ^a   Mori, Yasuo ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Ca2+ signaling; Cysteine modification; Oxidative stress; S nitrosylation; TRP channels; TRPA1; TRPC5; TRPV1

Indexed keywords

CALCIUM PERMEABLE CATION CHANNEL; CATION CHANNEL; CAVEOLIN 1; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYSTEINE; CYSTEINE SULFHYDRYL; DITHIOTHREITOL; ELECTROPHILE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GUANYLATE CYCLASE; HYDROGEN PEROXIDE; I KAPPA B KINASE BETA; KELCH LIKE ECH ASSOCIATED PROTEIN 1; NITRIC OXIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; THIOL DERIVATIVE; THIOREDOXIN; TRANSCRIPTION FACTOR RELA; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 5; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M2; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ARTICLE; CALCIUM BINDING; CALCIUM TRANSPORT; COMPLEX FORMATION; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; INFLAMMATORY PAIN; NERVE FIBER C; NERVOUS SYSTEM INFLAMMATION; NITROSYLATION; NOCICEPTIVE STIMULATION; OXIDATION REDUCTION STATE; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RESPIRATORY FUNCTION; SENSORY NERVE CELL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VASODILATATION;

EID: 84860511405     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2011.00058     Document Type: Article

References (155)

1. Aarts, M., Iihara, K., Wei, W. L., Xiong, Z. G., Arundine, M., Cerwinski, W., MacDonald, J. F., and Tymianski, M. (2003). A key role for TRPM7 chan- nels in anoxic neuronal death. Cell 115, 863-877.
2. Amadesi, S., Cottrell, G. S., Divino, L., Chapman, K., Grady, E. F., Bautista, F., Karanjia, R., Barajas-Lopez, C., Vanner, S., Vergnolle, N., and Bunnett, N. W. (2006). Protease-activated receptor 2 sensitizes TRPV1 by protein kinase C epsilon- and A-dependent mechanisms in rats and mice. J. Physiol. 575, 555-571.
3. Amadesi, S., Nie, J., Vergnolle, N., Cot- trell, G. S., Grady, E. F., Trevisani, M., Manni, C., Geppetti, P., McRoberts, J. A., Ennes, H., Davis, J. B., Mayer, E. A., and Bunnett, N. W. (2004). Protease-activated receptor 2 sensi- tizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J. Neurosci. 24, 4300-4312.
4. Andersson, D. A., Gentry, C., Moss, S., and Bevan, S. (2008). Tran- sient receptor potential A1 is a sen- sory receptor for multiple products of oxidative stress. J. Neurosci. 28, 2485-2494.
5. Andrè, E., Campi, B., Materazzi, S., Trevisani, M., Amadesi, S., Massi, D., Creminon, C., Vaksman, N., Nassini, R., Civelli, M., Baraldi, P. G., Poole, D. P., Bunnett, N. W., Geppetti, P., and Patac- chini, R. (2008). Cigarette smoke- induced neurogenic inflammation is mediated by α,β-unsaturated alde- hydes and the TRPA1 receptor in rodents. J. Clin. Invest. 118, 2574-2582.
6. Andrè, E., Gatti, R., Trevisani, M., Preti, D., Baraldi, P. G., Patacchini, R., and Geppetti, P. (2009). Transient receptor potential ankyrin recep- tor 1 is a novel target for pro- tussive agents. Br. J. Pharmacol. 158, 1621-1628.
7. Aracena-Parks, P., Goonasekera, S. A., Gilman, C. P., Dirksen, R. T., Hidalgo, C., and Hamilton, S. L. (2006). Identification of cys- teines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine recep- tortype1.J. Biol. Chem. 281, 40354-40368.
8. Bandell, M., Story, G. M., Hwang, S. W., Viswanath, V., Eid, S. R., Petrus, M. J., Earley, T. J., and Patapoutian, A. (2004). Noxious cold ion channel TRPA1 is activated by pungent com- pounds and bradykinin. Neuron 25, 849-857.
9. Barouch, L. A., Harrison, R. W., Skaf, M. W., Rosas, G. O., Cappola, T. P., Kobeissi, Z. A., Hobai, I. A., Lemmon, C. A., Burnett, A. L., O'Rourke, B., Rodriguez, E. R., Huang, P. L., Lima, J. A., Berkowitz, D. E., and Hare, J. M. (2002). Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416, 337-339.
10. 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. (2006). TRPA1 mediates the inflammatory actions of envi- ronmental irritants and proalgesic agents. Cell 124, 1269-1282.
11. Bautista, D. M., Movahed, P., Hin- man, A., Axelsson, H. E., Sterner, O., Högestätt, E. D., Julius, D., Jordt, S. E., and Zygmunt, P. M. (2005). Pungent products from garlic acti- vate the sensory ion channel TRPA1. Proc. Natl. Acad. Sci. U.S.A. 102, 12248-12252.
12. Bergdahl, A., Gomez, M. F., Dreja, K., Xu, S. Z., Adner, M., Beech, D. J., Broman, J., Hellstrand, P., and Swärd, K. (2003). Cholesterol depletion impairs vascular reactivity to endothelin-1 by reducing store- operated Ca2+ entry dependent on TRPC1. Circ. Res. 93, 839-847.
13. Berlett, B. S., and Stadtman, E. R. (1997). Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20313-20316.
14. Bernatchez, P. N., Bauer, P. M., and Yu, J. (2005). Dissecting the molecular control of endothelial NO synthase by caveolin-1 using cell-permeable peptides. Proc. Natl. Acad. Sci. U.S.A. 102, 761-766.
