The Effect of Chronic Exposure of Graphene Nanoplates on the Viability and Motility of A549 Cells

. 2022 Jun 16 ; 12 (12) : . [epub] 20220616

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35745421

Grantová podpora
CZ.02.1.01/0.0/0.0/17_048/0007421 ERDF-Project Strengthening interdisciplinary cooperation in research of nanomaterials and their effects on living organisms

Graphene and its derivatives are popular nanomaterials used worldwide in many technical fields and biomedical applications. Due to such massive use, their anticipated accumulation in the environment is inevitable, with a largely unknown chronic influence on living organisms. Although repeatedly tested in chronic in vivo studies, long-term cell culture experiments that explain the biological response to these nanomaterials are still scarce. In this study, we sought to evaluate the biological responses of established model A549 tumor cells exposed to a non-toxic dose of pristine graphene for eight weeks. Our results demonstrate that the viability of the A549 cells exposed to the tested graphene did not change as well as the rate of their growth and proliferation despite nanoplatelet accumulation inside the cells. In addition, while the enzymatic activity of mitochondrial dehydrogenases moderately increased in exposed cells, their overall mitochondrial damage along with energy production changes was also not detected. Conversely, chronic accumulation of graphene nanoplates in exposed cells was detected, as evidenced by electron microscopy associated with impaired cellular motility.

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Sang M., Shin J., Kim K., Yu K.J. Electronic and Thermal Properties of Graphene and Recent Advances in Graphene Based Electronics Applications. Nanomaterials. 2019;9:374. doi: 10.3390/nano9030374. PubMed DOI PMC

Mahmoudi T., Wang Y., Hahn Y.B. Graphene and its derivatives for solar cells application. Nano Energy. 2018;47:51–65. doi: 10.1016/j.nanoen.2018.02.047. DOI

Fahimi A., Jurewicz I., Smith R.J., Sharrock C.S., Bradley D.A., Henley S.J., Coleman J.N., Dalton A.B. Density controlled conductivity of pristine graphene films. Carbon. 2013;64:435–443. doi: 10.1016/j.carbon.2013.07.096. DOI

Ou L.L., Song B., Liang H.M., Liu J., Feng X.L., Deng B., Sun T., Shao L.Q. Toxicity of graphene-family nanoparticles: A general review of the origins and mechanisms. Part. Fibre Toxicol. 2016;13:57. doi: 10.1186/s12989-016-0168-y. PubMed DOI PMC

Rodriguez-Perez L., Herranz M.A., Martin N. The chemistry of pristine graphene. Chem. Commun. 2013;49:3721–3735. doi: 10.1039/c3cc38950b. PubMed DOI

Yan M.D. Pristine graphene: Functionalization, fabrication, and nanocomposite materials. Xvi Meet. Phys. 2018;1143 doi: 10.1088/1742-6596/1143/1/012012. DOI

Magne T.M., de Oliveira Vieira T., Alencar L.M.R., Junior F.F.M., Gemini-Piperni S., Carneiro S.V., Fechine L., Freire R.M., Golokhvast K., Metrangolo P., et al. Graphene and its derivatives: Understanding the main chemical and medicinal chemistry roles for biomedical applications. J. Nanostructure Chem. 2021;9:1–35. doi: 10.1007/s40097-021-00444-3. PubMed DOI PMC

Woltornist S.J., Oyer A.J., Carrillo J.M.Y., Dobrynin A.V., Adamson D.H. Conductive Thin Films of Pristine Graphene by Solvent Interface Trapping. Acs Nano. 2013;7:7062–7066. doi: 10.1021/nn402371c. PubMed DOI

Yang K., Feng L.Z., Shi X.Z., Liu Z. Nano-graphene in biomedicine: Theranostic applications. Chem. Soc. Rev. 2013;42:530–547. doi: 10.1039/C2CS35342C. PubMed DOI

Yang K., Zhang S., Zhang G., Sun X., Lee S.T., Liu Z. Graphene in mice: Ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett. 2010;10:3318–3323. doi: 10.1021/nl100996u. PubMed DOI

Guo X., Mei N. Assessment of the toxic potential of graphene family nanomaterials. J. Food Drug Anal. 2014;22:105–115. doi: 10.1016/j.jfda.2014.01.009. PubMed DOI PMC

