Role of oxidative stress on diesel-enhanced influenza infection in mice
Tóm tắt
Numerous studies have shown that air pollutants, including diesel exhaust (DE), reduce host defenses, resulting in decreased resistance to respiratory infections. This study sought to determine if DE exposure could affect the severity of an ongoing influenza infection in mice, and examine if this could be modulated with antioxidants. BALB/c mice were treated by oropharyngeal aspiration with 50 plaque forming units of influenza A/HongKong/8/68 and immediately exposed to air or 0.5 mg/m3 DE (4 hrs/day, 14 days). Mice were necropsied on days 1, 4, 8 and 14 post-infection and lungs were assessed for virus titers, lung inflammation, immune cytokine expression and pulmonary responsiveness (PR) to inhaled methacholine. Exposure to DE during the course of infection caused an increase in viral titers at days 4 and 8 post-infection, which was associated with increased neutrophils and protein in the BAL, and an early increase in PR. Increased virus load was not caused by decreased interferon levels, since IFN-β levels were enhanced in these mice. Expression and production of IL-4 was significantly increased on day 1 and 4 p.i. while expression of the Th1 cytokines, IFN-γ and IL-12p40 was decreased. Treatment with the antioxidant N-acetylcysteine did not affect diesel-enhanced virus titers but blocked the DE-induced changes in cytokine profiles and lung inflammation. We conclude that exposure to DE during an influenza infection polarizes the local immune responses to an IL-4 dominated profile in association with increased viral disease, and some aspects of this effect can be reversed with antioxidants.
Tài liệu tham khảo
Falsey AR, Walsh EE: Respiratory syncytial virus infection in adults. Clin Microbiol Rev 2000, 13: 371–384. 10.1128/CMR.13.3.371-384.2000
Klimov A, Simonsen L, Fukuda K, Cox N: Surveillance and impact of influenza in the United States. Vaccine 1999, 17(Suppl 1):S42–46. 10.1016/S0264-410X(99)00104-8
Monto AS, Rotthoff J, Teich E, Herlocher ML, Truscon R, Yen HL, Elias S, Ohmit SE: Detection and control of influenza outbreaks in well-vaccinated nursing home populations. Clin Infect Dis 2004, 39: 459–464. 10.1086/422646
Pope CA, Burnett RT, Thurston GD, Thun MJ, Calle EE, Krewski D, Godleski JJ: Cardiovascular mortality and long-term exposure to particulate air pollution: epidemiological evidence of general pathophysiological pathways of disease. Circulation 2004, 109: 71–77. 10.1161/01.CIR.0000108927.80044.7F
Pope CA, Dockery DW: Acute health effects of PM10 pollution on symptomatic and asymptomatic children. Am Rev Respir Dis 1992, 145: 1123–1128.
Ciencewicki J, Jaspers I: Air pollution and respiratory viral infection. Inhal Toxicol 2007, 19: 1135–1146. 10.1080/08958370701665434
Takizawa H, Ohtoshi T, Kawasaki S, Abe S, Sugawara I, Nakahara K, Matsushima K, Kudoh S: Diesel exhaust particles activate human bronchial epithelial cells to express inflammatory mediators in the airways: a review. Respirology 2000, 5: 197–203. 10.1046/j.1440-1843.2000.00245.x
Takizawa H, Abe S, Ohtoshi T, Kawasaki S, Takami K, Desaki M, Sugawara I, Hashimoto S, Azuma A, Nakahara K, Kudoh S: Diesel exhaust particles up-regulate expression of intercellular adhesion molecule-1 (ICAM-1) in human bronchial epithelial cells. Clin Exp Immunol 2000, 120: 356–362. 10.1046/j.1365-2249.2000.01213.x
Castranova V, Ma JY, Yang HM, Antonini JM, Butterworth L, Barger MW, Roberts J, Ma JK: Effect of exposure to diesel exhaust particles on the susceptibility of the lung to infection. Environ Health Perspect 2001, 109(Suppl 4):609–612. 10.2307/3454678
