Transient receptor potential channels in bladder function

Acta Physiologica

Volumn 207, Issue 1, 2013, Pages 110-122

  Avelino, A ^a   Charrua, A ^a,b,c,d   Frias, B ^a,c   Cruz, C ^a,c   Boudes, M ^e,f   de Ridder, D ^f   Cruz, F ^b,c  

^a University of Porto   (Portugal)

^b HOSPITAL DE SÃO JOÃO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

^e SKELETAL BIOLOGY AND ENGINEERING RESEARCH CENTER   (Belgium)

^f LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

Author keywords

Overactive; Vanilloid; Visceral

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CALCIUM ION; PROTEIN FOS; PROTEIN KINASE D; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; VANILLOID RECEPTOR; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 2; VANILLOID RECEPTOR 4;

BINDING KINETICS; BIOLOGICAL ACTIVITY; BLADDER DYSFUNCTION; BLADDER FUNCTION; BLADDER PRESSURE; CALCIUM TRANSPORT; DESENSITIZATION; DOWN REGULATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INHIBITION KINETICS; INTERSTITIAL CYSTITIS; MICTURITION; MICTURITION REFLEX; NEUROMODULATION; NONHUMAN; OVERACTIVE BLADDER; PAIN THRESHOLD; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SENSORY NERVE CELL; SMOOTH MUSCLE FIBER; TRANSITIONAL CELL CARCINOMA; UPREGULATION; UROTHELIUM;

AFFERENT PATHWAYS; ANIMALS; AUTONOMIC NERVOUS SYSTEM; HUMANS; INTERSTITIAL CELLS OF CAJAL; TRANSIENT RECEPTOR POTENTIAL CHANNELS; URINARY BLADDER;

EID: 84870769243     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12021     Document Type: Review

References (123)

