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Original Research

Lung Inflammatory Response to Environmental Dust Exposure in Mice Suggests a Link to Regional Respiratory Disease Risk

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Pages 4035-4052 | Published online: 21 Aug 2021

References

  • Hart CM, Gonzalez MR, Simpson EP, Hurlbert SH. Salinity and fish effects on Salton Sea microecosystems: zooplankton and nekton. Hydrobiologia. 1998;381(1–3):129–152.
  • Tompson AFB. Born from a flood: the Salton Sea and its story of survival. J Earth Sci. 2016;27(1):89–97. doi:10.1007/s12583-016-0630-7
  • Barnum DA, Bradley T, Cohen M, Wilcox B, Yanega G State of the Salton Sea–A science and monitoring meeting of scientists for the Salton Sea: U.S. Geological Survey Open-File Report 2017-1005. 2017.
  • Johnston JE, Razafy M, Lugo H, Olmedo L, Farzan SF. The disappearing Salton Sea: a critical reflection on the emerging environmental threat of disappearing saline lakes and potential impacts on children’s health. Sci Total Environ. 2019;663:804–817. doi:10.1016/j.scitotenv.2019.01.365
  • Franklin BA, Brook R, Arden Pope C. Air pollution and cardiovascular disease. Curr Probl Cardiol. 2015;40(5):207–238. doi:10.1016/j.cpcardiol.2015.01.003
  • Samoli E, Nastos P, Paliatsos A, Katsouyanni K, Priftis K. Acute effects of air pollution on pediatric asthma exacerbation: evidence of association and effect modification. Environ Res. 2011;111(3):418–424. doi:10.1016/j.envres.2011.01.014
  • Forastiere F, Stafoggia M, Tasco C, et al. Socioeconomic status, particulate air pollution, and daily mortality: differential exposure or differential susceptibility. Am J Ind Med. 2007;50(3):208–216. doi:10.1002/ajim.20368
  • Frie AL, Dingle JH, Ying SC, Bahreini R. The effect of a receding saline lake (the Salton Sea) on airborne particulate matter composition. Environ Sci Technol. 2017;51(15):8283–8292. doi:10.1021/acs.est.7b01773
  • Frie A, Garrison A, Schaefer M, et al. Dust sources in the Salton Sea basin: a clear case of an anthropogenically impacted dust budget. Environ Sci Technol. 2019;53(16):9378–9388. doi:10.1021/acs.est.9b02137
  • Marshall JR. Why emergency physicians should care about the Salton Sea. West J Emerg Med. 2017;18(6):1008–1009. doi:10.5811/westjem.2017.8.36034
  • Vogl RA, Henry RN. Characteristics and contaminants of the Salton Sea sediments. Feature. Hydrobiologia. 2002;473(1–3):47. doi:10.1023/A:1016509113214
  • Ahmed CMS, Cui Y, Frie AL, et al. Exposure to dimethyl selenide (DMSe)-derived secondary organic aerosol alters transcriptomic profiles in human airway epithelial cells. Environ Sci Technol. 2019;53(24):14660–14669. doi:10.1021/acs.est.9b04376
  • Anastasiou C. Fungi from Salt Lakes. I. A new species of Clavariopsis. Mycologia. 1961;53(1):11–16. doi:10.1080/00275514.1961.12017929
  • Carmichael WW, Li R. Cyanobacteria toxins in the Salton Sea. Saline Syst. 2006;2:5. doi:10.1186/1746-1448-2-5
  • Paul C, Pohnert G. Induction of protease release of the resistant diatom chaetoceros didymus in response to lytic enzymes from an algicidal bacterium. PLoS One. 2013;8(3):e57577. doi:10.1371/journal.pone.0057577
