Screening of Cellular Stress Responses Induced by Ambient Aerosol Ultrafine Particle Fraction PM0.5 in A549 Cells
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/0.0/0.0/15_003/0000495
Ministerstvo Školství, Mládeže a Tělovýchovy
P503-12-G147
Grantová Agentura České Republiky
PubMed
31847237
PubMed Central
PMC6940800
DOI
10.3390/ijms20246310
PII: ijms20246310
Knihovny.cz E-zdroje
- Klíčová slova
- AhR, PM0.5, early stress response, eicosanoids, inflammation, p53, ultrafine particulate matter, unfolded protein response (UPR),
- MeSH
- aerosoly MeSH
- buňky A549 MeSH
- epitelové buňky metabolismus patologie MeSH
- látky znečišťující vzduch toxicita MeSH
- lidé MeSH
- pevné částice toxicita MeSH
- plíce metabolismus patologie MeSH
- regulace genové exprese účinky léků MeSH
- signální transdukce účinky léků MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- aerosoly MeSH
- látky znečišťující vzduch MeSH
- pevné částice MeSH
Effects of airborne particles on the expression status of markers of cellular toxic stress and on the release of eicosanoids, linked with inflammation and oxidative damage, remain poorly characterized. Therefore, we proposed a set of various methodological approaches in order to address complexity of PM0.5-induced toxicity. For this purpose, we used a well-characterized model of A549 pulmonary epithelial cells exposed to a non-cytotoxic concentration of ambient aerosol particle fraction PM0.5 for 24 h. Electron microscopy confirmed accumulation of PM0.5 within A549 cells, yet, autophagy was not induced. Expression profiles of various cellular stress response genes that have been previously shown to be involved in early stress responses, namely unfolded protein response, DNA damage response, and in aryl hydrocarbon receptor (AhR) and p53 signaling, were analyzed. This analysis revealed induction of GREM1, EGR1, CYP1A1, CDK1A, PUMA, NOXA and GDF15 and suppression of SOX9 in response to PM0.5 exposure. Analysis of eicosanoids showed no oxidative damage and only a weak anti-inflammatory response. In conclusion, this study helps to identify novel gene markers, GREM1, EGR1, GDF15 and SOX9, that may represent a valuable tool for routine testing of PM0.5-induced in vitro toxicity in lung epithelial cells.
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IARC . Outdoor Air Pollution. Volume 109 IARC; Lyon, France: 2015. Monographs on the evaluation of carcinogenic risks to humans. PubMed PMC
Oberdorster G., Oberdorster E., Oberdorster J. Nanotoxicology: An emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 2005;113:823–839. doi: 10.1289/ehp.7339. PubMed DOI PMC
Gualtieri M., Mantecca P., Corvaja V., Longhin E., Perrone M.G., Bolzacchini E., Camatini M. Winter fine particulate matter from Milan induces morphological and functional alterations in human pulmonary epithelial cells (A549) Toxicol. Lett. 2009;188:52–62. doi: 10.1016/j.toxlet.2009.03.003. PubMed DOI
Longhin E., Capasso L., Battaglia C., Proverbio M.C., Cosentino C., Cifola I., Mangano E., Camatini M., Gualtieri M. Integrative transcriptomic and protein analysis of human bronchial BEAS-2B exposed to seasonal urban particulate matter. Environ. Pollut. 2016;209:87–98. doi: 10.1016/j.envpol.2015.11.013. PubMed DOI