1. Abelli, L., Nappi, F., Perretti, F., Maggi, C.A., Manzini, S. & Giachetti, A. 1992. Microvascular leakage induced by substance P in rat urinary bladder: involvement of cyclo-oxygenase metabolites of arachidonic acid. J Auton Pharmacol 12, 269-276.
2. Ahern, G.P., Brooks, I.M., Miyares, R.L. & Wang, X.B. 2005. Extracellular cations sensitize and gate capsaicin receptor TRPV1 modulating pain signaling. J Neurosci 25, 5109-5116.
3. Andrade, E.L., Forner, S., Bento, A.F., Leite, D.F., Dias, M.A., Leal, P.C., Koepp, J. & Calixto, J.B. 2011. TRPA1 receptor modulation attenuates bladder overactivity induced by spinal cord injury. Am J Physiol Renal Physiol 300, F1223-F1234.
4. Apostolidis, A., Brady, C.M., Yiangou, Y., Davis, J., Fowler, C.J. & Anand, P. 2005. Capsaicin receptor TRPV1 in urothelium of neurogenic human bladders and effect of intravesical resiniferatoxin. Urology 65, 400-405.
5. Avelino, A., Cruz, C., Nagy, I. & Cruz, F. 2002. Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 109, 787-798.
6. Bautista, D.M., Movahed, P., Hinman, A., Axelsson, H.E., Sterner, O., Hogestatt, E.D., Julius, D., Jordt, S.E. & Zygmunt, P.M. 2005. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci U S A 102, 12248-12252.
7. Bautista, D.M., Jordt, S.E., Nikai, T., Tsuruda, P.R., Read, A.J., Poblete, J., Yamoah, E.N., Basbaum, A.I. & Julius, D. 2006. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124, 1269-1282.
8. Becker, D., Muller, M., Leuner, K. & Jendrach, M. 2008. The C-terminal domain of TRPV4 is essential for plasma membrane localization. Mol Membr Biol 25, 139-151.
9. Bhave, G., Hu, H.J., Glauner, K.S., Zhu, W., Wang, H., Brasier, D.J., Oxford, G.S., Gereau, R.W.T. 2003. Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci U S A 100, 12480-12485.
10. Birder, L.A. 2010. Urothelial signaling. Auton Neurosci 153, 33-40.
11. Birder, L.A., Kanai, A.J., de Groat, W.C., Kiss, S., Nealen, M.L., Burke, N.E., Dineley, K.E., Watkins, S., Reynolds, I.J. & Caterina, M.J. 2001. Vanilloid receptor expression suggests a sensory role for urinary bladder epithelial cells. Proc Natl Acad Sci U S A 98, 13396-13401.
12. Birder, L., Kullmann, F.A., Lee, H., Barrick, S., de Groat, W., Kanai, A. & Caterina, M. 2007. Activation of urothelial transient receptor potential vanilloid 4 by 4alpha-phorbol 12, 13-didecanoate contributes to altered bladder reflexes in the rat. J Pharmacol Exp Ther 323, 227-235.
13. Bonnington, J.K. & McNaughton, P.A. 2003. Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. J Physiol 551, 433-446.
14. Boudes, M., Uvin, P. & De Ridder, D. 2011. TRPV4, new therapeutic target for urinary problems. Med Sci (Paris) 27, 232-234.
15. Brady, C.M., Apostolidis, A.N., Harper, M., Yiangou, Y., Beckett, A., Jacques, T.S., Freeman, A., Scaravilli, F., Fowler, C.J. & Anand, P. 2004. Parallel changes in bladder suburothelial vanilloid receptor TRPV1 and pan-neuronal marker PGP9.5 immunoreactivity in patients with neurogenic detrusor overactivity after intravesical resiniferatoxin treatment. BJU Int 93, 770-776.
16. Van Buren, J.J., Bhat, S., Rotello, R., Pauza, M.E. & Premkumar, L.S. 2005. Sensitization and translocation of TRPV1 by insulin and IGF-I. Mol Pain 1, 17.
17. Caprodossi, S., Lucciarini, R., Amantini, C., Nabissi, M., Canesin, G., Ballarini, P., Di Spilimbergo, A., Cardarelli, M.A., Servi, L., Mammana, G. & Santoni, G. 2008. Transient receptor potential vanilloid type 2 (TRPV2) expression in normal urothelium and in urothelial carcinoma of human bladder: correlation with the pathologic stage. Eur Urol 54, 612-620.
18. Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D. & Julius, D. 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824.
19. Caterina, M.J., Rosen, T.A., Tominaga, M., Brake, A.J. & Julius, D. 1999. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398, 436-441.
20. Caterina, M.J., Leffler, A., Malmberg, A.B., Martin, W.J., Trafton, J., Petersen-Zeitz, K.R., Koltzenburg, M., Basbaum, A.I. & Julius, D. 2000. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306-313.
21. Cavanaugh, D.J., Chesler, A.T., Jackson, A.C., Sigal, Y.M., Yamanaka, H., Grant, R., O'Donnell, D., Nicoll, R.A., Shah, N.M., Julius, D. & 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.
22. Chandiramani, V.A., Peterson, T., Duthie, G.S. & Fowler, C.J. 1996. Urodynamic changes during therapeutic intravesical instillations of capsaicin. Br J Urol 77, 792-797.
23. Charrua, A., Cruz, C.D., Cruz, F. & Avelino, A. 2007. Transient receptor potential vanilloid subfamily 1 is essential for the generation of noxious bladder input and bladder overactivity in cystitis. J Urol 177, 1537-1541.
24. Charrua, A., Reguenga, C., Paule, C.C., Nagy, I., Cruz, F. & Avelino, A. 2008. Cystitis is associated with TRPV1b-downregulation in rat dorsal root ganglia. NeuroReport 19, 1469-1472.
25. Charrua, A., Cruz, C.D., Narayanan, S., Gharat, L., Gullapalli, S., Cruz, F. & Avelino, A. 2009a. GRC-6211, a new oral specific TRPV1 antagonist, decreases bladder overactivity and noxious bladder input in cystitis animal models. J Urol 181, 379-386.
26. Charrua, A., Reguenga, C., Cordeiro, J.M., Correiade-Sa, P., Paule, C., Nagy, I., Cruz, F. & Avelino, A. 2009b. Functional transient receptor potential vanilloid 1 is expressed in human urothelial cells. J Urol 182, 2944-2950.
27. Charrua, A., Avelino, A. & Cruz, F. 2011. Modulation of urinary bladder innervation: TRPV1 and botulinum toxin A. Handb Exp Pharmacol 345-374.
28. Chuang, H.H., Prescott, E.D., Kong, H., Shields, S., Jordt, S.E., Basbaum, A.I., Chao, M.V. & Julius, D. 2001. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4, 5)P2-mediated inhibition. Nature 411, 957-962.
29. Chung, M.K., Lee, J., Duraes, G. & Ro, J.Y. 2011. Lipopolysaccharide-induced pulpitis up-regulates TRPV1 in trigeminal ganglia. J Dent Res 90, 1103-1107.
30. Clapham, D.E., Julius, D., Montell, C. & Schultz, G. 2005. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol Rev 57, 427-450.
31. Cruz, F., Guimaraes, M., Silva, C. & Reis, M. 1997. Suppression of bladder hyperreflexia by intravesical resiniferatoxin. Lancet 350, 640-641.
32. Cuajungco, M.P., Grimm, C., Oshima, K., D'Hoedt, D., Nilius, B., Mensenkamp, A.R., Bindels, R.J., Plomann, M. & Heller, S. 2006. PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4. J Biol Chem 281, 18753-18762.
33. Dai, Y., Wang, S., Tominaga, M., Yamamoto, S., Fukuoka, T., Higashi, T., Kobayashi, K., Obata, K., Yamanaka, H. & Noguchi, K. 2007. Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117, 1979-1987.
34. Dattilio, A. & Vizzard, M.A. 2005. Up-regulation of protease activated receptors in bladder after cyclophosphamide induced cystitis and colocalization with capsaicin receptor (VR1) in bladder nerve fibers. J Urol 173, 635-639.
35. DeFalco, J., Duncton, M.A. & Emerling, D. 2011. TRPM8 biology and medicinal chemistry. Curr Top Med Chem 11, 2237-2252.
36. Dinis, P., Charrua, A., Avelino, A., Yaqoob, M., Bevan, S., Nagy, I. & Cruz, F. 2004. Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. J Neurosci 24, 11253-11263.
