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Transient Receptor Potential Channels and Chronic Airway Inflammatory Diseases: A Comprehensive Review

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Abstract

Chronic airway inflammatory diseases remain a major problem worldwide, such that there is a need for additional therapeutic targets and novel drugs. Transient receptor potential (TRP) channels are a group of non-selective cation channels expressed throughout the body that are regulated by various stimuli. TRP channels have been identified in numerous cell types in the respiratory tract, including sensory neurons, airway epithelial cells, airway smooth muscle cells, and fibroblasts. Different types of TRP channels induce cough in sensory neurons via the vagus nerve. Permeability and cytokine production are also regulated by TRP channels in airway epithelial cells, and these channels also contribute to the modulation of bronchoconstriction. TRP channels may cooperate with other TRP channels, or act in concert with calcium-dependent potassium channels and calcium-activated chloride channel. Hence, TRP channels could be the potential therapeutic targets for chronic airway inflammatory diseases. In this review, we aim to discuss the expression profiles and physiological functions of TRP channels in the airway, and the roles they play in chronic airway inflammatory diseases.

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References

  1. Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224(5216):285–287

    Article  CAS  PubMed  Google Scholar 

  2. Owsianik G, Talavera K, Voets T, Nilius B (2006) Permeation and selectivity of TRP channels. Annu Rev Physiol 68:685–717. https://doi.org/10.1146/annurev.physiol.68.040204.101406

    Article  CAS  PubMed  Google Scholar 

  3. Ramsey IS, Delling M, Clapham DE (2006) An introduction to TRP channels. Annu Rev Physiol 68:619–647. https://doi.org/10.1146/annurev.physiol.68.040204.100431

    Article  CAS  PubMed  Google Scholar 

  4. Latorre R, Zaelzer C, Brauchi S (2009) Structure-functional intimacies of transient receptor potential channels. Q Rev Biophys 42(3):201–246. https://doi.org/10.1017/S0033583509990072

    Article  CAS  PubMed  Google Scholar 

  5. 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 (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112(6):819–829

    Article  CAS  PubMed  Google Scholar 

  6. Sabnis AS, Reilly CA, Veranth JM, Yost GS (2008) Increased transcription of cytokine genes in human lung epithelial cells through activation of a TRPM8 variant by cold temperatures. Am J Physiol Lung Cell Mol Physiol 295(1):L194–L200. https://doi.org/10.1152/ajplung.00072.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Plevkova J, Kollarik M, Poliacek I, Brozmanova M, Surdenikova L, Tatar M, Mori N, Canning BJ (2013) The role of trigeminal nasal TRPM8-expressing afferent neurons in the antitussive effects of menthol. J Appl Physiol (1985) 115(2):268–274. https://doi.org/10.1152/japplphysiol.01144.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427(6971):260–265. https://doi.org/10.1038/nature02282

    Article  CAS  PubMed  Google Scholar 

  9. Hondoh A, Ishida Y, Ugawa S, Ueda T, Shibata Y, Yamada T, Shikano M, Murakami S, Shimada S (2010) Distinct expression of cold receptors (TRPM8 and TRPA1) in the rat nodose-petrosal ganglion complex. Brain Res 1319:60–69. https://doi.org/10.1016/j.brainres.2010.01.016

    Article  CAS  PubMed  Google Scholar 

  10. Finney-Hayward TK, Popa MO, Bahra P, Li S, Poll CT, Gosling M, Nicholson AG, Russell RE, Kon OM, Jarai G, Westwick J, Barnes PJ, Donnelly LE (2010) Expression of transient receptor potential C6 channels in human lung macrophages. Am J Respir Cell Mol Biol 43(3):296–304. https://doi.org/10.1165/rcmb.2008-0373OC

    Article  CAS  PubMed  Google Scholar 

  11. Fernandez-Fernandez JM, Nobles M, Currid A, Vazquez E, Valverde MA (2002) Maxi K+ channel mediates regulatory volume decrease response in a human bronchial epithelial cell line. Am J Physiol Cell Physiol 283(6):C1705–C1714. https://doi.org/10.1152/ajpcell.00245.2002