Longhin E., Holme J.A., Gutzkow K.B., Arlt V.M., Kucab J.E., Camatini M., Gualtieri M. Cell cycle alterations induced by urban PM2.5 in bronchial epithelial cells: Characterization of the process and possible mechanisms involved. Part. Fibre Toxicol. 2013;10:63. doi: 10.1186/1743-8977-10-63. PubMed DOI PMC
Gualtieri M., Longhin E., Mattioli M., Mantecca P., Tinaglia V., Mangano E., Proverbio M.C., Bestetti G., Camatini M., Battaglia C. Gene expression profiling of A549 cells exposed to Milan PM2.5. Toxicol. Lett. 2012;209:136–145. doi: 10.1016/j.toxlet.2011.11.015. PubMed DOI
Deng X., Feng N., Zheng M., Ye X., Lin H., Yu X., Gan Z., Fang Z., Zhang H., Gao M., et al. PM2.5 exposure-induced autophagy is mediated by lncRNA loc146880 which also promotes the migration and invasion of lung cancer cells. Biochim. Biophys. Acta Gen. Subj. 2017;1861:112–125. doi: 10.1016/j.bbagen.2016.11.009. PubMed DOI
Reibman J., Hsu Y., Chen L.C., Kumar A., Su W.C., Choy W., Talbot A., Gordon T. Size fractions of ambient particulate matter induce granulocyte macrophage colony-stimulating factor in human bronchial epithelial cells by mitogen-activated protein kinase pathways. Am. J. Respir. Cell Mol. Biol. 2002;27:455–462. doi: 10.1165/rcmb.2001-0005OC. PubMed DOI
Jalava P.I., Salonen R.O., Halinen A.I., Penttinen P., Pennanen A.S., Sillanpaa M., Sandell E., Hillamo R., Hirvonen M.R. In vitro inflammatory and cytotoxic effects of size-segregated particulate samples collected during long-range transport of wildfire smoke to Helsinki. Toxicol. Appl. Pharmacol. 2006;215:341–353. doi: 10.1016/j.taap.2006.03.007. PubMed DOI
Jalava P.I., Wang Q., Kuuspalo K., Ruusunen J., Hao L., Fang D., Väisänen O., Ruuskanen A., Sippula O., Happo M.S., et al. Day and night variation in chemical composition and toxicological responses of size segregated urban air PM samples in a high air pollution situation. Atmos. Environ. 2015;120:427–437. doi: 10.1016/j.atmosenv.2015.08.089. DOI
Ramgolam K., Favez O., Cachier H., Gaudichet A., Marano F., Martinon L., Baeza-Squiban A. Size-partitioning of an urban aerosol to identify particle determinants involved in the proinflammatory response induced in airway epithelial cells. Part. Fibre Toxicol. 2009;6:10. doi: 10.1186/1743-8977-6-10. PubMed DOI PMC
Thomson E.M., Breznan D., Karthikeyan S., MacKinnon-Roy C., Charland J.P., Dabek-Zlotorzynska E., Celo V., Kumarathasan P., Brook J.R., Vincent R. Cytotoxic and inflammatory potential of size-fractionated particulate matter collected repeatedly within a small urban area. Part. Fibre Toxicol. 2015;12:24. doi: 10.1186/s12989-015-0099-z. PubMed DOI PMC
Mittal S., Sharma P.K., Tiwari R., Rayavarapu R.G., Shankar J., Chauhan L.K.S., Pandey A.K. Impaired lysosomal activity mediated autophagic flux disruption by graphite carbon nanofibers induce apoptosis in human lung epithelial cells through oxidative stress and energetic impairment. Part. Fibre Toxicol. 2017;14:15. doi: 10.1186/s12989-017-0194-4. PubMed DOI PMC
Stern S.T., Adiseshaiah P.P., Crist R.M. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part. Fibre Toxicol. 2012;9:20. doi: 10.1186/1743-8977-9-20. PubMed DOI PMC
Cao Y., Long J.M., Liu L.L., He T., Jiang L.Y., Zhao C.X., Li Z. A review of endoplasmic reticulum (ER) stress and nanoparticle (NP) exposure. Life Sci. 2017;186:33–42. doi: 10.1016/j.lfs.2017.08.003. PubMed DOI
