Roles of TRPA1 and TRPV1 in cigarette smoke -induced airway epithelial cell injury model

Free Radical Biology and Medicine

Volumn 134, Issue , 2019, Pages 229-238

  Wang, Muyun ^a,b   Zhang, Yanbei ^b   Xu, Mengmeng ^a,b   Zhang, Hai ^a   Chen, Yuqing ^a   Chung, Kian Fan ^c   Adcock, Ian M ^c   Li, Feng ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Airway epithelial cell injury; Cigarette smoke; COPD; Mitochondria damage; Oxidative stress; TRPA1; TRPV1

Indexed keywords

A 967079; CALCIUM; CATALASE; CIGARETTE SMOKE; CRYOPYRIN; DICHLORODIHYDROFLUORESCEIN DIACETATE; DYSTROPHIN RELATED PROTEIN 1; HEME OXYGENASE 1; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 33; INTERLEUKIN 8; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MITOCHONDRIAL FISSION FACTOR; MITOCHONDRIAL PROTEIN; MITOFUSIN 2; N (1,4 BENZODIOXAN 6 YL) 3 (4 TERT BUTYLPHENYL)ACRYLAMIDE; OPTIC ATROPHY 1 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SHORT HAIRPIN RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL AFFECTING AGENT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; ANTIOXIDANT; TRPA1 PROTEIN, HUMAN; TRPV1 PROTEIN, HUMAN; VANILLOID RECEPTOR;

A-549 CELL LINE; AIRWAY EPITHELIUM CELL; ARTICLE; BEAS-2B CELL LINE; BRONCHUS EPITHELIUM; CALCIUM TRANSPORT; CELL DAMAGE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE SILENCING; HUMAN; HUMAN CELL; INFLAMMATION; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ADVERSE EVENT; APOPTOSIS; BRONCHUS; CELL CULTURE; DRUG EFFECT; EPITHELIUM CELL; GENETICS; LUNG ALVEOLUS; METABOLISM; PATHOLOGY; SMOKE;

ANTIOXIDANTS; APOPTOSIS; BRONCHI; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; INFLAMMATION; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PULMONARY ALVEOLI; SMOKE; TRPA1 CATION CHANNEL; TRPV CATION CHANNELS;

EID: 85060090701     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2019.01.004     Document Type: Article

References (50)