15. Bessac, B. F., and Jordt, S. E. (2008). Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensa- tion and reflex control. Physiology (Bethesda) 23, 360-370.
16. Bessac, B. F., Sivula, M., von Hehn, C. A., Escalera, J., Cohn, L., and Jordt, S. E. (2008). TRPA1 is a major oxi- dant sensor in murine airway sen- sory neurons. J. Clin. Invest. 118, 1899-1910.
17. Blair, N. T., Kaczmarek, J. S., and Clapham, D. E. (2009). Intracel- lular calcium strongly potentiates agonist-activated TRPC5 channels. J. Gen. Physiol. 133, 525-546.
18. Boehning, D., and Snyder, S. H. (2003). Novel neural modulators. Annu. Rev. Neurosci. 26, 105-131.
19. Boo,Y. C., Hwang, J., Sykes, M., Michell, B. J., Kemp, B. E., Lum, H., and Jo, H. (2002). Shear stress stimulates phos- phorylation of eNOS at Ser635 by a protein kinase A-dependent mech- anism. Am. J. Physiol. Heart Circ. Physiol. 283, H1819-H1828.
20. Boo, Y. C., and Jo, H. (2003). Flow- dependent regulation of endothelial nitric oxide synthase: role of protein kinases. Am. J. Physiol. Cell Physiol. 285, C499-C508.
21. Brazer, S. C., Singh, B. B., Liu, X., Swaim, W., and Ambudkar, I. S. (2003). Caveolin-1 contributes to assembly of store-operated Ca2+ influx chan- nels by regulating plasma membrane localization of TRPC1. J. Biol. Chem. 278, 27208-27215.
22. Brierley, S. M., Carter, R., Jones, W., Xu, L., Robinson, D. R., Hicks, G. A., Gebhart, G. F., and Blackshaw, L. A. (2005). Differential chemosen- sory function and receptor expres- sion of splanchnic and pelvic colonic afferents in mice. J. Physiol. 567, 267-281.
23. Burke-Gaffney, A., Callister, M. E., and Nakamura, H. (2005). Thioredoxin: friend or foe in human disease? Trends Pharmacol. Sci. 26, 398-404
24. Caceres, A. I., Brackmann, M., Elia, M. D., Bessac, B. F., del Camino, D., D'Amours, M., Witek, J. S., Fanger, C. M., Chong, J. A., Hay- ward, N. J., Homer, R. J., Cohn, L., Huang, X., Moran, M. M., and Jordt, S. E. (2009). A sensory neu- ronal ion channel essential for air- way inflammation and hyperreactiv- ity in asthma. Proc. Natl. Acad. Sci. U.S.A. 106, 9099-9104.
25. Carr, M. J., Kollarik, M., Meeker, S. N., and Undem, B. J. (2003). A role for TRPV1 in bradykinin-induced exci- tation of vagal airway afferent nerve terminals. J. Pharmacol. Exp. Ther. 304, 1275-1279.
26. Caterina, M. J., Leffler, A., Malmberg, A. B.,Martin,W. J.,Trafton,J.,Petersen-Zeitz, K. R., Koltzenburg, M., Bas- baum, A. I., and Julius, D. (2000). Impaired nociception and pain sen- sation in mice lacking the capsaicin receptor. Science 288, 306-313.
27. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D. (1997). The cap- saicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824.
28. Cavanaugh, D. J., Chesler, A. T., Jack- son, A. C., Sigal, Y. M., Yamanaka, H., Grant, R., O'Donnell, D., Nicoll, R. A., Shah, N. M., Julius, D., and Basbaum, A. I. (2011). Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J. Neurosci. 31, 5067-5077.
29. Christianson, J. A., Traub, R. J., and Davis, B. M. (2006). Differences in spinal distribution and neurochem- ical phenotype of colonic afferents in mouse and rat. J. Comp. Neurol. 494, 246-259.
30. Chuang, H. H., and Lin, S. (2009). Oxidative challenges sensi- tize the capsaicin receptor by covalent cysteine modification. Proc. Natl. Acad. Sci. U.S.A. 106, 20097-20102.
31. Chuang, H. H., Prescott, E. D., Kong, H., Shields, S., Jordt, S. E., Basbaum, A. I., Chao, M. V., and Julius, D. (2001). Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411, 957-962.
32. Claiborne, A., Yeh, J. I., Mallett, T. C., Luba, J., Crane, E. J., Charrier, V., and Parsonage, D. (1999). Protein- sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry 38, 15407-15416.
33. Clapham, D. E. (2003). TRP chan- nels as cellular sensors. Nature 426, 517-524.
34. Couet, J., Li, S., Okamoto, T., Ikezu, T., and Lisanti, M. P. (1997). Iden- tification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the inter- action of caveolin with caveolae- associated proteins. J. Biol. Chem. 272, 6525-6533.
35. Cristino, L., de Petrocellis, L., Pryce, G., Baker, D., Guglielmotti, V., and Di Marzo, V. (2006). Immunohis- tochemical localization of cannabi- noid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neu- roscience 139, 1405-1415.
36. Dai, Y., Wang, S., Tominaga, M., Yamamoto, S., Fukuoka, T., Higashi, T., Kobayashi, K., Obata, K., Yamanaka, H., and Noguchi, K. (2007). Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J. Clin. Invest. 117, 1979-1987.
