TRPA1: A gatekeeper for inflammation

Annual Review of Physiology

Volumn 75, Issue , 2013, Pages 181-200

  Bautista, Diana M ^a   Pellegrino, Maurizio ^a   Tsunozaki, Makoto ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Inflammatory pain; Sensory transduction; Somatosensation; Transient receptor potential ion channel

Indexed keywords

NEUROPEPTIDE; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1;

ASTHMA; BRONCHOSPASM; COUGHING; DIGESTIVE SYSTEM INFLAMMATION; GASTROINTESTINAL TRACT; HUMAN; HYPERSENSITIVITY; INFLAMMATION; INTESTINE; MECHANICAL STIMULATION; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PRURITUS; RESPIRATORY TRACT INFECTION; REVIEW;

CALCIUM CHANNELS; HUMANS; INFLAMMATION; NERVE TISSUE PROTEINS; NEUROPEPTIDES; PAIN; SIGNAL TRANSDUCTION; TRANSIENT RECEPTOR POTENTIAL CHANNELS; VISCERA;

EID: 84873638826     PISSN: 00664278     EISSN: 15451585     Source Type: Book Series    
DOI: 10.1146/annurev-physiol-030212-183811     Document Type: Review

References (135)

1. Basbaum AI, Woolf CJ. 1999. Pain. Curr. Biol. 9:R429-31
2. Basbaum AI, Bautista DM, Scherrer G, Julius D. 2009. Cellular and molecular mechanisms of pain. Cell 139:267-84
3. Meyer RA, Ringkamp M, Campbell JN, Raja SN. 2006. Peripheral mechanisms of cutaneous nociception. In Wall and Melzack's Textbook of Pain, ed. SB MacMahon, M Koltzenburg, pp. 3-34. Philadelphia: Elsevier
4. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, et al. 2003. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819-29
5. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, et al. 2004. Mustard oils and cannabi-noids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260-65
6. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, et al. 2006. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-89
7. Caspani O, Heppenstall PA. 2009. TRPA1 and cold transduction: an unresolved issue? J. Gen. Physiol. 133:245-49
8. Bandell M, Macpherson LJ, Patapoutian A. 2007. From chills to chilis: mechanisms for thermosensation and chemesthesis via thermoTRPs. Curr. Opin. Neurobiol. 17:490-97
9. Nilius B, Prenen J, Owsianik G. 2011. Irritating channels: the case of TRPA1. J. Physiol. 589:1543-49
10. Moran MM, McAlexander MA, Biro T, Szallasi A. 2011. Transient receptor potential channels as therapeutic targets. Nat. Rev. Drug Discov. 10:601-20
11. Venkatachalam K, Montell C. 2007. TRP channels. Annu. Rev. Biochem. 76:387-417
12. Wu LJ, Sweet TB, Clapham DE. 2010. International Union ofBasic and Clinical Pharmacology. LXXVI. Current progress in the mammalian TRP ion channel family. Pharmacol. Rev. 62:381-404
13. Cvetkov TL, Huynh KW, Cohen MR, Moiseenkova-Bell VY. 2011. Molecular architecture and subunit organization of TRPA1 ion channel revealed by electron microscopy. J. Biol. Chem. 286:38168-76
14. Clapham DE, Runnels LW, Strubing C. 2001. The TRP ion channel family. Nat. Rev. Neurosci. 2:387-96
15. Montell C. 2005. The TRP superfamily of cation channels. Sci. STKE 2005:re3
16. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, et al. 2006. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269-82
17. Matta JA, Cornett PM, Miyares RL, Abe K, Sahibzada N, Ahern GP. 2008. General anesthetics activate a nociceptive ion channel to enhance pain and inflammation. Proc. Natl. Acad. Sci. USA 105:8784-89