  • Matsumura Y. Role of allergen source-derived proteases in sensitization via airway epithelial cells. J Allergy. 2012;2012(2012):903659. doi:10.1155/2012/903659
  • Jacquet A. Interactions of airway epithelium with protease allergens in the allergic response. Clin Exp Allergy. 2011;41(3):305–311. doi:10.1111/j.1365-2222.2010.03661.x
  • Kauffman HF, Tomee JF, van de Riet MA, Timmerman AJ, Borger P. Protease-dependent activation of epithelial cells by fungal allergens leads to morphologic changes and cytokine production. J Allergy Clin Immunol. 2000;105(6 Pt 1):1185–1193. doi:10.1067/mai.2000.106210
  • Reed C, Kita H. The role of protease activation of inflammation in allergic respiratory diseases. J Allergy Clin Immunol. 2004;114(5):997–1008. doi:10.1016/j.jaci.2004.07.060
  • Peng X, Maltz MR, Botthoff JK, et al. Establishment and characterization of a multi-purpose large animal exposure chamber for investigating health effects. Rev Sci Instrum. 2019;90(3):035115. doi:10.1063/1.5042097
  • Romberger DJ, Heires AJ, Nordgren TM, et al. Proteases in agricultural dust induce lung inflammation through PAR-1 and PAR-2 activation. Am J Physiol Lung Cell Mol Physiol. 2015;309(4):L388–99. doi:10.1152/ajplung.00025.2015
  • Poole JA, Wyatt TA, Oldenburg PJ, et al. Intranasal organic dust exposure-induced airway adaptation response marked by persistent lung inflammation and pathology in mice. Am J Physiol Lung Cell Mol Physiol. 2009;296(6):L1085–95. doi:10.1152/ajplung.90622.2008
  • Raftis E, Delday M, Cowie P, et al. Bifidobacterium breve MRx0004 protects against airway inflammation in a severe asthma model by suppressing both neutrophil and eosinophil lung infiltration. Sci Rep. 2018;8(1):1–13. doi:10.1038/s41598-018-30448-z
  • Gueders M, Balbin M, Rocks N, et al. Matrix metalloproteinase-8 deficiency promotes granulocytic allergen-induced airway inflammation. J Immunol. 2005;175(4):2589–2597. doi:10.4049/jimmunol.175.4.2589
  • Nordgren TM, Friemel TD, Heires AJ, Poole JA, Wyatt TA, Romberger DJ. The omega-3 Fatty Acid docosahexaenoic Acid attenuates organic dust-induced airway inflammation. Nutrients. 2014;6(12):5434–5452. doi:10.3390/nu6125434
  • Nordgren TM, Bailey KL, Heires AJ, Katafiasz D, Romberger DJ. Effects of agricultural organic dusts on human lung-resident mesenchymal stem (stromal) cell function. Toxicol Sci. 2018;162(2):635–644. doi:10.1093/toxsci/kfx286
  • Lantz MS, Ciborowski P. Zymographic techniques for detection and characterization of microbial proteases. Methods Enzymol. 1994;235:563–594.
  • Kan S, Hariyadi DM, Grainge C, Knight DA, Bartlett NW, Liang M. Airway epithelial-targeted nanoparticles for asthma therapy. Am J Physiol Lung Cell Mol Physiol. 2020;318(3):L500–l509. doi:10.1152/ajplung.00237.2019
  • Wu M, Du Y, Liu Y, et al. Low molecular weight hyaluronan induces lymphangiogenesis through LYVE-1-mediated signaling pathways. PLoS One. 2014;3:556.
  • Johnson L, Prevo R, Clasper S, Jackson D. Inflammation-induced uptake and degradation of the lymphatic endothelial hyaluronan receptor LYVE-1. J Biol Chem. 2007;282(46):33671–33680. doi:10.1074/jbc.M702889200
  • Takizawa H. Airway epithelial cells as regulators of airway inflammation (Review). Int J Mol Med. 1998;1(2):367–378.
