Wood smoke enhances cigarette smoke-induced inflammation by inducing the aryl hydrocarbon receptor repressor in airway epithelial cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 52, Issue 3, 2015, Pages 377-386

  Awji, Elias G ^a   Chand, Hitendra ^a   Bruse, Shannon ^a   Smith, Kevin R ^a   Colby, Jennifer K ^b   Mebratu, Yohannes ^a   Levy, Bruce D ^b   Tesfaigzi, Yohannes ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Air pollution; Arachidonic acid pathway; Exacerbation; Lipoxin; Neutrophilic inflammation

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CHEMOATTRACTANT; CIGARETTE SMOKE; CYCLOOXYGENASE 2 INHIBITOR; LIPOXIN A; PROSTAGLANDIN E SYNTHASE; PROSTAGLANDIN SYNTHASE; CHEMOKINE; CYCLOOXYGENASE 2; ISOMERASE; KERATINOCYTE DERIVED CHEMOKINE; LIPOXIN; PROSTAGLANDIN E2; SMOKE;

ANIMAL CELL; ARTICLE; CHRONIC BRONCHITIS; CONTROLLED STUDY; EPITHELIUM CELL; IMMUNOPRECIPITATION; LUNG LAVAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKE; ADVERSE EFFECTS; ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; CELL LINE; HUMAN; INFLAMMATION; LUNG; METABOLISM; SMOKING; WOOD;

MUS;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELL LINE; CHEMOKINES; CYCLOOXYGENASE 2; DINOPROSTONE; EPITHELIAL CELLS; HUMANS; INFLAMMATION; INTRAMOLECULAR OXIDOREDUCTASES; LIPOXINS; LUNG; MALE; MICE; MICE, INBRED C57BL; NEUTROPHILS; RECEPTORS, ARYL HYDROCARBON; SMOKE; SMOKING; WOOD;

EID: 84924096429     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0142OC     Document Type: Article

References (56)