18. Leffler A, Lattrell A, Kronewald S, Niedermirtl F, Nau C. 2011. Activation of TRPA1 by membrane permeable local anesthetics. Mol. Pain 7:62
19. Trevisani M, Siemens J, Materazzi S, Bautista DM, Nassini R, et al. 2007. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc. Natl. Acad. Sci. USA 104:13519-24
20. Taylor-Clark TE, McAlexander MA, Nassenstein C, Sheardown SA, Wilson S, et al. 2008. Relative contributions of TRPA1 and TRPV1 channels in the activation of vagal bronchopulmonary C-fibres by the endogenous autacoid 4-oxononenal. J. Physiol. 586:3447-59
21. Taylor-Clark TE, Ghatta S, Bettner W, Undem BJ. 2009. Nitrooleic acid, an endogenous product of nitrative stress, activates nociceptive sensory nerves via the direct activation of TRPA1. Mol. Pharmacol. 75:820-29
22. Baker PR, Schopfer FJ, O'Donnell VB, Freeman BA. 2009. Convergence of nitric oxide and lipid signaling: anti-inflammatory nitro-fatty acids. Free Radic. Biol. Med. 46:989-1003
23. Cruz-Orengo L, Dhaka A, Heuermann RJ, Young TJ, Montana MC, et al. 2008. Cutaneous nociception evoked by 15-delta PGJ2 via activation of ion channel TRPA1. Mol. Pain 4:30
24. Taylor-Clark TE, Undem BJ, Macglashan DW Jr, Ghatta S, Carr MJ, McAlexander MA. 2008. Prostaglandin-induced activation of nociceptive neurons via direct interaction with transient receptor potential A1 (TRPA1). Mol. Pharmacol. 73:274-81
25. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, et al. 2007. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445:541-45
26. Hinman A, Chuang HH, Bautista DM, Julius D. 2006. TRP channel activation by reversible covalent modification. Proc. Natl. Acad. Sci. USA 103:19564-68
27. Takahashi N, Mizuno Y, Kozai D, Yamamoto S, Kiyonaka S, et al. 2008. Molecular characterization of TRPA1 channel activation by cysteine-reactive inflammatory mediators. Channels 2:287-98
28. Bessac BF, Sivula M, von Hehn CA, Escalera J, Cohn L, Jordt SE. 2008. TRPA1 is a major oxidant sensor in murine airway sensory neurons. J. Clin. Investig. 118:1899-910
29. Cordero-Morales JF, Gracheva EO, Julius D. 2011. Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proc. Natl. Acad. Sci. USA 108:E1184-91
30. Yao J, Liu B, Qin F. 2011. Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. Proc. Natl. Acad. Sci. USA 108:11109-14
31. Zhong L, Bellemer A, Yan H, Honjo K, Robertson J, et al. 2012. Thermosensory and non-thermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat sensor domains of a thermoTRP channel. Cell Rep. 1:43-55
32. Petrus M, Peier AM, Bandell M, Hwang SW, Huynh T, et al. 2007. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol. Pain 3:40
33. Namer B, Seifert F, Handwerker HO, Maihofner C. 2005. TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. Neuroreport 16:955-59
34. Tsagareli MG, Tsiklauri N, Zanotto KL, Carstens MI, Klein AH, et al. 2010. Behavioral evidence of thermal hyperalgesia and mechanical allodynia induced by intradermal cinnamaldehyde in rats. Neurosci. Lett. 473:233-36
35. McMahon SB, Wood JN. 2006. Increasingly irritable and close to tears: TRPA1 in inflammatory pain. Cell 124:1123-25
36. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, et al. 2004. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-57
37. 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. Pflüg. Arch. 457:77-89
38. 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. 283:32691-703
