TRP channels and traffic-related environmental pollution-induced pulmonary disease

Seminars in Immunopathology

Volumn 38, Issue 3, 2016, Pages 331-338

  Akopian, Armen N ^a   Fanick, E Robert ^b   Brooks, Edward G ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b SOUTHWEST RESEARCH INSTITUTE   (United States)

Author keywords

Acute lung injury; Asthma; Clean diesel; Diesel exhaust particles (DEP); Polycyclic aromatic hydrocarbons (PAHs); TRPA1; TRPV1

Indexed keywords

2 NITROPYRENE; 3 NITROFLUORANTHENE; 4 NITROPYRENE; 9 NITROANTHRACENE; ANTHRACENE; ANTHRACENE DERIVATIVE; CHRYSENE; FLUORANTHENE; NITROGEN OXIDE; NITROPYRENE; PHENANTHRENE; POLYCYCLIC HYDROCARBON; PYRENE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; CALCIUM; EXHAUST GAS; PARTICULATE MATTER; REACTIVE OXYGEN METABOLITE;

AIR POLLUTION; ARTICLE; ECOTOXICITY; EXHAUST GAS; HUMAN; LUNG DISEASE; LUNG TOXICITY; PARTICULATE MATTER; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; TRAFFIC; URBAN AREA; ANIMAL; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; GENETICS; LUNG DISEASES; METABOLISM; POLLUTION; TOXICITY;

AIR POLLUTION; ANIMALS; CALCIUM; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTION; GENE EXPRESSION; HUMANS; LUNG DISEASES; PARTICULATE MATTER; REACTIVE OXYGEN SPECIES; TRANSIENT RECEPTOR POTENTIAL CHANNELS; VEHICLE EMISSIONS;

EID: 84964786368     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-016-0554-4     Document Type: Article

References (80)