  • Giang J, Seelen M, van Doorn M, Rissmann R, Prens E, Damman J. Complement activation in inflammatory skin diseases. Front Immunol. 2018;9:639. doi:10.3389/fimmu.2018.00639
  • Volanakis J, Narayana S. Complement factor D, a novel serine protease. Protein Sci. 1996;5(4):553–564. doi:10.1002/pro.5560050401
  • Russell J, Ley T. Lymphocyte-mediated cytotoxicity. Annu Rev Immunol. 2002;20:323–370. doi:10.1146/annurev.immunol.20.100201.131730
  • Pieper K, Grimbacher B, Eibel H. B-cell biology and development. J Allergy Clin Immunol. 2013;131(4):959–971. doi:10.1016/j.jaci.2013.01.046
  • Center D, Kornfeld H, Cruikshank W. Interleukin-16. Int J Biochem Cell Biol. 1997;29(11):757–766. doi:10.1016/s1357-2725(97)00053-8
  • Schmitt C, Tonnelle C, Dalloul A, Chabannon C, Debré P, Rebollo A. Aiolos and Ikaros: regulators of lymphocyte development, homeostasis and lymphoproliferation. Apoptosis. 2002;7(3):277–284. doi:10.1023/a:1015372322419
  • Medvedovic J, Ebert A, Tagoh H, Busslinger M. Pax5: a master regulator of B cell development and leukemogenesis. Adv Immunol. 2011;111:179–206. doi:10.1016/B978-0-12-385991-4.00005-2
  • McWilliam H, Villadangos J. MR1: a multi-faceted metabolite sensor for T cell activation. Curr Opin Immunol. 2020;64:124–129. doi:10.1016/j.coi.2020.05.006
  • Klemann C, Wagner L, Stephan M, von Hörsten S. Cut to the chase: a review of CD26/dipeptidyl peptidase-4’s (DPP4) entanglement in the immune system. Clin Exp Immunol. 2016;185(1):1–21. doi:10.1111/cei.12781
  • Gulati K, Gangele K, Agarwal N, Jamsandekar M, Kumar D, Poluri K. Molecular cloning and biophysical characterization of CXCL3 chemokine. Int J Biol Macromol. 2018;107(PtA):575–584. doi:10.1016/j.ijbiomac.2017.09.032
  • Larsson K. Inflammatory markers in COPD. Clin Respir J. 2008;2(Suppl 1):84–87. doi:10.1111/j.1752-699X.2008.00089.x
  • Palecanda A, Paulauskis J, Al-Mutairi E, et al. Role of the scavenger receptor MARCO in alveolar macrophage binding of unopsonized environmental particles. J Exp Med. 1999;189(9):1497–1506. doi:10.1084/jem.189.9.1497
  • Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol. 2004;36(10):1882–1886. doi:10.1016/j.biocel.2003.10.019
  • Tsuji K, Ebihara Y. Expression of G-CSF receptor on myeloid progenitors. Leuk Lymphoma. 2001;42(6):1351–1357. doi:10.3109/10428190109097763
  • Gordon S. Macrophage-restricted molecules: role in differentiation and activation. Immunol Lett. 1999;65(1–2):5–8. doi:10.1016/s0165-2478(98)00116-3
  • Lin H, Stacey M, Stein-Streilein J, Gordon S. F4/80: the macrophage-specific adhesion-GPCR and its role in immunoregulation. Adv Exp Med Biol. 2010;706:149–156. doi:10.1007/978-1-4419-7913-1_13
  • Wu Z, Zhang Z, Lei Z, Lei P. CD14: biology and role in the pathogenesis of disease. Cytokine Growth Factor Rev. 2019;48:24–31. doi:10.1016/j.cytogfr.2019.06.003
  • Hadebe S, Brombacher F, Brown G. C-Type lectin receptors in asthma. Front Immunol. 2018;9:733. doi:10.3389/fimmu.2018.00733
  • Negi S, Pahari S, Bashir H, Agrewala J. Gut Microbiota regulates mincle mediated activation of lung dendritic cells to protect against mycobacterium tuberculosis. Front Immunol. 2019;10:1142. doi:10.3389/fimmu.2019.01142