Liao C., Li Y., Tjong S.C. Graphene Nanomaterials: Synthesis, Biocompatibility, and Cytotoxicity. Int. J. Mol. Sci. 2018;19:3564. doi: 10.3390/ijms19113564. PubMed DOI PMC

Lee Y.S., Sung J.H., Song K.S., Kim J.K., Choi B.S., Yu I.J., Park J.D. Derivation of occupational exposure limits for multi-walled carbon nanotubes and graphene using subchronic inhalation toxicity data and a multi-path particle dosimetry model. Toxicol. Res. 2019;8:580–586. doi: 10.1039/C9TX00026G. PubMed DOI PMC

Pelin M., Sosa S., Prato M., Tubaro A. Occupational exposure to graphene based nanomaterials: Risk assessment. Nanoscale. 2018;10:15894–15903. doi: 10.1039/C8NR04950E. PubMed DOI

Spinazze A., Cattaneo A., Borghi F., Del Buono L., Campagnolo D., Rovelli S., Cavallo D.M. Probabilistic approach for the risk assessment of nanomaterials: A case study for graphene nanoplatelets. Int. J. Hyg. Environ. Health. 2019;222:76–83. doi: 10.1016/j.ijheh.2018.08.011. PubMed DOI

Ursini C.L., Fresegna A.M., Ciervo A., Maiello R., Del Frate V., Folesani G., Galetti M., Poli D., Buresti G., Di Cristo L., et al. Occupational exposure to graphene and silica nanoparticles. Part II: Pilot study to identify a panel of sensitive biomarkers of genotoxic, oxidative and inflammatory effects on suitable biological matrices. Nanotoxicology. 2021;15:223–237. doi: 10.1080/17435390.2020.1850903. PubMed DOI

Falagan-Lotsch P., Grzincic E.M., Murphy C.J. One low-dose exposure of gold nanoparticles induces long-term changes in human cells. Proc. Natl. Acad. Sci. USA. 2016;113:13318–13323. doi: 10.1073/pnas.1616400113. PubMed DOI PMC

Mohammadinejad R., Moosavi M.A., Tavakol S., Vardar D.O., Hosseini A., Rahmati M., Dini L., Hussain S., Mandegary A., Klionsky D.J. Necrotic, apoptotic and autophagic cell fates triggered by nanoparticles. Autophagy. 2019;15:4–33. doi: 10.1080/15548627.2018.1509171. PubMed DOI PMC

Mrakovcic M., Absenger M., Riedl R., Smole C., Roblegg E., Frohlich L.F., Frohlich E. Assessment of long-term effects of nanoparticles in a microcarrier cell culture system. PLoS ONE. 2013;8:e56791. doi: 10.1371/journal.pone.0056791. PubMed DOI PMC

Svadlakova T., Hubatka F., Turanek Knotigova P., Kulich P., Masek J., Kotoucek J., Macak J., Motola M., Kalbac M., Kolackova M., et al. Proinflammatory Effect of Carbon-Based Nanomaterials: In Vitro Study on Stimulation of Inflammasome NLRP3 via Destabilisation of Lysosomes. Nanomaterials. 2020;10:418. doi: 10.3390/nano10030418. PubMed DOI PMC

Svadlakova T., Kolackova M., Vankova R., Karakale R., Malkova A., Kulich P., Hubatka F., Turanek-Knotigova P., Kratochvilova I., Raska M., et al. Carbon-Based Nanomaterials Increase Reactivity of Primary Monocytes towards Various Bacteria and Modulate Their Differentiation into Macrophages. Nanomaterials. 2021;11:2510. doi: 10.3390/nano11102510. PubMed DOI PMC

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC

Cechakova L., Ondrej M., Pavlik V., Jost P., Cizkova D., Bezrouk A., Pejchal J., Amaravadi R.K., Winkler J.D., Tichy A. A Potent Autophagy Inhibitor (Lys05) Enhances the Impact of Ionizing Radiation on Human Lung Cancer Cells H1299. Int. J. Mol. Sci. 2019;20:5881. doi: 10.3390/ijms20235881. PubMed DOI PMC

Barosova H., Meldrum K., Karakocak B.B., Balog S., Doak S.H., Petri-Fink A., Clift M.J.D., Rothen-Rutishauser B. Inter-laboratory variability of A549 epithelial cells grown under submerged and air-liquid interface conditions. Toxicol. In Vitro. 2021;75:105178. doi: 10.1016/j.tiv.2021.105178. PubMed DOI