    Article  CAS  PubMed  Google Scholar 

  12. DeFalco J, Duncton MA, Emerling D (2011) TRPM8 biology and medicinal chemistry. Curr Top Med Chem 11(17):2237–2252

    Article  CAS  PubMed  Google Scholar 

  13. Corteling RL, Li S, Giddings J, Westwick J, Poll C, Hall IP (2004) Expression of transient receptor potential C6 and related transient receptor potential family members in human airway smooth muscle and lung tissue. Am J Respir Cell Mol Biol 30(2):145–154. https://doi.org/10.1165/rcmb.2003-0134OC

    Article  CAS  PubMed  Google Scholar 

  14. 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(6653):816–824. https://doi.org/10.1038/39807

    Article  CAS  PubMed  Google Scholar 

  15. Beech DJ, Xu SZ, McHugh D, Flemming R (2003) TRPC1 store-operated cationic channel subunit. Cell Calcium 33(5–6):433–440

    Article  CAS  PubMed  Google Scholar 

  16. Alvarez DF, King JA, Weber D, Addison E, Liedtke W, Townsley MI (2006) Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: a novel mechanism of acute lung injury. Circ Res 99(9):988–995. https://doi.org/10.1161/01.RES.0000247065.11756.19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Doherty MJ, Mister R, Pearson MG, Calverley PM (2000) Capsaicin responsiveness and cough in asthma and chronic obstructive pulmonary disease. Thorax 55(8):643–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. O’Connell F, Thomas VE, Studham JM, Pride NB, Fuller RW (1996) Capsaicin cough sensitivity increases during upper respiratory infection. Respir Med 90(5):279–286

    Article  PubMed  Google Scholar 

  19. Nakajima T, Nishimura Y, Nishiuma T, Kotani Y, Nakata H, Yokoyama M (2006) Cough sensitivity in pure cough variant asthma elicited using continuous capsaicin inhalation. Allergol Int 55(2):149–155. https://doi.org/10.2332/allergolint.55.149

    Article  PubMed  Google Scholar 

  20. Bessac BF, Jordt SE (2008) Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control. Physiology (Bethesda) 23:360–370. https://doi.org/10.1152/physiol.00026.2008

    Article  CAS  Google Scholar 

  21. Smit LA, Kogevinas M, Anto JM, Bouzigon E, Gonzalez JR, Le Moual N, Kromhout H, Carsin AE, Pin I, Jarvis D, Vermeulen R, Janson C, Heinrich J, Gut I, Lathrop M, Valverde MA, Demenais F, Kauffmann F (2012) Transient receptor potential genes, smoking, occupational exposures and cough in adults. Respir Res 13:26. https://doi.org/10.1186/1465-9921-13-26

    Article  PubMed  PubMed Central  Google Scholar 

  22. Groneberg DA, Niimi A, Dinh QT, Cosio B, Hew M, Fischer A, Chung KF (2004) Increased expression of transient receptor potential vanilloid-1 in airway nerves of chronic cough. Am J Respir Crit Care Med 170(12):1276–1280. https://doi.org/10.1164/rccm.200402-174OC

    Article  PubMed  Google Scholar 

  23. Maher MP, Bhattacharya A, Ao H, Swanson N, Wu NT, Freedman J, Kansagara M, Scott B, Li DH, Eckert WA 3rd, Liu Y, Sepassi K, Rizzolio M, Fitzgerald A, Liu J, Branstetter BJ, Rech JC, Lebsack AD, Breitenbucher JG, Wickenden AD, Chaplan SR (2011) Characterization of 2-(2,6-dichloro-benzyl)-thiazolo[5,4-d]pyrimidin-7-yl]-(4-trifluoromethyl-phenyl)-amine (JNJ-39729209) as a novel TRPV1 antagonist. Eur J Pharmacol 663(1–3):40–50. https://doi.org/10.1016/j.ejphar.2011.05.001

    Article  CAS  PubMed  Google Scholar 

  24. Khalid S, Murdoch R, Newlands A, Smart K, Kelsall A, Holt K, Dockry R, Woodcock A, Smith JA (2014) Transient receptor potential vanilloid 1 (TRPV1) antagonism in patients with refractory chronic cough: a double-blind randomized controlled trial. J Allergy Clin Immunol 134(1):56–62. https://doi.org/10.1016/j.jaci.2014.01.038