  • Wells C, Salvage-Jones J, Li X, et al. The macrophage-inducible C-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J Immunol. 2008;180(11):7404–7413. doi:10.4049/jimmunol.180.11.7404
  • Wang H, FitzPatrick M, Wilson N, et al. CSF3R/CD114 mediates infection-dependent transition to severe asthma. J Allergy Clin Immunol. 2019;143(2):785–788.e6. doi:10.1016/j.jaci.2018.10.001
  • Deng X, Mercer P, Scotton C, Gilchrist A, Chambers R. Thrombin induces fibroblast CCL2/JE production and release via coupling of PAR 1 to Gαq and cooperation between ERK1/2 and Rho kinase signaling pathways. Mol Biol Cell. 2008;19:2520–2533. doi:10.1091/mbc.e07-07-0720
  • Heuberger D, Schuepbach R. Protease-activated receptors (PARs): mechanisms of action and potential therapeutic modulators in PAR-driven inflammatory diseases. Thromb J. 2019;17:4. doi:10.1186/s12959-019-0194-8
  • Asokananthan N, Graham PT, Stewart DJ, et al. House dust mite allergens induce proinflammatory cytokines from respiratory epithelial cells: the cysteine protease allergen, Der p 1, activates protease-activated receptor (PAR)-2 and inactivates PAR-1. J Immunol. 2002;169(8):4572–4578. doi:10.4049/jimmunol.169.8.4572
  • Bhat RK, Page K, Tan A, Hershenson MB. German cockroach extract increases bronchial epithelial cell interleukin-8 expression. Clin Exp Allergy. 2003;33(1):35–42. doi:10.1046/j.1365-2222.2002.01481.x
  • Boitano S, Flynn AN, Sherwood CL, et al. Alternaria alternata serine proteases induce lung inflammation and airway epithelial cell activation via PAR2. Am J Physiol Lung Cell Mol Physiol. 2011;300(4):L605–14. doi:10.1152/ajplung.00359.2010
  • Bach AJ, Brazel AJ, Lancaster N. Temporal and spatial aspects of blowing dust in the Mojave and Colorado deserts of Southern California, 1973–1994. Analytic Serial. Physical Geography. 1996;17(4):329–353. doi:10.1080/02723646.1996.10642589
  • King J, Etyemezian V, Sweeney M, Buck BJ, Nikolich G. Dust emission variability at the Salton Sea, California, USA. Aeolian Res. 2011;3(1):67–79. doi:10.1016/j.aeolia.2011.03.005
  • Goudie AS. Desert dust and human health disorders. Environ Int. 2014;63:101–113. doi:10.1016/j.envint.2013.10.011
  • Kunii O, Hashizume M, Chiba M, et al. Respiratory symptoms and pulmonary function among school-age children in the Aral Sea region. Arch Environ Health. 2003;58(11):676–682. doi:10.3200/AEOH.58.11.676-682
  • Hong YC, Pan XC, Kim SY, et al. Asian Dust Storm and pulmonary function of school children in Seoul. Sci Total Environ. 2010;408(4):754–759. doi:10.1016/j.scitotenv.2009.11.015
  • Chien LC, Yang CH, Yu HL. Estimated effects of Asian dust storms on spatiotemporal distributions of clinic visits for respiratory diseases in Taipei children (Taiwan). Environ Health Perspect. 2012;120(8):1215–1220. doi:10.1289/ehp.1104417
  • Kanatani KT, Ito I, Al-Delaimy WK, et al. Desert dust exposure is associated with increased risk of asthma hospitalization in children. Am J Respir Crit Care Med. 2010;182(12):1475–1481. doi:10.1164/rccm.201002-0296OC
  • Chen S, Yao L, Huang P, et al. Blockade of the NLRP3/caspase-1 axis ameliorates airway neutrophilic inflammation in a toluene diisocyanate-induced murine asthma model. Toxicol Sci. 2019;170(2):462–475. doi:10.1093/toxsci/kfz099