37. Du, S., Araki, I., Kobayashi, H., Zakoji, H., Sawada, N. & Takeda, M. 2008. Differential expression profile of cold (TRPA1) and cool (TRPM8) receptors in human urogenital organs. Urology 72, 450-455.
38. Eilers, H., Lee, S.Y., Hau, C.W., Logvinova, A. & Schumacher, M.A. 2007. The rat vanilloid receptor splice variant VR.5′sv blocks TRPV1 activation. NeuroReport 18, 969-973.
39. Everaerts, W., Nilius, B. & Owsianik, G. 2010a. The vanilloid transient receptor potential channel TRPV4: from structure to disease. Prog Biophys Mol Biol 103, 2-17.
40. Everaerts, W., Vriens, J., Owsianik, G., Appendino, G., Voets, T., De Ridder, D. & Nilius, B. 2010b. Functional characterization of transient receptor potential channels in mouse urothelial cells. Am J Physiol Renal Physiol 298, F692-F701.
41. Everaerts, W., Zhen, X., Ghosh, D., Vriens, J., Gevaert, T., Gilbert, J.P., Hayward, N.J., McNamara, C.R., Xue, F., Moran, M.M. et al. 2010c. Inhibition of the cation channel TRPV4 improves bladder function in mice and rats with cyclophosphamide-induced cystitis. Proc Natl Acad Sci U S A 107, 19084-19089.
42. Ferreira, J., da Silva, G.L. & Calixto, J.B. 2004. Contribution of vanilloid receptors to the overt nociception induced by B2 kinin receptor activation in mice. Br J Pharmacol 141, 787-794.
43. Gevaert, T., Vriens, J., Segal, A., Everaerts, W., Roskams, T., Talavera, K., Owsianik, G., Liedtke, W., Daelemans, D., Dewachter, I., Van Leuven, F., Voets, T., De Ridder, D. & Nilius, B. 2007. Deletion of the transient receptor potential cation channel TRPV4 impairs murine bladder voiding. J Clin Invest 117, 3453-3462.
44. Grant, A., Amadesi, S. & Bunnett, N.W. 2007. Protease-activated receptors: mechanisms by which proteases sensitize TRPV channels to induce neurogenic inflammation and pain. In: W.B. Liedtke & S. Heller (eds) TRP Ion Channel Function in Sensory Transduction and Cellular Signaling Cascades. CRC Press, Boca Raton (FL).
45. Hayashi, T., Kondo, T., Ishimatsu, M., Takeya, M., Igata, S., Nakamura, K. & Matsuoka, K. 2011. Function and expression pattern of TRPM8 in bladder afferent neurons associated with bladder outlet obstruction in rats. Auton Neurosci 164, 27-33.
46. Hayes, P., Meadows, H.J., Gunthorpe, M.J., Harries, M.H., Duckworth, D.M., Cairns, W., Harrison, D.C., Clarke, C.E., Ellington, K., Prinjha, R.K. et al. 2000. Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain 88, 205-215.
47. Honan, S.A. & McNaughton, P.A. 2007. Sensitisation of TRPV1 in rat sensory neurones by activation of SNSRs. Neurosci Lett 422, 1-6.
48. Huang, W., Rubinstein, J., Prieto, A.R. & Wang, D.H. 2010. Enhanced postmyocardial infarction fibrosis via stimulation of the transforming growth factor-beta-Smad2 signaling pathway: role of transient receptor potential vanilloid type 1 channels. J Hypertens 28, 367-376.
49. Janssen, D.A., Hoenderop, J.G., Jansen, K.C., Kemp, A.W., Heesakkers, J.P. & Schalken, J.A. 2011. The mechanoreceptor TRPV4 is localized in adherence junctions of the human bladder urothelium: a morphological study. J Urol 186, 1121-1127.
50. Ji, R.R., Samad, T.A., Jin, S.X., Schmoll, R. & Woolf, C.J. 2002. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36, 57-68.
51. Jin, M., Wu, Z., Chen, L., Jaimes, J., Collins, D., Walters, E.T. & O'Neil, R.G. 2011. Determinants of TRPV4 activity following selective activation by small molecule agonist GSK1016790A. PLoS ONE 6, e16713.
52. Jordt, S.E. & Julius, D. 2002. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108, 421-430.