Hahon N, Booth JA, Green F, Lewis TR: Influenza virus infection in mice after exposure to coal dust and diesel engine emissions. Environ Res 1985, 37: 44–60. 10.1016/0013-9351(85)90048-9
Harrod KS, Jaramillo RJ, Rosenberger CL, Wang SZ, Berger JA, McDonald JD, Reed MD: Increased susceptibility to RSV infection by exposure to inhaled diesel engine emissions. Am J Respir Cell Mol Biol 2003, 28: 451–463. 10.1165/rcmb.2002-0100OC
Jaspers I, Ciencewicki JM, Zhang W, Brighton LE, Carson JL, Beck MA, Madden MC: Diesel exhaust enhances influenza virus infections in respiratory epithelial cells. Toxicol Sci 2005, 85: 990–1002. 10.1093/toxsci/kfi141
Ciencewicki J, Gowdy K, Krantz QT, Linak WP, Brighton L, Gilmour MI, Jaspers I: Diesel exhaust enhanced susceptibility to influenza infection is associated with decreased surfactant protein expression. Inhal Toxicol 2007, 19: 1121–1133. 10.1080/08958370701665426
Steerenberg P, Verlaan A, De Klerk A, Boere A, Loveren H, Cassee F: Sensitivity to ozone, diesel exhaust particles, and standardized ambient particulate matter in rats with a listeria monocytogenes-induced respiratory infection. Inhal Toxicol 2004, 16: 311–317. 10.1080/08958370490428436
Yang HM, Antonini JM, Barger MW, Butterworth L, Roberts BR, Ma JK, Castranova V, Ma JY: Diesel exhaust particles suppress macrophage function and slow the pulmonary clearance of Listeria monocytogenes in rats. Environ Health Perspect 2001, 109: 515–521. 10.1289/ehp.01109515
Yin XJ, Dong CC, Ma JY, Antonini JM, Roberts JR, Stanley CF, Schafer R, Ma JK: Suppression of cell-mediated immune responses to listeria infection by repeated exposure to diesel exhaust particles in brown Norway rats. Toxicol Sci 2004, 77: 263–271. 10.1093/toxsci/kfh035
Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K: Mortality associated with influenza and respiratory syncytial virus in the United States. Jama 2003, 289: 179–186. 10.1001/jama.289.2.179
Thompson WW, Shay DK, Weintraub E, Brammer L, Bridges CB, Cox NJ, Fukuda K: Influenza-associated hospitalizations in the United States. Jama 2004, 292: 1333–1340. 10.1001/jama.292.11.1333
Sarawar SR, Sangster M, Coffman RL, Doherty PC: Administration of anti-IFN-gamma antibody to beta 2-microglobulin-deficient mice delays influenza virus clearance but does not switch the response to a T helper cell 2 phenotype. J Immunol 1994, 153: 1246–1253.
Moran TM, Isobe H, Fernandez-Sesma A, Schulman JL: Interleukin-4 causes delayed virus clearance in influenza virus-infected mice. J Virol 1996, 70: 5230–5235.
Seneviratne SL, Jones L, Bailey AS, Samuel RV, Black AP, Ogg GS: Interleukin-4 induced down-regulation of skin homing receptor expression by human viral-specific CD8 T cells may contribute to atopic risk of cutaneous infection. Clin Exp Immunol 2005, 141: 107–115. 10.1111/j.1365-2249.2005.02823.x
Lopez CB, Moran TM, Schulman JL, Fernandez-Sesma A: Antiviral immunity and the role of dendritic cells. Int Rev Immunol 2002, 21: 339–353. 10.1080/08830180213280
Kato A, Kyono H, Kuwabara N: [Electron-microscopic observations on rat lungs after long term inhalation of diesel emissions--non-neoplastic lesions]. Nihon Kyobu Shikkan Gakkai Zasshi 1992, 30: 238–247.
Nightingale JA, Maggs R, Cullinan P, Donnelly LE, Rogers DF, Kinnersley R, Chung KF, Barnes PJ, Ashmore M, Newman-Taylor A: Airway inflammation after controlled exposure to diesel exhaust particulates. Am J Respir Crit Care Med 2000, 162: 161–166.