1. Diette GB, Accinelli RA, Balmes J.R., Buist AS, Checkley W, Garbe P, Hansel N.N., Kapil V., Gordon S, Lagat DK, et al. Obstructive lung disease and exposure to burning biomass fuel in the indoor environment. Glob Heart 2012; 7:265-270.
2. Larson TV, Koenig JQ. Wood smoke: emissions and noncancer respiratory effects. Annu Rev Public Health 1994; 15:133-156.
3. Orozco-Levi M, Garcia-Aymerich J, Villar J., Ramírez-Sarmiento A, Antó JM, Gea J. Wood smoke exposure and risk of chronic obstructive pulmonary disease. Eur Respir J 2006; 27:542-546.
4. Gan WQ, FitzGerald JM, Carlsten C, Sadatsafavi M., Brauer M. Associations of ambient air pollution with chronic obstructive pulmonary disease hospitalization and mortality. Am J Respir Crit Care Med 2013; 187:721-727.
5. Sood A, Petersen H, Blanchette C.M., Meek P., Picchi MA, Belinsky SA, Tesfaigzi Y. Wood smoke exposure and gene promoter methylation are associated with increased risk for COPD in smokers. Am J Respir Crit Care Med 2010; 182:1098-1104.
6. Pérez-Padilla R, Regalado J, Vedal S, Paré P, Chapela R, Sansores R, Selman M. Exposure to biomass smoke and chronic airway disease in Mexican women: a case-control study. Am J Respir Crit Care Med 1996; 154:701-706.
7. Profita M, Sala A, Bonanno A., Riccobono L, Ferraro M, La Grutta S, Albano GD, Montalbano AM, Gjomarkaj M. Chronic obstructive pulmonary disease and neutrophil infiltration: role of cigarette smoke and cyclooxygenase products. Am J Physiol Lung Cell Mol Physiol 2010; 298:L261-L269.
8. Baglole CJ, Maggirwar SB, Gasiewicz T.A., Thatcher TH, Phipps RP, Sime PJ. The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the NF-kappaB family member RelB. J Biol Chem 2008; 283:28944-28957.
9. Roh GS, Yi CO, Cho Y.J., Jeon BT, Nizamudtinova IT, Kim HJ, Kim J.H., Oh YM, Huh JW, Lee JH, et al. Anti-inflammatory effects of celecoxib in rat lungs with smoke-induced emphysema. Am J Physiol Lung Cell Mol Physiol 2010; 299:L184-L191.
10. Bonnans C, Fukunaga K, Levy M.A., Levy BD. Lipoxin A(4) regulates bronchial epithelial cell responses to acid injury. Am J Pathol 2006; 168:1064-1072.
11. Gilroy DW, Lawrence T, Perretti M., Rossi AG. Inflammatory resolution: new opportunities for drug discovery. Nat Rev Drug Discov 2004; 3: 401-416.
12. Gilroy DW, Colville-Nash PR, Willis D., Chivers J, Paul-Clark MJ, Willoughby DA. Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 1999; 5:698-701.
13. Levy BD, Clish CB, Schmidt B, Gronert K., Serhan CN. Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2001; 2:612-619.
14. Fukunaga K, Kohli P, Bonnans C., Fredenburgh LE, Levy BD. Cyclooxygenase 2 plays a pivotal role in the resolution of acute lung injury. J Immunol 2005; 174:5033-5039.
15. Blaho VA, Mitchell WJ, Brown CR. Arthritis develops but fails to resolve during inhibition of cyclooxygenase 2 in a murine model of Lyme disease. Arthritis Rheum 2008; 58:1485-1495.
16. Chan MM, Moore AR. Resolution of inflammation in murine autoimmune arthritis is disrupted by cyclooxygenase-2 inhibition and restored by prostaglandin E2-mediated lipoxin A4 production. J Immunol 2010; 184:6418-6426.
17. Reuter BK, Asfaha S, Buret A., Sharkey KA, Wallace JL. Exacerbation of inflammation-associated colonic injury in rat through inhibition of cyclooxygenase-2. J Clin Invest 1996; 98:2076-2085.
18. Wallace JL. Selective COX-2 inhibitors: is the water becoming muddy? Trends Pharmacol Sci 1999; 20:4-6.
19. Martey CA, Pollock SJ, Turner C.K., O'Reilly KM, Baglole CJ, Phipps R.P., Sime PJ. Cigarette smoke induces cyclooxygenase-2 and microsomal prostaglandin E2 synthase in human lung fibroblasts: implications for lung inflammation and cancer. Am J Physiol Lung Cell Mol Physiol 2004; 287:L981-L991.