53. Jung, J., Shin, J.S., Lee, S.Y., Hwang, S.W., Koo, J., Cho, H. & Oh, U. 2004. Phosphorylation of vanilloid receptor 1 by Ca2+/calmodulin-dependent kinase II regulates its vanilloid binding. J Biol Chem 279, 7048-7054.
54. Karashima, Y., Talavera, K., Everaerts, W., Janssens, A., Kwan, K.Y., Vennekens, R., Nilius, B. & Voets, T. 2009. TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci U S A 106, 1273-1278.
55. Khairatkar-Joshi, N. & Szallasi, A. 2009. TRPV1 antagonists: the challenges for therapeutic targeting. Trends Mol Med 15, 14-22.
56. Knowlton, W.M., Bifolck-Fisher, A., Bautista, D.M. & McKemy, D.D. 2010. TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo. Pain 150, 340-350.
57. Koplas, P.A., Rosenberg, R.L. & Oxford, G.S. 1997. The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17, 3525-3537.
58. Kullmann, F.A., Shah, M.A., Birder, L.A. & de Groat, W.C. 2009. Functional TRP and ASIC-like channels in cultured urothelial cells from the rat. Am J Physiol Renal Physiol 296, F892-F901.
59. Kwan, K.Y., Allchorne, A.J., Vollrath, M.A., Christensen, A.P., Zhang, D.S., Woolf, C.J. & Corey, D.P. 2006. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50, 277-289.
60. Lamb, K., Gebhart, G.F. & Bielefeldt, K. 2004. Increased nerve growth factor expression triggers bladder overactivity. J Pain 5, 150-156.
61. Lashinger, E.S., Steiginga, M.S., Hieble, J.P., Leon, L.A., Gardner, S.D., Nagilla, R., Davenport, E.A., Hoffman, B.E., Laping, N.J. & Su, X. 2008. AMTB, a TRPM8 channel blocker: evidence in rats for activity in overactive bladder and painful bladder syndrome. Am J Physiol Renal Physiol 295, F803-F810.
62. Liu, H.T. & Kuo, H.C. 2007. Increased expression of transient receptor potential vanilloid subfamily 1 in the bladder predicts the response to intravesical instillations of resiniferatoxin in patients with refractory idiopathic detrusor overactivity. BJU Int 100, 1086-1090.
63. + in the desensitization responses to capsaicin, zingerone and olvanil in rat trigeminal ganglion neurons. Brain Res 809, 246-252.
64. +) entry in vascular endothelial cells. Cell Calcium 50, 502-509.
65. Macpherson, L.J., Geierstanger, B.H., Viswanath, V., Bandell, M., Eid, S.R., Hwang, S. & Patapoutian, A. 2005. The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15, 929-934.
66. Macpherson, L.J., Hwang, S.W., Miyamoto, T., Dubin, A.E., Patapoutian, A. & Story, G.M. 2006. More than cool: promiscuous relationships of menthol and other sensory compounds. Mol Cell Neurosci 32, 335-343.
67. Macpherson, L.J., Dubin, A.E., Evans, M.J., Marr, F., Schultz, P.G., Cravatt, B.F. & Patapoutian, A. 2007. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445, 541-545.
68. McKemy, D.D., Neuhausser, W.M. & Julius, D. 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416, 52-58.
69. + influx and ATP release in primary urothelial cell cultures. J Biol Chem 284, 21257-21264.
70. Mohapatra, D.P. & Nau, C. 2003. Desensitization of capsaicin-activated currents in the vanilloid receptor TRPV1 is decreased by the cyclic AMP-dependent protein kinase pathway. J Biol Chem 278, 50080-50090.
71. Morenilla-Palao, C., Planells-Cases, R., Garcia-Sanz, N. & Ferrer-Montiel, A. 2004. Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J Biol Chem 279, 25665-25672.
72. Mukerji, G., Yiangou, Y., Agarwal, S.K. & Anand, P. 2006. Transient receptor potential vanilloid receptor subtype 1 in painful bladder syndrome and its correlation with pain. J Urol 176, 797-801.