39. Wilson SR, Gerhold KA, Bifolck-Fisher A, Liu Q, Patel KN, et al. 2011. TRPA1 is required for histamine-independent, Mas-related G protein-coupled receptor-mediated itch. Nat. Neurosci. 14:595-602
40. Eid SR, Crown ED, Moore EL, Liang HA, Choong KC, et al. 2008. HC-030031, a TRPA1 selective antagonist, attenuates inflammatory-and neuropathy-induced mechanical hypersensitivity. Mol. Pain 4:48
41. McGaraughty S, Chu KL, Perner RJ, Didomenico S, Kort ME, Kym PR. 2010. TRPA1 modulation of spontaneous and mechanically evoked firing of spinal neurons in uninjured, osteoarthritic, and inflamed rats. Mol. Pain 6:14
42. Okun A, Liu P, Davis P, Ren J, Remeniuk B, et al. 2012. Afferent drive elicits ongoing pain in a model of advanced osteoarthritis. Pain 153:924-33
43. Cent. Dis. Control Prev. (CDC). 2011. National Diabetes Fact Sheet: National Estimates and General Information on Diabetes and Prediabetes in the United States. Atlanta, GA: US Dep. Health Hum. Serv., CDC
44. Ji G, Zhou S, Carlton SM. 2008. Intact Aδ-fibers up-regulate transient receptor potential A1 and contribute to cold hypersensitivity in neuropathic rats. Neuroscience 154:1054-66
45. Vincent AM, Brownlee M, Russell JW. 2002. Oxidative stress and programmed cell death in diabetic neuropathy. Ann. NY Acad. Sci. 959:368-83
46. Pabbidi RM, Cao DS, Parihar A, Pauza ME, Premkumar LS. 2008. Direct role of streptozotocin in inducing thermal hyperalgesia by enhanced expression of transient receptor potential vanilloid 1 in sensory neurons. Mol. Pharmacol. 73:995-1004
47. Wei H, Hamalainen MM, Saarnilehto M, Koivisto A, Pertovaara A. 2009. Attenuation of mechanical hypersensitivityby an antagonistofthe TRPA1 ion channel indiabetic animals. Anesthesiology 111:147-54
48. Koivisto A, Hukkanen M, Saarnilehto M, Chapman H, Kuokkanen K, et al. 2012. Inhibiting TRPA1 ion channel reduces loss of cutaneous nerve fiber function in diabetic animals: sustained activation of the TRPA1 channel contributes to the pathogenesis of peripheral diabetic neuropathy. Pharmacol. Res. 65:149-58
49. + sensory neurons control β cell stress and islet inflammation in autoimmune diabetes. Cell 127:1123-35
50. Schwartz ES, Christianson JA, Chen X, La JH, Davis BM, et al. 2011. Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation. Gastroenterology 140:1283-91
51. Ceppa E, Cattaruzza F, Lyo V, Amadesi S, Pelayo JC, et al. 2010. Transient receptor potential ion channels V4 and A1 contribute to pancreatitis pain in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 299:G556-71
52. Goadsby PJ, Charbit AR, Andreou AP, Akerman S, Holland PR. 2009. Neurobiology of migraine. Neuroscience 161:327-41
53. Bergerot A, Holland PR, Akerman S, Bartsch T, Ahn AH, et al. 2006. Animal models of migraine: looking at the component parts of a complex disorder. Eur. J. Neurosci. 24:1517-34
54. Kunkler PE, Ballard CJ, Oxford GS, Hurley JH. 2011. TRPA1 receptors mediate environmental irritant-induced meningeal vasodilatation. Pain 152:38-44
55. Nassini R, Materazzi S, Vriens J, Prenen J, Benemei S, et al. 2012. The "headache tree" via umbellulone and TRPA1 activates the trigeminovascular system. Brain 135:376-90
56. Ikoma A, Steinhoff M, Stander S, Yosipovitch G, Schmelz M. 2006. The neurobiology of itch. Nat. Rev. Neurosci. 7:535-47