Foster K.A., Oster C.G., Mayer M.M., Avery M.L., Audus K.L. Characterization of the A549 cell line as a type II pulmonary epithelial cell model for drug metabolism. Exp. Cell. Res. 1998;243:359–366. doi: 10.1006/excr.1998.4172. PubMed DOI

Halim N.H.A., Zakaria N., Satar N.A., Yahaya B.H. Isolation and Characterization of Cancer Stem Cells of the Non-Small-Cell Lung Cancer (A549) Cell Line. Methods Mol. Biol. 2016;1516:371–388. doi: 10.1007/7651_2016_326. PubMed DOI

Chang Y., Yang S.T., Liu J.H., Dong E., Wang Y., Cao A., Liu Y., Wang H. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol. Lett. 2011;200:201–210. doi: 10.1016/j.toxlet.2010.11.016. PubMed DOI

Jin C., Wang F., Tang Y., Zhang X., Wang J., Yang Y. Distribution of graphene oxide and TiO2-graphene oxide composite in A549 cells. Biol. Trace. Elem. Res. 2014;159:393–398. doi: 10.1007/s12011-014-0027-3. PubMed DOI

Liao Y., Wang W., Huang X., Sun Y., Tian S., Cai P. Reduced graphene oxide triggered epithelial-mesenchymal transition in A549 cells. Sci. Rep. 2018;8:15188. doi: 10.1038/s41598-018-33414-x. PubMed DOI PMC

Wu B., Wu J.L., Liu S., Shen Z.Y., Chen L., Zhang X.X., Ren H.Q. Combined effects of graphene oxide and zinc oxide nanoparticle on human A549 cells: Bioavailability, toxicity and mechanisms. Environ. Sci. Nano. 2019;6:635–645. doi: 10.1039/C8EN00965A. DOI

Carreño E.A., Alberto A.V.P., de Souza C.A.M., de Mello H.L., Henriques-Pons A., Anastacio Alves L. Considerations and Technical Pitfalls in the Employment of the MTT Assay to Evaluate Photosensitizers for Photodynamic Therapy. Appl. Sci. 2021;11:2603. doi: 10.3390/app11062603. DOI

Jiao G.Z., He X., Li X., Qiu J.Q., Xu H.Y., Zhang N., Liu S.M. Limitations of MTT and CCK-8 assay for evaluation of graphene cytotoxicity. Rsc Adv. 2015;5:53240–53244. doi: 10.1039/C5RA08958A. DOI

Malkova A., Svadlakova T., Singh A., Kolackova M., Vankova R., Borsky P., Holmannova D., Karas A., Borska L., Fiala Z. In Vitro Assessment of the Genotoxic Potential of Pristine Graphene Platelets. Nanomaterials. 2021;11:2210. doi: 10.3390/nano11092210. PubMed DOI PMC

Rampersad S.N. Multiple applications of Alamar Blue as an indicator of metabolic function and cellular health in cell viability bioassays. Sensors. 2012;12:12347–12360. doi: 10.3390/s120912347. PubMed DOI PMC

Calabrese E.J., Bachmann K.A., Bailer A.J., Bolger P.M., Borak J., Cai L., Cedergreen N., Cherian M.G., Chiueh C.C., Clarkson T.W., et al. Biological stress response terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. Toxicol. Appl. Pharmacol. 2007;222:122–128. doi: 10.1016/j.taap.2007.02.015. PubMed DOI

Sanchez V.C., Jachak A., Hurt R.H., Kane A.B. Biological interactions of graphene-family nanomaterials: An interdisciplinary review. Chem. Res. Toxicol. 2012;25:15–34. doi: 10.1021/tx200339h. PubMed DOI PMC

Kucki M., Diener L., Bohmer N., Hirsch C., Krug H.F., Palermo V., Wick P. Uptake of label-free graphene oxide by Caco-2 cells is dependent on the cell differentiation status. J. Nanobiotechnol. 2017;15:46. doi: 10.1186/s12951-017-0280-7. PubMed DOI PMC

Li Y.F., Yuan H.Y., von dem Bussche A., Creighton M., Hurt R.H., Kane A.B., Gao H.J. Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites. Proc. Natl. Acad. Sci. USA. 2013;110:12295–12300. doi: 10.1073/pnas.1222276110. PubMed DOI PMC

