Effects of coal dust particulate matter exposure on H2O2, MDA, IL-13, TGF-β3 level and bronchioles sub-epithelial fibrosis in allergic asthma mice model

Fujiati .

Abstract

Objective: Pulmonary fibrosis in asthma is marked by a rapid decline in lung function. Unfortunately, the environmental factors aggravating this condition are still poorly understood. To date, the pathomechanism of exposure to coal dust affecting the subepithelial fibrosis in asthma remains unclear. Methods: Twenty-fourth female BALB/C mice were divided into four group. The first group was control, the second was mice exposed to coal dust particulate matter (PM) (days 46-75), the third was OVA sensitized mice  (Initial sensitization on day 0 and 14, re-sensitization days 21-75), and the fourth was made of OVA-sensitized mice and exposed coal dust PM. Results: The results showed coal dust PM significantly decreased levels of IL-13 BAL (p-value=0.001) but significantly elevated H2O2 BAL levels (p-value=0.001) and increased sub-epithelial bronchial fibrosis thickness (p-value= 0.000). This was based on the scale of fibrosis (0=<5 μm, 1=5-10 μm; 2=11-15 μm; 3=>15 μm; score 0-1=mild; 1-2=moderate; and 3= severe). The combination of ovalbumin sensitization and PM coal dust caused severe fibrosis (score 3).There was no significant association between IL-13, TGF-β3, H2O2, and MDA BAL with sub-epithelial fibrosis thickness. Conclusions:  PM exposure to coal dust may increase sub-epithelial fibrosis of the bronchioles by a mechanism independent of inflammation and oxidative stress.Objective:Pulmonary fibrosis in asthma is marked by a rapid decline in lung function. Unfortunately, the environmental factors aggravating this condition are still poorly understood. To date, the pathomechanism of exposure to coal dust affecting the subepithelial fibrosis in asthma remains unclear. Methods: Twenty-fourth female BALB/C micewere divided into four group. The first group was control, the second was mice exposed to coal dust particulate matter (PM) (days 46-75), the third was OVA sensitized mice (Initial sensitization on day 0 and 14, re-sensitization days 21-75), and the fourth was made of OVA-sensitized mice and exposed coal dust PM. Results: The results showed coal dust PM significantly decreased levels of IL-13 BAL (p-value=0.001) but significantly elevated H2O2 BAL levels (p-value=0.001) and increased sub-epithelial bronchial fibrosis thickness (p-value=0.000). This was based on the scale of fibrosis (0=<5μm, 1=5-10μm; 2=11-15μm; 3=>15μm; score 0-1=mild; 1-2=moderate; and 3= severe). The combination of ovalbumin sensitization and PM coal dust caused severe fibrosis (score 3).There was no significant association between IL-13, TGF-β3, H2O2, and MDA BAL with sub-epithelial fibrosis thickness.Conclusions:  PM exposure to coal dust may increase sub-epithelial fibrosis of the bronchioles by a mechanism independent of inflammation and oxidative stress.

Full Text:

PDF

References

Ram A, Mabalirajan U, Jaiswal A, Rehman R, Singh VP, Ghosh B. Parabromophenacyl bromide inhibits subepithelial fibrosis by reducing tgf-β1 in a chronic mouse model of allergic asthma. Int Arch Allergy Immunol. 2015;167(2):110-18.

Plantier L, Cazes A, Dinh-Xuan AT, Bancal C, Marchand-Adam S, Crestani B.. Physiology of the lung in idiopathic pulmonary fibrosis. Eur Respir Rev. 2018; 27(147): pii: 170062.

Al-Muhsen S, Johnson JR, andHamid Q. Remodeling in asthma. Journal of Allergy and Clinical Immunology. 2011; 128(3): 451-62.

Alagha K, Jarjour B, Bommart S, Aviles B, Varrin M, Gamez AS, et.al. Persistent severe hypereosinophilic asthma is not associated with airway remodeling. Respir Med. 2015;109(2):180-87.

Bates JHT, Rincon M, Irvin CG. Animal model of asthma. Am J Physiol Lung Cell Mol Physiol. 2009; 297:L401-10.

Kumar RK, Herbert C, Foster PS. The “classical” ovalbumin challenge model of asthma in mice Curr Drug Target. 2008; 9: 485-94.