    Article  CAS  PubMed  Google Scholar 

  25. Bhattacharya A, Scott BP, Nasser N, Ao H, Maher MP, Dubin AE, Swanson DM, Shankley NP, Wickenden AD, Chaplan SR (2007) Pharmacology and antitussive efficacy of 4-(3-trifluoromethyl-pyridin-2-yl)-piperazine-1-carboxylic acid (5-trifluoromethyl-pyridin-2-yl)-amide (JNJ17203212), a transient receptor potential vanilloid 1 antagonist in guinea pigs. J Pharmacol Exp Ther 323(2):665–674. https://doi.org/10.1124/jpet.107.127258

    Article  CAS  PubMed  Google Scholar 

  26. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2(10):695–702. https://doi.org/10.1038/35036318

    Article  CAS  PubMed  Google Scholar 

  27. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103(3):525–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zygmunt PM, Ermund A, Movahed P, Andersson DA, Simonsen C, Jonsson BA, Blomgren A, Birnir B, Bevan S, Eschalier A, Mallet C, Gomis A, Hogestatt ED (2013) Monoacylglycerols activate TRPV1—a link between phospholipase C and TRPV1. PLoS One 8(12):e81618. https://doi.org/10.1371/journal.pone.0081618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22(15):6408–6414. doi:20026679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jia Y, Wang X, Varty L, Rizzo CA, Yang R, Correll CC, Phelps PT, Egan RW, Hey JA (2004) Functional TRPV4 channels are expressed in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 287(2):L272–L278. https://doi.org/10.1152/ajplung.00393.2003

    Article  CAS  PubMed  Google Scholar 

  31. Fernandez-Fernandez JM, Andrade YN, Arniges M, Fernandes J, Plata C, Rubio-Moscardo F, Vazquez E, Valverde MA (2008) Functional coupling of TRPV4 cationic channel and large conductance, calcium-dependent potassium channel in human bronchial epithelial cell lines. Pflugers Arch 457(1):149–159. https://doi.org/10.1007/s00424-008-0516-3

    Article  CAS  PubMed  Google Scholar 

  32. Fontana GA, Lavorini F, Pistolesi M (2002) Water aerosols and cough. Pulm Pharmacol Ther 15(3):205–211. https://doi.org/10.1006/pupt.2002.0359

    Article  CAS  PubMed  Google Scholar 

  33. Bonvini SJ, Birrell MA, Grace MS, Maher SA, Adcock JJ, Wortley MA, Dubuis E, Ching YM, Ford AP, Shala F, Miralpeix M, Tarrason G, Smith JA, Belvisi MG (2016) Transient receptor potential cation channel, subfamily V, member 4 and airway sensory afferent activation: role of adenosine triphosphate. J Allergy Clin Immunol 138(1):249–261 e212. https://doi.org/10.1016/j.jaci.2015.10.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Nassini R, Pedretti P, Moretto N, Fusi C, Carnini C, Facchinetti F, Viscomi AR, Pisano AR, Stokesberry S, Brunmark C, Svitacheva N, McGarvey L, Patacchini R, Damholt AB, Geppetti P, Materazzi S (2012) Transient receptor potential ankyrin 1 channel localized to non-neuronal airway cells promotes non-neurogenic inflammation. PLoS One 7(8):e42454. https://doi.org/10.1371/journal.pone.0042454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Jaquemar D, Schenker T, Trueb B (1999) An ankyrin-like protein with transmembrane domains is specifically lost after oncogenic transformation of human fibroblasts. J Biol Chem 274(11):7325–7333

    Article  CAS  PubMed  Google Scholar 

  36. Buch TR, Schafer EA, Demmel MT, Boekhoff I, Thiermann H, Gudermann T, Steinritz D, Schmidt A (2013) Functional expression of the transient receptor potential channel TRPA1, a sensor for toxic lung inhalants, in pulmonary epithelial cells. Chem Biol Interact 206(3):462–471. https://doi.org/10.1016/j.cbi.2013.08.012

    Article  CAS  PubMed  Google Scholar 

  37. Talavera K, Gees M, Karashima Y, Meseguer VM, Vanoirbeek JA, Damann N, Everaerts W, Benoit M, Janssens A, Vennekens R, Viana F, Nemery B, Nilius B, Voets T (2009) Nicotine activates the chemosensory cation channel TRPA1. Nat Neurosci 12(10):1293–1299. https://doi.org/10.1038/nn.2379

