The thermo-TRP ion channel family: Properties and therapeutic implications

British Journal of Pharmacology

Volumn 165, Issue 4, 2012, Pages 787-801

  Vay, Laura ^a   Gu, Chunjing ^a   McNaughton, Peter A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

artemin; GDNF; hyperalgesia; neurotrophic factor; NGF; nociceptor; pain; sensitization; thermo TRP; TRP ion channels; TRPV1

Indexed keywords

(5 TERT BUTYL 2,3 DIHYDRO 1H INDEN 1 YL) 3 (1H INDAZOL 4 YL)UREA; 1 (2 BROMOPHENYL) 3 [1 (5 TRIFLUOROMETHYL 2 PYRIDINYL) 3 PYRROLIDINYL]UREA; ALLICIN; CAMPHOR; CAPSAZEPINE; CARVACROL; CINEOLE; CINNAMALDEHYDE; CLOTRIMAZOLE; ETOMIDATE; EUGENOL; GINGEROL; ISOFLURANE; LIDOCAINE ETHOBROMIDE; MENTHOL; N [4 [6 [4 (TRIFLUOROMETHYL)PHENYL] 4 PYRIMIDINYLOXY]BENZOTHIAZOL 2 YL]ACETAMIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROPOFOL; RESINIFERATOXIN; THYMOL; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; UNINDEXED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 1 ANTAGONIST; VANILLOID RECEPTOR 2; VANILLOID RECEPTOR 3; VANILLOID RECEPTOR 4; VANILLOID RECEPTOR AGONIST;

ALLODYNIA; ANALGESIC ACTIVITY; COLD SENSATION; DRUG RECEPTOR BINDING; DRUG TARGETING; HEAT SENSATION; HUMAN; HYPERALGESIA; HYPERTHERMIA; IC 50; INTRACELLULAR SIGNALING; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; REVIEW; SENSORY NERVE; STIMULUS RESPONSE;

ANIMALS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PAIN; RECEPTORS, G-PROTEIN-COUPLED; TEMPERATURE; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84856269228     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01601.x     Document Type: Review

References (184)

1. Airaksinen MS, Titievsky A, Saarma M, (1999). GDNF family neurotrophic factor signaling: four masters, one servant? Mol Cell Neurosci 13: 313-325. (Pubitemid 29256872)
2. Albers KM, Woodbury CJ, Ritter AM, Davis BM, Koerber HR, (2006). Glial cell-line-derived neurotrophic factor expression in skin alters the mechanical sensitivity of cutaneous nociceptors. J Neurosci 26: 2981-2990.
3. Alessandri-Haber N, Joseph E, Dina OA, Liedtke W, Levine JD, (2005). TRPV4 mediates pain-related behavior induced by mild hypertonic stimuli in the presence of inflammatory mediator. Pain 118: 70-79. (Pubitemid 41566587)
4. Babes A, Zorzon D, Reid G, (2004). Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur J Neurosci 20: 2276-2282. (Pubitemid 39472390)
5. Babes A, Zorzon D, Reid G, (2006). A novel type of cold-sensitive neuron in rat dorsal root ganglia with rapid adaptation to cooling stimuli. Eur J Neurosci 24: 691-698. (Pubitemid 44232515)
6. Backonja MM, Walk D, Edwards RR, Sehgal N, Moeller-Bertram T, Wasan A, et al,. (2009). Quantitative sensory testing in measurement of neuropathic pain phenomena and other sensory abnormalities. Clin J Pain 25: 641-647.
7. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, et al,. (2004). Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41: 849-857. (Pubitemid 38429729)
8. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Hogestatt ED, et al,. (2005). Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 102: 12248-12252. (Pubitemid 41291160)
9. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, et al,. (2006). TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124: 1269-1282.
10. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, et al,. (2007). The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448: 204-208. (Pubitemid 47067367)
11. Bavencoffe A, Gkika D, Kondratskyi A, Beck B, Borowiec AS, Bidaux G, et al,. (2010). The transient receptor potential channel TRPM8 is inhibited via the alpha 2A adrenoreceptor signaling pathway. J Biol Chem 285: 9410-9419.
12. Belmonte C, Brock JA, Viana F, (2009). Converting cold into pain. Exp Brain Res 196: 13-30.
13. Bender FL, Mederos YS, Li Y, Ji A, Weihe E, Gudermann T, et al,. (2005). The temperature-sensitive ion channel TRPV2 is endogenously expressed and functional in the primary sensory cell line F-11. Cell Physiol Biochem 15: 183-194.
14. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW, (2002). cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35: 721-731. (Pubitemid 35223031)
15. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, et al,. (2003). Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 100: 12480-12485. (Pubitemid 37271585)
16. Binshtok AM, Bean BP, Woolf CJ, (2007). Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 449: 607-610. (Pubitemid 47525153)
17. Binshtok AM, Gerner P, Oh SB, Puopolo M, Suzuki S, Roberson DP, et al,. (2009). Coapplication of lidocaine and the permanently charged sodium channel blocker QX-314 produces a long-lasting nociceptive blockade in rodents. Anesthesiology 111: 127-137.
18. Boels K, Glassmeier G, Herrmann D, Riedel IB, Hampe W, Kojima I, et al,. (2001). The neuropeptide head activator induces activation and translocation of the growth-factor-regulated Ca(2+)-permeable channel GRC. J Cell Sci 114: 3599-3606. (Pubitemid 33041042)
19. Bonnington JK, McNaughton PA, (2003). Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. J Physiol 551: 433-446. (Pubitemid 37121702)
20. Caceres AI, Brackmann M, Elia MD, Bessac BF, del Camino D, D'Amours M, et al,. (2009). A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc Natl Acad Sci USA 106: 9099-9104.
21. Camprubi-Robles M, Planells-Cases R, Ferrer-Montiel A, (2009). Differential contribution of SNARE-dependent exocytosis to inflammatory potentiation of TRPV1 in nociceptors. FASEB J 23: 3722-3733.
22. Caterina MJ, (2003). Vanilloid receptors take a TRP beyond the sensory afferent. Pain 105: 5-9. (Pubitemid 37162468)
23. Caterina MJ, Julius D, (1999). Sense and specificity: a molecular identity for nociceptors. Curr Opin Neurobiol 9: 525-530. (Pubitemid 29484374)
24. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D, (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824. (Pubitemid 27462969)
25. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D, (1999). A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398: 436-441. (Pubitemid 29180377)
26. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, et al,. (2000). Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313. (Pubitemid 30226186)
27. Cesare P, McNaughton PA, (1996). A novel heat-activated current in nociceptive neurons, and its sensitization by bradykinin. Proc Natl Acad Sci USA 93: 15435-15439. (Pubitemid 27009617)
28. Chizh BA, O'Donnell MB, Napolitano A, Wang J, Brooke AC, Aylott MC, et al,. (2007). The effects of the TRPV1 antagonist SB-705498 on TRPV1 receptor-mediated activity and inflammatory hyperalgesia in humans. Pain 132: 132-141. (Pubitemid 47494566)
29. Chrubasik S, Weiser T, Beime B, (2010). Effectiveness and safety of topical capsaicin cream in the treatment of chronic soft tissue pain. Phytother Res 24: 1877-1885.
30. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, et al,. (2001). Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411: 957-962. (Pubitemid 32601493)
31. Chuang HH, Neuhausser WM, Julius D, (2004). The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43: 859-869. (Pubitemid 39215016)
32. Chung MK, Guler AD, Caterina MJ, (2008). TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 11: 555-564. (Pubitemid 351595196)
33. Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D'Andrea MR, et al,. (2007). Attenuated cold sensitivity in TRPM8 null mice. Neuron 54: 379-386. (Pubitemid 46671410)
34. Colsoul B, Nilius B, Vennekens R, (2009). On the putative role of transient receptor potential cation channels in asthma. Clin Exp Allergy 39: 1456-1466.
35. Corey DP, Garcia-Anoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, et al,. (2004). TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432: 723-730. (Pubitemid 39656287)
36. Crutchlow M, Pharmacologic inhibition of TRPV1 impairs sensation of potentially injurious heat in healthy subjects. ASCPT 2009 annual meeting, 69. 2009.
37. Dai Y, Wang S, Tominaga M, Yamamoto S, Fukuoka T, Higashi T, et al,. (2007). Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117: 1979-1987. (Pubitemid 47036332)
38. Davis AJ, Perkins MN, (1996). Substance P and capsaicin-induced mechanical hyperalgesia in the rat knee joint; the involvement of bradykinin B1 and B2 receptors. Br J Pharmacol 118: 2206-2212. (Pubitemid 26292597)
39. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, et al,. (2000). Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405: 183-187. (Pubitemid 30313536)
40. De la Pena E, Malkia A, Cabedo H, Belmonte C, Viana F, (2005). The contribution of TRPM8 channels to cold sensing in mammalian neurones. J Physiol 567: 415-426. (Pubitemid 41301042)
41. Dhaka A, Viswanath V, Patapoutian A, (2006). Trp ion channels and temperature sensation. Annu Rev Neurosci 29: 135-161. (Pubitemid 44476842)
42. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A, (2007). TRPM8 is required for cold sensation in mice. Neuron 54: 371-378. (Pubitemid 46659806)
43. Diogenes A, Akopian AN, Hargreaves KM, (2007). NGF up-regulates TRPA1: implications for orofacial pain. J Dent Res 86: 550-555.
