Interaction between TRPA1 and TRPV1: Synergy on pulmonary sensory nerves

Lu-Yuan Lee, Chun-Chun Hsu, Yu-Jung Lin, Ruei-Lung Lin, Mehdi J. Khosravi

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Transient receptor potential ankyrin type 1 (TRPA1) and vanilloid type 1 (TRPV1) receptors are co-expressed in vagal pulmonary C-fiber sensory nerves. Because both these ligand-gated non-selective cation channels are sensitive to a number of endogenous inflammatory mediators, it is highly probable that they can be activated simultaneously during airway inflammation. Studies were carried out to investigate whether there is an interaction between these two polymodal transducers upon simultaneous activation, and how it modulates the activity of vagal pulmonary C-fiber sensory nerves. Our studies showed a distinct potentiating effect induced abruptly by simultaneous activations of TRPA1 and TRPV1 by their respective selective agonists, allyl isothiocyanate (AITC) and capsaicin (Cap), at near-threshold concentrations. This synergistic effect was demonstrated in the studies of single-unit recording of vagal bronchopulmonary C-fiber afferents and the reflex responses elicited by activation of these afferents in intact animals, as well as in the isolated nodose and jugular bronchopulmonary sensory neurons. This potentiating effect was absent when either AITC or Cap was replaced by non-TRPA1 and non-TRPV1 chemical activators of these neurons, demonstrating the selectivity of the interaction between these two TRP channels. Furthermore, the synergism was dependent upon the extracellular Ca2+, and the rapid onset of the action further suggests that the interaction probably occurred locally at the sites of these channels. These findings suggest that the TRPA1-TRPV1 interaction may play an important role in regulating the function and excitability of pulmonary sensory neurons during airway inflammation, but the mechanism underlying this positive interaction is not yet fully understood. © 2015 Elsevier Ltd.
Original languageEnglish
Pages (from-to)87-93
Number of pages7
JournalPulmonary Pharmacology and Therapeutics
Volume35
DOIs
Publication statusPublished - 2015
Externally publishedYes

Fingerprint

Ankyrins
Unmyelinated Nerve Fibers
Neurons
Lung
Capsaicin
Chemical activation
Sensory Receptor Cells
Fibers
Inflammation
Transducers
Reflex
Cations
Animals
Neck
Ligands
allyl isothiocyanate

Keywords

  • Airway
  • C fiber
  • Inflammation
  • TRPA1
  • TRPV1

Cite this

Interaction between TRPA1 and TRPV1: Synergy on pulmonary sensory nerves. / Lee, Lu-Yuan; Hsu, Chun-Chun; Lin, Yu-Jung; Lin, Ruei-Lung; Khosravi, Mehdi J.

In: Pulmonary Pharmacology and Therapeutics, Vol. 35, 2015, p. 87-93.