1. WHO Chronic Respiratory Diseases Fact Page（. Available from: 〈http://www.who.int/respiratory/copd/en/〉 (Accessed October 2015).
2. Kirkham, P.A., Barnes, P.J., Oxidative stress in copd. Chest 144 (2013), 266–273.
3. Domej, W., Oettl, K., Renner, W., Oxidative stress and free radicals in copd – implications and relevance for treatment. Int J. Chron. Obstruct Pulmon Dis. 9 (2014), 1207–1224.
4. Piantadosi, C.A., Suliman, H.B., Mitochondrial dysfunction in lung pathogenesis. Annu. Rev. Physiol. 79 (2017), 495–515.
5. Aravamudan, B., Thompson, M.A., Pabelick, C.M., Prakash, Y.S., Mitochondria in lung diseases. Expert Rev. Respir. Med. 7 (2013), 631–646.
6. Aravamudan, B., Thompson, M., Sieck, G.C., Vassallo, R., Pabelick, C.M., Prakash, Y.S., Functional effects of cigarette smoke-induced changes in airway smooth muscle mitochondrial morphology. J. Cell Physiol. 232 (2017), 1053–1068.
7. Kang, M.J., Shadel, G.S., A mitochondrial perspective of chronic obstructive pulmonary disease pathogenesis. Tuberc. Respir. Dis. 79 (2016), 207–213.
8. Zhou, R., Yazdi, A.S., Menu, P., Tschopp, J., A role for mitochondria in nlrp3 inflammasome activation. Nature 469 (2011), 221–225.
9. Murakami, T., Ockinger, J., Yu, J., Byles, V., Mccoll, A., Hofer, A.M., Horng, T., Critical role for calcium mobilization in activation of the nlrp3 inflammasome. Proc. Natl. Acad. Sci. USA 109 (2012), 11282–11287.
10. Preti, D., Szallasi, A., Patacchini, R., Trp channels as therapeutic targets in airway disorders: a patent review. Expert Opin. Ther. Pat. 22 (2012), 663–695.
11. Colsoul, B., Nilius, B., Vennekens, R., On the putative role of transient receptor potential cation channels in asthma. Clin. Exp. Allergy 39 (2009), 1456–1466.
12. Bautista, D.M., Pellegrino, M., Tsunozaki, M., TRPA1: a gatekeeper for inflammation. Annu. Rev. Physiol. 2013 (2013), 181–200.
13. Caterina, M., Julius, D., The vanilloid receptor: a molecular gateway to the pain pathway. Annu. Rev. Neurosci. 24 (2001), 487–517.
14. Kode, A., Yang, S.R., Rahman, I., Differential effects of cigarette smoke on oxidative stress and proinflammatory cytokine release in primary human airway epithelial cells and in a variety of transformed alveolar epithelial cells. Respir. Res., 7, 2006, 132.
15. Clunes, L.,A., Bridges, A., Alexis, N., Tarran, R., In vivo versus in vitro airway surface liquid nicotine levels following cigarette smoke exposure. J. Anal. Toxicol. 32 (2008), 201–207.
16. Dietrich, A., Steinritz, D., Gudermann, T., Transient receptor potential (trp) channels as molecular targets in lung toxicology and associated diseases. Cell Calcium 67 (2017), 123–137.
17. Andrè, E., Campi, B., Materazzi, S., Trevisani, M., Amadesi, S., Massi, D., Creminon, C., Vaksman, N., Nassini, R., Civelli, M., Baraldi, P.G., Poole, D.,P., Bunnett, N.W., Geppetti, P., Patacchini, R., Cigarette smoke-induced neurogenic inflammation is mediated by alpha,beta-unsaturated aldehydes and the trpa1 receptor in rodents. J. Clin. Investig. 118 (2008), 2574–2582.
18. Bang, S., Kim, K.Y., Yoo, S., Kim, Y.G., Hwang, S.W., Transient receptor potential a1 mediates acetaldehyde-evoked pain sensation. Eur. J. Neurosci. 26 (2007), 2516–2523.
19. Nilius, B., Transient receptor potential (trp) cation channels: rewarding unique proteins. Bull. Mem. Acad. R. Med. Belg. 162 (2007), 244–253.
20. Grace, M.S., Baxter, M., Dubuis, E., Birrell, M.A., Belvisi, M.G., Transient receptor potential (trp) channels in the airway: role in airway disease. Br. J. Pharmacol. 171 (2014), 2593–2607.