Nordenhall C, Pourazar J, Blomberg A, Levin JO, Sandstrom T, Adelroth E: Airway inflammation following exposure to diesel exhaust: a study of time kinetics using induced sputum. Eur Respir J 2000, 15: 1046–1051. 10.1034/j.1399-3003.2000.01512.x
Rudell B, Blomberg A, Helleday R, Ledin MC, Lundback B, Stjernberg N, Horstedt P, Sandstrom T: Bronchoalveolar inflammation after exposure to diesel exhaust: comparison between unfiltered and particle trap filtered exhaust. Occup Environ Med 1999, 56: 527–534. 10.1136/oem.56.8.527
Salvi S, Blomberg A, Rudell B, Kelly F, Sandstrom T, Holgate ST, Frew A: Acute inflammatory responses in the airways and peripheral blood after short-term exposure to diesel exhaust in healthy human volunteers. Am J Respir Crit Care Med 1999, 159: 702–709.
Hiura TS, Kaszubowski MP, Li N, Nel AE: Chemicals in diesel exhaust particles generate reactive oxygen radicals and induce apoptosis in macrophages. J Immunol 1999, 163: 5582–5591.
Singh P, DeMarini DM, Dick CA, Tabor DG, Ryan JV, Linak WP, Kobayashi T, Gilmour MI: Sample characterization of automobile and forklift diesel exhaust particles and comparative pulmonary toxicity in mice. Environ Health Perspect 2004, 112: 820–825. 10.1289/ehp.6579
Diaz Sanchez C, Laguna Martinez J, Iglesias Cadarso A, Vidal Pan C: Protein contact dermatitis associated with food allergy to fish. Contact Dermatitis 1994, 31: 55–57. 10.1111/j.1600-0536.1994.tb01913.x
Diaz-Sanchez D: The role of diesel exhaust particles and their associated polyaromatic hydrocarbons in the induction of allergic airway disease. Allergy 1997, 52: 52–56. discussion 57–58 10.1111/j.1398-9995.1997.tb04871.x
Diaz-Sanchez D, Penichet-Garcia M, Saxon A: Diesel exhaust particles directly induce activated mast cells to degranulate and increase histamine levels and symptom severity. J Allergy Clin Immunol 2000, 106: 1140–1146. 10.1067/mai.2000.111144
Xiao GG, Wang M, Li N, Loo JA, Nel AE: Use of proteomics to demonstrate a hierarchical oxidative stress response to diesel exhaust particle chemicals in a macrophage cell line. J Biol Chem 2003, 278: 50781–50790. 10.1074/jbc.M306423200
Li N, Kim S, Wang M, Froines J, Sioutas C, Nel A: Use of a stratified oxidative stress model to study the biological effects of ambient concentrated and diesel exhaust particulate matter. Inhal Toxicol 2002, 14: 459–486. 10.1080/089583701753678571
Kim HJ, Barajas B, Chan RC, Nel AE: Glutathione depletion inhibits dendritic cell maturation and delayed-type hypersensitivity: implications for systemic disease and immunosenescence. J Allergy Clin Immunol 2007, 119: 1225–1233. 10.1016/j.jaci.2007.01.016
Metzger JM, Peterson LB: Cyclosporin A enhances the pulmonary granuloma response induced by Schistosoma mansoni eggs. Immunopharmacology 1988, 15: 103–115. 10.1016/0162-3109(88)90057-4
LaBarre DD, Lowy RJ: Improvements in methods for calculating virus titer estimates from TCID50 and plaque assays. J Virol Methods 2001, 96: 107–126. 10.1016/S0166-0934(01)00316-0
Jaspers I, Zhang W, Fraser A, Samet JM, Reed W: Hydrogen peroxide has opposing effects on IKK activity and IkappaBalpha breakdown in airway epithelial cells. Am J Respir Cell Mol Biol 2001, 24: 769–777.
Jaspers I, Samet JM, Reed W: Arsenite exposure of cultured airway epithelial cells activates kappaB-dependent interleukin-8 gene expression in the absence of nuclear factor-kappaB nuclear translocation. J Biol Chem 1999, 274: 31025–31033. 10.1074/jbc.274.43.31025
Whitekus MJ, Li N, Zhang M, Wang M, Horwitz MA, Nelson SK, Horwitz LD, Brechun N, Diaz-Sanchez D, Nel AE: Thiol antioxidants inhibit the adjuvant effects of aerosolized diesel exhaust particles in a murine model for ovalbumin sensitization. J Immunol 2002, 168: 2560–2567.