Research output: Contribution to journalArticle

Lee, Lu-Yuan ; Hsu, Chun-Chun ; Lin, Yu-Jung ; Lin, Ruei-Lung ; Khosravi, Mehdi J. / Interaction between TRPA1 and TRPV1: Synergy on pulmonary sensory nerves. In: Pulmonary Pharmacology and Therapeutics. 2015 ; Vol. 35. pp. 87-93.
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title = "Interaction between TRPA1 and TRPV1: Synergy on pulmonary sensory nerves",
abstract = "Transient receptor potential ankyrin type 1 (TRPA1) and vanilloid type 1 (TRPV1) receptors are co-expressed in vagal pulmonary C-fiber sensory nerves. Because both these ligand-gated non-selective cation channels are sensitive to a number of endogenous inflammatory mediators, it is highly probable that they can be activated simultaneously during airway inflammation. Studies were carried out to investigate whether there is an interaction between these two polymodal transducers upon simultaneous activation, and how it modulates the activity of vagal pulmonary C-fiber sensory nerves. Our studies showed a distinct potentiating effect induced abruptly by simultaneous activations of TRPA1 and TRPV1 by their respective selective agonists, allyl isothiocyanate (AITC) and capsaicin (Cap), at near-threshold concentrations. This synergistic effect was demonstrated in the studies of single-unit recording of vagal bronchopulmonary C-fiber afferents and the reflex responses elicited by activation of these afferents in intact animals, as well as in the isolated nodose and jugular bronchopulmonary sensory neurons. This potentiating effect was absent when either AITC or Cap was replaced by non-TRPA1 and non-TRPV1 chemical activators of these neurons, demonstrating the selectivity of the interaction between these two TRP channels. Furthermore, the synergism was dependent upon the extracellular Ca2+, and the rapid onset of the action further suggests that the interaction probably occurred locally at the sites of these channels. These findings suggest that the TRPA1-TRPV1 interaction may play an important role in regulating the function and excitability of pulmonary sensory neurons during airway inflammation, but the mechanism underlying this positive interaction is not yet fully understood. {\circledC} 2015 Elsevier Ltd.",
keywords = "Airway, C fiber, Inflammation, TRPA1, TRPV1",
author = "Lu-Yuan Lee and Chun-Chun Hsu and Yu-Jung Lin and Ruei-Lung Lin and Khosravi, {Mehdi J.}",
note = "被引用次數:1 Export Date: 11 May 2016 CODEN: PPTHF 通訊地址: Lee, L.-Y.; Department of Physiology, University of Kentucky Medical CenterUnited States; 電子郵件: lylee@uky.edu 出資詳情: HL-96914, NIH, National Institutes of Health 出資詳情: UL1TR0000117, NIH, National Institutes of Health 參考文獻: Gees, M., Owsianik, G., Nilius, B., Voets, T., TRP channels (2012) Compr. Physiol, 2, pp. 563-608; Nilius, B., Owsianik, G., Voets, T., Peters, J.A., Transient receptor potential cation channels in disease (2007) Physiol. Rev, 87, pp. 165-217; Bautista, D.M., Pellegrino, M., Tsunozaki, M., TRPA1: A gatekeeper for inflammation (2013) Annu. Rev. Physiol, 75, pp. 181-200; Caterina, M.J., Julius, D., The vanilloid receptor: a molecular gateway to the pain pathway (2001) Annu. Rev. Neurosci, 24, pp. 