37. 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., Hughes, S. A., Rance, K., Grau, E., Harper, A. J., Pugh, P. L., Rogers, D. C., Bing- ham, S., Randall,A., and Sheardown, S. A. (2000). Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405, 183-187.
38. Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wak- abayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P. (2002). Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxi- dants. Proc. Natl.Acad. Sci. U.S.A. 99, 11908-11913.
39. Eggler, A. L., Liu, G., Pezzuto, J. M., van Breemen, R. B., and Mesecar, A. D. (2005). Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to dis- rupt binding to the Nrf2 domain Neh2. Proc. Natl. Acad. Sci. U.S.A. 102, 10070-10075.
40. Eu, J. P., Sun, J., Xu, L., Stamler, J. S., and Meissner, G. (2000). The skele- tal muscle calcium release channel: coupled O2 sensor and NO signaling functions. Cell 102, 499-509.
41. Everaerts, W., Gees, M., Alpizar, Y. A., Farre, R., Leten, C., Apetrei, A., Dewachter, I., van Leuven, F., Ven- nekens, R., De Ridder, D., Nilius, B., Voets, T., and Talavera, K. (2011). The capsaicin receptor TRPV1 is a crucial mediator of the noxious effects of mustard oil. Curr. Biol. 21, 316-321.
42. Foster, M. W., Hess, D. T., and Stamler, J. S. (2006). S-nitrosylation TRiPs a calcium Switch. Nat. Chem. Biol. 2, 570-571.
43. Freichel, M., Suh, S. H., Pfeifer, A., Schweig, U., Trost, C., Weissgerber, P., Biel, M., Philipp, S., Freise, D., Droogmans, G., Hofmann, F., Flock- erzi,V., and Nilius, B. (2001). Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4-/- mice. Nat. Cell Biol. 3, 121-127.
44. Fujita, F., Uchida, K., Moriyama, T., Shima, A., Shibasaki, K., Inada, H., Sokabe, T., and Tominaga, M. (2008). Intracellular alkalization causes pain sensation through acti- vation of TRPA1 in mice. J. Clin. Invest. 118, 4049-4057.
45. Fulton, D., Fontana, J., Sowa, G., Grat- ton, J. P., Lin, M., Li, K. X., Michell, B., Kemp, B. E., Rodman, D., and Sessa, W. C. (2002). Localization of endothelial nitric-oxide synthase phosphorylated on serine 1179 and nitric oxide in golgi and plasma membrane defines the existence of two pools of active enzyme. J. Biol. Chem. 277, 4277-4284.
46. Fulton, D., Gratton, J. P., McCabe, T. J., Fontana, J., Fujio, Y., Walsh, K., Franke, T. F., Papapetropou- los, A., and Sessa, W. C. (1999). Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399, 597-601.
47. García-Cardeña, G., Fan, R., Stern, D. F., Liu, J., and Sessa, W. C. (1996). Endothelial nitric oxide synthase is regulated by tyrosine phosphoryla- tion and interacts with caveolin-1. J. Biol. Chem. 271, 27237-27240.
48. García-Cardeña, G., Martasek, P., Mas- ters, B. S., Skidd, P. M., Couet, J., Li, S., Lisanti, M. P., and Sessa, W. C. (1997). Dissecting the interac- tion between nitric oxide synthase (NOS) and caveolin. Functional sig- nificance of the nos caveolin binding domain in vivo. J. Biol. Chem. 272, 25437-25440.
49. Gaudet, R. (2008). A primer on ankyrin repeat function in TRP channels and beyond. Mol. Biosyst. 4, 372-379.
50. Goel, M., Sinkins,W., Keightley,A., Kin- ter, M., and Schilling, W. P. (2005). Proteomic analysis of TRPC5- and TRPC6-binding partners reveals interaction with the plasmalemmal Na+/K+-ATPase. Pflügers Arch. 451, 87-98.
51. Gomis,A.,Soriano,S.,Belmonte,C.,and Viana, F. (2008). Hypoosmotic- and pressure-induced membrane stretch activate TRPC5 channels. J. Physiol. 586, 5633-5649.
52. Gow, A. J., Chen, Q., Hess, D. T., Day, B. J., Ischiropoulos, H., and Stamler, J. S. (2002). Basal and stimulated pro- tein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem. 277, 9637-9640.
53. Greka, A., Navarro, B., Oancea, E., Duggan, A., and Clapham, D. E. (2003). TRPC5 is a regulator of hip- pocampal neurite length and growth cone morphology. Nat. Neurosci. 6, 837-845.
54. Gross,S.A.,Guzmán,G.A.,Wissenbach, U., Philipp, S. E., Zhu, M. X., Bruns, D., and Cavalié, A. (2009). TRPC5 isaCa2+-activated channel func- tionally coupled to Ca2+-selective ion channels. J. Biol. Chem. 284, 34423-34432.
55. Gu, Q., and Lin, R. L. (2010). Heavy metals zinc, cadmium, and copper stimulate pulmonary sensory neu- rons via direct activation of TRPA1. J. Appl. Physiol. 108, 891-897.
56. Gu, Z., Kaul, M., Yan, B., Kridel, S. J., Cui, J., Strongin, A., Smith, J. W., Liddington, R. C., and Lipton, S. A. (2002). S-nitrosylation of matrix metalloproteinases: signaling path- way to neuronal cell death. Science 297, 1186-1190.