Jones DP, Carlson JL, Samiec PS, Sternberg P Jr, Mody VC Jr, Reed RL, Brown LA: Glutathione measurement in human plasma. Evaluation of sample collection, storage and derivatization conditions for analysis of dansyl derivatives by HPLC. Clin Chim Acta 1998, 275: 175–184. 10.1016/S0009-8981(98)00089-8
Gan J, Harper TW, Hsueh MM, Qu Q, Humphreys WG: Dansyl glutathione as a trapping agent for the quantitative estimation and identification of reactive metabolites. Chem Res Toxicol 2005, 18: 896–903. 10.1021/tx0496791
Li YJ, Kawada T, Matsumoto A, Azuma A, Kudoh S, Takizawa H, Sugawara I: Airway inflammatory responses to oxidative stress induced by low-dose diesel exhaust particle exposure differ between mouse strains. Exp Lung Res 2007, 33: 227–244. 10.1080/01902140701481062
Dye JA, Morgan KT, Neldon DL, Tepper JS, Burleson GR, Costa DL: Characterization of upper respiratory disease in rats following neonatal inoculation with a rat-adapted influenza virus. Vet Pathol 1996, 33: 43–54. 10.1177/030098589603300105
Baumgarth N, Kelso A: In vivo blockade of gamma interferon affects the influenza virus-induced humoral and the local cellular immune response in lung tissue. J Virol 1996, 70: 4411–4418.
Li N, Venkatesan MI, Miguel A, Kaplan R, Gujuluva C, Alam J, Nel A: Induction of heme oxygenase-1 expression in macrophages by diesel exhaust particle chemicals and quinones via the antioxidant-responsive element. J Immunol 2000, 165: 3393–3401.
Monick MM, Samavati L, Butler NS, Mohning M, Powers LS, Yarovinsky T, Spitz DR, Hunninghake GW: Intracellular thiols contribute to Th2 function via a positive role in IL-4 production. J Immunol 2003, 171: 5107–5115.
Gilmour MI, Daniels M, McCrillis RC, Winsett D, Selgrade MK: Air pollutant-enhanced respiratory disease in experimental animals. Environ Health Perspect 2001, 109(Suppl 4):619–622. 10.2307/3454680
Green GM, Jakab GJ, Low RB, Davis GS: Defense mechanisms of the respiratory membrane. Am Rev Respir Dis 1977, 115: 479–514.
Steerenberg PA, Withagen CE, van Dalen WJ, Dormans JA, van Loveren H: Adjuvant activity of ambient particulate matter in macrophage activity-suppressed, N-acetylcysteine-treated, iNOS- and IL-4-deficient mice. Inhal Toxicol 2004, 16: 835–843. 10.1080/08958370490506600
Gowdy K, Krantz QT, Daniels M, Linak WP, Jaspers I, Gilmour MI: Modulation of pulmonary inflammatory responses and antimicrobial defenses in mice exposed to diesel exhaust. Toxicol Appl Pharmacol 2008, 229: 310–319. 10.1016/j.taap.2008.01.040
Ciencewicki J, Brighton L, Wu WD, Madden M, Jaspers I: Diesel exhaust enhances virus- and poly(I:C)-induced Toll-like receptor 3 expression and signaling in respiratory epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006, 290: L1154–1163. 10.1152/ajplung.00318.2005
LeVine AM, Hartshorn K, Elliott J, Whitsett J, Korfhagen T: Absence of SP-A modulates innate and adaptive defense responses to pulmonary influenza infection. Am J Physiol Lung Cell Mol Physiol 2002, 282: L563–572.
LeVine AM, Whitsett JA, Hartshorn KL, Crouch EC, Korfhagen TR: Surfactant protein D enhances clearance of influenza A virus from the lung in vivo. J Immunol 2001, 167: 5868–5873.
Harrod KS, Trapnell BC, Otake K, Korfhagen TR, Whitsett JA: SP-A enhances viral clearance and inhibits inflammation after pulmonary adenoviral infection. Am J Physiol 1999, 277: L580–588.