44. Doerner JF, Gisselmann G, Hatt H, Wetzel CH, (2007). Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 282: 13180-13189. (Pubitemid 47100541)
45. Doherty EM, Fotsch C, Bannon AW, Bo Y, Chen N, Dominguez C, et al,. (2007). Novel vanilloid receptor-1 antagonists: 2. Structure-activity relationships of 4-oxopyrimidines leading to the selection of a clinical candidate. J Med Chem 50: 3515-3527. (Pubitemid 47195460)
46. Eid SR, Crown ED, Moore EL, Liang HA, Choong KC, Dima S, et al,. (2008). HC-030031, a TRPA1 selective antagonist, attenuates inflammatory- and neuropathy-induced mechanical hypersensitivity. Mol Pain 4: 48.
47. Fajardo O, Meseguer V, Belmonte C, Viana F, (2008). TRPA1 channels mediate cold temperature sensing in mammalian vagal sensory neurons: pharmacological and genetic evidence. J Neurosci 28: 7863-7875.
48. Fan HC, Zhang X, McNaughton PA, (2009). Activation of the TRPV4 ion channel is enhanced by phosphorylation. J Biol Chem 284: 27884-27891.
49. Farinas I, (1999). Neurotrophin actions during the development of the peripheral nervous system. Microsc Res Tech 45: 233-242. (Pubitemid 29264987)
50. Fleetwood-Walker SM, Proudfoot CW, Garry EM, Allchorne A, Vinuela-Fernandez I, Mitchell R, (2007). Cold comfort pharm. Trends Pharmacol Sci 28: 621-628. (Pubitemid 350166572)
51. Frederick J, Buck ME, Matson DJ, Cortright DN, (2007). Increased TRPA1, TRPM8, and TRPV2 expression in dorsal root ganglia by nerve injury. Biochem Biophys Res Commun 358: 1058-1064. (Pubitemid 46828995)
52. Gaudet R, (2009). Divide and conquer: high resolution structural information on TRP channel fragments. J Gen Physiol 133: 231-237.
53. Gavva NR, Bannon AW, Surapaneni S, Hovland DN Jr, Lehto SG, Gore A, et al,. (2007). The vanilloid receptor TRPV1 is tonically activated in vivo and involved in body temperature regulation. J Neurosci 27: 3366-3374. (Pubitemid 46515121)
54. Gavva NR, Treanor JJ, Garami A, Fang L, Surapaneni S, Akrami A, et al,. (2008). Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 136: 202-210.
55. Gevaert T, Vriens J, Segal A, Everaerts W, Roskams T, Talavera K, et al,. (2007). Deletion of the transient receptor potential cation channel TRPV4 impairs murine bladder voiding. J Clin Invest 117: 3453-3462. (Pubitemid 350097001)
56. Gomtsyan A, Faltynek CR, (2010). Vanilloid Receptor TRPV1 in Drug Discovery. John Wiley & Sons: Hoboken, NJ.
57. Gomtsyan A, Bayburt EK, Schmidt RG, Surowy CS, Honore P, Marsh KC, et al,. (2008). Identification of (R)-1-(5-tert-butyl-2, 3-dihydro-1H-inden-1-yl)- 3-(1H-indazol-4-yl)urea (ABT-102) as a potent TRPV1 antagonist for pain management. J Med Chem 51: 392-395. (Pubitemid 351252266)
58. Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, et al,. (2010). Molecular basis of infrared detection by snakes. Nature 464: 1006-1011.
59. Grandl J, Hu H, Bandell M, Bursulaya B, Schmidt M, Petrus M, et al,. (2008). Pore region of TRPV3 ion channel is specifically required for heat activation. Nat Neurosci 11: 1007-1013.
60. Hautkappe M, Roizen MF, Toledano A, Roth S, Jeffries JA, Ostermeier AM, (1998). Review of the effectiveness of capsaicin for painful cutaneous disorders and neural dysfunction. Clin J Pain 14: 97-106. (Pubitemid 28270206)
61. Hinman A, Chuang HH, Bautista DM, Julius D, (2006). TRP channel activation by reversible covalent modification. Proc Natl Acad Sci USA 103: 19564-19568. (Pubitemid 46026070)
62. Hisanaga E, Nagasawa M, Ueki K, Kulkarni RN, Mori M, Kojima I, (2009). Regulation of calcium-permeable TRPV2 channel by insulin in pancreatic beta-cells. Diabetes 58: 174-184.
63. Honore P, Chandran P, Hernandez G, Gauvin DM, Mikusa JP, Zhong C, et al,. (2009). Repeated dosing of ABT-102, a potent and selective TRPV1 antagonist, enhances TRPV1-mediated analgesic activity in rodents, but attenuates antagonist-induced hyperthermia. Pain 142: 27-35.
