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Extractable organic matter of Standard Reference Material 1649a influences immunological response induced by pathogen-associated molecular patterns

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Abstract

Background, aim, and scope

Lungs are permanently and simultaneously challenged by airborne microorganisms and airborne pollutants. Temporal increase of airborne particulate matter (APM), a potential carrier for extractable organic matter (EOM), degrades the situation of pulmonary patients. The Ah receptor (AhR) has been described as an important factor influencing the immunological challenge by viral infections. Molecular mechanisms underlying epidemiological observations are not well understood. Cytokine secretion (IL-6, IL-8, and TGF-β) from human bronchial epithelial cells (Beas2B) was determined as an indicator for immune responses upon co-stimulation with an artificial analog of viral dsRNA [polyinosinic/polycytidylic acid, (PIC)] and EOM of Standard Reference Material 1649a (SRM). Since polycyclic aromatic hydrocarbons are major components of APM usually acting via the AhR, particular focus was on AhR involvement.

Materials and methods

Cytokine secretion was demonstrated by enzyme-linked immunosorbent assay. To mimic the activation of organic matter during contact of particles with the human lung, Soxhlet extraction of SRM was performed. In some experiments, the AhR was blocked by α-naphthoflavone.

Results

Microbial stimulation (PIC) induced Beas2B cytokine release, whereas isolated exposure to EOM of APM did not. Co-stimulation with EOM and PIC increased IL-8 secretion, whereas neither IL-6 nor TGF-β was affected. Blocking of the AhR suppressed the release of IL-8.

Discussion

Organic compounds adsorbed on airborne particulate matter influence the cytokine secretion of lung epithelial cells induced by pathogen-associated molecular patterns.

Recommendations and perspectives

Further investigation of these observations is required to understand the molecular mechanisms underlying adverse health effects of APM reported in epidemiological studies.

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References

  • Abbey DE, Nishino N, McDonell WF, Burchette RJ, Knutsen SF, Beeson WW, Yang JX (1999) Longterm inhalable particles and other air pollutants related to mortality in nonsmokers. Am J Respir Crit Care Med 159:373–382

    CAS  Google Scholar 

  • Adair-Kirk TL, Atkinson JJ, Senior RM (2008) Smoke particulates stress lung cells. Nat Med 14(10):1024–1025

    Article  CAS  Google Scholar 

  • Almendros I, Acerbi I, Puig F, Montserrat JM, Navajas D, Farré R (2007) Upper-airway inflammation triggered by vibration in a rat model of snoring. Sleep 30(2):225–227

    Google Scholar 

  • Amakawa K, Terashima T, Matsuzaki T, Matsumaru A, Sagai M, Yamaguchi K (2003) Supressive effects of diesel exhaust particles on cytokine release from human and murine alveolar macrophages. Exp Lung Res 29:149–164

    Article  CAS  Google Scholar 

  • Augusto LA, Synguelakis M, Johansson J, Pedron T, Girard R, Chaby R (2003) Interaction of pulmonary surfactant protein C with CD14 and lipopolysaccharide. Infect Immun 71(1):61–67

    Article  CAS  Google Scholar 

  • Becker S, Mundandhara S, Devlin RB, Madden M (2005) Regulation of cytokine production in human alveolar macrophages and airway epithelial cells in response to ambient air pollution particles: further mechanistic studies. Toxicol Appl Pharmacol 207(2):S269–S275

    Article  CAS  Google Scholar 

  • Curtois A, Andujar P, Ladeiro Y, Baudrimont I, Delannoy E, Leblais V, Begueret H, Galland MAB, Brochard P, Marano F et al (2008) Impairment of NO-dependent relaxation in intralobar pulmonary arteries: comparison of urban particulate matter and manufactured nanoparticles. Environ Health Perspect 116(10):1294–1299

    Article  Google Scholar 

  • Dockery DW, Cunningham J, Damokosh AI, Neas LM, Spengler JD, Koutrakis P, Ware JH, Speizer FE (1996) Health effects of acid aerosols on North American children: respiratory symptoms. Environ Health Perspect 104:500–505