73. Muraki, K., Iwata, Y., Katanosaka, Y., Ito, T., Ohya, S., Shigekawa, M. & Imaizumi, Y. 2003. TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93, 829-838.
74. Nagata, K., Duggan, A., Kumar, G. & Garcia-Anoveros, J. 2005. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25, 4052-4061.
75. Nagy, I., Santha, P., Jancso, G. & Urban, L. 2004. The role of the vanilloid (capsaicin) receptor (TRPV1) in physiology and pathology. Eur J Pharmacol 500, 351-369.
76. Neeper, M.P., Liu, Y., Hutchinson, T.L., Wang, Y., Flores, C.M. & Qin, N. 2007. Activation properties of heterologously expressed mammalian TRPV2: evidence for species dependence. J Biol Chem 282, 15894-15902.
77. Nomoto, Y., Yoshida, A., Ikeda, S., Kamikawa, Y., Harada, K., Ohwatashi, A. & Kawahira, K. 2008. Effect of menthol on detrusor smooth-muscle contraction and the micturition reflex in rats. Urology 72, 701-705.
78. Park, U., Vastani, N., Guan, Y., Raja, S.N., Koltzenburg, M. & Caterina, M.J. 2011. TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. J Neurosci 31, 11425-11436.
79. Payne, C.K., Mosbaugh, P.G., Forrest, J.B., Evans, R.J., Whitmore, K.E., Antoci, J.P., Perez-Marrero, R., Jacoby, K., Diokno, A.C., O'Reilly, K.J., Griebling, T.L., Vasavada, S.P., Yu, A.S. & Frumkin, L.R. 2005. Intravesical resiniferatoxin for the treatment of interstitial cystitis: a randomized, double-blind, placebo controlled trial. J Urol 173, 1590-1594.
80. 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. & Patapoutian, A. 2002. A TRP channel that senses cold stimuli and menthol. Cell 108, 705-715.
81. Planells-Cases, R., Garcia-Sanz, N., Morenilla-Palao, C. & Ferrer-Montiel, A. 2005. Functional aspects and mechanisms of TRPV1 involvement in neurogenic inflammation that leads to thermal hyperalgesia. Pflugers Arch 451, 151-159.
82. Saban, M.R., Davis, C.A., Avelino, A., Cruz, F., Maier, J., Bjorling, D.E., Sferra, T.J., Hurst, R.E. & Saban, R. 2011. VEGF signaling mediates bladder neuroplasticity and inflammation in response to BCG. BMC Physiol 11, 16.
83. Sadofsky, L.R., Boa, A.N., Maher, S.A., Birrell, M.A., Belvisi, M.G. & Morice, A.H. 2011. TRPA1 is activated by direct addition of cysteine residues to the N-hydroxysuccinyl esters of acrylic and cinnamic acids. Pharmacol Res 63, 30-36.
84. Santos-Silva, A., Charrua, A., Cruz, C.D., Gharat, L., Avelino, A. & Cruz, F. 2011. Rat detrusor overactivity induced by chronic spinalization can be abolished by a transient receptor potential vanilloid 1 (TRPV1) antagonist. Auton Neurosci 166, 35-38.
85. Shibata, Y., Ugawa, S., Imura, M., Kubota, Y., Ueda, T., Kojima, Y., Ishida, Y., Sasaki, S., Hayashi, Y., Kohri, K. & Shimada, S. 2011. TRPM8-expressing dorsal root ganglion neurons project dichotomizing axons to both skin and bladder in rats. NeuroReport 22, 61-67.
86. Silva, C., Ribeiro, M.J. & Cruz, F. 2002. The effect of intravesical resiniferatoxin in patients with idiopathic detrusor instability suggests that involuntary detrusor contractions are triggered by C-fiber input. J Urol 168, 575-579.
87. Silva, C., Silva, J., Castro, H., Reis, F., Dinis, P., Avelino, A. & Cruz, F. 2007. Bladder sensory desensitization decreases urinary urgency. BMC Urol 7, 9.
88. Smith, P.L., Maloney, K.N., Pothen, R.G., Clardy, J. & Clapham, D.E. 2006. Bisandrographolide from Andrographis paniculata activates TRPV4 channels. J Biol Chem 281, 29897-29904.
89. Stein, R.J., Santos, S., Nagatomi, J., Hayashi, Y., Minnery, B.S., Xavier, M., Patel, A.S., Nelson, J.B., Futrell, W.J., Yoshimura, N., Chancellor, M.B. & De Miguel, F. 2004. Cool (TRPM8) and hot (TRPV1) receptors in the bladder and male genital tract. J Urol 172, 1175-1178.