64. Hu HZ, Gu Q, Wang C, Colton CK, Tang J, Kinoshita-Kawada M, et al,. (2004). 2-aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279: 35741-35748. (Pubitemid 39100579)
65. Hu H, Tian J, Zhu Y, Wang C, Xiao R, Herz JM, et al,. (2010). Activation of TRPA1 channels by fenamate nonsteroidal anti-inflammatory drugs. Pflugers Arch 459: 579-592.
66. Hua XY, Chen P, Hwang J, Yaksh TL, (1997). Antinociception induced by civamide, an orally active capsaicin analogue. Pain 71: 313-322. (Pubitemid 27288146)
67. Huang J, Zhang X, McNaughton PA, (2006). Modulation of temperature-sensitive TRP channels. Semin Cell Dev Biol 17: 638-645. (Pubitemid 46137021)
68. Huang SM, Lee H, Chung MK, Park U, Yu YY, Bradshaw HB, et al,. (2008). Overexpressed transient receptor potential vanilloid 3 ion channels in skin keratinocytes modulate pain sensitivity via prostaglandin E2. J Neurosci 28: 13727-13737.
69. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, et al,. (2000). Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97: 6155-6160. (Pubitemid 30367539)
70. Jeske NA, Diogenes A, Ruparel NB, Fehrenbacher JC, Henry M, Akopian AN, et al,. (2008). A-kinase anchoring protein mediates TRPV1 thermal hyperalgesia through PKA phosphorylation of TRPV1. Pain 138: 604-616.
71. Jeske NA, Patwardhan AM, Ruparel NB, Akopian AN, Shapiro MS, Henry MA, (2009). A-kinase anchoring protein 150 controls protein kinase C-mediated phosphorylation and sensitization of TRPV1. Pain 146: 301-307.
72. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ, (2002). p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36: 57-68.
73. Jung J, Sun WH, Kwak J, Lee S-Y, Kang C-J, Won BK, et al,. (1999). Capsaicin binds to the intracellular domain of the capsaicin-activated ion channel. J Neurosci 19: 529-538. (Pubitemid 29036004)
74. Kanzaki M, Zhang YQ, Mashima H, Li L, Shibata H, Kojima I, (1999). Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1: 165-170. (Pubitemid 129656021)
75. Karashima Y, Damann N, Prenen J, Talavera K, Segal A, Voets T, et al,. (2007). Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 27: 9874-9884. (Pubitemid 47403994)
76. Karashima Y, Prenen J, Meseguer V, Owsianik G, Voets T, Nilius B, (2008). Modulation of the transient receptor potential channel TRPA1 by phosphatidylinositol 4,5-biphosphate manipulators. Pflugers Arch 457: 77-89.
77. Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY, Vennekens R, et al,. (2009). TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci USA 106: 1273-1278.
78. Katsura H, Obata K, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, et al,. (2006). Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats. Exp Neurol 200: 112-123. (Pubitemid 44080752)
79. Kim D, Cavanaugh EJ, Simkin D, (2008). Inhibition of transient receptor potential A1 channel by phosphatidylinositol-4, 5-bisphosphate. Am J Physiol Cell Physiol 295: C92-C99. (Pubitemid 352755793)
80. Knowlton WM, Bifolck-Fisher A, Bautista DM, McKemy DD, (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.
81. Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, et al,. (2005). Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J Comp Neurol 493: 596-606. (Pubitemid 41780630)
82. Koerber HR, McIlwrath SL, Lawson JJ, Malin SA, Anderson CE, Jankowski MP, et al,. (2010). Cutaneous C-polymodal fibers lacking TRPV1 are sensitized to heat following inflammation, but fail to drive heat hyperalgesia in the absence of TPV1 containing C-heat fibers. Mol Pain 6: 58.
83. Kwak JY, Jung JY, Hwang SW, Lee WT, Oh U, (1998). A capsaicin-receptor antagonist, capsazepine, reduces inflammation-induced hyperalgesic responses in the rat: evidence for an endogenous capsaicin-like substance. Neuroscience 86: 619-626. (Pubitemid 28293938)
84. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, et al,. (2006). TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50: 277-289.
85. Kwan KY, Glazer JM, Corey DP, Rice FL, Stucky CL, (2009). TRPA1 modulates mechanotransduction in cutaneous sensory neurons. J Neurosci 29: 4808-4819.
86. Kym PR, Kort ME, Hutchins CW, (2009). Analgesic potential of TRPV1 antagonists. Biochem Pharmacol 78: 211-216.
87. Lawson JJ, McIlwrath SL, Woodbury CJ, Davis BM, Koerber HR, (2008). TRPV1 unlike TRPV2 is restricted to a subset of mechanically insensitive cutaneous nociceptors responding to heat. J Pain 9: 298-308.