    Article  CAS  PubMed  Google Scholar 

  38. Robinson RK, Birrell MA, Adcock JJ, Wortley MA, Dubuis ED, Chen S, McGilvery CM, Hu S, Shaffer MSP, Bonvini SJ, Maher SA, Mudway IS, Porter AE, Carlsten C, Tetley TD, Belvisi MG (2018) Mechanistic link between diesel exhaust particles and respiratory reflexes. J Allergy Clin Immunol 141(3):1074–1084 e1079. https://doi.org/10.1016/j.jaci.2017.04.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Bautista DM, Pellegrino M, Tsunozaki M (2013) TRPA1: a gatekeeper for inflammation. Annu Rev Physiol 75:181–200. https://doi.org/10.1146/annurev-physiol-030212-183811

    Article  CAS  PubMed  Google Scholar 

  40. Yang H, Li S (2016) Transient receptor potential ankyrin 1 (TRPA1) channel and neurogenic inflammation in pathogenesis of asthma. Med Sci Monit 22:2917–2923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Birrell MA, Belvisi MG, Grace M, Sadofsky L, Faruqi S, Hele DJ, Maher SA, Freund-Michel V, Morice AH (2009) TRPA1 agonists evoke coughing in guinea pig and human volunteers. Am J Respir Crit Care Med 180(11):1042–1047. https://doi.org/10.1164/rccm.200905-0665OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Andre E, Gatti R, Trevisani M, Preti D, Baraldi PG, Patacchini R, Geppetti P (2009) Transient receptor potential ankyrin receptor 1 is a novel target for pro-tussive agents. Br J Pharmacol 158(6):1621–1628. https://doi.org/10.1111/j.1476-5381.2009.00438.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mukhopadhyay I, Kulkarni A, Aranake S, Karnik P, Shetty M, Thorat S, Ghosh I, Wale D, Bhosale V, Khairatkar-Joshi N (2014) Transient receptor potential ankyrin 1 receptor activation in vitro and in vivo by pro-tussive agents: GRC 17536 as a promising anti-tussive therapeutic. PLoS One 9(5):e97005. https://doi.org/10.1371/journal.pone.0097005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Ruparel NB, Patwardhan AM, Akopian AN, Hargreaves KM (2008) Homologous and heterologous desensitization of capsaicin and mustard oil responses utilize different cellular pathways in nociceptors. Pain 135(3):271–279. https://doi.org/10.1016/j.pain.2007.06.005

    Article  CAS  PubMed  Google Scholar 

  45. Akopian AN, Ruparel NB, Jeske NA, Hargreaves KM (2007) Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization. J Physiol 583(Pt 1):175–193. https://doi.org/10.1113/jphysiol.2007.133231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sadofsky LR, Sreekrishna KT, Lin Y, Schinaman R, Gorka K, Mantri Y, Haught JC, Huggins TG, Isfort RJ, Bascom CC, Morice AH (2014) Unique responses are observed in transient receptor potential ankyrin 1 and vanilloid 1 (TRPA1 and TRPV1) co-expressing cells. Cells 3(2):616–626. https://doi.org/10.3390/cells3020616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lin YJ, Lin RL, Ruan T, Khosravi M, Lee LY (2015) A synergistic effect of simultaneous TRPA1 and TRPV1 activations on vagal pulmonary C-fiber afferents. J Appl Physiol (1985) 118(3):273–281. https://doi.org/10.1152/japplphysiol.00805.2014

    Article  CAS  PubMed  Google Scholar 

  48. Hsu CC, Lee LY (2015) Role of calcium ions in the positive interaction between TRPA1 and TRPV1 channels in bronchopulmonary sensory neurons. J Appl Physiol (1985) 118(12):1533–1543. https://doi.org/10.1152/japplphysiol.00043.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Staruschenko A, Jeske NA, Akopian AN (2010) Contribution of TRPV1-TRPA1 interaction to the single channel properties of the TRPA1 channel. J Biol Chem 285(20):15167–15177. https://doi.org/10.1074/jbc.M110.106153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Li M, Li Q, Yang G, Kolosov VP, Perelman JM, Zhou XD (2011) Cold temperature induces mucin hypersecretion from normal human bronchial epithelial cells in vitro through a transient receptor potential melastatin 8 (TRPM8)-mediated mechanism. J Allergy Clin Immunol 128(3):626–634 e621–e625. https://doi.org/10.1016/j.jaci.2011.04.032