Fulda S., Gorman A.M., Hori O., Samali A. Cellular stress responses: Cell survival and cell death. Int. J. Cell Biol. 2010;2010:214074. doi: 10.1155/2010/214074. PubMed DOI PMC
Marvanova S., Kulich P., Skoupy R., Hubatka F., Ciganek M., Bendl J., Hovorka J., Machala M. Size-segregated urban aerosol characterization by electron microscopy and dynamic light scattering and influence of sample preparation. Atmos. Environ. 2018;178:181–190. doi: 10.1016/j.atmosenv.2018.02.004. DOI
Zhang J.D., Berntenis N., Roth A., Ebeling M. Data mining reveals a network of early-response genes as a consensus signature of drug-induced in vitro and in vivo toxicity. Pharmacogen. J. 2014;14:208–216. doi: 10.1038/tpj.2013.39. PubMed DOI PMC
Prochazkova J., Strapacova S., Svrzkova L., Andrysik Z., Hyzd’alova M., Hruba E., Pencikova K., Libalova H., Topinka J., Klema J., et al. Adaptive changes in global gene expression profile of lung carcinoma A549 cells acutely exposed to distinct types of AhR ligands. Toxicol. Lett. 2018;292:162–174. doi: 10.1016/j.toxlet.2018.04.024. PubMed DOI
Chu L., Wang T., Hu Y., Gu Y., Su Z., Jiang H. Activation of Egr-1 in human lung epithelial cells exposed to silica through MAPKs signaling pathways. PLoS ONE. 2013;8:e68943. doi: 10.1371/journal.pone.0068943. PubMed DOI PMC
Yan F., Wu Y., Liu H., Wu Y., Shen H., Li W. ATF3 is positively involved in particulate matter-induced airway inflammation in vitro and in vivo. Toxicol. Lett. 2018;287:113–121. doi: 10.1016/j.toxlet.2018.01.022. PubMed DOI
Clark B.J., Bull T.M., Benson A.B., Stream A.R., Macht M., Gaydos J., Meadows C., Burnham E.L., Moss M., Investigators A.N. Growth differentiation factor-15 and prognosis in acute respiratory distress syndrome: A retrospective cohort study. Crit. Care. 2013;17:R92. doi: 10.1186/cc12737. PubMed DOI PMC
Bhattacharyya S., Fang F., Tourtellotte W., Varga J. Egr-1: New conductor for the tissue repair orchestra directs harmony (regeneration) or cacophony (fibrosis) J. Pathol. 2013;229:286–297. doi: 10.1002/path.4131. PubMed DOI PMC
Hai T., Wolford C.C., Chang Y.S. ATF3, a hub of the cellular adaptive-response network, in the pathogenesis of diseases: Is modulation of inflammation a unifying component? Gene Expr. J. Liver Res. 2010;15:1–11. doi: 10.3727/105221610X12819686555015. PubMed DOI PMC
Rohini M., Haritha Menon A., Selvamurugan N. Role of activating transcription factor 3 and its interacting proteins under physiological and pathological conditions. Int. J. Biol. Macromol. 2018;120:310–317. doi: 10.1016/j.ijbiomac.2018.08.107. PubMed DOI
Tiwari K.K., Moorthy B., Lingappan K. Role of GDF15 (growth and differentiation factor 15) in pulmonary oxygen toxicity. Toxicol. Vitr. 2015;29:1369–1376. doi: 10.1016/j.tiv.2015.05.008. PubMed DOI PMC
Wallentin L., Hijazi Z., Andersson U., Alexander J.H., De Caterina R., Hanna M., Horowitz J.D., Hylek E.M., Lopes R.D., Asberg S., et al. Growth differentiation factor 15, a marker of oxidative stress and inflammation, for risk assessment in patients with atrial fibrillation insights from the Apixaban for Reduction in Stroke and Other Thromboembolic Events in Atrial Fibrillation (ARISTOTLE) trial. Circulation. 2014;130:1847–1858. PubMed