88. Lechner SG, Frenzel H, Wang R, Lewin GR, (2009). Developmental waves of mechanosensitivity acquisition in sensory neuron subtypes during embryonic development. EMBO J 28: 1479-1491.
89. Lee H, Iida T, Mizuno A, Suzuki M, Caterina MJ, (2005). Altered thermal selection behavior in mice lacking transient receptor potential vanilloid 4. J Neurosci 25: 1304-1310. (Pubitemid 40268973)
90. Lehto SG, Tamir R, Deng H, Klionsky L, Kuang R, Le A, et al,. (2008). Antihyperalgesic effects of (R,E)-N-(2-hydroxy-2,3-dihydro-1H-inden-4-yl)-3-(2- (piperidin-1-yl)-4-(tri fluoromethyl)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. (Pubitemid 351872146)
91. Lewin GR, Barde YA, (1996). Physiology of the neurotrophins. Annu Rev Neurosci 19: 289-317. (Pubitemid 26080831)
92. Lewin GR, Mendell LM, (1993). Nerve growth factor and nociception. Trends Neurosci 16: 353-359. (Pubitemid 23232008)
93. Lewin GR, Rueff A, Mendell LM, (1994). Peripheral and central mechanisms of NGF-induced hyperalgesia. European. J Neurosci 6: 1903-1912.
94. Link TM, Park U, Vonakis BM, Raben DM, Soloski MJ, Caterina MJ, (2010). TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat Immunol 11: 232-239.
95. Linte RM, Ciobanu C, Reid G, Babes A, (2007). Desensitization of cold- and menthol-sensitive rat dorsal root ganglion neurones by inflammatory mediators. Exp Brain Res 178: 89-98. (Pubitemid 46364862)
96. Lopshire JC, Nicol GD, (1998). The cAMP transduction cascade mediates the prostaglandin E2 enhancement of the capsaicin-elicited current in rat sensory neurons: whole-cell and single-channel studies. J Neurosci 18: 6081-6092. (Pubitemid 28373217)
97. McKemy DD, Neuhausser WM, Julius D, (2002). Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52-58. (Pubitemid 34215395)
98. McMahon SB, Armanini MP, Ling LH, Phillips HS, (1994). Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12: 1161-1171. (Pubitemid 24178207)
99. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, et al,. (2007). TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci USA 104: 13525-13530. (Pubitemid 47293978)
100. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF, et al,. (2007). Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445: 541-545. (Pubitemid 46197634)
101. Malin SA, Molliver DC, Koerber HR, Cornuet P, Frye R, Albers KM, et al,. (2006). Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J Neurosci 26: 8588-8599. (Pubitemid 44316188)
102. Malkia A, Madrid R, Meseguer V, De La PE, Valero M, Belmonte C, et al,. (2007). Bidirectional shifts of TRPM8 channel gating by temperature and chemical agents modulate the cold sensitivity of mammalian thermoreceptors. J Physiol 581: 155-174. (Pubitemid 46712034)
103. Mandadi S, Tominaga T, Numazaki M, Murayama N, Saito N, Armati PJ, et al,. (2006). Increased sensitivity of desensitized TRPV1 by PMA occurs through PKCepsilon-mediated phosphorylation at S800. Pain 123: 106-116. (Pubitemid 43816763)
104. Mandadi S, Sokabe T, Shibasaki K, Katanosaka K, Mizuno A, Moqrich A, et al,. (2009). TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pflugers Arch 458: 1093-1102.
105. Milenkovic N, Frahm C, Gassmann M, Griffel C, Erdmann B, Birchmeier C, et al,. (2007). Nociceptive tuning by stem cell factor/c-Kit signaling. Neuron 56: 893-906. (Pubitemid 350181357)
106. Moiseenkova-Bell VY, Wensel TG, (2009). Hot on the trail of TRP channel structure. J Gen Physiol 133: 239-244.
107. Montell C, (2005). The TRP superfamily of cation channels. Sci STKE 272: re3.
108. Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, et al,. (2005). Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307: 1468-1472. (Pubitemid 40321945)
109. Moriyama T, Iida T, Kobayashi K, Higashi T, Fukuoka T, Tsumura H, et al,. (2003). Possible involvement of P2Y2 metabotropic receptors in ATP-induced transient receptor potential vanilloid receptor 1-mediated thermal hypersensitivity. J Neurosci 23: 6058-6062. (Pubitemid 36868990)
110. Moriyama T, Higashi T, Togashi K, Iida T, Segi E, Sugimoto Y, et al,. (2005). Sensitization of TRPV1 by EP1 and IP reveals peripheral nociceptive mechanism of prostaglandins. Mol Pain 1: 3.