21. Mcleod, R.L., Fernandez, X., Correll, C.C., Phelps, T.P., Jia, Y., Wang, X., Hey, J.A., Trpv1 antagonists attenuate antigen-provoked cough in ovalbumin sensitized guinea pigs. Cough, 2, 2006, 10.
22. Doherty, M.J., Mister, R., Pearson, M.G., Calverley, P.M., Capsaicin responsiveness and cough in asthma and chronic obstructive pulmonary disease. Thorax 55 (2000), 643–649.
23. Nakajima, T., Nishimura, Y., Nishiuma, T., Kotani, Y., Nakata, H., Yokoyama, M., Cough sensitivity in pure cough variant asthma elicited using continuous capsaicin inhalation. Allergol. Int. 55:2006 (2006), 149–155.
24. Carr, M.J., Hunter, D.D., Jacoby, D.B., Undem, B.J., Expression of tachykinins in nonnociceptive vagal afferent neurons during respiratory viral infection in guinea pigs. Am. J. Respir. Crit. Care Med. 165 (2002), 1071–1075.
25. Lewis, C.A., Ambrose, C., Banner, K., Battram, C., Butler, K., Giddings, J., Mok, J., Nasra, J., Winny, C., Poll, C., Animal models of cough: literature review and presentation of a novel cigarette smoke-enhanced cough model in the guinea-pig. Pulm. Pharmacol. Ther. 20 (2007), 325–333.
26. Lieu, T.M., Myers, A.C., Meeker, S., Undem, B.J., Trpv1 induction in airway vagal low-threshold mechanosensory neurons by allergen challenge and neurotrophic factors. Am. J. Physiol. Lung Cell. Mol. Physiol. 302 (2012), 941–948.
27. Ye, X.M., Zhong, N.S., Liu, C.L., Chen, R.C., Cough reflex sensitivity is increased in guinea pigs with parainfluenza virus infection. Exp. Lung Res. 37 (2011), 186–194.
28. Zhang, G., Lin, R.L., Wiggers, M., Snow, D.M., Lee, L.Y., Altered expression of trpv1 and sensitivity to capsaicin in pulmonary myelinated afferents following chronic airway inflammation in the rat. J. Physiol. 586 (2008), 5771–5786.
29. Michaeloudes, C., Bhavsar, P.K., Mumby, S., Chung, K.F., Adcock, I.M., Dealing with stress: defective metabolic adaptation in chronic obstructive pulmonary disease pathogenesis. Ann. Am. Thorac. Soc. 14:Supplement_5 (2017), S374–S382.
30. Lin, A.H., Liu, M.H., Ko, H.K., Perng, D.W., Lee, T.S., Kou, Y.R., Lung epithelial trpa1 transduces the extracellular ros into transcriptional regulation of lung inflammation induced by cigarette smoke: the role of influxed ca2+. Mediat. Inflamm., 2015, 2015, 148367.
31. Jiang, F., Zhang, Y., Dusting, G. J, Nadph oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol. Rev. 63 (2011), 218–242.
32. Hoffmann, R.F., Zarrintan, S., Brandenburg, S.M., Kol, A., Bruin, H.G.D., Jafari, S., et al. Prolonged cigarette smoke exposure alters mitochondrial structure and function in airway epithelial cells. Respir. Res., 14, 2013, 97.
33. Wiegman, C.H., Michaeloudes, C., Haji, G., Narang, P., Clarke, C.J., Russell, K.E., Bao, W., Pavlidis, S., Barnes, P.J., Kanerva, J., Bittner, A., Rao, N., Murphy, M.P., Kirkham, P.A., Chung, K.F., Adcock, I.M., COPDMAP, Oxidative stress–induced mitochondrial dysfunction drives inflammation and airway smooth muscle remodeling in patients with chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 136 (2015), 769–780.
34. van der Toorn, M., Slebos, D.J., de Bruin, H.G., Leuvenink, H.G., Bakker, S.J., Gans, R.O., Koëter, G.H., van Oosterhout, A.J., Kauffman, H.F., Cigarette smoke-induced blockade of the mitochondrial respiratory chain switches lung epithelial cell apoptosisinto necrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 292:5 (2007), L1211–L1218.
35. Yang, J., Yu, H.M., Zhou, X.D., Huang, H.P., Han, Zh, Kolosov, V.P., Perelman, J.M., Cigarette smoke induces mucin hypersecretion and inflammatory response through the p66shc adaptor protein-mediated mechanism in human bronchial epithelial cells. Mol. Immunol. 69 (2016), 86–98.