57. Hara, M. R., Agrawal, N., Kim, S. F., Cascio, M. B., Fujimuro, M., Ozeki, Y., Takahashi, M., Cheah, J. H., Tankou, S. K., Hester, L. D., Fer- ris, C. D., Hayward, S. D., Sny- der, S. H., and Sawa, A. (2005). S- nitrosylated GAPDH initiates apop- totic cell death by nuclear translo- cation following Siah1 binding. Nat. Cell Biol. 7, 665-674.
58. Hara, Y., Wakamori, M., Ishii, M., Maeno, E., Nishida, M., Yoshida, T., Yamada, H., Shimizu, S., Mori, E., Kudoh, J., Shimizu, N., Kurose, H., Okada, Y., Imoto, K., and Mori, Y. (2002). LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol. Cell 9, 163-173.
59. Heijnen, H. F., Waaijenborg, S., Crapo, J. D., Bowler, R. P., Akkerman, J. W., and Slot, J. W. (2004). Colocal- ization of eNOS and the catalytic subunit of PKA in endothelial cell junctions: a clue for regulated NO production. J. Histochem. Cytochem. 52, 1277-1285.
60. Helliwell, R. J., McLatchie, L. M., Clarke, M., Winter, J., Bevan, S., and McIn- tyre, P. (1998). Capsaicin sensitiv- ity is associated with the expression of the vanilloid (capsaicin) receptor (VR1) mRNA in adult rat sensory ganglia. Neurosci. Lett. 250, 177-180
61. Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E., and Stamler, J. S. (2005). Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150-166.
62. Hinman, A., Chuang, H. H., Bautista, D. M., and Julius, D. (2006). TRP chan- nel activation by reversible covalent modification. Proc. Natl. Acad. Sci. U.S.A. 103, 19564-19568.
63. Ho, C. Y., and Lee, L. Y. (1998). Ozone enhances excitabilities of pulmonary C fibers to chemical and mechanical stimuli in anesthetized rats. J. Appl. Physiol. 85, 1509-1515.
64. Hong, F., Sekhar, K. R., Freeman, M. L., and Liebler, D. C. (2005). Spe- cific patterns of electrophile adduc- tion trigger Keap1 ubiquitination and Nrf2 activation. J. Biol. Chem. 280, 31768-31775.
65. Hu, H., Bandell, M., Petrus, M. J., Zhu, M. X., and Patapoutian, A. (2009). Zinc activates damage- sensing TRPA1 ion channels. Nat. Chem. Biol. 5, 183-190.
66. Hwang, S. W., Cho, H., Kwak, J., Lee, S. Y., Kang, C. J., Jung, J., Cho, S., Min, K. H., Suh, Y. G., Kim, D., and Oh, U. (2000). Direct activa- tion of capsaicin receptors by prod- ucts of lipoxygenases: endogenous capsaicin-like substances. Proc. Natl. Acad. Sci. U.S.A. 97, 6155-6160.
67. Jaffrey, S. R., Erdjument-Bromage, H., Ferris, C. D., Tempst, P., and Snyder, S. H. (2001). Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3, 193-197.
68. Jancsó, N., Jancsó-Gábor, A., and Szolc- sányi, J. (1967). Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br. J. Pharmacol. Chemother. 31, 138-151
69. Jaquemar, D., Schenker, T., and Trueb, B. (1999). An ankyrin-like protein with transmembrane domains is specif- ically lost after oncogenic transfor- mation of human fibroblasts. J. Biol. Chem. 274, 7325-7333.
70. Ji, R. R., Samad, T. A., Jin, S. X., Schmoll, R., and Woolf, C. J. (2002). p38 MAPK activation by NGF in pri- mary sensory neurons after inflam- mation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36, 57-68.
71. Jordt, S. E., Bautista, D. M., Chuang, H. H., McKemy, D. D., Zygmunt, P. M., Högestätt, E. D., Meng, I. D., and Julius, D. (2004). Mus- tard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265.
72. Joseph, E. K., Chen, X., Bogen, O., and Levine, J. D. (2008). Oxali- platin acts on IB4-positive nocicep- tors to induce an oxidative stress- dependent acute painful peripheral neuropathy. J. Pain 9, 463-472.
73. Ju, H., Zou, R., Venema, V. J., and Ven- ema, R. C. (1997). Direct interac- tion of endothelial nitric-oxide syn- thase and caveolin-1 inhibits syn- thase activity. J. Biol. Chem. 272, 18522-18525.
74. Julius, D., and Basbaum, A. I. (2001). Molecular mechanisms of nocicep- tion. Nature 413, 203-210.
75. Kamboj, S. S., Vasishta, R. K., and Sandhir, R. (2010). N-acetylcysteine inhibits hyperglycemia-induced oxidative stress and apoptosis markers in diabetic neuropathy. J. Neurochem. 112, 77-91.
76. Kone, B. C., Kuncewicz, T., Zhang, W., and Yu, Z. Y. (2003). Protein inter- actions with nitric oxide synthases: controlling the right time, the right place, and the right amount of nitric oxide. Am. J. Physiol. Renal Physiol. 285, F178-F190.
77. Kubin, L., Alheid, G. F., Zuperku, E. J., and McCrimmon, D. R. (2006). Central pathways of pulmonary and lower airway vagal afferents. J. Appl. Physiol. 101, 618-627.
78. Kuhad, A., and Chopra, K. (2009). Tocotrienol attenuates oxidative- nitrosative stress and inflammatory cascade in experimental model of diabetic neuropathy. Neuropharma- cology 57, 456-462.