    Article  CAS  PubMed  Google Scholar 

  51. Preti D, Szallasi A, Patacchini R (2012) TRP channels as therapeutic targets in airway disorders: a patent review. Expert Opin Ther Pat 22(6):663–695. https://doi.org/10.1517/13543776.2012.696099

    Article  CAS  PubMed  Google Scholar 

  52. Buday T, Brozmanova M, Biringerova Z, Gavliakova S, Poliacek I, Calkovsky V, Shetthalli MV, Plevkova J (2012) Modulation of cough response by sensory inputs from the nose—role of trigeminal TRPA1 versus TRPM8 channels. Cough 8(1):11. https://doi.org/10.1186/1745-9974-8-11

    Article  PubMed  PubMed Central  Google Scholar 

  53. Nassenstein C, Kwong K, Taylor-Clark T, Kollarik M, Macglashan DM, Braun A, Undem BJ (2008) Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J Physiol 586(6):1595–1604. https://doi.org/10.1113/jphysiol.2007.148379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Denda M, Sokabe T, Fukumi-Tominaga T, Tominaga M (2007) Effects of skin surface temperature on epidermal permeability barrier homeostasis. J Invest Dermatol 127(3):654–659. https://doi.org/10.1038/sj.jid.5700590

    Article  CAS  PubMed  Google Scholar 

  55. Akazawa Y, Yuki T, Yoshida H, Sugiyama Y, Inoue S (2013) Activation of TRPV4 strengthens the tight-junction barrier in human epidermal keratinocytes. Skin Pharmacol Physiol 26(1):15–21. https://doi.org/10.1159/000343173

    Article  CAS  PubMed  Google Scholar 

  56. Post S, Nawijn MC, Jonker MR, Kliphuis N, van den Berge M, van Oosterhout AJ, Heijink IH (2013) House dust mite-induced calcium signaling instigates epithelial barrier dysfunction and CCL20 production. Allergy 68(9):1117–1125. https://doi.org/10.1111/all.12202

    Article  CAS  PubMed  Google Scholar 

  57. Post S, Nawijn MC, Hackett TL, Baranowska M, Gras R, van Oosterhout AJ, Heijink IH (2012) The composition of house dust mite is critical for mucosal barrier dysfunction and allergic sensitisation. Thorax 67(6):488–495. https://doi.org/10.1136/thoraxjnl-2011-200606

    Article  CAS  PubMed  Google Scholar 

  58. Piacentini GL, Peroni D, Crestani E, Zardini F, Bodini A, Costella S, Boner AL (2007) Exhaled air temperature in asthma: methods and relationship with markers of disease. Clin Exp Allergy 37(3):415–419. https://doi.org/10.1111/j.1365-2222.2007.02663.x

    Article  CAS  PubMed  Google Scholar 

  59. Nilsson H, Dragomir A, Ahlander A, Johannesson M, Roomans GM (2007) Effects of hyperosmotic stress on cultured airway epithelial cells. Cell Tissue Res 330(2):257–269. https://doi.org/10.1007/s00441-007-0482-7

    Article  PubMed  Google Scholar 

  60. Yocum GT, Chen J, Choi CH, Townsend EA, Zhang Y, Xu D, Fu XW, Sanderson MJ, Emala CW (2017) Role of transient receptor potential vanilloid 1 in the modulation of airway smooth muscle tone and calcium handling. Am J Physiol Lung Cell Mol Physiol 312(6):L812–L821. https://doi.org/10.1152/ajplung.00064.2017

    Article  PubMed  PubMed Central  Google Scholar 

  61. Lin RL, Hayes D Jr, Lee LY (2009) Bronchoconstriction induced by hyperventilation with humidified hot air: role of TRPV1-expressing airway afferents. J Appl Physiol (1985) 106(6):1917–1924. https://doi.org/10.1152/japplphysiol.00065.2009

    Article  Google Scholar 

  62. Rousseau E, Cloutier M, Morin C, Proteau S (2005) Capsazepine, a vanilloid antagonist, abolishes tonic responses induced by 20-HETE on guinea pig airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 288(3):L460–L470. https://doi.org/10.1152/ajplung.00252.2004