1. Mar TF, Koenig JQ, Primomo J (2010) Associations between asthma emergency visits and particulate matter sources, including diesel emissions from stationary generators in Tacoma, Washington. Inhal Toxicol 22:445–448
2. Ostro B, Roth L, Malig B, Marty M (2009) The effects of fine particle components on respiratory hospital admissions in children. Environ Health Perspect 117:475–480
3. Patel MM, Chillrud SN, Correa JC, Hazi Y, Feinberg M, Deepti KC, Prakash S, Ross JM, Levy D, Kinney PL (2010) Traffic-related particulate matter and acute respiratory symptoms among New York City area adolescents. Environ Health Perspect 118:1338–1343
4. Ghio AJ, Kim C, Devlin RB (2000) Concentrated ambient air particles induce mild pulmonary inflammation in healthy human volunteers. Am J Respir Crit Care Med 162:981–988
5. Devouassoux G, Saxon A, Metcalfe DD, Prussin C, Colomb MG, Brambilla C, Diaz-Sanchez D (2002) Chemical constituents of diesel exhaust particles induce IL-4 production and histamine release by human basophils. J Allergy Clin Immunol 109:847–853
6. Diaz-Sanchez D (1997) The role of diesel exhaust particles and their associated polyaromatic hydrocarbons in the induction of allergic airway disease. Allergy 52:52–56
7. Dunmore RE, Hopkins JR, Lidster RT, Lee JD, Evans MJ, Rickard AR, Lewis AC, Hamilton JF (2015) Diesel-related hydrocarbons can dominate gas phase reactive carbon in megacities. Atmos Chem Phys 15:9983–9996
8. Nel AE, Diaz-Sanchez D, Li N (2001) The role of particulate pollutants in pulmonary inflammation and asthma: evidence for the involvement of organic chemicals and oxidative stress. Curr Opin Pulm Med 7:20–26
9. Takano H, Ichinose T, Miyabara Y, Shibuya T, Lim HB, Yoshikawa T, Sagai M (1998) Inhalation of diesel exhaust enhances allergen-related eosinophil recruitment and airway hyperresponsiveness in mice. Toxicol Appl Pharmacol 150:328–337
10. Stevens T, Cho SH, Linak WP, Gilmour MI (2009) Differential potentiation of allergic lung disease in mice exposed to chemically distinct diesel samples. Toxicol Sci 107:522–534
11. Behndig AF, Larsson N, Brown JL, Stenfors N, Helleday R, Duggan ST, Dove RE, Wilson SJ, Sandstrom T, Kelly FJ, Mudway IS, Blomberg A (2011) Proinflammatory doses of diesel exhaust in healthy subjects fail to elicit equivalent or augmented airway inflammation in subjects with asthma. Thorax 66:12–19
12. Ghio AJ, Smith CB, Madden MC (2012) Diesel exhaust particles and airway inflammation. Curr Opin Pulm Med 18:144–150
13. Nightingale JA, Maggs R, Cullinan P, Donnelly LE, Rogers DF, Kinnersley R, Chung KF, Barnes PJ, Ashmore M, Newman-Taylor A (2000) Airway inflammation after controlled exposure to diesel exhaust particulates. Am J Respir Crit Care Med 162:161–166
14. Bayram H, Devalia JL, Khair OA, Abdelaziz MM, Sapsford RJ, Sagai M, Davies RJ (1998) Comparison of ciliary activity and inflammatory mediator release from bronchial epithelial cells of nonatopic nonasthmatic subjects and atopic asthmatic patients and the effect of diesel exhaust particles in vitro. J Allergy Clin Immunol 102:771–782
15. Diaz-Sanchez D, Jyrala M, Ng D, Nel A, Saxon A (2000) In vivo nasal challenge with diesel exhaust particles enhances expression of the CC chemokines rantes, MIP-1alpha, and MCP-3 in humans. Clin Immunol 97:140–145
16. Diaz-Sanchez D, Proietti L, Polosa R (2003) Diesel fumes and the rising prevalence of atopy: an urban legend? Curr Allergy Asthma Rep 3:146–152
17. Diaz-Sanchez D, Tsien A, Casillas A, Dotson AR, Saxon A (1996) Enhanced nasal cytokine production in human beings after in vivo challenge with diesel exhaust particles. J Allergy Clin Immunol 98:114–123
18. Kobayashi T (2000) Exposure to diesel exhaust aggravates nasal allergic reaction in guinea pigs. Am J Respir Crit Care Med 162:352–356