57. Davidson S, Giesler GJ. 2010. The multiple pathways for itch and their interactions with pain. Trends Neurosci. 33:550-58
58. Shim WS, Tak MH, Lee MH, Kim M, Koo JY, et al. 2007. TRPV1 mediates histamine-induced itching via the activation of phospholipase A2 and 12-lipoxygenase. J. Neurosci. 27:2331-37
59. Liu Q, Tang Z, Surdenikova L, Kim S, Patel KN, et al. 2009. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 139:1353-65
60. Undem BJ, McAlexander M, Hunter DD. 1999. Neurobiology of the upper and lower airways. Allergy 54(Suppl. 57):81-93
61. Kummer W, Fischer A, Kurkowski R, Heym C. 1992. The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohis-tochemistry. Neuroscience 49:715-37
62. Riccio MM, Myers AC, Undem BJ. 1996. Immunomodulation of afferent neurons in guinea-pig isolated airway. J. Physiol. 491(Pt. 2):499-509
63. Larsell O, Dow RS. 1933. The innervation of the human lung. Am. J. Anat. 52:125-46
64. Plato M, Kummer W, Haberberger RV. 2006. Structural and neurochemical comparison of vagal and spinal afferent neurons projecting to the rat lung. Neurosci. Lett. 395:215-19
65. Oh EJ, Mazzone SB, Canning BJ, Weinreich D. 2006. Reflex regulation of airway sympathetic nerves in guinea-pigs. J. Physiol. 573:549-64
66. Coleridge JC, Coleridge HM. 1984. Afferent vagal C fibre innervation of the lungs and airways and its functional significance. Rev. Physiol. Biochem. Pharmacol. 99:1-110
67. Undem BJ, Chuaychoo B, Lee MG, Weinreich D, Myers AC, Kollarik M. 2004. Subtypes of vagal afferent C-fibres in guinea-pig lungs. J. Physiol. 556:905-17
68. Richardson JD, Vasko MR. 2002. Cellular mechanisms of neurogenic inflammation. J. Pharmacol. Exp. Ther. 302:839-45
69. Nassenstein C, Kwong K, Taylor-Clark T, Kollarik M, Macglashan DM, et al. 2008. Expression and functionofthe ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J. Physiol. 586:1595-604
70. 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. 25:4052-61
71. Hu H, Bandell M, Petrus MJ, Zhu MX, Patapoutian A. 2009. Zinc activates damage-sensing TRPA1 ion channels. Nat. Chem. Biol. 5:183-90
72. Bessac BF, Sivula M, von Hehn CA, Caceres AI, Escalera J, Jordt SE. 2009. Transient receptor potential ankyrin 1 antagonists block the noxious effects of toxic industrial isocyanates and tear gases. FASEB J. 23:1102-14
73. Barnes PJ, Chung KF, Page CP. 1998. Inflammatory mediators of asthma: an update. Pharmacol. Rev. 50:515-96
74. Kroll F, Karlsson JA, Lundberg JM, Persson CG. 1990. Capsaicin-induced bronchoconstriction and neuropeptide release in guinea pig perfused lungs. J. Appl. Physiol. 68:1679-87
75. Dakhama A, Larsen GL, Gelfand EW. 2004. Calcitonin gene-related peptide: role inairway homeostasis. Curr. Opin. Pharmacol. 4:215-20
76. Facchinetti F, Amadei F, Geppetti P, Tarantini F, Di Serio C, et al. 2007. α, β-Unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am. J. Respir. Cell Mol. Biol. 37:617-23
77. Huber GL, First MW, Grubner O. 1991. Marijuana and tobacco smoke gas-phase cytotoxins. Pharmacol. Biochem. Behav. 40:629-36
78. Andre E, Campi B, Materazzi S, Trevisani M, Amadesi S, et al. 2008. Cigarette smoke-induced neu-rogenic inflammation is mediated by α, β-unsaturated aldehydes and the TRPA1 receptor in rodents. J. Clin. Investig. 118:2574-82