79. Kwong, K., and Lee, L. Y. (2005). Prostaglandin E2 potentiates a TTX- resistant sodium current in rat capsaicin-sensitive vagal pulmonary sensory neurones. J. Physiol. 564, 437-450.
80. Lee, L. Y., Burki, N. K., Gerhardstein, D. C., Gu, Q., Kou, Y. R., and Xu, J. (2007). Airway irritation and cough evoked by inhaled cigarette smoke: role of neuronal nicotinic acetyl- choline receptors. Pulm. Pharmacol. Ther. 20, 355-364.
81. Lin, Y. S., Hsu, C. C., Bien, M. Y., Hsu, H. C., Weng, H. T., and Kou, Y. R. (2010). Activations of TRPA1 and P2X receptors are important in ROS- mediated stimulation of capsaicin- sensitive lung vagal afferents by cig- arette smoke in rats. J. Appl. Physiol. 108, 1293-1303.
82. Lipton, S. A., Choi, Y. B., Takahashi, H., Zhang, D., Li, W., Godzik, A., and Bankston, L. A. (2002). Cys- teine regulation of protein function- as exemplified by NMDA-receptor modulation. Trends Neurosci. 25, 474-480.
83. Lockwich, T. P., Liu, X., Singh, B. B., Jadlowiec, J., Weiland, S., and Ambudkar, I. S. (2000). Assembly of Trp1 in a signaling complex associ- ated with caveolin-scaffolding lipid raft domains. J. Biol. Chem. 275, 11934-11942.
84. Macpherson, L. J., Dubin, A. E., Evans, M. J., Marr, F., Schultz, P. G., Cra- vatt, B. F., and Patapoutian, A. (2007). Noxious compounds acti- vate TRPA1 ion channels through covalent modification of cysteines. Nature 445, 541-545.
85. Macpherson, L. J., Geierstanger, B. H., Viswanath, V., Bandell, M., Eid, S. R., Hwang, S., and Patapoutian, A. (2005). The pungency of garlic: acti- vation of TRPA1 and TRPV1 in response to allicin. Curr. Biol. 15, 929-934.
86. Maher, M., Ao, H., Banke, T., Nasser, N., Wu, N. T., Breitenbucher, J. G., Chaplan, S. R., and Wickenden, A. D. (2008). Activation of TRPA1 by farnesyl thiosalicylic acid. Mol. Phar- macol. 73, 1225-1234.
87. Mezey, E., Tóth, Z. E., Cortright, D. N., Arzubi, M. K., Krause, J. E., Elde, R., Guo, A., Blumberg, P. M., and Szallasi, A. (2000). Distribu- tion of mRNA for vanilloid recep- tor subtype 1 (VR1), and VR1- like immunoreactivity, in the cen- tral nervous system of the rat and human. Proc. Natl. Acad. Sci. U.S.A. 97, 3655-3660.
88. Michel, J. B., Feron, O., Sacks, D., and Michel, T. (1997a). Recipro- cal regulation of endothelial nitric- oxide synthase by Ca2+-calmodulin and caveolin. J. Biol. Chem. 272, 15583-15586.
89. Michel, J. B., Feron, O., Sase, K., Prabhakar, P., and Michel, T. (1997b). Caveolin versus calmod- ulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J. Biol. Chem. 272, 25907-25912.
90. Michell, B. J., Chen, Z. P., Tiganis, T., Stapleton, D., Katsis, F., Power, D. A., Sim, A. T., and Kemp, B. E. (2001). Coordinated Control of endothelial nitric-oxide synthase phosphoryla- tion by protein kinase C and the cAMP-dependent protein kinase. J. Biol. Chem. 276, 17625-17628.
91. Miehe, S., Bieberstein, A., Arnould, I., Ihdene, O., Rütten, H., and Strübing, C. (2010). The phospholipid- binding protein SESTD1 is a novel regulator of the transient receptor potential channels TRPC4 and TRPC5. J. Biol. Chem. 285, 12426-12434.
92. Murad, F. (1986). Cyclic guanosine monophosphate as a mediator of vasodilation. J. Clin. Invest. 78, 1-53
93. Murad, F. (2006). Shattuck lecture. nitric oxide and cyclic GMP in cell signaling and drug development. N. Engl.J.Med.355, 2003-2011.
94. Nagatomo, K., and Kubo,Y. (2008). Caf- feine activates mouse TRPA1 chan- nels but suppresses human TRPA1 channels. Proc. Natl.Acad. Sci. U.S.A. 105, 17373-17378.
95. Obukhov, A. G., and Nowycky, M. C. (2004). TRPC5 activation kinetics are modulated by the scaffolding protein ezrin/radixin/moesin- binding phosphoprotein-50 (EBP50). J. Cell. Physiol. 201, 227-235.
96. Okada, T., Shimizu, S., Wakamori, M., Maeda, A., Kurosaki, T., Takada, N., Imoto, K., and Mori, Y. (1998). Mol- ecular cloning and functional char- acterization of a novel receptor- activated TRP Ca2+ channel from mouse brain. J. Biol. Chem. 273, 10279-10287.
97. Ordaz, B., Tang, J., Xiao, R., Salgado, A., Sampieri, A., Zhu, M. X., and Vaca, L. (2005). Calmodulin and calcium interplay in the modula- tion of TRPC5 channel activity. Identification of a novel C-terminal domain for calcium/calmodulin- mediated facilitation. J. Biol. Chem. 280, 30788-30796.