487-517; Kobayashi, K., Fukuoka, T., Obata, K., Yamanaka, H., Dai, Y., Tokunaga, A., Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors (2005) J. Comp. Neurol, 493, pp. 596-606; Diogenes, A., Akopian, A.N., Hargreaves, K.M., NGF up-regulates TRPA1: implications for orofacial pain (2007) J. Dent. Res, 86, pp. 550-555; Nassenstein, C., Kwong, K., Taylor-Clark, T., Kollarik, M., Macglashan, D.M., Braun, A., Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs (2008) J. Physiol, 586, pp. 1595-1604; Jammes, Y., Fornaris, E., Mei, N., Barrat, E., Afferent and efferent components of the bronchial vagal branches in cats (1982) J. Aut. Nerv. Syst, 5, pp. 165-176; Coleridge, J.C., Coleridge, H.M., Afferent vagal C fibre innervation of the lungs and airways and its functional significance (1984) Rev. Physiol. Biochem. Pharmacol, 99, pp. 1-110; Lee, L.Y., Yu, J., Sensory nerves in lung and airways (2014) Compr. Physiol, 4, pp. 287-324; Bessac, B.F., Jordt, S.E., Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control (2008) Physiology (Bethesda, Md), 23, pp. 360-370; De Swert, K.O., Joos, G.F., Extending the understanding of sensory neuropeptides (2006) Eur. J. Pharmacol, 533, pp. 171-181; Lee, L.Y., Gu, Q., Role of TRPV1 in inflammation-induced airway hypersensitivity (2009) Curr. Opin. Pharmacol, 9, pp. 243-249; Geppetti, P., Materazzi, S., Nicoletti, P., The transient receptor potential vanilloid 1: role in airway inflammation and disease (2006) Eur. J. Pharmacol, 533, pp. 207-214; Gu, Q., Lee, L.Y., Characterization of acid signaling in rat vagal pulmonary sensory neurons (2006) Am. J. Physiol. Lung Cell. Mol. Physiol, 291, pp. L58-L65; Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D., Julius, D., The capsaicin receptor: a heat-activated ion channel in the pain pathway (1997) Nature, 389, pp. 816-824; Bandell, M., Story, G.M., Hwang, S.W., Viswanath, V., Eid, S.R., Petrus, M.J., Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin (2004) Neuron, 41, pp. 849-857; Taylor-Clark, T.E., McAlexander, M.A., Nassenstein, C., Sheardown, S.A., Wilson, S., Thornton, J., Relative contributions of TRPA1 and TRPV1 channels in the activation of vagal bronchopulmonary C-fibres by the endogenous autacoid 4-oxononenal (2008) J. Physiol, 586, pp. 3447-3459; Nilius, B., Appendino, G., Owsianik, G., The transient receptor potential channel TRPA1: from gene to pathophysiology (2012) Pflugers Archiv. Eur. J. Physiol, 464, pp. 425-458; Dai, Y., Wang, S., Tominaga, M., Yamamoto, S., Fukuoka, T., Higashi, T., Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain (2007) J. Clin. Investig, 117, pp. 1979-1987; Gu, Q., Kwong, K., Lee, L.Y., Ca2+ transient evoked by chemical stimulation is enhanced by PGE2 in vagal sensory neurons: role of cAMP/PKA signaling pathway (2003) J. Neurophysiol, 89, pp. 1985-1993; Kwong, K., Lee, L.Y., PGE(2) sensitizes cultured pulmonary vagal sensory neurons to chemical and electrical stimuli (2002) J. Appl. Physiol, 93, pp. 1419-1428; Patil, M.J., Jeske, N.A., Akopian, A.N., Transient receptor potential V1 regulates activation and modulation of transient receptor potential A1 by Ca2+ (2010) Neuroscience, 171, pp. 1109-1119; Salas, M.M., Hargreaves, K.M., Akopian, A.N., TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1 (2009) Eur. J. Neurosci, 29, pp. 1568-1578; Everaerts, W., Gees, M., Alpizar, Y.A., Farre, R., Leten, C., Apetrei, A., The capsaicin receptor TRPV1 is a crucial mediator of the noxious effects of mustard oil (2011) Curr. Biol, 21, pp. 316-321; Alpizar, Y.A., Boonen, B., Gees, M., Sanchez, A., Nilius, B., Voets, T., Allyl isothiocyanate sensitizes TRPV1 to heat stimulation (2014) Pflugers Archiv. Eur. J. Physiol, 466, pp. 507-515; Gees, M., Alpizar, Y.A., Boonen, B., Sanchez, A., Everaerts, W., Segal, A., Mechanisms of transient receptor potential vanilloid 1 activation and sensitization by allyl isothiocyanate (2013) Mol. Pharmacol, 84, pp. 325-334; Lin, Y.J., Lin, R.L., Ruan, T., Khosravi, M., Lee, L.Y., A synergistic effect of simultaneous TRPA1 and TRPV1 activations on vagal pulmonary C-fiber afferents (2015) J. Appl. Physiol, 118, pp. 273-281; Fernandes, E.S., Fernandes, M.A., Keeble, J.E., The functions of TRPA1 and TRPV1: moving away from sensory nerves (2012) Br. J. Pharmacol, 166, pp. 510-521; McGarvey, L.P., Butler, C.A., Stokesberry, S., Polley, L., McQuaid, S., Abdullah, H., Increased expression of bronchial epithelial transient receptor potential vanilloid 1 channels in patients with severe asthma (2014) J. Allergy Clin. Immunol, 133, pp. 704-712. , e4; Nassini, R., Pedretti, P., Moretto, N., Fusi, C., Carnini, C., Facchinetti, F., Transient receptor potential ankyrin 1 channel localized to non-neuronal airway cells promotes non-neurogenic inflammation (2012) PloS One, 7, p. e42454; Reilly, C.A., Johansen, M.E., Lanza, D.L., Lee, J., Lim, J.O., Yost, G.S., Calcium-dependent and independent mechanisms of capsaicin receptor (TRPV1)-mediated cytokine production and cell death in human bronchial epithelial cells (2005) J. Biochem. Mol. Toxicol, 19, pp. 266-275; Ni, D., Gu, Q., Hu, H.Z., Gao, N., Zhu, M.X., Lee, L.Y., Thermal sensitivity of isolated vagal pulmonary sensory neurons: role of transient receptor potential vanilloid receptors (2006) Am. J. Physiol. Regul. Integr. Comp. Physiol, 291, pp. R541-R550; Hsu, C.C., Lee, L.Y., Role of calcium ions in the positive interaction between TRPA1 and TRPV1 channels in bronchopulmonary sensory neurons (2015) J. Appl. Physiol, 118, pp. 1533-1543; Story, G.M., Peier, A.M., Reeve, A.J., Eid, S.R., Mosbacher, J., Hricik, T.R., ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures (2003) Cell, 112, pp. 819-829; Bautista, D.M., Jordt, S.E., Nikai, T., Tsuruda, P.R., Read, A.J., Poblete, J., TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents (2006) Cell, 124, pp. 1269-1282; Cavanaugh, E.J., Simkin, D., Kim, D., Activation of transient receptor potential A1 channels by mustard oil, tetrahydrocannabinol and Ca2+ reveals different functional channel states (2008) Neuroscience, 154, pp. 1467-1476; Doerner, J.F., Gisselmann, G., Hatt, H., Wetzel, C.H., Transient receptor potential channel A1 is directly gated by calcium ions (2007) J. Biol. Chem, 282, pp. 13180-13189; Zurborg, S., Yurgionas, B., Jira, J.A., Caspani, O., Heppenstall, P.A., Direct activation of the ion channel TRPA1 by Ca2+ (2007) Nat. Neurosci, 10, pp. 277-279; Wang, Y.Y., Chang, R.B., Waters, H.N., McKemy, D.D., Liman, E.R., The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions (2008) J. Biol. Chem, 283, pp. 32691-32703; McMahon, S.B., Wood, J.N., Increasingly irritable and close to tears: TRPA1 in inflammatory pain (2006) Cell, 124, pp. 1123-1125; Tominaga, M., Tominaga, T., Structure and function of TRPV1 (2005) Pflugers Archiv. Eur. J. Physiol, 451, pp. 143-150; Vellani, V., Mapplebeck, S., Moriondo, A., Davis, J.B., McNaughton, P.A., Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide (2001) J. Physiol, 534, pp. 813-825; Carr, M.J., Kollarik, M., Meeker, S.N., Undem, B.J., A role for TRPV1 in bradykinin-induced excitation of vagal airway afferent nerve terminals (2003) J. Pharmacol. Exp. Ther, 304, pp. 1275-1279; Spahn, V., Stein, C., Zollner, C., Modulation of transient receptor vanilloid 1 activity by transient receptor potential ankyrin 1 (2014) Mol. Pharmacol, 85, pp. 335-344; Schmidt, M., Dubin, A.E., Petrus, M.J., Earley, T.J., Patapoutian, A., Nociceptive signals induce trafficking of TRPA1 to the plasma membrane (2009) Neuron, 64, pp. 498-509; Hellwig, N., Albrecht, N., Harteneck, C., Schultz, G., Schaefer, M., Homo- and heteromeric assembly of TRPV channel subunits (2005) J. Cell Sci, 118, pp. 917-928; Park, J.Y., Hwang, E.M., Yarishkin, O., Seo, J.H., Kim, E., Yoo, J., TRPM4b channel suppresses store-operated Ca2+ entry by a novel protein-protein interaction with the TRPC3 channel (2008) Biochem. Biophys. Res. Commun, 368, pp. 677-683; Ruparel, N.B., Patwardhan, A.M., Akopian, A.N., Hargreaves, K.M., Desensitization of transient receptor potential ankyrin 1 (TRPA1) by the TRP vanilloid 1-selective cannabinoid arachidonoyl-2 chloroethanolamine (2011) Mol. Pharmacol, 80, pp. 117-123; Staruschenko, A., Jeske, N.A., Akopian, A.N., Contribution of TRPV1-TRPA1 interaction to the single channel properties of the TRPA1 channel (2010) J. Biol. Chem, 285, pp. 15167-15177; Akopian, A.N., Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions (2011) Curr. Pharm. Biotechnol, 12, pp. 89-94; Fischer, M.J., Balasuriya, D., Jeggle, P., Goetze, T.A., McNaughton, P.A., Reeh, P.W., Direct evidence for functional TRPV1/TRPA1 heteromers (2014) Pflugers Archiv. Eur. J. Physiol, 466, pp. 2229-2241; Weng, H.J., Patel, K.N., Jeske, N.A., Bierbower, S.M., Zou, W., Tiwari, V., Tmem100 is a regulator of TRPA1-TRPV1 complex and contributes to persistent pain (2015) Neuron, 85, pp. 833-846; Birrell, M.A., Belvisi, M.G., Grace, M., Sadofsky, L., Faruqi, S., Hele, D.J., TRPA1 agonists evoke coughing in guinea pig and human volunteers (2009) Am. J. Respir. Crit. Care Med, 180, pp. 1042-1047; Brozmanova, M., Mazurova, L., Ru, F., Tatar, M., Kollarik, M., Comparison of TRPA1-versus TRPV1-mediated cough in guinea pigs (2012) Eur. J. Pharmacol, 689, pp. 211-218; Talavera, K., Gees, M., Karashima, Y., Meseguer, V.M., Vanoirbeek, J.A., Damann, N., Nicotine activates the chemosensory cation channel TRPA1 (2009) Nat. Neurosci, 12, pp. 1293-1299",
year = "2015",
doi = "10.1016/j.pupt.2015.08.003",
language = "English",
volume = "35",
pages = "87--93",
journal = "Pulmonary Pharmacology and Therapeutics",
issn = "1094-5539",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Interaction between TRPA1 and TRPV1: Synergy on pulmonary sensory nerves