79. Eilers H, Cattaruzza F, Nassini R, Materazzi S, Andre E, et al. 2010. Pungent general anesthetics activate transient receptor potential-A1 to produce hyperalgesia and neurogenic bronchoconstriction. Anesthesiology 112:1452-63
80. Satoh J, Yamakage M. 2009. Desflurane induces airway contraction mainly by activating transient receptor potential A1 of sensory C-fibers. J. Anesth. 23:620-23
81. Brooks SM. 2011. Perspective on the human cough reflex. Cough 7:10
82. Canning BJ, Mori N, Mazzone SB. 2006. Vagal afferent nerves regulating the cough reflex. Respir. Physiol. Neurobiol. 152:223-42
83. Birrell MA, Belvisi MG, Grace M, Sadofsky L, Faruqi S, et al. 2009. TRPA1 agonists evoke coughing in guinea pig and human volunteers. Am. J. Respir. Crit. Care Med. 180:1042-47
84. Andre E, Gatti R, Trevisani M, Preti D, Baraldi PG, et al. 2009. Transient receptor potential ankyrin receptor 1 is a novel target for pro-tussive agents. Br. J. Pharmacol. 158:1621-28
85. Taylor-Clark TE, Kiros F, Carr MJ, McAlexander MA. 2009. Transient receptor potential ankyrin 1 mediates toluene diisocyanate-evoked respiratory irritation. Am. J. Respir. Cell Mol. Biol. 40:756-62
86. Gu Q, Lin RL. 2010. Heavy metals zinc, cadmium, and copper stimulate pulmonary sensory neurons via direct activation of TRPA1. J. Appl. Physiol. 108:891-97
87. Barnes PJ. 2008. Immunology of asthma and chronic obstructive pulmonary disease. Nat. Rev. Immunol. 8:183-92
88. Dakhama A, Kanehiro A, Makela MJ, Loader JE, Larsen GL, Gelfand EW. 2002. Regulation of airway hyperresponsiveness by calcitonin gene-related peptide in allergen sensitized and challenged mice. Am. J. Respir. Crit. Care Med. 165:1137-44
89. White FA, Wilson NM. 2008. Chemokines as pain mediators and modulators. Curr. Opin. Anaesthesiol. 21:580-85
90. McLeod RL, Fernandez X, Correll CC, Phelps TP, Jia Y, et al. 2006. TRPV1 antagonists attenuate antigen-provoked cough in ovalbumin sensitized guinea pigs. Cough 2:10
91. Kuo YL, Lai CJ. 2008. Ovalbumin sensitizes vagal pulmonary C-fiber afferents in Brown Norway rats. J. Appl. Physiol. 105:611-20
92. Lalloo UG, Fox AJ, Belvisi MG, Chung KF, Barnes PJ. 1995. Capsazepine inhibits cough induced by capsaicin and citric acid but not by hypertonic saline in guinea pigs. J. Appl. Physiol. 79:1082-87
93. Raemdonck K, de Alba J, Birrell MA, Grace M, Maher SA, et al. 2012. A role for sensory nerves in the late asthmatic response. Thorax 67:19-25
94. Caceres AI, Brackmann M, Elia MD, Bessac BF, del Camino D, et al. 2009. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc. Natl. Acad. Sci. USA 106:9099-104
95. Stokes A, Wakano C, Koblan-Huberson M, Adra CN, Fleig A, Turner H. 2006. TRPA1 is a substrate for de-ubiquitination by the tumor suppressor CYLD. Cell. Signal. 18:1584-94
96. Sekirov I, Russell SL, Antunes LC, Finlay BB. 2010. Gut microbiota in health and disease. Physiol. Rev. 90:859-904
97. Xavier RJ, Podolsky DK. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448:427-34
98. Tavano F, di Mola FF, Latiano A, Palmieri O, Bossa F, et al. 2012. Neuroimmune interactions in patients with inflammatory bowel diseases: disease activity and clinical behavior based on Substance P serum levels. J. Crohns Colitis 6:563-70
99. Johansson M, Jonsson M, Norrgard O, Forsgren S. 2008. New aspects concerning ulcerative colitis and colonic carcinoma: analysis of levels of neuropeptides, neurotrophins, and TNFα/TNF receptor in plasma and mucosainparallel with histological evaluationofthe intestine. Inflamm. Bowel Dis. 14:1331-40