98. Perraud, A. L., Takanishi, C. L., Shen, B., Kang, S., Smith, M. K., Schmitz, C., Knowles, H. M., Ferraris, D., Li, W., Zhang, J., Stoddard, B. L., and Scharenberg, A. M. (2005). Accumulation of free ADP-ribose from mitochondria mediates oxida- tive stress-induced gating of TRPM2 cation channels. J. Biol. Chem. 280, 6138-6148.
99. Philipp, S., Hambrecht, J., Braslavski, L., Schroth, G., Freichel, M., Murakami, M., Cavalié, A., and Flockerzi, V. (1998). A novel capacitative calcium entry channel expressed in excitable cells. EMBO J. 17, 4274-4282.
100. Premkumar, L. S., and Ahern, G. P. (2000). Induction of vanilloid recep- tor channel activity by protein kinase C. Nature 408, 985-990.
101. Quest, A. F., Gutierrez-Pajares, J. L., and Torres, V. A. (2008). Caveolin-1: an ambiguous partner in cell signalling and cancer. J.Cell.Mol.Med.12, 1130-1150.
102. Rizzo, V., McIntosh, D. P., Oh, P., and Schnitzer, J. E. (1998). In situ flow activates endothelial nitric oxide synthase in luminal cave- olae of endothelium with rapid caveolin dissociation and calmod- ulin association. J. Biol. Chem. 273, 34724-34729.
103. 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.
104. Rossi, A., Kapahi, P., Natoli, G., Takahashi, T., Chen, Y., Karin, M., and Santoro, M. G. (2000). Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase. Nature 403, 103-108.
105. Salazar, H., Llorente, I., Jara-Oseguera, A., García-Villegas, R., Munari, M., Gordon, S. E., Islas, L. D., and Rosen- baum,T. (2008).A single N-terminal cysteine in TRPV1 determines acti- vation by pungent compounds from onion and garlic. Nat. Neurosci. 11, 255-261.
106. Sato, Y., Sagami, I., and Shimizu, T. (2004). Identification of caveolin- 1-interacting sites in neuronal nitric-oxide synthase. Molecular mechanism for inhibition of NO formation. J. Biol. Chem. 279, 8827-8836.
107. Satoh, T., and Lipton, S. A. (2006). Redox regulation of neuronal sur- vival mediated by electrophilic com- pounds. Trends Neurosci. 30, 37-45
108. Sawada, Y., Hosokawa, H., Matsumura, K., and Kobayashi, S. (2008). Activa- tion of transient receptor potential ankyrin 1 by hydrogen peroxide. Eur. J. Neurosci. 27, 1131-1142.
109. Schindl, R., Frischauf, I., Kahr, H., Fritsch, R., Krenn, M., Derndl, A., Vales, E., Muik, M., Derler, I., Groschner, K., and Romanin, C. (2008). The first ankyrin-like repeat is the minimum indispens- able key structure for functional assembly of homo- and heteromeric TRPC4/TRPC5 channels. Cell Cal- cium 43, 260-269.
110. Schmidt, M., Dubin, A. E., Petrus, M. J., Earley, T. J., and Patapoutian, A. (2009). Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron 64, 498-509.
111. Shibata, T., Yamada, T., Ishii, T., Kumazawa, S., Nakamura, H., Masu- tani, H., Yodoi, J., and Uchida, K. (2003). Thioredoxin as a mol- ecular target of cyclopentenone prostaglandins. J. Biol. Chem. 278, 26046-26054.
112. Shimizu, S., Yoshida, T., Wakamori, M., Ishii, M., Okada, T., Takahashi, M., Seto, M., Sakurada, K., Kiuchi, Y., and Mori, Y. (2006). Ca2+- calmodulin-dependent myosin light chain kinase is essential for activa- tion of TRPC5 channels expressed in HEK 293 cells. J. Physiol. 570, 219-235.
113. Shin, J., Cho, H., Hwang, S. W., Jung, J., Shin, C. Y., Lee, S. Y., Kim, S. H., Lee, M. G., Choi, Y. H., Kim, J., Haber, N. A., Reichling, D. B., Khasar, S., Levine, J. D., and Oh, U. (2002). Bradykinin-12- lipoxygenase-VR1 signaling path- way for inflammatory hyperalge- sia. Proc. Natl. Acad. Sci. U.S.A. 99, 10150-10155.
114. Shiraki, T., Kamiya, N., Shiki, S., Kodama, T. S., Kakizuka, A., and Jingami, H. (2005). α,β-unsaturated ketone is a core moiety of nat- ural ligands for covalent binding to peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 280, 14145-14153.
115. Smolen, J. S., Aletaha, D., Koeller, M., Weisman, M. H., and Emery, P. (2007). New therapies for treatment of rheumatoid arthritis. Lancet 370, 1861-1874.
116. Stamler, J. S., Lamas, S., and Fang, F. C. (2001). Nitrosylation. the prototypic redox-based signaling mechanism. Cell 106, 675-683.
117. Stamler, J. S., Simon, D. I., Jaraki, O., Osborne, J. A., Francis, S., Mullins, M., Singel, D., and Loscalzo, J. (1992a). S-nitrosylation of tissue- type plasminogen activator confers vasodilatory and antiplatelet proper- ties on the enzyme. Proc. Natl. Acad. Sci. U.S.A. 89, 8087-8091.