111. Munns C, Alqatari M, Koltzenburg M, (2007). Many cold sensitive peripheral neurons of the mouse do not express TRPM8 or TRPA1. Cell Calcium 41: 331-342. (Pubitemid 46277391)
112. Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M, et al,. (2003). TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93: 829-838. (Pubitemid 37363057)
113. Nagy I, Rang H, (1999a). Noxious heat activates all capsaicin-sensitive and also a sub-population of capsaicin-insensitive dorsal root ganglion neurons. Neuroscience 88: 995-997. (Pubitemid 28546981)
114. Nagy I, Rang HP, (1999b). Similarities and differences between the responses of rat sensory neurons to noxious heat and capsaicin. J Neurosci 19: 10647-10655. (Pubitemid 30235711)
115. Nilius B, Voets T, (2005). TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch 451: 1-10. (Pubitemid 41424901)
116. Nilius B, Owsianik G, Voets T, Peters JA, (2007). Transient receptor potential cation channels in disease. Physiol Rev 87: 165-217. (Pubitemid 46207713)
117. Novakova-Tousova K, Vyklicky L, Susankova K, Benedikt J, Samad A, Teisinger J, et al,. (2007). Functional changes in the vanilloid receptor subtype 1 channel during and after acute desensitization. Neuroscience 149: 144-154. (Pubitemid 47496200)
118. Numazaki M, Tominaga T, Toyooka H, Tominaga M, (2002). Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J Biol Chem 277: 13375-13378. (Pubitemid 34967929)
119. Obata K, Katsura H, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, et al,. (2005). TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 115: 2393-2401. (Pubitemid 41266201)
120. Oh U, Sun WH, Kim D, (1996). Capsaicin activates a nonselective cation channel in cultured neonatal rat dorsal root ganglion neurons. J Neurosci 16: 1659-1667. (Pubitemid 26145943)
121. Okazawa M, Inoue W, Hori A, Hosokawa H, Matsumura K, Kobayashi S, (2004). Noxious heat receptors present in cold-sensory cells in rats. Neurosci Lett 359: 33-36. (Pubitemid 38446632)
122. Park U, Vastani N, Guan Y, Srinivasa NR, Koltzenburg M, Caterina MJ, (2011). TRP Vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. J Neurosci 31: 11425-11436.
123. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, et al,. (2002a). A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715. (Pubitemid 34241429)
124. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, et al,. (2002b). A heat-sensitive TRP channel expressed in keratinocytes. Science 296: 2046-2049. (Pubitemid 34627531)
125. Penna A, Juvin V, Chemin J, Compan V, Monet M, Rassendren FA, (2006). PI3-kinase promotes TRPV2 activity independently of channel translocation to the plasma membrane. Cell Calcium 39: 495-507.
126. Petrus M, Peier AM, Bandell M, Hwang SW, Huynh T, Olney N, et al,. (2007). A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol Pain 3: 40.
127. Pezet S, McMahon SB, (2006). Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29: 507-538. (Pubitemid 44476854)
128. Plant TD, Zollner C, Kepura F, Mousa SS, Eichhorst J, Schaefer M, et al,. (2007). Endothelin potentiates TRPV1 via ETA receptor-mediated activation of protein kinase C. Mol Pain 3: 35.
129. Premkumar LS, Ahern GP, (2000). Induction of vanilloid receptor channel activity by protein kinase C. Nature 408: 985-990. (Pubitemid 32101646)
130. Premkumar LS, Raisinghani M, Pingle SC, Long C, Pimentel F, (2005). Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. J Neurosci 25: 11322-11329. (Pubitemid 43083706)
131. Prescott ED, Julius D, (2003). A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300: 1284-1288. (Pubitemid 36618238)
132. Proudfoot CJ, Garry EM, Cottrell DF, Rosie R, Anderson H, Robertson DC, et al,. (2006). Analgesia mediated by the TRPM8 cold receptor in chronic neuropathic pain. Curr Biol 16: 1591-1605. (Pubitemid 44233290)
133. Qin N, Neeper MP, Liu Y, Hutchinson TL, Lubin ML, Flores CM, (2008). TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons. J Neurosci 28: 6231-6238.
134. Rathee PK, Distler C, Obreja O, Neuhuber W, Wang GK, Wang SY, et al,. (2002). PKA/AKAP/VR-1 module: a common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 22: 4740-4745. (Pubitemid 37465689)
135. Reid G, Babes A, Pluteanu F, (2002). A cold- and menthol-activated current in rat dorsal root ganglion neurones: properties and role in cold transduction. J Physiol 545: 595-614. (Pubitemid 36004391)
136. Roberson D, Binshtok A, Blasl F, Bean B, Woolf C, (2011). Targeting of sodium channel blockers into nociceptors to produce long-duration analgesia: a systematic study and review. Br J Pharmacol 164: 48-58.