36. Green, D.R., Kroemer, G., The pathophysiology of mitochondrial cell death. Science 305 (2004), 626–629.
37. Uh, S.T., Koo, S.M., Kim, Y., Kim, K., Park, S., Jang, A.S., Kim, D., Kim, Y.H., Park, C.S., The activation of nlrp3-inflammsome by stimulation of diesel exhaust particles in lung tissues from emphysema model and raw 264.7 cell line. Korean J. Intern. Med. 32 (2017), 865–874.
38. Wu, X., Zhang, H., Qi, W., Zhang, Y., Li, J., Li, Z., Lin, Y., Bai, X., Liu, X., Chen, X., Yang, H., Xu, C., Zhang, Y., Yang, B., Nicotine promotes atherosclerosis via ros-nlrp3-mediated endothelial cell pyroptosis. Cell Death Dis., 9, 2018, 171.
39. Barnes, P.J., Adcock, I.M., Ito, K., Histone acetylation and deacetylation: importance in inflammatory lung diseases. Eur. Respir. J. 25 (2005), 552–563.
40. Rahman, I., Macnee, W., Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches. Free Radic. Biol. Med. 28 (2000), 1405–1420.
41. Hoshimoto, A., Suzuki, Y., Katsuno, T., Nakajima, H., Saito, Y., Caprylic acid and medium-chain triglycerides inhibit il-8 gene transcription in caco-2 cells: comparison with the potent histone deacetylase inhibitor trichostatin a. Br. J. Pharmacol. 136 (2002), 280–286.
42. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T.K., Zurawski, G., Moshrefi, M., Qin, J., Li, X., Gorman, D.M., Bazan, J.F., Kastelein, R.A., IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23 (2005), 479–490.
43. Cassel, S.L., Eisenbarth, S.C., Iyer, S.S., Sadler, J.J., Colegio, O.R., Tephly, L.A., Carter, A.B., Rothman, P.B., Flavell, R.A., Sutterwala, F.S., The Nalp3 inflammasome is essential for the development of silicosis. Proc. Natl. Acad. Sci. USA 105 (2008), 9035–9040.
44. Lee, S., Suh, G.Y., Ryter, S.W., Choi, A.M., Regulation and function of the nucleotide binding domain leucine-rich repeat-containing receptor, pyrin domain-containing-3 inflammasome in lung disease. Am. J. Respir. Cell. Mol. Biol. 54 (2016), 151–160.
45. Cruz, C.M., Rinna, A., Forman, H.J., Ventura, A.L.M., Persechini, P.M., Ojcius, D.M., Atp activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J. Biol. Chem. 282 (2007), 2871–2879.
46. Faner, R., Sobradillo, P., Noguera, A., Gomez, C., Cruz, T., López-Giraldo, A., Ballester, E., Soler, N., Arostegui, J.I., Pelegrín, P., Rodriguez-Roisin, R., Yagüe, J., Cosio, B.G., Juan, M., Agustí, A., The inflammasome pathway in stable COPD and acute exacerbations: ERJ Open Res., 2, 2016 (pii: 00002-2016).
47. Di Stefano, A., Caramori, G., Barczyk, A., Vicari, C., Brun, P., Zanini, A., Cappello, F., Garofano, E., Padovani, A., Contoli, M., Casolari, P., Durham, A.L., Chung, K.F., Barnes, P.J., Papi, A., Adcock, I., Balbi, B., Innate immunity but not nlrp3 inflammasome activation correlates with severity of stable copd. Thorax 69 (2014), 516–524.
48. Calverley, P.M.A., Sethi, S., Dawson, M., Ward, C.K., Finch, D.K., Penney, M., Newbold, P., van der Merwe, R., A randomised, placebo-controlled trial of anti–interleukin-1 receptor 1 monoclonal antibody medi8968 in chronic obstructive pulmonary disease. Respir. Res., 18, 2017, 153.
49. Salas, M.M., Hargreaves, K.M., Akopian, A.N., Trpa1-mediated responses in trigeminal sensory neurons: interaction between trpa1 and trpv1. Eur. J. Neurosci. 29 (2009), 1568–1578.
50. Lee, L.Y., Hsu, C.C., Lin, Y.J., Lin, R.L., Khosravi, M., Interaction between TRPA1 and TRPV1: synergy on pulmonary sensory nerves. Pulm. Pharmacol. Ther. 35 (2015), 87–93.