118. Stamler, J. S., Simon, D. I., Osborne, J. A., Mullins, M. E., Jaraki, O., Michel, T., Singel, D. J., and Loscalzo, J. (1992b). S-nitrosylation of proteins with nitric oxide: synthesis and char- acterization of biologically active compounds. Proc. Natl. Acad. Sci. U.S.A. 89, 444-448.
119. Steenland, H. W., Ko, S. W., Wu, L. J., and Zhuo, M. (2006). Hot receptors in the brain. Mol. Pain 2, 34.
120. 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 noci- ceptive neurons, is activated by cold temperatures. Cell 112, 819-829.
121. Straus, D. S., Pascual, G., Li, M., Welch, J. S., Ricote, M., Hsiang, C. H., Sengchanthalangsy, L. L., Ghosh, G., and Glass, C. K. (2000). 15-deoxy-Δ12,14-prostaglandin J2 inhibits multiple steps in the NF-κB signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 97, 4844-4849.
122. Strübing, C., Krapivinsky, G., Krapivin- sky, L., and Clapham, D. E. (2001). TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29, 645-655.
123. Sugiuar, T., Bielefeldt, K., and Geb- hart, G. F. (2004). TRPV1 func- tion in mouse colon sensory neu- rons is enhanced by metabotropic 5-hydroxytryptamine receptor acti- vation. J. Neurosci. 24, 9521-9530.
124. Susankova, K., Tousova, K., Vyklicky, L., Teisinger, J., and Vlachova,V. (2006). Reducing and oxidizing agents sensi- tize heat-activated vanilloid receptor (TRPV1) current. Mol. Pharmacol. 70, 383-394.
125. Szallasi, A., Nilsson, S., Farkas-Szallasi, T., Blumberg, P. M., Hökfelt, T., and Lundberg, J. M. (1995). Vanil- loid (capsaicin) receptors in the rat: distribution in the brain, regional differences in the spinal cord, axonal transport to the periphery, and depletion by systemic vanilloid treatment. Brain Res. 703, 175-183
126. Takahashi, N., Kuwaki, T., Kiyonaka, S., Numata, T., Kozai, D., Mizuno, Y., Yamamoto, S., Naito, S., Knevels, E., Carmeliet, P., Oga, T., Kaneko, S., Suga, S., Nokami, T., Yoshida, J., and Mori, Y. (2011). TRPA1 underlies a sensing mechanism for O2. Nat. Chem. Biol. 7, 701-711.
127. Takahashi, N., Mizuno, Y., Kozai, D., Yamamoto, S., Kiyonaka, S., Shi- bata, T., Uchida, K., and Mori, Y. (2008). Molecular characteri- zation of TRPA1 channel activa- tion by cysteine-reactive inflamma- tory mediators. Channels (Austin) 2, 287-298.
128. 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.
129. Tang, Y., Tang, J., Chen, Z., Trost, C., Flockerzi, V., Li, M., Ramesh, V., and Zhu, M. X. (2000). Asso- ciation of mammalian Trp4 and phospholipase C isozymes with a PDZ domain-containing pro- tein, NHERF. J. Biol. Chem. 275, 37559-37564.
130. Taylor-Clark, T. E., Ghatta, S., Bet- tner, W., and Undem, B. J. (2009). Nitrooleic acid, an endogenous product of nitrative stress, activates nociceptive sensory nerves via the direct activation of TRPA1. Mol. Pharmacol. 75, 820-829.
131. Taylor-Clark, T. E., McAlexander, M. A., Nassenstein, C., Sheardown, S. A., Wilson, S., Thornton, J., Carr, M. J., and Undem, B. J. (2008a). Relative contributions of TRPA1 and TRPV1 channels in the activation of vagal bronchopulmonary C-fibres by the endogenous autacoid 4-oxononenal. J. Physiol. 586, 3447-3459.
132. Taylor-Clark, T. E., Undem, B. J., Macglashan, D. W., Ghatta, S., Carr, M. J., and McAlexander, M. A. (2008b). Prostaglandin-induced activation of nociceptive neurons via direct interaction with transient receptor potential A1 (TRPA1). Mol. Pharmacol. 73, 274-281.
133. Taylor-Clark, T. E., Nassenstein, C., and Undem, B. J. (2008c). Leukotriene D4 increases the excitability of capsaicin-sensitive nasal sensory nerves to electrical and chemi- cal stimuli. Br. J. Pharmacol. 154, 1359-1368.
134. Taylor-Clark, T. E., and Undem, B. J. (2010). Ozone activates airway nerves via the selective stimulation of TRPA1 ion channels. J. Physiol. 588, 423-433.
135. Taylor-Clark, T. E., and Undem, B. J. (2011). Sensing pulmonary oxida- tive stress by lung vagal affer- ents. Respir. Physiol. Neurobiol. 178, 406-413.
136. Togashi, K., Hara, Y., Tominaga, T., Higashi, T., Konishi, Y., Mori, Y., and Tominaga, M. (2006). TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J. 25, 1804-1815.
137. Tominaga, M., Caterina, M. J., Malm- berg, A. B., Rosen, T. A., Gilbert, H., Skinner, K., Raumann, B. E., Basbaum,A. I., and Julius, D. (1998). The cloned capsaicin receptor inte- grates multiple pain-producing stimuli. Neuron 21, 531-543.