    Article  CAS  Google Scholar 

  • Erdinger L, Dörr I, Dürr M, Höpker KA (2004) Analysis of mutagenic activity of airborne particulate matter, standard reference materials and reference compounds using base pair-specific Salmonella typhimurium tester strains. Mut Res-Genet Toxicol Environ Mutagenesis 564(2):149–157

    Article  CAS  Google Scholar 

  • Erdinger L, Dürr M, Höpker K-A (2005) Correlations between mutagenic activity of organic extracts of airborne particulate matter, NOx and sulphur dioxide in southern Germany—results of a two-year study. Environ Sci Pollut Res 12(1):10–20

    Article  CAS  Google Scholar 

  • Esser C, Rannug A, Stockinger B (2009) The aryl hydrocarbon receptor in immunity. Trends Immunol 30(9):447–454

    Article  CAS  Google Scholar 

  • Fried M (2001) Charakterisierung von gentoxischen organischen Luftstaubextrakten. http://www.ub.uni-heidelberg.de/archiv/1936

  • Gavett SH, Haykal-Coates N, Highfill JW, Ledbetter AD, Chen LC, Cohen MD, Harkema JR, Wagner JG, Costa DL (2003) World Trade Center fine particulate matter causes respiratory tract hyperresponsiveness in mice. Environ Health Perspect 111(7):981–991

    Google Scholar 

  • Head JL, Lawrence BP (2008) The aryl hydrocarbon receptor is a modulator of anti-viral immunity. Biochem Pharmacol. doi:10.1016/j.bcp.2008.10.031

    Google Scholar 

  • Heeg K, Dalpke A (2003) TLR-induced negative regulatory circuits: role of suppressor of cytokine signaling (SOCS) proteins in innate immunity. Vaccine 21(S2):61–67

    Article  Google Scholar 

  • Heinrich J, Hölscher B, Wichmann HE (2000) Decline of ambient air pollution and respiratory symptoms in children. Am J Respir Crit Care Med 161:1930–1936

    CAS  Google Scholar 

  • Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216

    Article  CAS  Google Scholar 

  • Kendall M (2007) Fine airborne urban particles (PM2.5) sequester lung surfactant and amino acids from human lung lavage. Am J Physiol Lung Cell Mol Physiol 293:L1053–L1058

    Article  CAS  Google Scholar 

  • Matsukura S, Kokubu F, Kurokawa M, Kawaguchi M, Ieki K, Kuga H, Odaka M, Suzuki S, Watanabe S, Takeuchi H et al (2006) Synthetic double-stranded RNA induces multiple genes related to inflammation through Toll-like receptor 3 depending on NF-jB and/or IRF-3 in airway epithelial cells. Clin Exp Allergy 36:1049–1062

    Article  CAS  Google Scholar 

  • May WE, Benner BA Jr, Wise SA, Schuetzle D, Lewtas J (1992) Standard reference materials for chemical and biological studies of complex environmental samples. Mutat Res 276:11–22

    CAS  Google Scholar 

  • Mayer AK, Dalpke AH (2007) Regulation of local immunity by airway epithelial cells. Arch Immunol Ther Exp 55:353–362

    Article  CAS  Google Scholar 

  • Mayer AK, Muehmer M, Mages J, Gueinzius K, Hess C, Heeg K, Bals R, Lang R, Dalpke AH (2007) Differential recognition of TLR-dependent microbial ligands in human bronchial epithelial cells. J Immunol 178:3134–3142

    CAS  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation an cytotoxic assays. J Immunol Methods 65:55–63

    Article  CAS  Google Scholar 

  • Ovrevik J, Arlt VM, Oya E, Nagy E, Mollerup S, Phillips DH, Låg M, Holme JA (2010) Differential effects of nitro-PAHs and amino-PAHs on cytokine and chemokine responses in human bronchial epithelial BEAS-2B cells. Toxicol Appl Pharmacol 242:270–280

    Article  CAS  Google Scholar 

  • Pace E, Ferraro M, Siena L, Melis M, Montalbano AM, Johnson M, Bonsignore MR, Bonsignore G, Gjomarkaj M (2008) Cigarette smoke increases Toll-like receptor 4 and modifies lipopolysaccharide-mediated responses in airway epithelial cells. Immunology 124:401–411