90. Stotz, S.C., Vriens, J., Martyn, D., Clardy, J. & Clapham, D.E. 2008. Citral sensing by Transient [corrected] receptor potential channels in dorsal root ganglion neurons. PLoS ONE 3, e2082.
91. Streng, T., Axelsson, H.E., Hedlund, P., Andersson, D.A., Jordt, S.E., Bevan, S., Andersson, K.E., Hogestatt, E.D. & Zygmunt, P.M. 2008. Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder. Eur Urol 53, 391-399.
92. Studer, M. & McNaughton, P.A. 2010. Modulation of single-channel properties of TRPV1 by phosphorylation. J Physiol 588, 3743-3756.
93. Sun, Y. & Chai, T.C. 2006. Augmented extracellular ATP signaling in bladder urothelial cells from patients with interstitial cystitis. Am J Physiol Cell Physiol 290, C27-C34.
94. Sun, Y., Keay, S., De Deyne, P.G. & Chai, T.C. 2001. Augmented stretch activated adenosine triphosphate release from bladder uroepithelial cells in patients with interstitial cystitis. J Urol 166, 1951-1956.
95. Surprenant, A. 2007. Pain TRP-ed up by PARs. J Physiol 578, 631.
96. Suzuki, M., Mizuno, A., Kodaira, K. & Imai, M. 2003. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278, 22664-22668.
97. Szallasi, A. & Blumberg, P.M. 1989. Resiniferatoxin, a phorbol-related diterpene, acts as an ultrapotent analog of capsaicin, the irritant constituent in red pepper. Neuroscience 30, 515-520.
98. Szallasi, A. & Blumberg, P.M. 1999. Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol Rev 51, 159-212.
99. Thorneloe, K.S., Sulpizio, A.C., Lin, Z., Figueroa, D.J., Clouse, A.K., McCafferty, G.P., Chendrimada, T.P., Lashinger, E.S., Gordon, E., Evans, L. et al. 2008. N-((1S)-1-{[4-((2S)-2-{[(2, 4-dichlorophenyl)sulfonyl]amino}-3-hydroxypropa noyl)-1-piperazinyl]carbonyl}-3-methylbutyl)-1-benzothiophene-2-carboxamid e (GSK1016790A), a novel and potent transient receptor potential vanilloid 4 channel agonist induces urinary bladder contraction and hyperactivity: Part I. J Pharmacol Exp Ther 326, 432-442.
100. Tominaga, M., Caterina, M.J., Malmberg, A.B., Rosen, T.A., Gilbert, H., Skinner, K., Raumann, B.E., Basbaum, A.I. & Julius, D. 1998. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21, 531-543.
101. Tsukimi, Y., Mizuyachi, K., Yamasaki, T., Niki, T. & Hayashi, F. 2005. Cold response of the bladder in guinea pig: involvement of transient receptor potential channel, TRPM8. Urology 65, 406-410.
102. Vellani, V., Mapplebeck, S., Moriondo, A., Davis, J.B. & McNaughton, P.A. 2001. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534, 813-825.
103. Vellani, V., Kinsey, A.M., Prandini, M., Hechtfischer, S.C., Reeh, P., Magherini, P.C., Giacomoni, C. & McNaughton, P.A. 2010. Protease activated receptors 1 and 4 sensitize TRPV1 in nociceptive neurones. Mol Pain 6, 61.
104. Vergnolle, N., Cenac, N., Altier, C., Cellars, L., Chapman, K., Zamponi, G.W., Materazzi, S., Nassini, R., Liedtke, W., Cattaruzza, F., Grady, E.F., Geppetti, P. & Bunnett, N.W. 2010. A role for transient receptor potential vanilloid 4 in tonicity-induced neurogenic inflammation. Br J Pharmacol 159, 1161-1173.
105. Vincent, F., Acevedo, A., Nguyen, M.T., Dourado, M., DeFalco, J., Gustafson, A., Spiro, P., Emerling, D.E., Kelly, M.G. & Duncton, M.A. 2009. Identification and characterization of novel TRPV4 modulators. Biochem Biophys Res Commun 389, 490-494.
106. Vos, M.H., Neelands, T.R., McDonald, H.A., Choi, W., Kroeger, P.E., Puttfarcken, P.S., Faltynek, C.R., Moreland, R.B. & Han, P. 2006. TRPV1b overexpression negatively regulates TRPV1 responsiveness to capsaicin, heat and low pH in HEK293 cells. J Neurochem 99, 1088-1102.