Ma Y, Ge A, Zhu W, Liu Y, Ji N, Zha W, Zhang J, Zeng X, Huang M. Morin attenuates ovalbumin-induced airway inflammation by modulating oxidative stress-responsive MAPK signaling. Oxid Med Cell Longev. 2016; 4: 1-13

Nakamura Y, Sugano A, Ohta M, Takaoka Y. Docking analysis and the possibility of prediction efficacy for an anti-IL-13 biopharmaceutical treatment with tralokinumab and lebrikizumab for bronchial asthma. PLoS One. 2017 Nov 20;12(11):e0188407.

Barlianto W, Kusuma MSC., Karyono S, and Mintaroem K. The development of allergic mouse model following chronic ovalbumin exposure. Jurnal Kedokteran Brawijaya. 2009; XXV(1): 1-5.

Auerbach A, Hernandez ML .The effect of environmental oxidative stress on airway inflammation. Curr Opin Allergy Clin Immunol. 2012; 12(2):133-9

Kania N, Setiawan B, Nurdiana, Widodo MA, Widjayanto E, and Kusuma HMSC. Peroxidative index as novel marker of hydrogen peroxide involvement in lipid peroxidation from coal dust exposure. Oxid Antioxid Med Sci. 2012;1(3): 209-215.

Yang JCT, and Liu KL. Coal workers’ pneumoconiosis with progressive massive fibrosis. Canadian Medical Association Journa. 2012;184(16): E878.

Saputri RK, Setiawan B, Nugrahenny D, Kania N, Wahyuni ES, and Widodo MA. The effects of eucheuma cottonii on alveolar macrophages and malondialdehyde levels in bronchoalveolar lavage fluid in chronically particulate matter 10 coal dust-exposed rats. Iranian Journal of Basic Medical Sciences. 2014;17(7): 541-45.

Kinnula VL, Fattman CL, Tan RJ, Oury TD. Oxidative stress in pulmonary fibrosis: a possible role for redox modulatory therapy. Am J Respir Crit Care Med. 2005;172(4): 417-22.

Gorowiec MR, Borthwick LA, Parker SM, Kirby JA, Saretzki GC, Fisher AJ. Free radical generation induces epithelial-to-mesenchymal transition in lung epithelium via a TGF-β1-dependent mechanism. Free Radic Biol Med. 2012 Mar 15;52(6):1024-32

Liu YN, Zha WJ, Ma Y, Chen FF, Zhu W, Ge A, Zeng XN, Huang M. Galangin attenuates airway remodelling by inhibiting TGF-β1-mediated ROS generation and MAPK/Akt phosphorylation in asthma. Sci Rep. 2015 Jul 9;5:11758

Faner R, Rojas M, Macnee W, Agustí A. Abnormal lung aging in chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2012 Aug 15;186(4):306-13.

Brass DM, Spencer JC, Li Z, Potts-Kant E, Reilly SM, Dunkel MK, Latoche JD, Auten RL, Hollingsworth JW, Fattman CL. Innate immune activation by inhaled lipopolysaccharide, independent of oxidative stress, exacerbates silica-induced pulmonary fibrosis in mice. PLoS One. 2012;7(7):e40789

Yu H, Li Q, Kolosov VP, Perelman JM, Zhou X. Interleukin-13 induces mucin 5AC production involving STAT6/SPDEF in human airway epithelial cells. Cell Commun Adhes. 2010;17(4-6):83-92.

Jaffer OA, Carter AB, Sanders PN, Dibbern ME, Winters CJ, Murthy S, Ryan AJ, Rokita AG, Prasad AM, Zabner J, Kline JN, Grumbach IM, Anderson ME. Mitochondrial-targeted antioxidant therapy decreases transforming growth factor-β-mediated collagen production in a murine asthma model. Am J Respir Cell Mol Biol. 2015;52(1):106-15.

Li G, Fox J, Liu Z, Liu J, Gao GF, Jin Y, Gao H, & Wu M. Lyn mitigates mouse airway remodeling by downregulating the TGF-β3 isoform in house dust mite models. J Immunol. 2013;191(11):5359-70.

Ask K, Bonniaud P, Maass K, Eickelberg O, Margetts PJ, Warburton D, Groffen J, Gauldie J, Kolb M. Progressive pulmonary fibrosis is mediated by TGF-beta isoform 1 but not TGF-beta3. Int J Biochem Cell Biol. 2008;40(3):484-95.

Day BJ. Antioxidants as potential therapeutics for lung fibrosis. Antioxid Redox Signal. 2008;10(2):355-70.

Plantier L, Cazes A, Dinh-Xuan AT, Bancal C, Marchand-Adam S, Crestani B. Physiology of the lung in idiopathic pulmonary fibrosis. Eur Respir Rev. 2018 Jan 24;27(147).