19. Pourazar J, Frew AJ, Blomberg A, Helleday R, Kelly FJ, Wilson S, Sandstrom T (2004) Diesel exhaust exposure enhances the expression of IL-13 in the bronchial epithelium of healthy subjects. Respir Med 98:821–825
20. Agopyan N, Head J, Yu S, Simon SA (2004) TRPV1 receptors mediate particulate matter-induced apoptosis. Am J Physiol Lung Cell Mol Physiol 286:L563–L572
21. Agopyan N, Bhatti T, Yu S, Simon SA (2003) Vanilloid receptor activation by 2- and 10-microm particles induces responses leading to apoptosis in human airway epithelial cells. Toxicol Appl Pharmacol 192:21–35
22. Veronesi B, Oortgiesen M, Roy J, Carter JD, Simon SA, Gavett SH (2000) Vanilloid (capsaicin) receptors influence inflammatory sensitivity in response to particulate matter. Toxicol Appl Pharmacol 169:66–76
23. Deering-Rice CE, Romero EG, Shapiro D, Hughen RW, Light AR, Yost GS, Veranth JM, Reilly CA (2011) Electrophilic components of diesel exhaust particles (DEP) activate transient receptor potential ankyrin-1 (TRPA1): a probable mechanism of acute pulmonary toxicity for DEP. Chem Res Toxicol 24:950–959
24. Ibarra Y, Blair NT (2012) Benzoquinone reveals a cysteine-dependent desensitization mechanism of TRPA1. Mol Pharmacol 83:1120–1132
25. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, Mori Y (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2:596–607
26. Hadley SH, Bahia PK, Taylor-Clark TE (2014) Sensory nerve terminal mitochondrial dysfunction induces hyperexcitability in airway nociceptors via protein kinase C. Mol Pharmacol 85:839–848
27. Tominaga M (2007) The role of TRP channels in thermosensation. In: Liedtke WB, Heller S (eds) TRP Ion Channel Function in Sensory Transduction and Cellular Signaling Cascades. CRC Press/Taylor & Francis, Boca Raton, Florida; Chapter 20, Frontiers in Neuroscience
28. Gregus AM, Doolen S, Dumlao DS, Buczynski MW, Takasusuki T, Fitzsimmons BL, Hua XY, Taylor BK, Dennis EA, Yaksh TL (2012) Spinal 12-lipoxygenase-derived hepoxilin A3 contributes to inflammatory hyperalgesia via activation of TRPV1 and TRPA1 receptors. Proc Natl Acad Sci U S A 109:6721–6726
29. Patwardhan AM, Scotland PE, Akopian AN, Hargreaves KM (2009) Activation of TRPV1 in the spinal cord by oxidized linoleic acid metabolites contributes to inflammatory hyperalgesia. Proc Natl Acad Sci U S A 106:18820–18824
30. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452–457
31. Patwardhan AM, Jeske NA, Price TJ, Gamper N, Akopian AN, Hargreaves KM (2006) The cannabinoid WIN 55,212-2 inhibits transient receptor potential vanilloid 1 (TRPV1) and evokes peripheral antihyperalgesia via calcineurin. Proc Natl Acad Sci U S A 103:11393–11398
32. Patwardhan AM, Akopian AN, Ruparel NB, Diogenes A, Weintraub ST, Uhlson C, Murphy RC, Hargreaves KM (2010) Heat generates oxidized linoleic acid metabolites that activate TRPV1 and produce pain in rodents. J Clin Invest 120:1617–1626
33. Ruparel S, Green D, Chen P, Hargreaves KM (2012) The cytochrome P450 inhibitor, ketoconazole, inhibits oxidized linoleic acid metabolite-mediated peripheral inflammatory pain. Mol Pain 8:73
34. Gallo EM, Cante-Barrett K, Crabtree GR (2006) Lymphocyte calcium signaling from membrane to nucleus. Nat Immunol 7:25–32
35. Hogan PG, Chen L, Nardone J, Rao A (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 17:2205–2232
36. Uchida S, Yamamoto H, Iio S, Matsumoto N, Wang XB, Yonehara N, Imai Y, Inoki R, Yoshida H (1990) Release of calcitonin gene-related peptide-like immunoreactive substance from neuromuscular junction by nerve excitation and its action on striated muscle. J Neurochem 54:1000–1003
37. Belai A, Burnstock G (1988) Release of calcitonin gene-related peptide from rat enteric nerves is Ca2+−dependent but is not induced by K+ depolarization. Regul Pept 23:227–235
38. 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 106:9099–9104