Kannan K., Amariglio N., Rechavi G., Givol D. Profile of gene expression regulated by induced p53: Connection to the TGF-beta family. FEBS Lett. 2000;470:77–82. doi: 10.1016/S0014-5793(00)01291-6. PubMed DOI
Rynning I., Neca J., Vrbova K., Libalova H., Rossner P., Holme J.A., Gutzkow K.B., Afanou A.K.J., Arnoldussen Y.J., Hruba E., et al. In vitro transformation of human bronchial epithelial cells by diesel exhaust particles: Gene expression profiling and early toxic responses. Toxicol. Sci. 2018;166:51–64. doi: 10.1093/toxsci/kfy183. PubMed DOI PMC
Wang D.Z., Dubois R.N. Eicosanoids and cancer. Nat. Rev. Cancer. 2010;10:181–193. doi: 10.1038/nrc2809. PubMed DOI PMC
Hruba E., Trilecova L., Marvanova S., Krcmar P., Vykopalova L., Milcova A., Libalova H., Topinka J., Starsichova A., Soucek K., et al. Genotoxic polycyclic aromatic hydrocarbons fail to induce the p53-dependent DNA damage response, apoptosis or cell-cycle arrest in human prostate carcinoma LNCaP cells. Toxicol. Lett. 2010;197:227–235. doi: 10.1016/j.toxlet.2010.06.004. PubMed DOI
Albino A.P., Huang X., Jorgensen E., Yang J., Gietl D., Traganos F., Darzynkiewicz Z. Induction of H2AX phosphorylation in pulmonary cells by tobacco smoke: A new assay for carcinogens. Cell Cycle. 2004;3:1062–1068. doi: 10.4161/cc.3.8.988. PubMed DOI
Zamarbide M., Martinez-Pinilla E., Ricobaraza A., Aragon T., Franco R., Perez-Mediavilla A. Phenyl acyl acids attenuate the unfolded protein response in tunicamycin-treated neuroblastoma cells. PLoS ONE. 2013;8:e71082. doi: 10.1371/journal.pone.0071082. PubMed DOI PMC
Simmons S.O., Fan C.Y., Ramabhadran R. Cellular stress response pathway system as a sentinel ensemble in toxicological screening. Toxicol. Sci. 2009;111:202–225. doi: 10.1093/toxsci/kfp140. PubMed DOI
Etteieb S., Kawachi A., Han J., Elayni F., Tarhouni J., Isoda H. Assessment of organic micropollutants occurrence in treated wastewater using heat shock protein 47 stress responses in Chinese hamster ovary cells and GC/MS-based non-target screening. Water Sci. Technol. 2016;74:2407–2416. doi: 10.2166/wst.2016.426. PubMed DOI
Wink S., Hiemstra S.W., Huppelschoten S., Klip J.E., van de Water B. Dynamic imaging of adaptive stress response pathway activation for prediction of drug induced liver injury. Arch. Toxicol. 2018;92:1797–1814. doi: 10.1007/s00204-018-2178-z. PubMed DOI PMC
Zhao D.Y., Jacobs K.M., Hallahan D.E., Thotala D. Silencing Egr1 attenuates radiation-induced apoptosis in normal tissues while killing cancer cells and delaying tumor growth. Mol. Cancer Ther. 2015;14:2343–2352. doi: 10.1158/1535-7163.MCT-14-1051. PubMed DOI PMC
Chang Y., Lee H.H., Chen Y.T., Lu J., Wu S.Y., Chen C.W., Takada K., Tsai C.H. Induction of the early growth response 1 gene by Epstein-Barr virus lytic transactivator Zta. J. Virol. 2006;80:7748–7755. doi: 10.1128/JVI.02608-05. PubMed DOI PMC
Martinez J.M., Baek S.J., Mays D.M., Tithof P.K., Eling T.E., Walker N.J. EGR1 is a novel target for AhR agonists in human lung epithelial cells. Toxicol. Sci. 2004;82:429–435. doi: 10.1093/toxsci/kfh272. PubMed DOI
Brauze D., Zawierucha P., Kiwerska K., Bednarek K., Oleszak M., Rydzanicz M., Jarmuz-Szymczak M. Induction of expression of aryl hydrocarbon receptor-dependent genes in human HepaRG cell line modified by shRNA and treated with beta-naphthoflavone. Mol. Cell Biochem. 2017;425:59–75. doi: 10.1007/s11010-016-2862-3. PubMed DOI PMC
