The Korean journal of internal medicine

  • 제32권5호
  • /
  • Pages.865-874
  • /
  • 2017
  • /
  • 1226-3303(pISSN)
  • /
  • 2005-6648(eISSN)
대한내과학회 (The Korean Association of Internal Medicine)
권호 표지
DOI QR코드

DOI QR Code

The activation of NLRP3-inflammsome by stimulation of diesel exhaust particles in lung tissues from emphysema model and RAW 264.7 cell line

  • Uh, Soo-Taek (Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Seoul Hospital) ;
  • Koo, So My (Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Seoul Hospital) ;
  • Kim, Yangki (Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Seoul Hospital) ;
  • Kim, Kiup (Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Seoul Hospital) ;
  • Park, Sungwoo (Genome Research Center and Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Bucheon Hospital) ;
  • Jang, An Soo (Genome Research Center and Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Bucheon Hospital) ;
  • Kim, Dojin (Genome Research Center and Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Bucheon Hospital) ;
  • Kim, Yong Hoon (Division of Respiratory Medicine, Soon Chun Hyang University Cheonan Hospital) ;
  • Park, Choon-Sik (Genome Research Center and Division of Allergy and Respiratory Medicine, Soon Chun Hyang University Bucheon Hospital)
  • 투고 : 2016.01.29
  • 심사 : 2016.10.06
  • 발행 : 2017.09.01
⟨ 이전 논문 다음 논문 ⟩

초록

Background/Aims: Diesel exhaust particles (DEPs) lead to elevation of reactive oxygen species, which can activate the nucleotide-binding oligomerization domain-like receptor (NLR) family members containing the pyrin domain 3 (NLRP3)-inflammasome. In this study, we elucidated whether NLRP3-inflammasome is activated by DEPs and whether antioxidants (N-acetylcysteine [NAC]) could inhibit such activation. Methods: RAW 264.7 cells and ex vivo lung tissues explants obtained from elastase-induced emphysema animal models were stimulated with cigarette smoking extract (CSE), DEPs, and lipopolysaccharide, and levels of $interleukin-1{\beta}$ ($IL-1{\beta}$), caspase-1 and nucleotide-binding oligomerization domain-like receptor (NLR) family members containing the pyrin domain (NLRP3)-inflammasome were assessed by Western blotting and immunohistochemistry. Results: NAC and caspase-1 inhibitor suppressed CSE- and DEP-induced secretion of $IL-1{\beta}$ in RAW 264.7 cells. The expression levels of the NLRP3-inflammasome and caspase-1 were upregulated in RAW 264.7 cells by stimulation with CSE and DEPs and were inhibited by NAC. CSE and DEPs increased the secretion of $IL-1{\beta}$ in lung tissues from both the normal and elastase-induced emphysema groups. The secretion of $IL-1{\beta}$ by CSE and DEPs was increased in the elastin-induced emphysema group more than that in the normal group (CSE: $309{\pm}19pg/mL$ vs. $151{\pm}13pg/mL$, respectively, p < 0.05; DEP: $350{\pm}24pg/mL$ vs. $281{\pm}15pg/mL$, respectively, p < 0.05). NAC inhibited CSE- and DEP-induced $IL-1{\beta}$ secretion in both the normal and elastase-induced emphysema groups. NLRP3-inflammasome expression as determined by immunohistochemistry was increased by CSE and DEPs in both the normal and elastin-induced emphysema groups, and was suppressed by NAC. Conclusions: The NLRP3-inflammasome is activated by DEPs in ex vivo tissue explants from elastase-induced emphysema animal model, and this activation is inhibited by NAC.