Hidayat T, Yuliarto S, Barlianto W, Sujuti H, & Kusuma HMSC. Increase of Bcl-2/Bax ratio corelated with decrease oflymphocyte apoptosis: A study in the bronchiolus and lung of asthmatic mice. Int. J. Med. Med. Sci. 2013; 5(4);191-197.

Stone JR, Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal. 2006 Mar-Apr;8(3-4):243-70.

Caffarelli C, Calcinai E, Rinaldi L, Povesi Dascola C, Terracciano L, Corradi M. Hydrogen peroxide in exhaled breath condensate in asthmatic children during acute exacerbation and after treatment. Respiration. 2012;84(4):291-8.

Fitzpatrick AM, Holguin F, Teague WG, Brown LA. Alveolar macrophage phagocytosis is impaired in children with poorly controlled asthma. J Allergy Clin Immunol. 2008 Jun;121(6):1372-8, 1378.e1-3

Cohn CA, Laffers R, Simon SR, O'Riordan T, Schoonen MA. Role of pyrite in formation of hydroxyl radicals in coal: possible implications for human health. Part Fibre Toxicol. 2006 Dec 19;3:16.

Charrier JG, Richards-Henderson NK, Bein KJ, McFall AS, Wexler AS, and Anastasio C. Oxidant production from source-oriented particulate matter-Part 1: Oxidative potential using the dithiothreitol (DTT) assay. Atmos. Chem. Phys 2015;15: 2327-2340.

Wang Y, Branicky R, Noë A, and Hekimi S. Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol 2018; pii: jcb.201708007.

Bao HR, Liu XJ, Li YL, Men X, Zeng XL. Sinomenine attenuates airway inflammation and remodeling in a mouse model of asthma. Mol Med Rep. 2016 Mar;13(3):2415-22.

Lee JS, Shin JH, Hwang JH, Baek JE, Choi BS. Malondialdehyde and 3-nitrotyrosine in exhaled breath condensate in retired elderly coal miners with chronic obstructive pulmonary disease. Saf Health Work. 2014 Jun;5(2):91-6.

Kinnula VL, Fattman CL, Tan RJ, Oury TD.Oxidative stress in pulmonary fibrosis: a possible role for redox modulatory therapy. Am J Respir Crit Care Med. 2005 Aug 15;172(4):417-22.

Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev. 2014;2014:360438.

Wilgus TA, Bergdall VK, Dipietro LA, Oberyszyn TM. Hydrogen peroxide disrupts scarless fetal wound repair. Wound Repair Regen. 2005 Sep-Oct;13(5):513-9. PubMed PMID: 16176460.

Hemmerlein B, Johanns U, Halbfass J, Böttcher T, Heuser M, Radzun HJ, Thelen P. The balance between MMP-2/-9 and TIMP-1/-2 is shifted towards MMP in renal cell carcinomas and can be further disturbed by hydrogen peroxide. Int J Oncol. 2004 May;24(5):1069-76. PubMed PMID: 15067327.

Reis AC, Alessandri AL, Athayde RM, Perez DA, Vago JP, Ávila TV, Ferreira TP, de Arantes AC, Coutinho Dde S, Rachid MA, Sousa LP, Martins MA, Menezes GB, Rossi AG, Teixeira MM, Pinho V. Induction of eosinophil apoptosis by hydrogen peroxide promotes the resolution of allergic inflammation. Cell Death Dis. 2015 Feb 12;6:e1632.

Hanada T, Yoshimura A. Regulation of cytokine signaling and inflammation. Cytokine Growth Factor Rev. 2002 Aug-Oct;13(4-5):413-21. Review. PubMed PMID: 12220554.

Zhu J, Paul WE. Peripheral CD4+ T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol Rev. 2010 Nov;238(1):247-62.

Han M, Hong JY, Jaipalli S, Rajput C, Lei J, Hinde JL, Chen Q, Hershenson NM, Bentley JK, Hershenson MB. IFN-γ Blocks Development of an Asthma Phenotype in Rhinovirus-Infected Baby Mice by Inhibiting Type 2 Innate Lymphoid Cells. Am J Respir Cell Mol Biol. 2017 Feb;56(2):242-251. doi: 10.1165/rcmb.2016-0056OC.

Lighvani AA, Frucht DM, Jankovic D, Yamane H, Aliberti J, Hissong BD, Nguyen BV, Gadina M, Sher A, Paul WE, O'Shea JJ. T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15137-42.