AU - Lee, Lu-Yuan

AU - Hsu, Chun-Chun

AU - Lin, Yu-Jung

AU - Lin, Ruei-Lung

AU - Khosravi, Mehdi J.

N1 - 被引用次數:1 Export Date: 11 May 2016 CODEN: PPTHF 通訊地址: Lee, L.-Y.; Department of Physiology, University of Kentucky Medical CenterUnited States; 電子郵件: lylee@uky.edu 出資詳情: HL-96914, NIH, National Institutes of Health 出資詳情: UL1TR0000117, NIH, National Institutes of Health 參考文獻: Gees, M., Owsianik, G., Nilius, B., Voets, T., TRP channels (2012) Compr. Physiol, 2, pp. 563-608; Nilius, B., Owsianik, G., Voets, T., Peters, J.A., Transient receptor potential cation channels in disease (2007) Physiol. Rev, 87, pp. 165-217; Bautista, D.M., Pellegrino, M., Tsunozaki, M., TRPA1: A gatekeeper for inflammation (2013) Annu. Rev. Physiol, 75, pp. 181-200; Caterina, M.J., Julius, D., The vanilloid receptor: a molecular gateway to the pain pathway (2001) Annu. Rev. Neurosci, 24, pp. 487-517; Kobayashi, K., Fukuoka, T., Obata, K., Yamanaka, H., Dai, Y., Tokunaga, A., Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors (2005) J. Comp. Neurol, 493, pp. 596-606; Diogenes, A., Akopian, A.N., Hargreaves, K.M., NGF up-regulates TRPA1: implications for orofacial pain (2007) J. Dent. Res, 86, pp. 550-555; Nassenstein, C., Kwong, K., Taylor-Clark, T., Kollarik, M., Macglashan, D.M., Braun, A., Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs (2008) J. Physiol, 586, pp. 1595-1604; Jammes, Y., Fornaris, E., Mei, N., Barrat, E., Afferent and efferent components of the bronchial vagal branches in cats (1982) J. Aut. Nerv. Syst, 5, pp. 165-176; Coleridge, J.C., Coleridge, H.M., Afferent vagal C fibre innervation of the lungs and airways and its functional significance (1984) Rev. Physiol. Biochem. Pharmacol, 99, pp. 1-110; Lee, L.Y., Yu, J., Sensory nerves in lung and airways (2014) Compr. Physiol, 4, pp. 287-324; Bessac, B.F., Jordt, S.E., Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control (2008) Physiology (Bethesda, Md), 23, pp. 360-370; De Swert, K.O., Joos, G.F., Extending the understanding of sensory neuropeptides (2006) Eur. J. Pharmacol, 533, pp. 171-181; Lee, L.Y., Gu, Q., Role of TRPV1 in inflammation-induced airway hypersensitivity (2009) Curr. Opin. Pharmacol, 9, pp. 243-249; Geppetti, P., Materazzi, S., Nicoletti, P., The transient receptor potential vanilloid 1: role in airway inflammation and disease (2006) Eur. J. Pharmacol, 533, pp. 207-214; Gu, Q., Lee, L.Y., Characterization of acid signaling in rat vagal pulmonary sensory neurons (2006) Am. J. Physiol. Lung Cell. Mol. Physiol, 291, pp. L58-L65; Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D., Julius, D., The capsaicin receptor: a heat-activated ion channel in the pain pathway (1997) Nature, 389, pp. 816-824; Bandell, M., Story, G.M., Hwang, S.W., Viswanath, V., Eid, S.R., Petrus, M.J., Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin (2004) Neuron, 41, pp. 849-857; Taylor-Clark, T.E., McAlexander, M.A., Nassenstein, C., Sheardown, S.A., Wilson, S., Thornton, J., Relative contributions of TRPA1 and TRPV1 channels in the activation of vagal bronchopulmonary C-fibres by the endogenous autacoid 4-oxononenal (2008) J. Physiol, 586, pp. 3447-3459; Nilius, B., Appendino, G., Owsianik, G., The transient receptor potential channel TRPA1: from gene to pathophysiology (2012) Pflugers Archiv. Eur. J. Physiol, 464, pp. 425-458; Dai, Y., Wang, S., Tominaga, M., Yamamoto, S., Fukuoka, T., Higashi, T., Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain (2007) J. Clin. Investig, 117, pp. 1979-1987; Gu, Q., Kwong, K., Lee, L.Y., Ca2+ transient evoked by chemical stimulation is enhanced by PGE2 in vagal sensory neurons: role of cAMP/PKA signaling pathway (2003) J. Neurophysiol, 89, pp. 1985-1993; Kwong, K., Lee, L.Y., PGE(2) sensitizes cultured pulmonary vagal sensory neurons to chemical and electrical stimuli (2002) J. Appl. Physiol, 93, pp. 1419-1428; Patil, M.J., Jeske, N.A., Akopian, A.N., Transient receptor potential V1 regulates activation and modulation of transient receptor potential A1 by Ca2+ (2010) Neuroscience, 171, pp. 