Reynolds P.R., Cosio M.G., Hoidal J.R. Cigarette smoke-induced Egr-1 upregulates proinflammatory cytokines in pulmonary epithelial cells. Am. J. Respir. Cell Mol. Biol. 2006;35:314–319. doi: 10.1165/rcmb.2005-0428OC. PubMed DOI PMC
Shen N., Gong T., Wang J.D., Meng F.L., Qiao L., Yang R.L., Xue B., Pan F.Y., Zhou X.J., Chen H.Q., et al. Cigarette smoke-induced pulmonary inflammatory responses are mediated by EGR-1/GGPPS/MAPK signaling. Am. J. Pathol. 2011;178:110–118. doi: 10.1016/j.ajpath.2010.11.016. PubMed DOI PMC
Li C.J., Ning W., Matthay M.A., Feghali-Bostwick C.A., Choi A.M. MAPK pathway mediates EGR-1-HSP70-dependent cigarette smoke-induced chemokine production. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007;292:L1297–L1303. doi: 10.1152/ajplung.00194.2006. PubMed DOI
Sarill M., Zago M., Sheridan J.A., Nair P., Matthews J., Gomez A., Roussel L., Rousseau S., Hamid Q., Eidelman D.H., et al. The aryl hydrocarbon receptor suppresses cigarette-smoke-induced oxidative stress in association with dioxin response element (DRE)-independent regulation of sulfiredoxin 1. Free Radic. Biol. Med. 2015;89:342–357. doi: 10.1016/j.freeradbiomed.2015.08.007. PubMed DOI
Jiang G., Liu C.T., Zhang W.D. IL-17a and GDF15 are able to induce epithelial-mesenchymal transition of lung epithelial cells in response to cigarette smoke. Exp. Ther. Med. 2018;16:12–20. doi: 10.3892/etm.2018.6145. PubMed DOI PMC
Menendez D., Inga A., Resnick M.A. The expanding universe of p53 targets. Nat. Rev. Cancer. 2009;9:724–737. doi: 10.1038/nrc2730. PubMed DOI
Li Z.D., Wang K., Yang X.W., Zhuang Z.G., Wang J.J., Tong X.W. Expression of aryl hydrocarbon receptor in relation to p53 status and clinicopathological parameters in breast cancer. Int. J. Clin. Exp. Pathol. 2014;7:7931–7937. PubMed PMC
Kochhar A., Kopelovich L., Sue E., Guttenplan J.B., Herbert B.S., Dannenberg A.J., Subbaramaiah K. P53 modulates Hsp90 ATPase activity and regulates aryl hydrocarbon receptor signaling. Cancer Prev. Res. (Phila) 2014;7:596–606. doi: 10.1158/1940-6207.CAPR-14-0051. PubMed DOI PMC
Li X.B., Zhou X.X., Li Y.W., Zu L.L., Pan H.L., Liu B.N., Shen W., Fan Y.G., Zhou Q.H. Activating transcription factor 3 promotes malignance of lung cancer cells in vitro. Thorac. Cancer. 2017;8:181–191. doi: 10.1111/1759-7714.12421. PubMed DOI PMC
Fan F., Jin S., Amundson S.A., Tong T., Fan W., Zhao H., Zhu X., Mazzacurati L., Li X., Petrik K.L., et al. ATF3 induction following DNA damage is regulated by distinct signaling pathways and over-expression of ATF3 protein suppresses cells growth. Oncogene. 2002;21:7488–7496. doi: 10.1038/sj.onc.1205896. PubMed DOI
Harizi H., Corcuff J.B., Gualde N. Arachidonic-acid-derived eicosanoids: Roles in biology and immunopathology. Trends Mol. Med. 2008;14:461–469. doi: 10.1016/j.molmed.2008.08.005. PubMed DOI
Maayah Z.H., El-Kadi A.O.S. The role of mid-chain hydroxyeicosatetraenoic acids in the pathogenesis of hypertension and cardiac hypertrophy. Arch. Toxicol. 2016;90:119–136. doi: 10.1007/s00204-015-1620-8. PubMed DOI
Yin F., Lawal A., Ricks J., Fox J.R., Larson T., Navab M., Fogelman A.M., Rosenfeld M.E., Araujo J.A. Diesel exhaust induces systemic lipid peroxidation and development of dysfunctional pro-oxidant and pro-inflammatory high-density lipoprotein. Arterioscler. Thromb. Vasc. Biol. 2013;33:1153–1161. doi: 10.1161/ATVBAHA.112.300552. PubMed DOI