Afkarian M, Sedy JR, Yang J, Jacobson NG, Cereb N, Yang SY, Murphy TL, Murphy KM. T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ Tcells. Nat Immunol. 2002 Jun;3(6):549-57. Epub 2002 May 13. PubMed PMID:12006974.

Nguyen TH, Maltby S, Tay HL, Eyers F, Foster PS, Yang M. Identification of IFN-γ and IL-27 as Critical Regulators of Respiratory Syncytial Virus-Induced Exacerbation of Allergic Airways Disease in a Mouse Model. J Immunol. 2018 Jan 1;200(1):237-247. doi: 10.4049/jimmunol.1601950. Epub 2017 Nov 22. PubMed PMID: 29167232.

Khalil N, Parekh TV, O'Connor R, et al. Regulation of the effects of TGF-beta 1 by activation of latent TGF-beta 1 and differential expression of TGF-beta receptors (T beta R-I and T beta R-II) in idiopathic pulmonary fibrosis. Thorax. 2001;56(12):907-15.

Andrade-Sousa AS, Rogério Pereira P, MacKenzie B, Oliveira-Junior MC,

Assumpção-Neto E, Brandão-Rangel MA, Damaceno-Rodrigues NR, Garcia Caldini E,Velosa AP, Teodoro WR, Ligeiro de Oliveira AP, Dolhnikoff M, Eickelberg O, Vieira RP. Aerobic Exercise Attenuated Bleomycin-Induced Lung Fibrosis in Th2-Dominant Mice. PLoS One 2016;11(9):e0163420.

Bailey JR, Bland PW, Tarlton JF, Peters I, Moorghen M, Sylvester, P.A., Probert, C.S.J., Whiting, C.V.. IL-13 Promotes collagen accumulation in Crohn’s Disease fibrosis by down-regulation of fibroblast MMP synthesis: A Role for Innate Lymphoid Cells? PLoS ONE 2012;7(12): e52332. doi:10.1371/journal.pone.0052332.

Lu J, Zhu Y, Feng W, Pan Y, Li S, Han D, Liu L, Xie X, Wang G, & Li M. Platelet-derived growth factor mediates interleukin-13-induced collagen I production in mouse airway fibroblasts. J. Biosci 2014;39: 693-670.

O'reilly, S., Ciechomska, M., Fullard, N., Przyborski, S., & Van Laar, J.,M. 2016. IL-13 mediates collagen deposition via STAT6 and microRNA-135b: A role for epigenetics. Scientific Reports (Nature Publisher Group), 6, 25066. doi:http://dx.doi.org/10.1038/ srep25066

Wick G, Backovic A, Rabensteiner E, Plank N, Schwentner C, Sgonc R. The immunology of fibrosis: innate and adaptive responses. Trends Immunol 2010;31(3):110-119.

Xu L, Xiong S, Guo R, Yang Z, Wang Q, Xiao F, Wang H, Pan X, Zhu M.Transforming growth factor β3 attenuates the development of radiation-induced pulmonary fibrosis in mice by decreasing fibrocyte recruitment and regulating IFN-γ/IL-4 balance. Immunol Lett 2014;162(1 Pt A):27-33.

Lu L, Saulis AS, Liu WR, Roy NK, Chao JD, Ledbetter S, Mustoe TA.. The temporal effects of anti-TGF-beta1, 2, and 3 monoclonal antibody on wound healing and hypertrophic scar formation. J Am Coll Surg 2005;201(3):391-397.

Akhurst RJ, and Hata A. Targeting the TGFβ signalling pathway in disease. Nat Rev Drug Discov 2012; 11(10): 790–811.

Li YJ, Shimizu T, Shinkai Y, Hirata Y, Inagaki, H, Takeda K, Azuma A, Yamamoto M, and Kawada, T. Nrf2 Regulates the risk of a diesel exhaust inhalation-induced immune response during bleomycin lung injury and fibrosis in mice. Int J Mol Sci 2017;18(3). pii: E649. doi: 10.3390/ ijms18030649.

Diana Lyrawati, Amalia G.Muslimah, Dewi Laksmita, Dian I. Santoso, Erlien L. Poernomo, Karina Larasati, et al. Hepatoprotective and hepatoregenerative therapeutic effects of polyherbal medicine on Rattus norvegicus Wistar with liver fibrosis. Thai Journal of Pharmaceutical Sciences. 2017; 41 (4): 123-9

Karkhanis VS, Joshi JM. Combined pulmonary fibrosis and emphysema in a tyre industry worker. Lung India 2012;29:273-6.

Refbacks

  • There are currently no refbacks.


Bookmark and Share