    Article  CAS  Google Scholar 

  • Parsanejad R, Fields WR, Steichen TJ, Bombick BR, Doolittle DJ (2008) Distinct regulatory profiles of interleukins and chemokines in response to cigarette smoke condensate in normal human bronchial epithelial (NHBE) cells. J Interferon Cytokine Res 28:703–712

    Article  CAS  Google Scholar 

  • Peters JM, Avol E, Gaudermann WJ, Lurmann F, Linn WS, Margolis H, Rappaport E, Gong H, Thomas DC (1999a) A study of twelve Southern California communities with differing levels and types of air pollution. I. Prevalence of respiratory morbidity. Am J Respir Crit Care Med 159:760–767

    CAS  Google Scholar 

  • Peters JM, Avol E, Gaudermann WJ, Linn WS, Navidi W, London SJ, Margolis H, Rappaport E, Vora H, Gong H et al (1999b) A study of twelve Southern California communities with differing levels and types of air pollution. II. Effects on pulmonary function. Am J Respir Crit Care Med 159:768–775

    CAS  Google Scholar 

  • Rehli M (2002) Of mice and man: species variations of Toll-like receptor expression. Trends Immunol 23(8):375–378

    Article  CAS  Google Scholar 

  • Sartor MA, Schnekenburger M, Marlowe JL, Reichard JF, Wang Y, Fan Y, Ma C, Karyala S, Halbleib D, Liu X et al (2009) Genomewide analysis of aryl hydrocarbon receptor binding targets reveals an extensive array of gene clusters that control morphogenetic and developmental programs. Environ Health Perspect 117(7):1139–1146

    CAS  Google Scholar 

  • Seagrave JC (2008) Mechanisms and implications of air pollution particle associations with chemokines. Toxicol Appl Pharmacol 232:469–477

    Article  CAS  Google Scholar 

  • Tian Y, Rabson AB, Gallo MA (2002) Ah receptor and NFκB interactions: mechanisms and physiological implications. Chem Biol Interact 141:97–115

    Article  CAS  Google Scholar 

  • Vogel CF, Matsumura F (2008a) A new cross-talk between the aryl hydrocarbon receptor and RelB, a member of the NF-kappaB family. Biochem Pharmacol. doi:10.1016/j.bcp.2008.09.036

    Google Scholar 

  • Vogel CFA, Matsumura F (2008b) A new crosstalk between the Aryl hydrocarbon receptor and RelB, a member of the NFκB family. Biochem Pharmacol. doi:10.1016/j.bcp.2008.09.036

    Google Scholar 

  • von Mutius E, Sherrill DL, Fritzsch C, Martinez FD, Lebowitz MD (1995) Air pollution and upper respiratory symptoms in children from East Germany. Eur Respir J 8:723–728

    Google Scholar 

  • Wenger D, Gerecke AC, Heeb NV, Zennegg M, Kohler M, Naegeli H, Zenobi R (2008) Secondary effects of catalytic diesel particulate filters: reduced aryl hydrocarbon receptor-mediated activity of the exhaust. Environ Sci Technol 42:2992–2998

    Article  CAS  Google Scholar 

  • Wichmann HE, Mueller W, Allhoff P, Beckmann M, Bocter N, Csicsaky MJ, Jung M, Molik B, Schoeneberg G (1989) Health effects during a smog episode in West Germany in 1985. Environ Health Perspect 79:89–99

    Article  CAS  Google Scholar 

  • Wright JR (2005) Immunoregulatory functions of surfactant proteins. Nature 5:58–68

    CAS  Google Scholar 

  • Yang H-M, Antonini JM, Barger MW, Butterworth L, Roberts JR, Ma JKH, Castranova V, Ma JYC (2001) Diesel exhaust particles suppress macrophage function and slow the pulmonary clearance of Listeria monocytogenes in rats. Environ Health Perspect 109(5):515–521

    Article  CAS  Google Scholar 

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Acknowledgement

We appreciate the excellent technical help from Aline Gierschke.

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Correspondence to Kerstin Ulrich.

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Responsible editor: Markus Hecker

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Ulrich, K., Wölfle, S., Mayer, A. et al. Extractable organic matter of Standard Reference Material 1649a influences immunological response induced by pathogen-associated molecular patterns. Environ Sci Pollut Res 17, 1257–1267 (2010). https://doi.org/10.1007/s11356-010-0305-3

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