    Article  CAS  PubMed  Google Scholar 

  63. Delescluse I, Mace H, Adcock JJ (2012) Inhibition of airway hyper-responsiveness by TRPV1 antagonists (SB-705498 and PF-04065463) in the unanaesthetized, ovalbumin-sensitized guinea pig. Br J Pharmacol 166(6):1822–1832. https://doi.org/10.1111/j.1476-5381.2012.01891.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Ricciardolo FL (2001) Mechanisms of citric acid-induced bronchoconstriction. Am J Med 111(Suppl 8A):18S–24S

    Article  PubMed  Google Scholar 

  65. Bolser DC, Aziz SM, Chapman RW (1991) Ruthenium red decreases capsaicin and citric acid-induced cough in guinea pigs. Neurosci Lett 126(2):131–133

    Article  CAS  PubMed  Google Scholar 

  66. Kikuno S, Taguchi K, Iwamoto N, Yamano S, Cho AK, Froines JR, Kumagai Y (2006) 1,2-Naphthoquinone activates vanilloid receptor 1 through increased protein tyrosine phosphorylation, leading to contraction of guinea pig trachea. Toxicol Appl Pharmacol 210(1–2):47–54. https://doi.org/10.1016/j.taap.2005.06.015

    Article  CAS  PubMed  Google Scholar 

  67. McAlexander MA, Luttmann MA, Hunsberger GE, Undem BJ (2014) Transient receptor potential vanilloid 4 activation constricts the human bronchus via the release of cysteinyl leukotrienes. J Pharmacol Exp Ther 349(1):118–125. https://doi.org/10.1124/jpet.113.210203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Cheah EY, Burcham PC, Mann TS, Henry PJ (2014) Acrolein relaxes mouse isolated tracheal smooth muscle via a TRPA1-dependent mechanism. Biochem Pharmacol 89(1):148–156. https://doi.org/10.1016/j.bcp.2014.02.009

    Article  CAS  PubMed  Google Scholar 

  69. Cheah EY, Mann TS, Burcham PC, Henry PJ (2015) Influenza A infection attenuates relaxation responses of mouse tracheal smooth muscle evoked by acrolein. Biochem Pharmacol 93(4):519–526. https://doi.org/10.1016/j.bcp.2014.12.015

    Article  CAS  PubMed  Google Scholar 

  70. Danielsson J, Yim P, Rinderspacher A, Fu XW, Zhang Y, Landry DW, Emala CW (2014) Chloride channel blockade relaxes airway smooth muscle and potentiates relaxation by beta-agonists. Am J Physiol Lung Cell Mol Physiol 307(3):L273–L282. https://doi.org/10.1152/ajplung.00351.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Zhang CH, Li Y, Zhao W, Lifshitz LM, Li H, Harfe BD, Zhu MS, ZhuGe R (2013) The transmembrane protein 16A Ca(2+)-activated Cl- channel in airway smooth muscle contributes to airway hyperresponsiveness. Am J Respir Crit Care Med 187(4):374–381. https://doi.org/10.1164/rccm.201207-1303OC

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Scudieri P, Caci E, Bruno S, Ferrera L, Schiavon M, Sondo E, Tomati V, Gianotti A, Zegarra-Moran O, Pedemonte N, Rea F, Ravazzolo R, Galietta LJ (2012) Association of TMEM16A chloride channel overexpression with airway goblet cell metaplasia. J Physiol 590(23):6141–6155. https://doi.org/10.1113/jphysiol.2012.240838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kondo M, Tsuji M, Hara K, Arimura K, Yagi O, Tagaya E, Takeyama K, Tamaoki J (2017) Chloride ion transport and overexpression of TMEM16A in a guinea-pig asthma model. Clin Exp Allergy 47(6):795–804. https://doi.org/10.1111/cea.12887

    Article  CAS  PubMed  Google Scholar 

  74. Andrade YN, Fernandes J, Vazquez E, Fernandez-Fernandez JM, Arniges M, Sanchez TM, Villalon M, Valverde MA (2005) TRPV4 channel is involved in the coupling of fluid viscosity changes to epithelial ciliary activity. J Cell Biol 168(6):869–874. https://doi.org/10.1083/jcb.200409070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Alenmyr L, Uller L, Greiff L, Hogestatt ED, Zygmunt PM (2014) TRPV4-mediated calcium influx and ciliary activity in human native airway epithelial cells. Basic Clin Pharmacol Toxicol 114(2):210–216. https://doi.org/10.1111/bcpt.12135