Cathcart M.C., Reynolds J.V., O’Byrne K.J., Pidgeon G.P. The role of prostacyclin synthase and thromboxane synthase signaling in the development and progression of cancer. Biochim. Biophys. Acta. 2010;1805:153–166. doi: 10.1016/j.bbcan.2010.01.006. PubMed DOI
Yoshida Y., Umeno A., Shichiri M. Lipid peroxidation biomarkers for evaluating oxidative stress and assessing antioxidant capacity in vivo. J. Clin. Biochem. Nutr. 2013;52:9–16. doi: 10.3164/jcbn.12-112. PubMed DOI PMC
Donaldson K., Tran L., Jimenez L.A., Duffin R., Newby D.E., Mills N., MacNee W., Stone V. Combustion-derived nanoparticles: A review of their toxicology following inhalation exposure. Part. Fibre Toxicol. 2005;2:10. doi: 10.1186/1743-8977-2-10. PubMed DOI PMC
Billet S., Abbas I., Le Goff J., Verdin A., Andre V., Lafargue P.E., Hachimi A., Cazier F., Sichel F., Shirali P., et al. Genotoxic potential of polycyclic aromatic hydrocarbons-coated onto airborne particulate matter (PM 2.5) in human lung epithelial A549 cells. Cancer Lett. 2008;270:144–155. doi: 10.1016/j.canlet.2008.04.044. PubMed DOI
Libalova H., Krckova S., Uhlirova K., Klema J., Ciganek M., Rossner P., Jr., Sram R.J., Vondracek J., Machala M., Topinka J. Analysis of gene expression changes in A549 cells induced by organic compounds from respirable air particles. Mutat. Res. 2014;770:94–105. doi: 10.1016/j.mrfmmm.2014.10.002. PubMed DOI
Abbas I., Badran G., Verdin A., Ledoux F., Roumie M., Lo Guidice J.M., Courcot D., Garcon G. In vitro evaluation of organic extractable matter from ambient PM2.5 using human bronchial epithelial BEAS-2B cells: Cytotoxicity, oxidative stress, pro-inflammatory response, genotoxicity, and cell cycle deregulation. Environ. Res. 2019;171:510–522. doi: 10.1016/j.envres.2019.01.052. PubMed DOI
Souček K., Malenovská A., Kahounová Z., Remšík J., Holubcová Z., Soukup T., Kurfürstová D., Bouchal J., Suchánková T., Slabáková E., et al. Presence of growth/differentiation factor-15 cytokine in human follicular fluid, granulosa cells, and oocytes. J. Assist. Reprod. Genet. 2018;35:1407–1417. doi: 10.1007/s10815-018-1230-5. PubMed DOI PMC
Van Schadewijk A., van’t Wout E.F., Stolk J., Hiemstra P.S. A quantitative method for detection of spliced x-box binding protein-1 (XBP1) mrna as a measure of endoplasmic reticulum (ER) stress. Cell Stress Chaperon. 2012;17:275–279. doi: 10.1007/s12192-011-0306-2. PubMed DOI PMC
Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C-T method. Nat. Protoc. 2008;3:1101–1108. doi: 10.1038/nprot.2008.73. PubMed DOI
Ho Sui S.J., Mortimer J.R., Arenillas D.J., Brumm J., Walsh C.J., Kennedy B.P., Wasserman W.W. Opossum: Identification of over-represented transcription factor binding sites in co-expressed genes. Nucl. Acids Res. 2005;33:3154–3164. doi: 10.1093/nar/gki624. PubMed DOI PMC
Pencikova K., Svrzkova L., Strapacova S., Neca J., Bartonkova I., Dvorak Z., Hyzdalova M., Pivnicka J., Palkova L., Lehmler H.J., et al. In vitro profiling of toxic effects of prominent environmental lower-chlorinated PCB congeners linked with endocrine disruption and tumor promotion. Environ. Pollut. 2018;237:473–486. doi: 10.1016/j.envpol.2018.02.067. PubMed DOI PMC