39. Rehman R, Bhat YA, Panda L, Mabalirajan U (2013) TRPV1 inhibition attenuates IL-13 mediated asthma features in mice by reducing airway epithelial injury. Int Immunopharmacol 15:597–605
40. Trankner D, Hahne N, Sugino K, Hoon MA, Zuker C (2014) Population of sensory neurons essential for asthmatic hyperreactivity of inflamed airways. Proc Natl Acad Sci U S A 111:11515–11520
41. Maricq MM (2007) Chemical characterization of particulate emissions from diesel engines: a review. J Aero Sci 38:1079–1118
42. Hammerle R, Schuetzle D, Adams W (1994) A perspective on the potential development of environmentally acceptable light-duty diesel vehicles. Environ Health Perspect 102:25–30
43. Hussain S, Laumbach R, Coleman J, Youssef H, Kelly-McNeil K, Ohman-Strickland P, Zhang J, Kipen H (2012) Controlled exposure to diesel exhaust causes increased nitrite in exhaled breath condensate among subjects with asthma. J Occup Environ Med 54:1186–1191
44. Karthikeyan S, Thomson EM, Kumarathasan P, Guenette J, Rosenblatt D, Chan T, Rideout G, Vincent R (2013) Nitrogen dioxide and ultrafine particles dominate the biological effects of inhaled diesel exhaust treated by a catalyzed diesel particulate filter. Toxicol Sci 135:437–450
45. Shvedova AA, Yanamala N, Murray AR, Kisin ER, Khaliullin T, Hatfield MK, Tkach AV, Krantz QT, Nash D, King C, Ian Gilmour M, Gavett SH (2013) Oxidative stress, inflammatory biomarkers, and toxicity in mouse lung and liver after inhalation exposure to 100% biodiesel or petroleum diesel emissions. J Toxicol Environ Health A 76:907–921
46. Tsukue N, Kato A, Ito T, Sugiyama G, Nakajima T (2010) Acute effects of diesel emission from the urea selective catalytic reduction engine system on male rats. Inhal Toxicol 22:309–320
47. Deering-Rice CE, Johansen ME, Roberts JK, Thomas KC, Romero EG, Lee J, Yost GS, Veranth JM, Reilly CA (2012) Transient receptor potential vanilloid-1 (TRPV1) is a mediator of lung toxicity for coal fly ash particulate material. Mol Pharmacol 81:411–419
48. Sekimoto K, Inomata S, Tanimoto H, Fushimi A, Fujitani Y, Sato K, Yamada H (2013) Characterization of nitromethane emission from automotive exhaust. Atmos Environ 81:523–531
49. Inomata S, Tanimoto H, Fujitani Y, Sekimoto K, Sato K, Fushimi A, Yamada H, Hori S, Kumazawa Y, Shimono A, Hikida T (2013) On-line measurements of gaseous nitro-organic compounds in diesel vehicle exhaust by proton-transfer-reaction mass spectrometry. Atmos Environ 73:195–203
50. Inomata S, Fushimi A, Sato K, Fujitani Y, Yamada H (2015) 4-Nitrophenol, 1-nitropyrene, and 9-nitroanthracene emissions in exhaust particles from diesel vehicles with different exhaust gas treatments. Atmos Environ 110:93–102
51. Reilly CA, Johansen ME, Lanza DL, Lee J, Lim JO, Yost GS (2005) Calcium-dependent and independent mechanisms of capsaicin receptor (TRPV1)-mediated cytokine production and cell death in human bronchial epithelial cells. J Biochem Mol Toxicol 19:266–275
52. Kunert-Keil C, Bisping F, Kruger J, Brinkmeier H (2006) Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics 7:159
53. Jang Y, Lee Y, Kim SM, Yang YD, Jung J, Oh U (2012) Quantitative analysis of TRP channel genes in mouse organs. Arch Pharm Res 35:1823–1830
54. Daller JR, Wong J, Brooks BD, McKee JS (2012) An inexpensive system for evaluating the tussive and anti-tussive properties of chemicals in conscious, unrestrained guinea pigs. J Pharmacol Toxicol Methods 66:232–237
55. 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 133:704–12.e4
56. 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:e42454
57. Barnes PJ (1986) Asthma as an axon reflex. Lancet 1:242–245
58. Lundberg JM, Alving K, Karlsson JA, Matran R, Nilsson G (1991) Sensory neuropeptide involvement in animal models of airway irritation and of allergen-evoked asthma. Am Rev Respir Dis 143:1429–1430