137. Ross RA, (2003). Anandamide and vanilloid TRPV1 receptors. Br J Pharmacol 140: 790-801. (Pubitemid 37464060)
138. Schmidt M, Dubin AE, Petrus MJ, Earley TJ, Patapoutian A, (2009). Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron 64: 498-509.
139. Schnizler K, Shutov LP, Van Kanegan MJ, Merrill MA, Nichols B, McKnight GS, et al,. (2008). Protein kinase A anchoring via AKAP150 is essential for TRPV1 modulation by forskolin and prostaglandin E2 in mouse sensory neurons. J Neurosci 28: 4904-4917.
140. Sherrington CS, (1906). The Integrative Action of the Nervous System. Scribner: New York.
141. Shimosato G, Amaya F, Ueda M, Tanaka Y, Decosterd I, Tanaka M, (2005). Peripheral inflammation induces up-regulation of TRPV2 expression in rat DRG. Pain 119: 225-232. (Pubitemid 41752983)
142. Shukla AK, Kim J, Ahn S, Xiao K, Shenoy SK, Liedtke W, et al,. (2010). Arresting a transient receptor potential (TRP) channel: beta-arrestin 1 mediates ubiquitination and functional down-regulation of TRPV4. J Biol Chem 285: 30115-30125.
143. Simpson DM, Brown S, Tobias J, (2008). Controlled trial of high-concentration capsaicin patch for treatment of painful HIV neuropathy. Neurology 70: 2305-2313.
144. Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P, Facer P, et al,. (2002). TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418: 186-190. (Pubitemid 34773773)
145. Smith PL, Maloney KN, Pothen RG, Clardy J, Clapham DE, (2006). Bisandrographolide from Andrographis paniculata activates TRPV4 channels. J Biol Chem 281: 29897-29904. (Pubitemid 44536998)
146. Sowa NA, Street SE, Vihko P, Zylka MJ, (2010). Prostatic acid phosphatase reduces thermal sensitivity and chronic pain sensitization by depleting phosphatidylinositol 4,5-bisphosphate. J Neurosci 30: 10282-10293.
147. Staaf S, Franck MC, Marmigere F, Mattsson JP, Ernfors P, (2010). Dynamic expression of the TRPM subgroup of ion channels in developing mouse sensory neurons. Gene Expr Patterns 10: 65-74.
148. Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE, (2006). Phosphoinositide 3-Kinase Binds to TRPV1 and Mediates NGF-stimulated TRPV1 Trafficking to the Plasma Membrane. J Gen Physiol 128: 509-522. (Pubitemid 44664629)
149. Steiner AA, Turek VF, Almeida MC, Burmeister JJ, Oliveira DL, Roberts JL, et al,. (2007). Nonthermal activation of transient receptor potential vanilloid-1 channels in abdominal viscera tonically inhibits autonomic cold-defense effectors. J Neurosci 27: 7459-7468. (Pubitemid 47066573)
150. Stokes AJ, Shimoda LM, Koblan-Huberson M, Adra CN, Turner H, (2004). A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells. J Exp Med 200: 137-147. (Pubitemid 38982173)
151. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, et al,. (2003). ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112: 819-829. (Pubitemid 36378884)
152. Stucky CL, Rossi J, Airaksinen MS, Lewin GR, (2002). GFR alpha2/neurturin signalling regulates noxious heat transduction in isolectin B4-binding mouse sensory neurons. J Physiol 545: 43-50. (Pubitemid 35390328)
153. Studer M, McNaughton PA, (2010). Modulation of single-channel properties of TRPV1 by phosphorylation. J Physiol 588: 3743-3756.
154. Szallasi A, Cortright DN, Blum CA, Eid SR, (2007). The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat Rev Drug Discov 6: 357-372. (Pubitemid 46705200)
155. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, et al,. (2005). Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438: 1022-1025. (Pubitemid 43093975)
156. Todaka H, Taniguchi J, Satoh J, Mizuno A, Suzuki M, (2004). Warm temperature-sensitive transient receptor potential vanilloid 4 (TRPV4) plays an essential role in thermal hyperalgesia. J Biol Chem 279: 35133-35138. (Pubitemid 39100509)
157. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, et al,. (1998). The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531-543. (Pubitemid 28475505)
158. Trevisani M, Smart D, Gunthorpe MJ, Tognetto M, Barbieri M, Campi B, et al,. (2002). Ethanol elicits and potentiates nociceptor responses via the vanilloid receptor-1. Nat Neurosci 5: 546-551. (Pubitemid 34568996)
159. Van Buren JJ, Bhat S, Rotello R, Pauza ME, Premkumar LS, (2005). Sensitization and translocation of TRPV1 by insulin and IGF-I. Mol Pain 1: 17.