    Article  CAS  PubMed  Google Scholar 

  76. Lorenzo IM, Liedtke W, Sanderson MJ, Valverde MA (2008) TRPV4 channel participates in receptor-operated calcium entry and ciliary beat frequency regulation in mouse airway epithelial cells. Proc Natl Acad Sci USA 105(34):12611–12616. https://doi.org/10.1073/pnas.0803970105

    Article  PubMed  PubMed Central  Google Scholar 

  77. McGarvey LP, Butler CA, Stokesberry S, Polley L, McQuaid S, Abdullah H, Ashraf S, McGahon MK, Curtis TM, Arron J, Choy D, Warke TJ, Bradding P, Ennis M, Zholos A, Costello RW, Heaney LG (2014) Increased expression of bronchial epithelial transient receptor potential vanilloid 1 channels in patients with severe asthma. J Allergy Clin Immunol 133(3):704–712. https://doi.org/10.1016/j.jaci.2013.09.016

    Article  CAS  PubMed  Google Scholar 

  78. Cantero-Recasens G, Gonzalez JR, Fandos C, Duran-Tauleria E, Smit LA, Kauffmann F, Anto JM, Valverde MA (2010) Loss of function of transient receptor potential vanilloid 1 (TRPV1) genetic variant is associated with lower risk of active childhood asthma. J Biol Chem 285(36):27532–27535. https://doi.org/10.1074/jbc.C110.159491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Mori T, Saito K, Ohki Y, Arakawa H, Tominaga M, Tokuyama K (2011) Lack of transient receptor potential vanilloid-1 enhances Th2-biased immune response of the airways in mice receiving intranasal, but not intraperitoneal, sensitization. Int Arch Allergy Immunol 156(3):305–312. https://doi.org/10.1159/000323889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Tsuji F, Murai M, Oki K, Inoue H, Sasano M, Tanaka H, Inagaki N, Aono H (2010) Effects of SA13353, a transient receptor potential vanilloid 1 agonist, on leukocyte infiltration in lipopolysaccharide-induced acute lung injury and ovalbumin-induced allergic airway inflammation. J Pharmacol Sci 112(4):487–490

    Article  CAS  PubMed  Google Scholar 

  81. Zhu G, Investigators I, Gulsvik A, Bakke P, Ghatta S, Anderson W, Lomas DA, Silverman EK, Pillai SG (2009) Association of TRPV4 gene polymorphisms with chronic obstructive pulmonary disease. Hum Mol Genet 18(11):2053–2062. https://doi.org/10.1093/hmg/ddp111

    Article  CAS  PubMed  Google Scholar 

  82. Baxter M, Eltom S, Dekkak B, Yew-Booth L, Dubuis ED, Maher SA, Belvisi MG, Birrell MA (2014) Role of transient receptor potential and pannexin channels in cigarette smoke-triggered ATP release in the lung. Thorax 69(12):1080–1089. https://doi.org/10.1136/thoraxjnl-2014-205467

    Article  PubMed  Google Scholar 

  83. Henry CO, Dalloneau E, Perez-Berezo MT, Plata C, Wu Y, Guillon A, Morello E, Aimar RF, Potier-Cartereau M, Esnard F, Coraux C, Bornchen C, Kiefmann R, Vandier C, Touqui L, Valverde MA, Cenac N, Si-Tahar M (2016) In vitro and in vivo evidence for an inflammatory role of the calcium channel TRPV4 in lung epithelium: potential involvement in cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 311(3):L664–L675. https://doi.org/10.1152/ajplung.00442.2015

    Article  PubMed  Google Scholar 

  84. Prandini P, De Logu F, Fusi C, Provezza L, Nassini R, Montagner G, Materazzi S, Munari S, Gilioli E, Bezzerri V, Finotti A, Lampronti I, Tamanini A, Dechecchi MC, Lippi G, Ribeiro CM, Rimessi A, Pinton P, Gambari R, Geppetti P, Cabrini G (2016) Transient receptor potential ankyrin 1 channels modulate inflammatory response in respiratory cells from patients with cystic fibrosis. Am J Respir Cell Mol Biol 55(5):645–656. https://doi.org/10.1165/rcmb.2016-0089OC