59. Adriaensen D, Timmermans JP, Brouns I, Berthoud HR, Neuhuber WL, Scheuermann DW (1998) Pulmonary intraepithelial vagal nodose afferent nerve terminals are confined to neuroepithelial bodies: an anterograde tracing and confocal microscopy study in adult rats. Cell Tissue Res 293:395–405
60. Baluk P, Nadel JA, McDonald DM (1992) Substance P-immunoreactive sensory axons in the rat respiratory tract: a quantitative study of their distribution and role in neurogenic inflammation. J Comp Neurol 319:586–598
61. Dinh QT, Mingomataj E, Quarcoo D, Groneberg DA, Witt C, Klapp BF, Braun A, Fischer A (2005) Allergic airway inflammation induces tachykinin peptides expression in vagal sensory neurons innervating mouse airways. Clin Exp Allergy 35:820–825
62. Mauser PJ, Skeans S, Ritacco G, Fernandez X, House A, Chapman RW (2001) Effect of tachykinins on airway function in cynomolgus monkeys. Pulm Pharmacol Ther 14:121–127
63. Maghni K, Taha R, Afif W, Hamid Q, Martin JG (2000) Dichotomy between neurokinin receptor actions in modulating allergic airway responses in an animal model of helper T cell type 2 cytokine-associated inflammation. Am J Respir Crit Care Med 162:1068–1074
64. Joos GF, Germonpre PR, Pauwels RA (2000) Role of tachykinins in asthma. Allergy 55:321–337
65. 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 165:1137–1144
66. Spina D, Matera GM, Riccio MM, Page CP (1998) A comparison of sensory nerve function in human, guinea-pig, rabbit and marmoset airways. Life Sci 63:1629–1642
67. Van Schoor J, Joos GF, Chasson BL, Brouard RJ, Pauwels RA (1998) The effect of the NK2 tachykinin receptor antagonist SR 48968 (saredutant) on neurokinin A-induced bronchoconstriction in asthmatics. Eur Respir J 12:17–23
68. Andre 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 (2008) Cigarette smoke-induced neurogenic inflammation is mediated by alpha, beta-unsaturated aldehydes and the TRPA1 receptor in rodents. J Clin Invest 118:2574–2582
69. Weng WH, Hsu CC, Chiang LL, Lin YJ, Lin YS, Su CL (2013) Role of TRPV1 and P2X receptors in the activation of lung vagal C-fiber afferents by inhaled cigarette smoke in rats. Mol Med Rep 7:1300–1304
70. Lieu TM, Myers AC, Meeker S, Undem BJ (2012) TRPV1 induction in airway vagal low-threshold mechanosensory neurons by allergen challenge and neurotrophic factors. Am J Physiol Lung Cell Mol Physiol 302:L941-8
71. 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 586:5771–5786
72. Tang G, Wu L, Wang R (2010) Interaction of hydrogen sulfide with ion channels. Clin Exp Pharmacol Physiol 37:753–763
73. Helyes Z, Elekes K, Nemeth J, Pozsgai G, Sandor K, Kereskai L, Borzsei R, Pinter E, Szabo A, Szolcsanyi J (2007) Role of transient receptor potential vanilloid 1 receptors in endotoxin-induced airway inflammation in the mouse. Am J Physiol Lung Cell Mol Physiol 292:L1173-81
74. Raemdonck K, de Alba J, Birrell MA, Grace M, Maher SA, Irvin CG, Fozard JR, O’Byrne PM, Belvisi MG (2012) A role for sensory nerves in the late asthmatic response. Thorax 67:19–25
75. 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 166:1822–1832
76. Akopian AN (2011) Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Curr Pharm Biotechnol 12:89–94
77. 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 583:175–193
78. Lee LY, Hsu CC, Lin YJ, Lin RL, Khosravi M (2015) Interaction between TRPA1 and TRPV1: synergy on pulmonary sensory nerves. Pulm Pharmacol Ther 35:87–93
79. Weng HJ, Patel KN, Jeske NA, Bierbower SM, Zou W, Tiwari V, Zheng Q, Tang Z, Mo GC, Wang Y, Geng Y, Zhang J, Guan Y, Akopian AN, Dong X (2015) Tmem100 is a regulator of TRPA1-TRPV1 complex and contributes to persistent pain. Neuron 85:833–846
80. Salas MM, Hargreaves KM, Akopian AN (2009) TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1. Eur J Neurosci 29:1568–1578