키워드

과제정보

연구 과제 주관 기관 : National Research Foundation of Korea

참고문헌

  1. Global Initiative for Chronic Obstructive Lung Disease (GOLD). Global strategy for the diagnosis, management and prevention of COPD, 2011 [Internet]. GOLD, c2016 [cited 2017 Jul 7]. Available from: http://www.goldcopd.org.
  2. Chapman KR, Mannino DM, Soriano JB, et al. Epidemiology and costs of chronic obstructive pulmonary disease. Eur Respir J 2006;27:188-207. https://doi.org/10.1183/09031936.06.00024505
  3. Patil SP, Krishnan JA, Lechtzin N, Diette GB. In-hospital mortality following acute exacerbations of chronic obstructive pulmonary disease. Arch Intern Med 2003;163:1180-1186. https://doi.org/10.1001/archinte.163.10.1180
  4. Berkius J, Nolin T, Mardh C, Karlstrom G, Walther SM; Swedish Intensive Care Registry. Characteristics and long-term outcome of acute exacerbations in chronic obstructive pulmonary disease: an analysis of cases in the Swedish Intensive Care Registry during 2002-2006. Acta Anaesthesiol Scand 2008;52:759-765. https://doi.org/10.1111/j.1399-6576.2008.01632.x
  5. De Nardo D, De Nardo CM, Latz E. New insights into mechanisms controlling the NLRP3 inflammasome and its role in lung disease. Am J Pathol 2014;184:42-54. https://doi.org/10.1016/j.ajpath.2013.09.007
  6. Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 2009;27:519-550. https://doi.org/10.1146/annurev.immunol.021908.132612
  7. Kuschner WG, D'Alessandro A, Wong H, Blanc PD. Dosedependent cigarette smoking-related inflammatory responses in healthy adults. Eur Respir J 1996;9:1989-1994. https://doi.org/10.1183/09031936.96.09101989
  8. Rovina N, Dima E, Gerassimou C, Kollintza A, Gratziou C, Roussos C. Interleukin-18 in induced sputum: association with lung function in chronic obstructive pulmonary disease. Respir Med 2009;103:1056-1062. https://doi.org/10.1016/j.rmed.2009.01.011
  9. Imaoka H, Hoshino T, Takei S, et al. Interleukin-18 production and pulmonary function in COPD. Eur Respir J 2008;31:287-297. https://doi.org/10.1183/09031936.00019207
  10. Decramer M, Janssens W, Miravitlles M. Chronic obstructive pulmonary disease. Lancet 2012;379:1341-1351. https://doi.org/10.1016/S0140-6736(11)60968-9
  11. Rotta Detto Loria J, Rohmann K, Droemann D, et al. Nontypeable Haemophilus influenzae infection upregulates the NLRP3 inflammasome and leads to caspase-1-dependent secretion of interleukin-$1{\beta}$: a possible pathway of exacerbations in COPD. PLoS One 2013;8:e66818. https://doi.org/10.1371/journal.pone.0066818
  12. Torres-Duque C, Maldonado D, Perez-Padilla R, Ezzati M, Viegi G; Forum of International Respiratory Studies (FIRS) Task Force on Health Effects of Biomass Exposure. Biomass fuels and respiratory diseases: a review of the evidence. Proc Am Thorac Soc 2008;5:577-590. https://doi.org/10.1513/pats.200707-100RP
  13. Sydbom A, Blomberg A, Parnia S, Stenfors N, Sandstrom T, Dahlen SE. Health effects of diesel exhaust emissions. Eur Respir J 2001;17:733-746. https://doi.org/10.1183/09031936.01.17407330
  14. Bayram H, Devalia JL, Sapsford RJ, et al. The effect of diesel exhaust particles on cell function and release of inflammatory mediators from human bronchial epithelial cells in vitro. Am J Respir Cell Mol Biol 1998;18:441-448. https://doi.org/10.1165/ajrcmb.18.3.2882
  15. Ghio AJ, Richards JH, Carter JD, Madden MC. Accumulation of iron in the rat lung after tracheal instillation of diesel particles. Toxicol Pathol 2000;28:619-627. https://doi.org/10.1177/019262330002800416
  16. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011;469:221-225. https://doi.org/10.1038/nature09663
  17. Khedoe PP, Wong MC, Wagenaar GT, et al. The effect of PPE-induced emphysema and chronic LPS-induced pulmonary inflammation on atherosclerosis development in APOE*3-LEIDEN mice. PLoS One 2013;8:e80196. https://doi.org/10.1371/journal.pone.0080196
  18. Smelter DF, Sathish V, Thompson MA, Pabelick CM, Vassallo R, Prakash YS. Thymic stromal lymphopoietin in cigarette smoke-exposed human airway smooth muscle. J Immunol 2010;185:3035-3040. https://doi.org/10.4049/jimmunol.1000252
  19. Haque R, Umstead TM, Freeman WM, Floros J, Phelps DS. The impact of surfactant protein-A on ozone-induced changes in the mouse bronchoalveolar lavage proteome. Proteome Sci 2009;7:12. https://doi.org/10.1186/1477-5956-7-12