  • Moore WC, Hastie AT, Li X, et al. Sputum neutrophil counts are associated with more severe asthma phenotypes using cluster analysis. J Allergy Clin Immunol. 2014;133(6):1557–63.e5. doi:10.1016/j.jaci.2013.10.011
  • Davoine F, Lacy P. Eosinophil cytokines, chemokines, and growth factors: emerging roles in immunity. Front Immunol. 2014;5:570. doi:10.3389/fimmu.2014.00570
  • Rincon M, Irvin CG. Role of IL-6 in asthma and other inflammatory pulmonary diseases. Int J Biol Sci. 2012;8(9):1281–1290. doi:10.7150/ijbs.4874
  • Arredouani MS, Franco F, Imrich A, et al. Scavenger receptors SR-AI/II and MARCO limit pulmonary dendritic cell migration and allergic airway inflammation. J Immunol. 2007;178(9):5912–5920. doi:10.4049/jimmunol.178.9.5912
  • Sakai H, Suto W, Kai Y, Chiba Y. Mechanisms underlying the pathogenesis of hyper-contractility of bronchial smooth muscle in allergic asthma. J Smooth Muscle Res. 2017;53:37–47. doi:10.1540/jsmr.53.37
  • Alitalo K, Tammela T, Petrova TV. Lymphangiogenesis in development and human disease. Nature. 2005;438(7070):946–953. doi:10.1038/nature04480
  • Stump B, Cui Y, Kidambi P, Lamattina A, El-Chemaly S. Lymphatic changes in respiratory diseases: more than just remodeling of the lung? Am J Respir Cell Mol Biol. 2017;57(3):272–279. doi:10.1165/rcmb.2016-0290TR
  • Hardavella G, Tzortzaki EG, Siozopoulou V, et al. Lymphangiogenesis in COPD: another link in the pathogenesis of the disease. Respir Med. 2012;106(5):687–693. doi:10.1016/j.rmed.2011.11.011
  • Ebina M. Remodeling of airway walls in fatal asthmatics decreases lymphatic distribution; beyond thickening of airway smooth muscle layers. Allergol Int. 2008;57(2):165–174. doi:10.2332/allergolint.O-07-497
  • El-Chemaly S, Levine S, Moss J. Lymphatics in lung disease. Ann N Y Acad Sci. 2008;1131:195–202. doi:10.1196/annals.1413.017
  • Hewitt CR, Brown AP, Hart BJ, Pritchard DI. A major house dust mite allergen disrupts the immunoglobulin E network by selectively cleaving CD23: innate protection by antiproteases. J Exp Med. 1995;182(5):1537–1544. doi:10.1084/jem.182.5.1537
  • Schulz O, Sewell HF, Shakib F. Proteolytic cleavage of CD25, the alpha subunit of the human T cell interleukin 2 receptor, by Der p 1, a major mite allergen with cysteine protease activity. J Exp Med. 1998;187(2):271–275. doi:10.1084/jem.187.2.271
  • Kolattukudy PE, Lee JD, Rogers LM, et al. Evidence for possible involvement of an elastolytic serine protease in aspergillosis. Infect Immun. 1993;61(6):2357–2368. doi:10.1128/iai.61.6.2357-2368.1993
  • Kheradmand F, Kiss A, Xu J, Lee SH, Kolattukudy PE, Corry DB. A protease-activated pathway underlying Th cell type 2 activation and allergic lung disease. J Immunol. 2002;169(10):5904–5911. doi:10.4049/jimmunol.169.10.5904
  • Kale S, Agrawal K, Gaur S, Arora N. Cockroach protease allergen induces allergic airway inflammation via epithelial cell activation. Sci Rep. 2017;7:42341. doi:10.1038/srep42341
  • Cayrol C, Duval A, Schmitt P, et al. Environmental allergens induce allergic inflammation through proteolytic maturation of IL-33. Nat Immunol. 2018;19(4):375–385. doi:10.1038/s41590-018-0067-5
  • Page K. Role of cockroach proteases in allergic disease. Curr Allergy Asthma Rep. 2012;12(5):448–455. doi:10.1007/s11882-012-0276-1