1109-1119; Salas, M.M., Hargreaves, K.M., Akopian, A.N., TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1 (2009) Eur. J. Neurosci, 29, pp. 1568-1578; Everaerts, W., Gees, M., Alpizar, Y.A., Farre, R., Leten, C., Apetrei, A., The capsaicin receptor TRPV1 is a crucial mediator of the noxious effects of mustard oil (2011) Curr. Biol, 21, pp. 316-321; Alpizar, Y.A., Boonen, B., Gees, M., Sanchez, A., Nilius, B., Voets, T., Allyl isothiocyanate sensitizes TRPV1 to heat stimulation (2014) Pflugers Archiv. Eur. J. Physiol, 466, pp. 507-515; Gees, M., Alpizar, Y.A., Boonen, B., Sanchez, A., Everaerts, W., Segal, A., Mechanisms of transient receptor potential vanilloid 1 activation and sensitization by allyl isothiocyanate (2013) Mol. Pharmacol, 84, pp. 325-334; Lin, Y.J., Lin, R.L., Ruan, T., Khosravi, M., Lee, L.Y., A synergistic effect of simultaneous TRPA1 and TRPV1 activations on vagal pulmonary C-fiber afferents (2015) J. Appl. Physiol, 118, pp. 273-281; Fernandes, E.S., Fernandes, M.A., Keeble, J.E., The functions of TRPA1 and TRPV1: moving away from sensory nerves (2012) Br. J. Pharmacol, 166, pp. 510-521; McGarvey, L.P., Butler, C.A., Stokesberry, S., Polley, L., McQuaid, S., Abdullah, H., Increased expression of bronchial epithelial transient receptor potential vanilloid 1 channels in patients with severe asthma (2014) J. Allergy Clin. Immunol, 133, pp. 704-712. , e4; Nassini, R., Pedretti, P., Moretto, N., Fusi, C., Carnini, C., Facchinetti, F., Transient receptor potential ankyrin 1 channel localized to non-neuronal airway cells promotes non-neurogenic inflammation (2012) PloS One, 7, p. e42454; Reilly, C.A., Johansen, M.E., Lanza, D.L., Lee, J., Lim, J.O., Yost, G.S., Calcium-dependent and independent mechanisms of capsaicin receptor (TRPV1)-mediated cytokine production and cell death in human bronchial epithelial cells (2005) J. Biochem. Mol. Toxicol, 19, pp. 266-275; Ni, D., Gu, Q., Hu, H.Z., Gao, N., Zhu, M.X., Lee, L.Y., Thermal sensitivity of isolated vagal pulmonary sensory neurons: role of transient receptor potential vanilloid receptors (2006) Am. J. Physiol. Regul. Integr. Comp. Physiol, 291, pp. R541-R550; Hsu, C.C., Lee, L.Y., Role of calcium ions in the positive interaction between TRPA1 and TRPV1 channels in bronchopulmonary sensory neurons (2015) J. Appl. Physiol, 118, pp. 1533-1543; Story, G.M., Peier, A.M., Reeve, A.J., Eid, S.R., Mosbacher, J., Hricik, T.R., ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures (2003) Cell, 112, pp. 819-829; Bautista, D.M., Jordt, S.E., Nikai, T., Tsuruda, P.R., Read, A.J., Poblete, J., TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents (2006) Cell, 124, pp. 1269-1282; Cavanaugh, E.J., Simkin, D., Kim, D., Activation of transient receptor potential A1 channels by mustard oil, tetrahydrocannabinol and Ca2+ reveals different functional channel states (2008) Neuroscience, 154, pp. 1467-1476; Doerner, J.F., Gisselmann, G., Hatt, H., Wetzel, C.H., Transient receptor potential channel A1 is directly gated by calcium ions (2007) J. Biol. Chem, 282, pp. 13180-13189; Zurborg, S., Yurgionas, B., Jira, J.A., Caspani, O., Heppenstall, P.A., Direct activation of the ion channel TRPA1 by Ca2+ (2007) Nat. Neurosci, 10, pp. 277-279; Wang, Y.Y., Chang, R.B., Waters, H.N., McKemy, D.D., Liman, E.R., The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions (2008) J. Biol. Chem, 283, pp. 32691-32703; McMahon, S.B., Wood, J.N., Increasingly irritable and close to tears: TRPA1 in inflammatory pain (2006) Cell, 124, pp. 1123-1125; Tominaga, M., Tominaga, T., Structure and function of TRPV1 (2005) Pflugers Archiv. Eur. J. Physiol, 451, pp. 143-150; Vellani, V., Mapplebeck, S., Moriondo, A., Davis, J.B., McNaughton, P.A., Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide (2001) J. Physiol, 534, pp. 813-825; Carr, M.J., Kollarik, M., Meeker, S.N., Undem, B.J., A role for TRPV1 in bradykinin-induced excitation of vagal airway afferent nerve terminals (2003) J. Pharmacol. Exp. 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PY - 2015