160. Vellani V, Mapplebeck S, Moriondo A, Davis JB, McNaughton PA, (2001). Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534: 813-825. (Pubitemid 32700878)
161. Vellani V, Colucci M, Lattanzi R, Giannini E, Negri L, Melchiorri P, et al,. (2006). Sensitization of transient receptor potential vanilloid 1 by the prokineticin receptor agonist Bv8. J Neurosci 26: 5109-5116. (Pubitemid 44315292)
162. Viana F, Ferrer-Montiel A, (2009). TRPA1 modulators in preclinical development. Expert Opin Ther Pat 19: 1787-1799.
163. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B, (2004). The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430: 748-754. (Pubitemid 39071340)
164. Wang YY, Chang RB, Waters HN, McKemy DD, Liman ER, (2008). The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions. J Biol Chem 283: 32691-32703.
165. Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, et al,. (2002a). Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277: 13569-13577. (Pubitemid 34967954)
166. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B, (2002b). 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. (Pubitemid 36159212)
167. Wegierski T, Lewandrowski U, Muller B, Sickmann A, Walz G, (2009). Tyrosine phosphorylation modulates the activity of TRPV4 in response to defined stimuli. J Biol Chem 284: 2923-2933.
168. Weskamp G, Otten U, (1987). An enzyme-linked immunoassay for nerve growth factor (NGF): a tool for studying regulatory mechanisms involved in NGF production in brain and in peripheral tissues. J Neurochem 48: 1779-1786. (Pubitemid 17101549)
169. Wong GY, Gavva NR, (2009). Therapeutic potential of vanilloid receptor TRPV1 agonists and antagonists as analgesics: recent advances and setbacks. Brain Res Rev 60: 267-277.
170. Wood JN, Perl ER, (1999). Pain. Curr Opin Genet Dev 9: 328-332. (Pubitemid 29289974)
171. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, et al,. (2004). Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci 24: 6410-6415. (Pubitemid 38944232)
172. Xiao B, Dubin AE, Bursulaya B, Viswanath V, Jegla TJ, Patapoutian A, (2008). Identification of transmembrane domain 5 as a critical molecular determinant of menthol sensitivity in mammalian TRPA1 channels. J Neurosci 28: 9640-9651.
173. Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, et al,. (2002). TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418: 181-186. (Pubitemid 34773772)
174. Xu F, Satoh E, Iijima T, (2003a). Protein kinase C-mediated Ca2+ entry in HEK 293 cells transiently expressing human TRPV4. Br J Pharmacol 140: 413-421. (Pubitemid 37249202)
175. Xu H, Zhao H, Tian W, Yoshida K, Roullet JB, Cohen DM, (2003b). Regulation of a transient receptor potential (TRP) channel by tyrosine phosphorylation. SRC family kinase-dependent tyrosine phosphorylation of TRPV4 on TYR-253 mediates its response to hypotonic stress. J Biol Chem 278: 11520-11527. (Pubitemid 36792713)
176. Xu H, Delling M, Jun JC, Clapham DE, (2006). Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat Neurosci 9: 628-635. (Pubitemid 44012260)
177. Yang F, Cui Y, Wang K, Zheng J, (2010). Thermosensitive TRP channel pore turret is part of the temperature activation pathway. Proc Natl Acad Sci USA 107: 7083-7088.
178. Zhang X, McNaughton PA, (2006). Why pain gets worse: the mechanism of heat hyperalgesia. J Gen Physiol 128: 491-493. (Pubitemid 44664627)
179. Zhang X, Huang J, McNaughton PA, (2005). NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24: 4211-4223. (Pubitemid 41828897)
180. Zhang X, Li L, McNaughton PA, (2008). Proinflammatory mediators modulate the heat-activated ion channel TRPV1 via the scaffolding protein AKAP79/150. Neuron 59: 450-461.
181. Zhu MX, (2007). Understanding the role of voltage gating of polymodal TRP channels. J Physiol 585: 321-322. (Pubitemid 350193907)
182. Zhu W, Oxford GS, (2007). Phosphoinositide-3-kinase and mitogen activated protein kinase signaling pathways mediate acute NGF sensitization of TRPV1. Mol Cell Neurosci 34: 689-700. (Pubitemid 46486710)
183. Zimmermann K, Leffler A, Fischer MM, Messlinger K, Nau C, Reeh PW, (2005). The TRPV1/2/3 activator 2-aminoethoxydiphenyl borate sensitizes native nociceptive neurons to heat in wildtype but not TRPV1 deficient mice. Neuroscience 135: 1277-1284. (Pubitemid 41416688)
184. Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA, (2007). Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci 10: 277-279.