Tate MD, Deng YM, Jones JE, Anderson GP, Brooks AG, Reading PC: Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J Immunol 2009, 183: 7441–7450. 10.4049/jimmunol.0902497
Tate MD, Brooks AG, Reading PC: The role of neutrophils in the upper and lower respiratory tract during influenza virus infection of mice. Respir Res 2008, 9: 57. 10.1186/1465-9921-9-57
Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM: H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 2008, 4: e1000115. 10.1371/journal.ppat.1000115
Mbawuike IN, Acuna CL, Walz KC, Atmar RL, Greenberg SB, Couch RB: Cytokines and impaired CD8+ CTL activity among elderly persons and the enhancing effect of IL-12. Mech Ageing Dev 1997, 94: 25–39. 10.1016/S0047-6374(96)01855-6
Carding SR, Allan W, McMickle A, Doherty PC: Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J Exp Med 1993, 177: 475–482. 10.1084/jem.177.2.475
Bot A, Holz A, Christen U, Wolfe T, Temann A, Flavell R, von Herrath M: Local IL-4 expression in the lung reduces pulmonary influenza-virus-specific secondary cytotoxic T cell responses. Virology 2000, 269: 66–77. 10.1006/viro.2000.0187
Bot A, Smith KA, von Herrath M: Molecular and cellular control of T1/T2 immunity at the interface between antimicrobial defense and immune pathology. DNA Cell Biol 2004, 23: 341–350. 10.1089/104454904323145227
Monteiro JM, Harvey C, Trinchieri G: Role of interleukin-12 in primary influenza virus infection. J Virol 1998, 72: 4825–4831.
Weiss ID, Wald O, Wald H, Beider K, Abraham M, Galun E, Nagler A, Peled A: IFN-gamma Treatment at Early Stages of Influenza Virus Infection Protects Mice From Death in a NK Cell-Dependent Manner. J Interferon Cytokine Res 2010, 30: 439–449. 10.1089/jir.2009.0084
Siegle JS, Hansbro N, Herbert C, Rosenberg HF, Domachowske JB, Asquith KL, Foster PS, Kumar RK: Early-life viral infection and allergen exposure interact to induce an asthmatic phenotype in mice. Respir Res 2010, 11: 14. 10.1186/1465-9921-11-14
Bergmann KC, Lachmann B, Noack K: Lung mechanics in orally immunized mice after aerolized exposure to influenza virus. Respiration 1984, 46: 218–221. 10.1159/000194692
Chong BT, Agrawal DK, Romero FA, Townley RG: Measurement of bronchoconstriction using whole-body plethysmograph: comparison of freely moving versus restrained guinea pigs. J Pharmacol Toxicol Methods 1998, 39: 163–168. 10.1016/S1056-8719(98)00021-5
Piedimonte G, Hegele RG, Auais A: Persistent airway inflammation after resolution of respiratory syncytial virus infection in rats. Pediatr Res 2004, 55: 657–665. 10.1203/01.PDR.0000112244.72924.26
Chan RC, Wang M, Li N, Yanagawa Y, Onoe K, Lee JJ, Nel AE: Pro-oxidative diesel exhaust particle chemicals inhibit LPS-induced dendritic cell responses involved in T-helper differentiation. J Allergy Clin Immunol 2006, 118: 455–465. 10.1016/j.jaci.2006.06.006
Peterson JD, Herzenberg LA, Vasquez K, Waltenbaugh C: Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc Natl Acad Sci USA 1998, 95: 3071–3076. 10.1073/pnas.95.6.3071
Bengtsson A, Lundberg M, Avila-Carino J, Jacobsson G, Holmgren A, Scheynius A: Thiols decrease cytokine levels and down-regulate the expression of CD30 on human allergen-specific T helper (Th) 0 and Th2 cells. Clin Exp Immunol 2001, 123: 350–360. 10.1046/j.1365-2249.2001.01453.x
Devouassoux G, Saxon A, Metcalfe DD, Prussin C, Colomb MG, Brambilla C, Diaz-Sanchez D: Chemical constituents of diesel exhaust particles induce IL-4 production and histamine release by human basophils. J Allergy Clin Immunol 2002, 109: 847–853. 10.1067/mai.2002.122843
Jaspers I, Sheridan PA, Zhang W, Brighton LE, Chason KD, Hua X, Tilley SL: Exacerbation of allergic inflammation in mice exposed to diesel exhaust particles prior to viral infection. Part Fibre Toxicol 2009, 6: 22. 10.1186/1743-8977-6-22