138. Tominaga, M., Wada, M., and Masu, M. (2001). Potentiation of capsaicin receptor activity by metabotropic ATP receptors as a possible mech- anism for ATP-evoked pain and hyperalgesia. Proc. Natl. Acad. Sci. U.S.A. 98, 6951-6956.
139. Tóth, A., Boczán, J., Kedei, N., Lizanecz, E., Bagi, Z., Papp, Z., Edes, I., Csiba, L., and Blumberg, P. M. (2005). Expression and distribution of vanil- loid receptor 1 (TRPV1) in the adult rat brain. Brain Res. Mol. Brain Res. 135, 162-168.
140. Trebak, M., Lemonnier, L., DeHaven, W. I., Wedel, B. J., Bird, G. S., and Putney, J. W. (2009). Com- plex functions of phosphatidylinos- itol 4,5-bisphosphate in regulation of TRPC5 cation channels. Pflügers Arch. 457, 757-769.
141. Trevisani, M., Siemens, J., Materazzi, S., Bautista, D. M., Nassini, R., Campi, B., Imamachi, N., Andrè, E., Patacchini, R., Cottrell, G. S., Gatti, R., Basbaum, A. I., Bunnett, N. W., Julius, D., and Geppetti, P. (2007). 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neuro- genic inflammation through activa- tion of the irritant receptor TRPA1. Proc. Natl. Acad. Sci. U.S.A. 104, 13519-13524.
142. Uchida, K., Dezaki, K., Damdindorj, B., Inada, H., Shiuchi, T., Mori, Y., Yada, T., Minokoshi, Y., and Tom- inaga, M. (2011). Lack of TRPM2 impaired insulin secretion and glu- cose metabolisms in mice. Diabetes 60, 119-126.
143. Uehara, T., Nakamura, T., Yao, D., Shi, Z. Q., Gu, Z., Ma, Y., Masliah, E., Nomura, Y., and Lipton, S. A. (2006). S-nitrosylated protein- disulphide isomerase links protein misfolding to neurodegeneration. Nature 441, 513-517.
144. Voets, T., Talavera, K., Owsianik, G., and Nilius, B. (2005). Sensing with TRP channels. Nat. Chem. Biol. 1, 85-92
145. Wang, S., Dai, Y., Fukuoka, T., Yamanaka, H., Kobayashi, K., Obata, K., Cui, X., Tominaga, M., and Noguchi, K. (2008). Phos- pholipase C and protein kinase A mediate bradykinin sensitization of TRPA1: a molecular mechanism of inflammatory pain. Brain 131, 1241-1251.
146. Wang, Y. Y., Chang, R. B., and Liman, E. R. (2010). TRPA1 is a component of the nociceptive response to CO2. J. Neurosci. 30, 12958-12963.
147. Ward, S. M., Bayguinov, J., Won, K. J., Grundy, D., and Berthoud, H. R. (2003). Distribution of the vanil- loid receptor (VR1) in the gastroin- testinal tract. J. Comp. Neurol. 465, 121-135.
148. Wong, C. O., Sukumar, P., Beech, D. J., and Yao, X. (2010). Nitric oxide lacks direct effect on TRPC5 channels but suppresses endoge- nous TRPC5-containing channels in endothelial cells. Pflugers Arch. 460, 121-130.
149. Xu, H., Blair, N. T., and Clapham, D. E. (2005). Camphor activates and strongly desensitizes the tran- sient receptor potential vanilloid subtype 1 channel in a vanilloid- independent mechanism. J. Neu- rosci. 25, 8924-8937.
150. Xu, S. Z., Sukumar, P., Zeng, F., Li, J., Jairaman, A., English, A., Naylor, J., Ciurtin, C., Majeed, Y., Milligan, C. J., Bahnasi, Y. M., Al-Shawaf, E., Porter, K. E., Jiang, L. H., Emery, P., Sivaprasadarao, A., and Beech, D. J. (2008). TRPC channel activation by extracellular thioredoxin. Nature 451, 69-72.
151. Yamamoto, S., Shimizu, S., Kiyon- aka, S., Takahashi, N., Wajima, T., Hara, Y., Negoro, T., Hiroi, T., Kiuchi, Y., Okada, T., Kaneko, S., Lange, I., Fleig, A., Penner, R., Nishi, M., Takeshima, H., and Mori, Y. (2008). TRPM2-mediated Ca2+ influx induces chemokine produc- tion in monocytes that aggravates inflammatory neutrophil infiltra- tion. Nat. Med. 14, 738-747.
152. Yoshida, T., Inoue, R., Morii, T., Taka- hashi, N., Yamamoto, S., Hara, Y., Tominaga, M., Shimizu, S., Sato, Y., and Mori, Y. (2006). Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat. Chem. Biol. 2, 596-607.
153. Yuan, J. P., Kiselyov, K., Shin, D. M., Chen, J., Shcheynikov, N., Kang, S. H., Dehoff, M. H., Schwarz, M. K., Seeburg, P. H., Muallem, S., and Worley, P. F. (2003). Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 114, 777-789.
154. Zhang, N., Beuve, A., and Townes-Anderson, E. (2005). The nitric oxide-cGMP signaling pathway differentially regulates presynaptic structural plasticity in cone and rod cells. J. Neurosci. 25, 2761-2770.
155. Zygmunt, P. M., Petersson, J., Andersson, D. A., Chuang, H., Sørgård, M., Di Marzo, V., Julius, D., and Högestätt, E. D. (1999). Vanil- loid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400, 452-457.