Screening of Cellular Stress Responses Induced by Ambient Aerosol Ultrafine Particle Fraction PM0.5 in A549 Cells

. 2019 Dec 13 ; 20 (24) : . [epub] 20191213

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31847237

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

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.

Zobrazit více v PubMed

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...