    Article  CAS  PubMed  Google Scholar 

  85. Caceres AI, Brackmann M, Elia MD, Bessac BF, del Camino D, D’Amours M, Witek JS, Fanger CM, Chong JA, Hayward NJ, Homer RJ, Cohn L, Huang X, Moran MM, Jordt SE (2009) A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc Natl Acad Sci U S A 106(22):9099–9104. https://doi.org/10.1073/pnas.0900591106

    Article  PubMed  PubMed Central  Google Scholar 

  86. Nesuashvili L, Hadley SH, Bahia PK, Taylor-Clark TE (2013) Sensory nerve terminal mitochondrial dysfunction activates airway sensory nerves via transient receptor potential (TRP) channels. Mol Pharmacol 83(5):1007–1019. https://doi.org/10.1124/mol.112.084319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Wang L, Cvetkov TL, Chance MR, Moiseenkova-Bell VY (2012) Identification of in vivo disulfide conformation of TRPA1 ion channel. J Biol Chem 287(9):6169–6176. https://doi.org/10.1074/jbc.M111.329748

    Article  CAS  PubMed  Google Scholar 

  88. 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 Invest 118(5):1899–1910. https://doi.org/10.1172/JCI34192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Yildirim E, Carey MA, Card JW, Dietrich A, Flake GP, Zhang Y, Bradbury JA, Rebolloso Y, Germolec DR, Morgan DL, Zeldin DC, Birnbaumer L (2012) Severely blunted allergen-induced pulmonary Th2 cell response and lung hyperresponsiveness in type 1 transient receptor potential channel-deficient mice. Am J Physiol Lung Cell Mol Physiol 303(6):L539–L549. https://doi.org/10.1152/ajplung.00389.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Sel S, Rost BR, Yildirim AO, Sel B, Kalwa H, Fehrenbach H, Renz H, Gudermann T, Dietrich A (2008) Loss of classical transient receptor potential 6 channel reduces allergic airway response. Clin Exp Allergy 38(9):1548–1558. https://doi.org/10.1111/j.1365-2222.2008.03043.x

    Article  CAS  PubMed  Google Scholar 

  91. Pedersen F, Marwitz S, Holz O, Kirsten A, Bahmer T, Waschki B, Magnussen H, Rabe KF, Goldmann T, Uddin M, Watz H (2015) Neutrophil extracellular trap formation and extracellular DNA in sputum of stable COPD patients. Respir Med 109(10):1360–1362. https://doi.org/10.1016/j.rmed.2015.08.008

    Article  PubMed  Google Scholar 

  92. O’Donnell R, Breen D, Wilson S, Djukanovic R (2006) Inflammatory cells in the airways in COPD. Thorax 61(5):448–454. https://doi.org/10.1136/thx.2004.024463

    Article  PubMed  PubMed Central  Google Scholar 

  93. Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2001) TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29(3):645–655

    Article  CAS  PubMed  Google Scholar 

  94. Hofmann T, Schaefer M, Schultz G, Gudermann T (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci U S A 99(11):7461–7466. https://doi.org/10.1073/pnas.102596199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Yuan JP, Kiselyov K, Shin DM, Chen J, Shcheynikov N, Kang SH, Dehoff MH, Schwarz MK, Seeburg PH, Muallem S, Worley PF (2003) Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 114(6):777–789

    Article  CAS  PubMed  Google Scholar 

  96. Naumov DE, Perelman JM, Kolosov VP, Potapova TA, Maksimov VN, Zhou X (2015) Transient receptor potential melastatin 8 gene polymorphism is associated with cold-induced airway hyperresponsiveness in bronchial asthma. Respirology 20(8):1192–1197. https://doi.org/10.1111/resp.12605

    Article  PubMed  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (81500012), the Zhejiang Provincial Natural Science Foundation of China (LQ16H010001), the Medical and Health Technology Program of Zhejiang Province (2015111464, 2017204226) and the Program of Zhejiang Province Health High-level Personnel (2017) to Yang Xia.

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Xia, Y., Xia, L., Lou, L. et al. Transient Receptor Potential Channels and Chronic Airway Inflammatory Diseases: A Comprehensive Review. Lung 196, 505–516 (2018). https://doi.org/10.1007/s00408-018-0145-3

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