Allergy, Asthma & Respiratory Disease

The Korean Academy of Asthma, Allergy and Clinical Immunology (대한천식알레르기학회)
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Impact of ozone on circulating tight junction protein claudin 4 and claudin 5 in patients with asthma

  • Pureun-Haneul Lee (Department of Internal Medicine, Soonchunhyang University Bucheon Hospital) ;
  • Min-Hyeok An (Department of Internal Medicine, Soonchunhyang University Bucheon Hospital) ;
  • DaYeon Hwang (Department of Internal Medicine, Soonchunhyang University Bucheon Hospital) ;
  • Byeong-Gon Kim (Department of Internal Medicine, Soonchunhyang University Bucheon Hospital) ;
  • An-Soo Jang (Department of Internal Medicine, Soonchunhyang University Bucheon Hospital)
  • Received : 2023.02.20
  • Accepted : 2024.03.22
  • Published : 2024.07.30
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Abstract

Purpose: Claudins are a type of tight junction proteins in human endothelia and epithelia. Ozone brings about oxidative stress and lung inflammation in humans and experimental models. However, the impact of ozone on claudins in subjects with asthma remains poorly understood. The aim of this study was to find variations in the tight junction proteins claudin-4 and claudin-5 in subjects with asthma in relation to ambient ozone concentration. Methods: We previously recruited 50 patients with stable/exacerbated asthmatics and 25 controls. Furthermore, to examine the influence of ozone concentration, we reanalyzed 18 patients with stable or exacerbated asthma and 3 controls. The plasma claudin-4 and claudin-5 levels in response to high concentrations of ozone were compared to stable/exacerbated asthma, and controls. Results: The lung functions were significantly lower in subjects with asthma than those in controls. Blood eosinophil proportions were significantly higher in exacerbated asthmatics than in subjects with stable asthma. In high concentration period of ozone, plasma claudin-4 levels were significantly higher in subjects with exacerbated asthma (0.44±0.30 ng/mL, P= 0.005) or stable asthma (0.38±0.31 ng/mL, P= 0.009) compared to those in control subjects (0.16±0.1 ng/mL). Plasma claudin-5 levels were lower in subjects with stable asthma (2.97±1.38 ng/mL, P= 0.011) than in control subjects (6.92±3.9 ng/mL), and higher in subjects with exacerbated asthma (7.49±4.23 ng/mL, P< 0.001) than those with stable asthma. Conclusion: These results reveal that claudins be changed in patients with asthma following ozone exposure in subjects with asthma.

Keywords

Acknowledgement

This research was supported by Soonchunhyang University.