20. Yoshida T, Tuder RM. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol Rev 2007; 87:1047-1082.
21. Kang MJ, Lee CG, Lee J.Y., Dela Cruz CS, Chen ZJ, Enelow R, Elias JA. Cigarette smoke selectively enhances viral PAMP- and virus-induced pulmonary innate immune and remodeling responses in mice. J Clin Invest 2008; 118:2771-2784.
22. Fulcher ML, Gabriel S, Burns K.A., Yankaskas JR, Randell SH. Well-differentiated human airway epithelial cell cultures. Methods Mol Med 2005; 107:183-206.
23. Mebratu YA, Dickey BF, Evans C, Tesfaigzi Y. The BH3-only protein Bik/Blk/Nbk inhibits nuclear translocation of activated ERK1/2 to mediate IFNgamma-induced cell death. J Cell Biol 2008; 183: 429-439.
24. Contreras AU, Mebratu Y, Delgado M., Montano G, Hu CA, Ryter S.W., Choi AM, Lin Y, Xiang J, Chand H, et al. Deacetylation of p53 induces autophagy by suppressing Bmf expression. J Cell Biol 2013; 201: 427-437.
25. Serhan CN, Savill J. Resolution of inflammation: the beginning programs the end. Nat Immunol 2005; 6:1191-1197.
26. Lees MJ, Peet DJ, Whitelaw ML. Defining the role for XAP2 in stabilization of the dioxin receptor. J Biol Chem 2003; 278: 35878-35888.
27. Song J, Clagett-Dame M, Peterson R.E., Hahn ME, Westler WM, Sicinski RR, DeLuca HF. A ligand for the aryl hydrocarbon receptor isolated from lung. Proc Natl Acad Sci USA 2002; 99:14694-14699.
28. Pollenz RS, Barbour ER. Analysis of the complex relationship between nuclear export and aryl hydrocarbon receptor-mediated gene regulation. Mol Cell Biol 2000; 20:6095-6104.
29. Denison MS, Soshilov AA, He G, DeGroot D.E., Zhao B. Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol Sci 2011; 124:1-22.
30. Hahn ME, Allan LL, Sherr DH. Regulation of constitutive and inducible AHR signaling: complex interactions involving the AHR repressor. Biochem Pharmacol 2009; 77:485-497.
31. McMahon B, Godson C. Lipoxins: endogenous regulators of inflammation. Am J Physiol Renal Physiol 2004; 286:F189-F201.
32. He R, Sang H, Ye RD. Serum amyloid A induces IL-8 secretion through a G protein-coupled receptor, FPRL1/LXA4R. Blood 2003; 101: 1572-1581.
33. 4 to mediate glucocorticoid refractory lung inflammation in chronic obstructive pulmonary disease. Proc Natl Acad Sci USA 2012; 109:935-940.
34. Hodges RJ, Jenkins RG, Wheeler-Jones CP, Copeman D.M., Bottoms SE, Bellingan GJ, Nanthakumar CB, Laurent G.J., Hart SL, Foster ML, et al. Severity of lung injury in cyclooxygenase-2-deficient mice is dependent on reduced prostaglandin E(2) production. Am J Pathol 2004; 165:1663-1676.
35. Danielsen PH, Loft S, Jacobsen N.R., Jensen KA, Autrup H, Ravanat JL, Wallin H, Møller P. Oxidative stress, inflammation, and DNA damage in rats after intratracheal instillation or oral exposure to ambient air and wood smoke particulate matter. Toxicol Sci 2010; 118:574-585.
36. Tesfaigzi Y, Singh SP, Foster J.E., Kubatko J., Barr EB, Fine PM, McDonald JD, Hahn F.F., Mauderly JL. Health effects of subchronic exposure to low levels of wood smoke in rats. Toxicol Sci 2002; 65: 115-125.
37. Tesfaigzi Y, McDonald JD, Reed M.D., Singh SP, De Sanctis GT, Eynott PR, Hahn FF, Campen MJ, Mauderly JL. Low-level subchronic exposure to wood smoke exacerbates inflammatory responses in allergic rats. Toxicol Sci 2005; 88:505-513.
38. Riddervold IS, Bønløkke JH, Olin AC, Grønborg TK, Schlünssen V, Skogstrand K, Hougaard D, Massling A, Sigsgaard T. Effects of wood smoke particles from wood-burning stoves on the respiratory health of atopic humans. Part Fibre Toxicol 2012; 9:12.