107. Vriens, J., Watanabe, H., Janssens, A., Droogmans, G., Voets, T. & Nilius, B. 2004. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci U S A 101, 396-401.
108. Vriens, J., Owsianik, G., Fisslthaler, B., Suzuki, M., Janssens, A., Voets, T., Morisseau, C., Hammock, B.D., Fleming, I., Busse, R. & Nilius, B. 2005. Modulation of the Ca2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res 97, 908-915.
109. Vyklicky, L., Novakova-Tousova, K., Benedikt, J., Samad, A., Touska, F. & Vlachova, V. 2008. Calcium-dependent desensitization of vanilloid receptor TRPV1: a mechanism possibly involved in analgesia induced by topical application of capsaicin. Physiol Res 57(Suppl. 3), S59-S68.
110. Wang, C., Hu, H.Z., Colton, C.K., Wood, J.D. & Zhu, M.X. 2004. An alternative splicing product of the murine trpv1 gene dominant negatively modulates the activity of TRPV1 channels. J Biol Chem 279, 37423-37430.
111. Wang, Z.Y., Wang, P., Merriam, F.V. & Bjorling, D.E. 2008. Lack of TRPV1 inhibits cystitis-induced increased mechanical sensitivity in mice. Pain 139, 158-167.
112. 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. & Nilius, B. 2002. Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277, 13569-13577.
113. Wegierski, T., Hill, K., Schaefer, M. & Walz, G. 2006. The HECT ubiquitin ligase AIP4 regulates the cell surface expression of select TRP channels. EMBO J 25, 5659-5669.
114. Welch, J.M., Simon, S.A. & Reinhart, P.H. 2000. The activation mechanism of rat vanilloid receptor 1 by capsaicin involves the pore domain and differs from the activation by either acid or heat. Proc Natl Acad Sci USA 97, 13889-13894.
115. Xu, X., Gordon, E., Lin, Z., Lozinskaya, I.M., Chen, Y. & Thorneloe, K.S. 2009. Functional TRPV4 channels and an absence of capsaicin-evoked currents in freshly-isolated, guinea-pig urothelial cells. Channels (Austin) 3, 156-160.
116. Xue, Q., Jong, B., Chen, T. & Schumacher, M.A. 2007. Transcription of rat TRPV1 utilizes a dual promoter system that is positively regulated by nerve growth factor. J Neurochem 101, 212-222.
117. Yamada, T., Ueda, T., Shibata, Y., Ikegami, Y., Saito, M., Ishida, Y., Ugawa, S., Kohri, K. & Shimada, S. 2010. TRPV2 activation induces apoptotic cell death in human T24 bladder cancer cells: a potential therapeutic target for bladder cancer. Urology 76(509), e1-e7.
118. Yu, Y.B., Yang, J., Zuo, X.L., Gao, L.J., Wang, P. & Li, Y.Q. 2010. Transient receptor potential vanilloid-1 (TRPV1) and ankyrin-1 (TRPA1) participate in visceral hyperalgesia in chronic water avoidance stress rat model. Neurochem Res 35, 797-803.
119. Yu, W., Hill, W.G., Apodaca, G. & Zeidel, M.L. 2011. Expression and distribution of transient receptor potential (TRP) channels in bladder epithelium. Am J Physiol Renal Physiol 300, F49-F59.
120. Zhang, X., Huang, J. & McNaughton, P.A. 2005. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24, 4211-4223.
121. Zhuang, Z.Y., Xu, H., Clapham, D.E. & Ji, R.R. 2004. Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 24, 8300-8309.
122. Zvara, P. & Vizzard, M.A. 2007. Exogenous overexpression of nerve growth factor in the urinary bladder produces bladder overactivity and altered micturition circuitry in the lumbosacral spinal cord. BMC Physiol 7, 9.
123. Zygmunt, P.M., Petersson, J., Andersson, D.A., Chuang, H., Sorgard, M., Di Marzo, V., Julius, D. & Hogestatt, E.D. 1999. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400, 452-457.