Y1 - 2015

N2 - Transient receptor potential ankyrin type 1 (TRPA1) and vanilloid type 1 (TRPV1) receptors are co-expressed in vagal pulmonary C-fiber sensory nerves. Because both these ligand-gated non-selective cation channels are sensitive to a number of endogenous inflammatory mediators, it is highly probable that they can be activated simultaneously during airway inflammation. Studies were carried out to investigate whether there is an interaction between these two polymodal transducers upon simultaneous activation, and how it modulates the activity of vagal pulmonary C-fiber sensory nerves. Our studies showed a distinct potentiating effect induced abruptly by simultaneous activations of TRPA1 and TRPV1 by their respective selective agonists, allyl isothiocyanate (AITC) and capsaicin (Cap), at near-threshold concentrations. This synergistic effect was demonstrated in the studies of single-unit recording of vagal bronchopulmonary C-fiber afferents and the reflex responses elicited by activation of these afferents in intact animals, as well as in the isolated nodose and jugular bronchopulmonary sensory neurons. This potentiating effect was absent when either AITC or Cap was replaced by non-TRPA1 and non-TRPV1 chemical activators of these neurons, demonstrating the selectivity of the interaction between these two TRP channels. Furthermore, the synergism was dependent upon the extracellular Ca2+, and the rapid onset of the action further suggests that the interaction probably occurred locally at the sites of these channels. These findings suggest that the TRPA1-TRPV1 interaction may play an important role in regulating the function and excitability of pulmonary sensory neurons during airway inflammation, but the mechanism underlying this positive interaction is not yet fully understood. © 2015 Elsevier Ltd.

AB - Transient receptor potential ankyrin type 1 (TRPA1) and vanilloid type 1 (TRPV1) receptors are co-expressed in vagal pulmonary C-fiber sensory nerves. Because both these ligand-gated non-selective cation channels are sensitive to a number of endogenous inflammatory mediators, it is highly probable that they can be activated simultaneously during airway inflammation. Studies were carried out to investigate whether there is an interaction between these two polymodal transducers upon simultaneous activation, and how it modulates the activity of vagal pulmonary C-fiber sensory nerves. Our studies showed a distinct potentiating effect induced abruptly by simultaneous activations of TRPA1 and TRPV1 by their respective selective agonists, allyl isothiocyanate (AITC) and capsaicin (Cap), at near-threshold concentrations. This synergistic effect was demonstrated in the studies of single-unit recording of vagal bronchopulmonary C-fiber afferents and the reflex responses elicited by activation of these afferents in intact animals, as well as in the isolated nodose and jugular bronchopulmonary sensory neurons. This potentiating effect was absent when either AITC or Cap was replaced by non-TRPA1 and non-TRPV1 chemical activators of these neurons, demonstrating the selectivity of the interaction between these two TRP channels. Furthermore, the synergism was dependent upon the extracellular Ca2+, and the rapid onset of the action further suggests that the interaction probably occurred locally at the sites of these channels. These findings suggest that the TRPA1-TRPV1 interaction may play an important role in regulating the function and excitability of pulmonary sensory neurons during airway inflammation, but the mechanism underlying this positive interaction is not yet fully understood. © 2015 Elsevier Ltd.

KW - Airway

KW - C fiber

KW - Inflammation

KW - TRPA1

KW - TRPV1

U2 - 10.1016/j.pupt.2015.08.003

DO - 10.1016/j.pupt.2015.08.003

M3 - Article

VL - 35

SP - 87

EP - 93

JO - Pulmonary Pharmacology and Therapeutics

JF - Pulmonary Pharmacology and Therapeutics

SN - 1094-5539

ER -