100. Reinshagen M, Flamig G, Ernst S, Geerling I, Wong H, et al. 1998. Calcitonin gene-related peptide mediates the protective effect of sensory nerves in a model of colonic injury. J. Pharmacol. Exp. Ther. 286:657-61
101. Holzer P, Holzer-Petsche U. 2001. Tachykinin receptors in the gut: physiological and pathological implications. Curr. Opin. Pharmacol. 1:583-90
102. Podolsky DK. 2002. Inflammatory bowel disease. N. Engl. J. Med. 347:417-29
103. Brierley SM, Hughes PA, Page AJ, Kwan KY, Martin CM, et al. 2009. The ionchannelTRPA1isrequired for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137:2084-95
104. Kondo T, Obata K, Miyoshi K, Sakurai J, Tanaka J, et al. 2009. Transient receptor potential A1 mediates gastric distention-induced visceral pain in rats. Gut 58:1342-52
105. Christianson JA, Bielefeldt K, Malin SA, Davis BM. 2010. Neonatal colon insult alters growth factor expression and TRPA1 responses in adult mice. Pain 151:540-49
106. Malin S, Molliver D, Christianson JA, Schwartz ES, Cornuet P, et al. 2011. TRPV1 and TRPA1 function and modulation are target tissue dependent. J. Neurosci. 31:10516-28
107. Penuelas A, Tashima K, Tsuchiya S, Matsumoto K, Nakamura T, et al. 2007. Contractile effect of TRPA1 receptor agonists in the isolated mouse intestine. Eur. J. Pharmacol. 576:143-50
108. 4-mediated anion secretion in human and rat colon. Am. J. Physiol. Gastrointest. Liver Physiol. 302:G690-701
109. Poole DP, Pelayo JC, Cattaruzza F, Kuo YM, Gai G, et al. 2011. Transient receptor potential ankyrin 1 is expressed by inhibitory motoneurons of the mouse intestine. Gastroenterology 141:565-75
110. Nozawa K, Kawabata-Shoda E, Doihara H, Kojima R, Okada H, et al. 2009. TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. Proc. Natl. Acad. Sci. USA 106:3408-13
111. Wirtz S, Neurath MF. 2007. Mouse models of inflammatory bowel disease. Adv. Drug Deliv. Rev. 59:1073-83
112. Cattaruzza F, Spreadbury I, Miranda-Morales M, Grady EF, Vanner S, Bunnett NW. 2010. Transient receptor potential ankyrin-1 has a major role in mediating visceral pain in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 298:G81-91
113. Yang J, Li Y, Zuo X, Zhen Y, Yu Y, Gao L. 2008. Transient receptor potential ankyrin-1 participates in visceral hyperalgesia following experimental colitis. Neurosci. Lett. 440:237-41
114. Suzuki T, Kagoshima M, Shibata M, Inaba N, Onodera S, et al. 1997. Effects of several denervation procedures on distribution of calcitonin gene-related peptide and substance P immunoreactive in rat stomach. Dig. Dis. Sci. 42:1242-54
115. Green T, Dockray GJ. 1988. Characterization of the peptidergic afferent innervation of the stomach in the rat, mouse and guinea-pig. Neuroscience 25:181-93
116. Weller K, Reeh PW, Sauer SK. 2011. TRPV1, TRPA1, and CB1 in the isolated vagus nerve-axonal chemosensitivity and control of neuropeptide release. Neuropeptides 45:391-400
117. Engel MA, Leffler A, Niedermirtl F, Babes A, Zimmermann K, et al. 2011. TRPA1 and substance P mediate colitis in mice. Gastroenterology 141:1346-58
118. Zwiers A, Fuss IJ, Seegers D, Konijn T, Garcia-Vallejo JJ, et al. 2011. A polymorphism in the coding region of Il12b promotes IL-12p70 and IL-23 heterodimer formation. J. Immunol. 186:3572-80
