TRPA1 in mast cell activation-induced long-lasting mechanical hypersensitivity of vagal afferent C-fibers in guinea pig esophagus

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 1, 2009, Pages

  Yu, Shaoyong ^a   Gao, Guofeng ^a   Peterson, Blaise Z ^a   Ouyang, Ann ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Nociception; Protease activated receptor 2; Sensitization; Transient receptor potential A1; Visceral afferent

Indexed keywords

BETA TUBULIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HC 030031; MESSENGER RNA; PROTEIN INHIBITOR; PROTEINASE ACTIVATED RECEPTOR 2; TRANSIENT RECEPTOR POTENTIAL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRYPTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; ESOPHAGUS; EVOKED RESPONSE; EX VIVO STUDY; GUINEA PIG; HYPERALGESIA; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; MALE; MAST CELL; NERVE FIBER C; NOCICEPTION; NONHUMAN; PERFUSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIZATION; SENSORY NERVE; VAGUS NERVE; WESTERN BLOTTING;

AFFERENT PATHWAYS; ANIMALS; DISEASE MODELS, ANIMAL; ESOPHAGUS; EVOKED POTENTIALS; GUINEA PIGS; HYPERALGESIA; HYPERSENSITIVITY; MALE; MAST CELLS; MECHANOTRANSDUCTION, CELLULAR; NERVE FIBERS, UNMYELINATED; NODOSE GANGLION; OVALBUMIN; PHYSICAL STIMULATION; PRESSURE; RECEPTOR, PAR-2; STIMULATION, CHEMICAL; STRESS, MECHANICAL; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRYPTASES; VAGUS NERVE;

EID: 67650088003     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00068.2009     Document Type: Article

References (39)