39. Warheit DB, Sayes CM, Frame S.R., Reed KL. Pulmonary exposures to Sepiolite nanoclay particulates in rats: resolution following multinucleate giant cell formation. Toxicol Lett 2010; 192:286-293.
40. McNally AK, Anderson JM. Macrophage fusion and multinucleated giant cells of inflammation. Adv Exp Med Biol 2011; 713:97-111.
41. Tesfaigzi Y, Fischer MJ, Daheshia M, Green F.H., De Sanctis GT, Wilder JA. Bax is crucial for IFN-γ-induced resolution of allergen-induced mucus cell metaplasia. J Immunol 2002; 169:5919-5925.
42. Baba T, Mimura J, Gradin K., Kuroiwa A, Watanabe T, Matsuda Y., Inazawa J, Sogawa K, Fujii-Kuriyama Y. Structure and expression of the Ah receptor repressor gene. J Biol Chem 2001; 276: 33101-33110.
43. Lachocki TM, Church DF, Pryor WA. Persistent free radicals in woodsmoke: an ESR spin trapping study. Free Radic Biol Med 1989; 7:17-21.
44. Danielsen PH, Loft S, Kocbach A., Schwarze PE, Møller P. Oxidative damage to DNA and repair induced by Norwegian wood smoke particles in human A549 and THP-1 cell lines. Mutat Res 2009; 674: 116-122.
45. Kuhn C III, Homer R.J., Zhu Z., Ward N, Flavell RA, Geba G.P., Elias JA. Airway hyperresponsiveness and airway obstruction in transgenic mice: morphologic correlates in mice overexpressing interleukin (IL)-11 and IL-6 in the lung. Am J Respir Cell Mol Biol 2000; 22:289-295.
46. Mercer BA, Lemaitre V, Powell C.A., D'Armiento J. The epithelial cell in lung health and emphysema pathogenesis. Curr Respir Med Rev 2006; 2:101-142.
47. Sturm EM, Schratl P, Schuligoi R., Konya V, Sturm GJ, Lippe I.T., Peskar BA, Heinemann A. Prostaglandin E2 inhibits eosinophil trafficking through E-prostanoid 2 receptors. J Immunol 2008; 181:7273-7283.
48. Gauvreau GM, Watson RM, O'Byrne PM. Protective effects of inhaled PGE2 on allergen-induced airway responses and airway inflammation. Am J Respir Crit Care Med 1999; 159:31-36.
49. Pavord ID, Wong CS, Williams J, Tattersfield AE. Effect of inhaled prostaglandin E2 on allergen-induced asthma. Am Rev Respir Dis 1993; 148:87-90.
50. Davies NM, Sharkey KA, Asfaha S, Macnaughton W.K., Wallace JL. Aspirin causes rapid up-regulation of cyclo-oxygenase-2 expression in the stomach of rats. Aliment Pharmacol Ther 1997; 11:1101-1108.
51. Elizondo G, Rodríguez-Sosa M, Estrada-Muñiz E, Gonzalez FJ, Vega L. Deletion of the aryl hydrocarbon receptor enhances the inflammatory response to Leishmania major infection. Int J Biol Sci 2011; 7: 1220-1229.
52. Degner SC, Papoutsis AJ, Selmin O, Romagnolo DF. Targeting of aryl hydrocarbon receptor-mediated activation of cyclooxygenase-2 expression by the indole-3-carbinol metabolite 3, 39-diindolylmethane in breast cancer cells. J Nutr 2009; 139:26-32.
53. Clària J, Lee MH, Serhan CN. Aspirin-triggered lipoxins (15-epi-LX) are generated by the human lung adenocarcinoma cell line (A549)-neutrophil interactions and are potent inhibitors of cell proliferation. Mol Med 1996; 2:583-596.
54. Levy BD, Bonnans C, Silverman E.S., Palmer LJ, Marigowda G, Israel E; Severe Asthma Research Program, National Heart, Lung, and Blood Institute. Diminished lipoxin biosynthesis in severe asthma. Am J Respir Crit Care Med 2005; 172:824-830.
55. Karp CL, Flick LM, Park K.W., Softic S., Greer TM, Keledjian R, Yang R, Uddin J., Guggino WB, Atabani SF, et al. Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway. Nat Immunol 2004; 5:388-392.
56. Starosta V, Ratjen F, Rietschel E., Paul K, Griese M. Anti-inflammatory cytokines in cystic fibrosis lung disease. Eur Respir J 2006; 28: 581-587.