  • Holgate S. The airway epithelium is central to the pathogenesis of asthma. Allergol Int. 2008;57(1):1–10. doi:10.2332/allergolint.R-07-154
  • Holgate ST. Epithelial damage and response. Clin Exp Allergy. 2000;30(Suppl 1):37–41. doi:10.1046/j.1365-2222.2000.00095.x
  • Holgate S. Epithelium dysfunction in asthma. J Allergy Clin Immunol. 2007;120(6):1233–1244. doi:10.1016/j.jaci.2007.10.025
  • Gon Y, Hashimoto S. Role of airway epithelial barrier dysfunction in pathogenesis of asthma. Allergol Int. 2018;67(1):12–17. doi:10.1016/j.alit.2017.08.011
  • Bartemes K, Kita H. Dynamic role of epithelium-derived cytokines in asthma. Clin Immunol. 2012;143(3):222–235. doi:10.1016/j.clim.2012.03.001
  • Schmidlin F, Amadesi S, Dabbagh K, et al. Protease-activated receptor 2 mediates eosinophil infiltration and hyperreactivity in allergic inflammation of the airway. J Immunol. 2002;169(9):5315–5321. doi:10.4049/jimmunol.169.9.5315
  • Reed C. Inflammatory effect of environmental proteases on airway mucosa. Curr Allergy Asthma Rep. 2007;7(5):368–374. doi:10.1007/s11882-007-0056-5
  • Nordgren TM, Bauer CD, Heires AJ, et al. Maresin-1 reduces airway inflammation associated with acute and repetitive exposures to organic dust. Translational Res. 2015;166(1):57–69. doi:10.1016/j.trsl.2015.01.001
  • Nordgren TM, Heires AJ, Bailey KL, et al. Docosahexaenoic acid enhances amphiregulin-mediated bronchial epithelial cell repair processes following organic dust exposure. Am J Physiol Lung Cell Mol Physiol. 2018;314(3):L421–L431. doi:10.1152/ajplung.00273.2017
  • Nordgren TM, Heires AJ, Zempleni J, Swanson BJ, Wichman C, Romberger DJ. Bovine milk-derived extracellular vesicles enhance inflammation and promote M1 polarization following agricultural dust exposure in mice. J Nutr Biochem. 2019;64:110–120. doi:10.1016/j.jnutbio.2018.10.017
  • Poole JA, Gleason AM, Bauer C, et al. CD11c +/CD11b+cells are critical for organic dust–elicited murine lung inflammation. Am J Respir Cell Mol Biol. 2012;47(5):652–659. doi:10.1165/rcmb.2012-0095OC
  • Poole JA, Wyatt TA, Romberger DJ, et al. MyD88 in lung resident cells governs airway inflammatory and pulmonary function responses to organic dust treatment. Respir Res. 2015;16:111. doi:10.1186/s12931-015-0272-9
  • Poole JA, Nordgren TM, Heires AJ, et al. Amphiregulin modulates murine lung recovery and fibroblast function following exposure to agriculture organic dust. Am J Physiol Lung Cell Mol Physiol. 2020;318(1):L180–l191. doi:10.1152/ajplung.00039.2019
  • Romberger DJ, Heires AJ, Nordgren TM, et al. Beta2-adrenergic agonists attenuate organic dust-induced lung inflammation. Am J Physiol Lung Cell Mol Physiol. 2016;311(1):L101–10. doi:10.1152/ajplung.00125.2016
  • Lin C, Lin L, Wang S, et al. The effect of serine protease inhibitors on airway inflammation in a chronic allergen-induced asthma mouse model. Mediators Inflamm. 2014;2014(2014):879326. doi:10.1155/2014/879326
  • Oh S, Pae C, Lee D, et al. Tryptase inhibition blocks airway inflammation in a mouse asthma model. J Immunol. 2002;168(4):1992–2000. doi:10.4049/jimmunol.168.4.1992
  • Asaduzzaman M, Nadeem A, Arizmendi N, et al. Functional inhibition of PAR2 alleviates allergen-induced airway hyperresponsiveness and inflammation. Clin Exp Allergy. 2015;45(12):1844–1855. doi:10.1111/cea.12628