1. Abbas AK, Lichtman AH. Cellular and Molecular Immunology (5th ed.). Philadelphia, PA: Elsevier, 2005.
2. Amadesi S, Cottrell GS, Divino L, Chapman K, Grady EF, Bautista F, Karanjia R, Barajas-Lopez C, Vanner S, Vergnolle N, Bunnett NW. Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cepsilon-and A-dependent mechanisms in rats and mice. J Physiol 575: 555-571, 2006.
3. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, Manni C, Geppetti P, McRoberts JA, Ennes H, Davis JB, Mayer EA, Bunnett NW. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24: 4300-4312, 2004.
4. Andrè E, Campi B, Materazzi S, Trevisani M, Amadesi S, Massi D, Creminon C, Vaksman N, Nassini R, Civelli M, Baraldi PG, Poole DP, Bunnett NW, Geppetti P, Patacchini R. Cigarette smoke-induced neurogenic inflammation is mediated by alpha,beta-unsaturated aldehydes and the TRPA1 receptor in rodents. J Clin Invest 118: 2574-2582, 2008.
5. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41: 849-857, 2004.
6. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124: 1269-1282, 2006.
7. Bielefeldt K, Davis BM. Differential effects of ASIC3 and TRPV1 deletion on gastroesophageal sensation in mice. Am J Physiol Gastrointest Liver Physiol 294: G130-G138, 2008.
8. Corey DP, García-Añoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Géléoc GS, Gray PA, Hoffman MP, Rehm HL, Tamasauskas D, Zhang DS. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432: 723-730, 2004.
9. Corvera CU, Dery O, McConalogue K, Gamp P, Thoma M, Al-Ani B, Caughey GH, Hollenberg MD, Bunnett NW. Thrombin and mast cell tryptase regulate guinea-pig myenteric neurons through proteinase-activated receptors-1 and -2. J Physiol 517: 741-756, 1999.
10. Dai Y, Moriyama T, Higashi T, Togashi K, Kobayashi K, Yamanaka H, Tominaga M, Noguchi K. Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 24: 4293-4299, 2004.
11. Dai Y, Wang S, Tominaga M, Yamamoto S, Fukuoka T, Higashi T, Kobayashi K, Obata K, Yamanaka H, Noguchi K. Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117: 1979-1987, 2007.
12. Fajardo O, Meseguer V, Belmonte C, Viana F. TRPA1 channels mediate cold temperature sensing in mammalian vagal sensory neurons: pharmacological and genetic evidence. J Neurosci 28: 7863-7875, 2008.
13. Gao C, Liu S, Hu HZ, Gao N, Kim GY, Xia Y, Wood JD. Serine proteases excite myenteric neurons through protease-activated receptors in guinea pig small intestine. Gastroenterology 123: 1554-1564, 2002.
14. Gebhart GF. Pathobiology of visceral pain: molecular mechanisms and therapeutic implications. IV. Visceral afferent contributions to the pathobiology of visceral pain. Am J Physiol Gastrointest Liver Physiol 278: G834-G838, 2000.
15. Grant AD, Cottrell GS, Amadesi S, Trevisani M, Nicoletti P, Materazzi S, Altier C, Cenac N, Zamponi GW, Bautista-Cruz F, Lopez CB, Joseph EK, Levine JD, Liedtke W, Vanner S, Vergnolle N, Geppetti P, Bunnett NW. Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 578: 715-733, 2007.
16. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Högestätt ED, Meng ID, Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427: 260-265, 2004.
17. Kirkup AJ, Jiang W, Bunnett NW, Grundy D. Stimulation of proteinase-activated receptor 2 excites jejunal afferent nerves in anaesthetised rats. J Physiol 552: 589-601, 2003.
18. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50: 277-289, 2006.
19. McGuire JJ, Saifeddine M, Triggle CR, Sun K, Hollenberg MD. 2-furoyl-LIGRLO-amide: a potent and selective proteinase-activated receptor 2 agonist. J Pharmacol Exp Ther 309: 1124-1131, 2004.
20. Nagata K, Duggan A, Kumar G, García-Añoveros J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25: 4052-4061, 2005.
21. Neuhuber WL, Raab M, Berthoud HR, Wörl J. Innervation of the mammalian esophagus. Adv Anat Embryol Cell Biol 185: 1-73, 2006.
22. Nystedt S, Emilsson K, Wahlestedt C, Sundelin J. Molecular cloning of a potential proteinase activated receptor. Proc Natl Acad Sci USA 91: 9208-9212, 1994.
23. Obata K, Katsura H, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Tominaga M, Noguchi K. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 115: 2393-2401, 2005.
24. Ossovskaya VS, Bunnett NW. Protease-activated receptors: contribution to physiology and disease. Physiol Rev 84: 579-621, 2004.
25. Page AJ, Blackshaw LA. An in vitro study of the properties of vagal afferent fibres innervating the ferret oesophagus and stomach. J Physiol 512: 907-916, 1998.
26. Preisig-Müller R, Mederos y Schnitzler M, Derst C, Daut J. Separation of cardiomyocytes and coronary endothelial cells for cell-specific RT-PCR. Am J Physiol Heart Circ Physiol 277: H413-H416, 1999.
27. Qin C, Chandler MJ, Jou CJ, Foreman RD. Responses and afferent pathways of C1-C2 spinal neurons to cervical and thoracic esophageal stimulation in rats. J Neurophysiol 91: 2227-2235, 2004.
28. Reed DE, Barajas-Lopez C, Cottrell G, Velazquez-Rocha S, Dery O, Grady EF, Bunnett NW, Vanner SJ. Mast cell tryptase and proteinase-activated receptor 2 induce hyperexcitability of guinea-pig submucosal neurons. J Physiol 547: 531-542, 2003.
29. Sarkar S, Hobson AR, Furlong PL, Woolf CJ, Thompson DG, Aziz Q. Central neural mechanisms mediating human visceral hypersensitivity. Am J Physiol Gastrointest Liver Physiol 281: G1196-G1202, 2001.
30. Sengupta JN, Kauvar D, Goyal RK. Characteristics of vagal esophageal tension-sensitive afferent fibers in the opossum. J Neurophysiol 61: 1001-1010, 1989.
31. Sengupta JN, Saha JK, Goyal RK. Stimulus-response function studies of esophageal mechanosensitive nociceptors in sympathetic afferents of opossum. J Neurophysiol 64: 796-812, 1990.
32. Sipe WE, Brierley SM, Martin CM, Phillis BD, Cruz FB, Grady EF, Liedtke W, Cohen DM, Vanner S, Blackshaw LA, Bunnett NW. Transient receptor potential vanilloid 4 mediates protease activated receptor 2-induced sensitization of colonic afferent nerves and visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol 294: G1288-G1298, 2008.
33. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112: 819-829, 2003.
34. Yu S, Kollarik M, Ouyang A, Myers AC, Undem BJ. Mast cell-mediated long-lasting increases in excitability of vagal C-fibers in guinea pig esophagus. Am J Physiol Gastrointest Liver Physiol 293: G850-G856, 2007.
35. Yu S, Ouyang A. TRPA1 in Bradykinin-induced Mechano- hypersensitivity of Vagal C Fibers in Guinea Pig Esophagus. Am J Physiol Gastrointest Liver Physiol 296: G255-G265, 2009.
36. Yu S, Ru F, Ouyang A, Kollarik M. 5-Hydroxytryptamine selectively activates the vagal nodose C-fibre subtype in the guinea-pig oesophagus. Neurogastroenterol Motil 20: 1042-1050, 2008.
37. Yu S, Undem BJ, Kollarik M. Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus. J Physiol 563: 831-842, 2005.
38. Zagorodnyuk VP, Brookes SJ. Transduction sites of vagal mechanoreceptors in the guinea pig esophagus. J Neurosci 20: 6249-6255, 2000.
39. Zhu WJ, Yamanaka H, Obata K, Dai Y, Kobayashi K, Kozai T, Tokunaga A, Noguchi K. Expression of mRNA for four subtypes of the proteinase-activated receptor in rat dorsal root ganglia. Brain Res 1041: 205-211, 2005.