  20. Luthje L, Raupach T, Michels H, et al. Exercise intolerance and systemic manifestations of pulmonary emphysema in a mouse model. Respir Res 2009;10:7. https://doi.org/10.1186/1465-9921-10-7
  21. Lim HB, Ichinose T, Miyabara Y, et al. Involvement of superoxide and nitric oxide on airway inflammation and hyperresponsiveness induced by diesel exhaust particles in mice. Free Radic Biol Med 1998;25:635-644. https://doi.org/10.1016/S0891-5849(98)00073-2
  22. Gross O, Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev 2011;243:136-151. https://doi.org/10.1111/j.1600-065X.2011.01046.x
  23. Bauernfeind F, Ablasser A, Bartok E, et al. Inflammasomes: current understanding and open questions. Cell Mol Life Sci 2011;68:765-783. https://doi.org/10.1007/s00018-010-0567-4
  24. Kanneganti TD, Ozoren N, Body-Malapel M, et al. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 2006;440:233-236. https://doi.org/10.1038/nature04517
  25. Peacock JL, Anderson HR, Bremner SA, et al. Outdoor air pollution and respiratory health in patients with COPD. Thorax 2011;66:591-596. https://doi.org/10.1136/thx.2010.155358
  26. Ling SH, van Eeden SF. Particulate matter air pollution exposure: role in the development and exacerbation of chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 2009;4:233-243.
  27. Papi A, Luppi F, Franco F, Fabbri LM. Pathophysiology of exacerbations of chronic obstructive pulmonary disease. Proc Am Thorac Soc 2006;3:245-251. https://doi.org/10.1513/pats.200512-125SF
  28. 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. https://doi.org/10.1034/j.1399-3003.2000.01512.x
  29. Ohtoshi T, Takizawa H, Okazaki H, et al. Diesel exhaust particles stimulate human airway epithelial cells to produce cytokines relevant to airway inflammation in vitro. J Allergy Clin Immunol 1998;101(6 Pt 1):778-785. https://doi.org/10.1016/S0091-6749(98)70307-0
  30. Ritz SA, Wan J, Diaz-Sanchez D. Sulforaphane-stimulated phase II enzyme induction inhibits cytokine production by airway epithelial cells stimulated with diesel extract. Am J Physiol Lung Cell Mol Physiol 2007;292:L33-L39. https://doi.org/10.1152/ajplung.00170.2006
  31. Hirota JA, Hirota SA, Warner SM, et al. The airway epithelium nucleotide-binding domain and leucine-rich repeat protein 3 inflammasome is activated by urban particulate matter. J Allergy Clin Immunol 2012;129:1116-1125. https://doi.org/10.1016/j.jaci.2011.11.033
  32. Bauer CM, Zavitz CC, Botelho FM, et al. Treating viral exacerbations of chronic obstructive pulmonary disease: insights from a mouse model of cigarette smoke and H1N1 influenza infection. PLoS One 2010;5:e13251. https://doi.org/10.1371/journal.pone.0013251
  33. Bauer CM, Morissette MC, Stampfli MR. The influence of cigarette smoking on viral infections: translating bench science to impact COPD pathogenesis and acute exacerbations of COPD clinically. Chest 2013;143:196-206. https://doi.org/10.1378/chest.12-0930
  34. Inoue K, Koike E, Takano H. Comprehensive analysis of elastase-induced pulmonary emphysema in mice: effects of ambient existing particulate matters. Int Immunopharmacol 2010;10:1380-1389. https://doi.org/10.1016/j.intimp.2010.07.016
  35. Castro P, Legora-Machado A, Cardilo-Reis L, et al. Inhibition of interleukin-1beta reduces mouse lung inflammation induced by exposure to cigarette smoke. Eur J Pharmacol 2004;498:279-286. https://doi.org/10.1016/j.ejphar.2004.07.047
  36. Eltom S, Stevenson CS, Rastrick J, et al. P2X7 receptor and caspase 1 activation are central to airway inflammation observed after exposure to tobacco smoke. PLoS One 2011;6:e24097. https://doi.org/10.1371/journal.pone.0024097
  37. Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 2001;11:173-186. https://doi.org/10.1159/000047804
  38. Schwarze PE, Totlandsdal AI, Lag M, Refsnes M, Holme JA, Ovrevik J. Inflammation-related effects of diesel engine exhaust particles: studies on lung cells in vitro. Biomed Res Int 2013;2013:685142.
  39. Rudell B, Blomberg A, Helleday R, et al. Bronchoalveolar inflammation after exposure to diesel exhaust: comparison between unfiltered and particle trap filtered exhaust. Occup Environ Med 1999;56:527-534. https://doi.org/10.1136/oem.56.8.527
  40. Rudell B, Ledin MC, Hammarstrom U, Stjernberg N, Lundback B, Sandstrom T. Effects on symptoms and lung function in humans experimentally exposed to diesel exhaust. Occup Environ Med 1996;53:658-662. https://doi.org/10.1136/oem.53.10.658