References

  1. Lee KY, Wu SM, Kou HY, Chen KY, Chuang HC, Feng PH, et al. Association of air pollution exposure with exercise-induced oxygen desaturation in COPD. Respir Res 2022;23:77.
  2. Albano GD, Gagliardo RP, Montalbano AM, Profita M. Overview of the mechanisms of oxidative stress: impact in inflammation of the airway diseases. Antioxidants (Basel) 2022;11:2237.
  3. Wiegman CH, Michaeloudes C, Haji G, Narang P, Clarke CJ, Russell KE, et al. Oxidative stress-induced mitochondrial dysfunction drives inflammation and airway smooth muscle remodeling in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol 2015;136:769-80.
  4. Acute Respiratory Barrier Disruption by Ozone Exposure in Mice. Acute respiratory barrier disruption by ozone exposure in mice. Front Immunol 2019;10:2169.
  5. Patial S, Saini Y. Lung macrophages: current understanding of their roles in ozone-induced lung diseases. Crit Rev Toxicol 2020;50:310-23.
  6. Roberts RA, Smith RA, Safe S, Szabo C, Tjalkens RB, Robertson FM. Toxicological and pathophysiological roles of reactive oxygen and nitrogen species. Toxicology 2010;276:85-94.
  7. Liu Y, Pan J, Zhang H, Shi C, Li G, Peng Z, et al. Short-term exposure to ambient air pollution and asthma mortality. Am J Respir Crit Care Med 2019;200:24-32.
  8. Shah PL, Herth FJ, van Geffen WH, Deslee G, Slebos DJ. Lung volume reduction for emphysema. Lancet Respir Med 2017;5:47-56.
  9. Georas SN, Rezaee F. Epithelial barrier function: at the front line of asthma immunology and allergic airway inflammation. J Allergy Clin Immunol 2014;134:509-20.
  10. Lambrecht BN, Hammad H. Allergens and the airway epithelium response: gateway to allergic sensitization. J Allergy Clin Immunol 2014;134:499-507.
  11. Price ME, Sisson JH. Redox regulation of motile cilia in airway disease. Redox Biol 2019;27:101146.
  12. Rothenberg ME, Saito H, Peebles RS Jr. Advances in mechanisms of allergic disease in 2016. J Allergy Clin Immunol 2017;140:1622-31.
  13. Soini Y. Claudins in lung diseases. Res Res 2011;12:70.
  14. Kage H. Claudin heterogeneity and control of lung tight junctions. Annu Rev Physiol 2013;75:551-67.
  15. Jin W, Rong L, Liu Y, Song Y, Li Y, Pan J. Increased claudin-3, -4 and -18 levels in bronchoalveolar lavage fluid reflect severity of acute lung injury. Respirol 2013;18:643-51.
  16. Lappi-Blanco E, Lehtonen ST, Sormunen R, Merikallio HM, Soini Y, Kaarteenaho RL. Divergence of tight and adherens junction factors in alveolar epithelium in pulmonary fibrosis. Hum Pathol 2013;44:895-907.
  17. Moon KY, Lee PH, Kim BG, Park CS, Leikauf GD, Jang AS. Claudin 5 in a murine model of allergic asthma: its implication and response to steroid treatment. J Allergy Clin Immunol 2015;136:1694-6.e5.
  18. Kaarteenaho R, Soini Y. Claudin-1, -2, -3, -4, -5, and -7 in usual interstitial pneumonia and sarcoidosis. J Histochem Cytochem 2009;57:187-95.
  19. Kim BG, Lee PH, Lee SH, Park CS, Jang AS. Impact of ozone on claudins and tight junctions in the lungs. Environ Toxicol 2018;33:798-806.
  20. Becker AB, Abrams EM. Asthma guidelines: the Global Initiative for Asthma in relation to national guidelines. Curr Opin Allergy Clin Immunol 2017;17:99-103.
  21. Yeo MJ, Kim YP. Long-term trends of surface ozone in Korea. J Clean Prod 2021;294:125352.
  22. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J 2005;26:319-38.
  23. Lee PH, Kim BG, Lee SH, Lee JH, Park SW, Kim DJ, et al. Alteration in claudin-4 contributes to airway inflammation and responsiveness in asthma. Allergy Asthma Immunol Res 2018;10:25-33.
  24. Sokolowska M, Quesniaux VFJ, Akdis CA, Chung KF, Ryffel B, Togbe D. Acute respiratory barrier disruption by ozone exposure in mice. Front Immunol 2019;10:2169.
  25. Kong X, Bennett WC, Jania CM, Chason KD, German Z, Adouli J, et al. Identification of an ATP/P2X7/mast cell pathway mediating ozone-induced bronchial hyperresponsiveness. JCI Insight 2021;6:e140207.
  26. Mumby S, Chung KF, Adcock IM. Transcriptional effects of ozone and impact on airway inflammation. Front Immunol 2019;10:1610.
  27. Michaudel C, Mackowiak C, Maillet I, Fauconnier L, Akdis CA, Sokolowska M, et al. Ozone exposure induces respiratory barrier biphasic injury and inflammation controlled by IL-33. J Allergy Clin Immunol 2018;142:942-58.
  28. Lee PH, Park S, Lee YG, Choi SM, An MH, Jang AS. The impact of environmental pollutants on barrier dysfunction in respiratory disease. Allergy Asthma Immunol Res 2021;13:850-62.
  29. Cho HY, Jedlicka AE, Chang FH, Marzec J, Bauer AK, Kleeberger SR. Transcriptomics underlying pulmonary ozone pathogenesis regulated by inflammatory mediators in mice. Antioxidants (Basel) 2021;10:1489.
  30. Chung KF. Neutrophilic asthma: a distinct target for treatment? Lancet Respir Med 2016;4:765-7.
  31. Madani NA, Carpenter DO. Patterns of emergency room visits for respiratory diseases in New York State in relation to air pollution, poverty and smoking. Int J Environ Res Public Health 2023;20:3267.
  32. Ivanov AI, Naydenov NG. Dynamics and regulation of epithelial adherens junctions: recent discoveries and controversies. Int Rev Cell Mol Biol 2013;303:27-99.
  33. De Benedetto A, Rafaels NM, McGirt LY, Ivanov AI, Georas SN, Cheadle C, et al. Tight junction defects in patients with atopic dermatitis. J Allergy Clin Immunol 2011;127:773-86.e1-7.
  34. Sugita K, Steer CA, Martinez-Gonzalez I, Altunbulakli C, Morita H, Castro-Giner F, et al. Type 2 innate lymphoid cells disrupt bronchial epithelial barrier integrity by targeting tight junctions through IL-13 in asthmatic patients. J Allergy Clin Immunol 2018;141:300-10.e11.
  35. Wawrzyniak P, Wawrzyniak M, Wanke K, Sokolowska M, Bendelja K, Ruckert B, et al. Regulation of bronchial epithelial barrier integrity by type 2 cytokines and histone deacetylases in asthmatic patients. J Allergy Clin Immunol 2017;139:93-103.
  36. Tan HT, Hagner S, Ruchti F, Radzikowska U, Tan G, Altunbulakli C, et al. Tight junction, mucin, and inflammasome-related molecules are differentially expressed in eosinophilic, mixed, and neutrophilic experimental asthma in mice. Allergy 2019;74:294-307.
  37. Kim BG, Lee PH, Lee SH, Baek AR, Park JS, Lee J, et al. Impact of the endothelial tight junction protein claudin-5 on clinical profiles of patients with COPD. Allergy Asthma Immunol Res 2018;10:533-42.
  38. Kim JS, Chen Z, Alderete TL, Toledo-Corral C, Lurmann F, Berhane K, et al. Associations of air pollution, obesity and cardiometabolic health in young adults: the Meta-AIR study. Environ Int 2019;133(Pt A):105180.
  39. Moon KY, Park MK, Leikauf GD, Park CS, Jang AS. Diesel exhaust particle-induced airway responses are augmented in obese rats. Int J Toxicol 2014;33:21-8.