119. Bouma G, Kaushiva A, Strober W. 2002. Experimental murine colitis is regulated by two genetic loci, including one on chromosome 11 that regulates IL-12 responses. Gastroenterology 123:554-65
120. Thompson BJ, Washington MK, Kurre U, Singh M, Rula EY, Emeson RB. 2008. Protective roles of α-calcitonin and β-calcitonin gene-related peptide in spontaneous and experimentally induced colitis. Dig. Dis. Sci. 53:229-41
121. Clifton MS, Hoy JJ, Chang J, Idumalla PS, Fakhruddin H, et al. 2007. Role of calcitonin receptor-like receptor in colonic motility and inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 293:G36-44
122. Engel MA, Khalil M, Siklosi N, Mueller-Tribbensee SM, Neuhuber WL, et al. 2012. Opposite effects of substance P and calcitonin gene-related peptide in oxazolone colitis. Dig. Liver Dis. 44:24-29
123. Lorusso G, Ruegg C. 2008. The tumor microenvironment and its contribution to tumor evolution toward metastasis. Histochem. Cell Biol. 130:1091-103
124. Ye Y, Dang D, Zhang J, Viet CT, Lam DK, et al. 2011. Nerve growth factor links oral cancer progression, pain, and cachexia. Mol. Cancer Ther. 10:1667-76
125. Fujino K, Takami Y, de la Fuente SG, Ludwig KA, Mantyh CR. 2004. Inhibition of the vanilloid receptor subtype-1 attenuates TNBS-colitis. J. Gastrointest. Surg. 8:842-47; discussion 847-48
126. Miranda A, Nordstrom E, Mannem A, Smith C, Banerjee B, Sengupta JN. 2007. The role of transient receptor potential vanilloid 1 in mechanical and chemical visceral hyperalgesia following experimental colitis. Neuroscience 148:1021-32
127. Phillis BD, Martin CM, Kang D, Larsson H, Lindstrom EA, et al. 2009. Role of TRPV1 in high-threshold rat colonic splanchnic afferents is revealed by inflammation. Neurosci. Lett. 459:57-61
128. Brozmanova M, Ru F, Surdenikova L, Mazurova L, Taylor-Clark T, Kollarik M. 2011. Preferential activation of the vagal nodose nociceptive subtype by TRPA1 agonists in the guinea pig esophagus. Neurogastroenterol. Motil. 23:e437-45
129. Laude EA, Higgins KS, Morice AH. 1993. A comparative study of the effects of citric acid, capsaicin and resiniferatoxin on the cough challenge in guinea-pig and man. Pulm. Pharmacol. 6:171-75
130. Zhang G, Lin RL, Wiggers M, Snow DM, Lee LY. 2008. Altered expression of TRPV1 and sensitivity to capsaicin in pulmonary myelinated afferents following chronic airway inflammation in the rat. J. Physiol. 586:5771-86
131. Delescluse I, Mace H, Adcock J. 2012. Inhibition of airway hyperresponsiveness by TRPV1 antagonists (SB-705498 And PF-04065463) in the unanaesthetised, ovalbumin-sensitized guinea pig. Br. J. Pharmacol. 166:1822-32
132. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, et al. 2000. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-13
133. Ji RR, Xu ZZ, Strichartz G, Serhan CN. 2011. Emerging roles of resolvins in the resolution of inflammation and pain. Trends Neurosci. 34:599-609
134. Park CK, Xu ZZ, Liu T, Lu N, Serhan CN, Ji RR. 2011. Resolvin D2 is a potent endogenous inhibitor for transient receptor potential subtype V1/A1, inflammatory pain, and spinal cord synaptic plasticity in mice: distinct roles of resolvin D1, D2, and E1. J. Neurosci. 31:18433-38
135. Kremeyer B, Lopera F, Cox JJ, Momin A, Rugiero F, et al. 2010. A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome. Neuron 66:671-80