피인용 문헌

  1. Nasal DNA methylation is associated with childhood asthma vol.10, pp.5, 2018, https://doi.org/10.2217/epi-2017-0127
  2. Effects of particulate matter on allergic respiratory diseases vol.4, pp.2, 2017, https://doi.org/10.1016/j.cdtm.2018.04.001
  3. Melatonin in macrophage biology: Current understanding and future perspectives vol.66, pp.2, 2017, https://doi.org/10.1111/jpi.12547
  4. Hydrogen Sulfide Attenuates Particulate Matter-Induced Emphysema and Airway Inflammation Through Nrf2-Dependent Manner vol.11, pp.None, 2017, https://doi.org/10.3389/fphar.2020.00029
  5. Current perspectives on the role of interleukin-1 signalling in the pathogenesis of asthma and COPD vol.55, pp.2, 2017, https://doi.org/10.1183/13993003.00563-2019
  6. Cumulative Lifetime Burden of Cardiovascular Disease From Early Exposure to Air Pollution vol.9, pp.6, 2017, https://doi.org/10.1161/jaha.119.014944
  7. Immunomodulatory Effects of a Low-Molecular Weight Polysaccharide from Enteromorpha prolifera on RAW 264.7 Macrophages and Cyclophosphamide- Induced Immunosuppression Mouse Models vol.18, pp.7, 2017, https://doi.org/10.3390/md18070340
  8. Nanoceria distribution and effects are mouse-strain dependent vol.14, pp.6, 2017, https://doi.org/10.1080/17435390.2020.1770887
  9. Inflammatory effects of particulate matter air pollution vol.27, pp.34, 2017, https://doi.org/10.1007/s11356-020-10574-w
  10. New Insights into the Role of NLRP3 Inflammasome in Pathogenesis and Treatment of Chronic Obstructive Pulmonary Disease vol.14, pp.None, 2017, https://doi.org/10.2147/jir.s324323
  11. Pathogen‐associated molecular patterns and extracellular Hsp70 interplay in NLRP3 inflammasome activation in monocytic and bronchial epithelial cellular models of COPD exacerbations vol.129, pp.2, 2021, https://doi.org/10.1111/apm.13089
  12. Air Pollution and the Airways: Lessons from a Century of Human Urbanization vol.12, pp.7, 2021, https://doi.org/10.3390/atmos12070898
  13. Smoking increases oral mucosa susceptibility to Candida albicans infection via the Nrf2 pathway: In vitro and animal studies vol.25, pp.16, 2017, https://doi.org/10.1111/jcmm.16724
  14. Effects of Air Pollutants on Airway Diseases vol.18, pp.18, 2021, https://doi.org/10.3390/ijerph18189905