Jaworski S., Sawosz E., Grodzik M., Winnicka A., Prasek M., Wierzbicki M., Chwalibog A. In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. Int. J. Nanomed. 2013;8:413–420. doi: 10.2147/IJN.S39456. PubMed DOI PMC

Wan B., Wang Z.X., Lv Q.Y., Dong P.X., Zhao L.X., Yang Y., Guo L.H. Single-walled carbon nanotubes and graphene oxides induce autophagosome accumulation and lysosome impairment in primarily cultured murine peritoneal macrophages. Toxicol. Lett. 2013;221:118–127. doi: 10.1016/j.toxlet.2013.06.208. PubMed DOI

Chen G.Y., Chen C.L., Tuan H.Y., Yuan P.X., Li K.C., Yang H.J., Hu Y.C. Graphene oxide triggers toll-like receptors/autophagy responses in vitro and inhibits tumor growth in vivo. Adv. Healthc. Mater. 2014;3:1486–1495. doi: 10.1002/adhm.201300591. PubMed DOI

Chen G.Y., Yang H.J., Lu C.H., Chao Y.C., Hwang S.M., Chen C.L., Lo K.W., Sung L.Y., Luo W.Y., Tuan H.Y., et al. Simultaneous induction of autophagy and toll-like receptor signaling pathways by graphene oxide. Biomaterials. 2012;33:6559–6569. doi: 10.1016/j.biomaterials.2012.05.064. PubMed DOI

Liu Y., Wang X., Wang J., Nie Y., Du H., Dai H., Wang J., Wang M., Chen S., Hei T.K., et al. Graphene Oxide Attenuates the Cytotoxicity and Mutagenicity of PCB 52 via Activation of Genuine Autophagy. Environ. Sci. Technol. 2016;50:3154–3164. doi: 10.1021/acs.est.5b03895. PubMed DOI

Park E.J., Lee G.H., Han B.S., Lee B.S., Lee S., Cho M.H., Kim J.H., Kim D.W. Toxic response of graphene nanoplatelets in vivo and in vitro. Arch. Toxicol. 2015;89:1557–1568. doi: 10.1007/s00204-014-1303-x. PubMed DOI

Park S.Y., Song W.C., Kim B., Oh J.W., Park G. Nano-Graphene Oxide-Promoted Epithelial-Mesenchymal Transition of Human Retinal Pigment Epithelial Cells through Regulation of Phospholipase D Signaling. Nanomaterials. 2021;11:2546. doi: 10.3390/nano11102546. PubMed DOI PMC

Park J., Kravchuk P., Krishnaprasad A., Roy T., Kang E.H. Graphene Enhances Actin Filament Assembly Kinetics and Modulates NIH-3T3 Fibroblast Cell Spreading. Int. J. Mol. Sci. 2022;23:509. doi: 10.3390/ijms23010509. PubMed DOI PMC

Mukhopadhyay A., Basu S., Singha S., Patra H.K. Inner-View of Nanomaterial Incited Protein Conformational Changes: Insights into Designable Interaction. Research. 2018;2018:9712832. doi: 10.1155/2018/9712832. PubMed DOI PMC

Sasidharan A., Panchakarla L.S., Chandran P., Menon D., Nair S., Rao C.N., Koyakutty M. Differential nano-bio interactions and toxicity effects of pristine versus functionalized graphene. Nanoscale. 2011;3:2461–2464. doi: 10.1039/c1nr10172b. PubMed DOI

Zhou H.J., Zhao K., Li W., Yang N., Liu Y., Chen C.Y., Wei T.T. The interactions between pristine graphene and macrophages and the production of cytokines/chemokines via TLR- and NF-kappa B-related signaling pathways. Biomaterials. 2012;33:6933–6942. doi: 10.1016/j.biomaterials.2012.06.064. PubMed DOI

Li T., Oloyede A., Gu Y.T. Adhesive characteristics of low dimensional carbon nanomaterial on actin. Appl. Phys. Lett. 2014;104:023702. doi: 10.1063/1.4862200. DOI

Zhou H., Zhang B., Zheng J., Yu M., Zhou T., Zhao K., Jia Y., Gao X., Chen C., Wei T. The inhibition of migration and invasion of cancer cells by graphene via the impairment of mitochondrial respiration. Biomaterials. 2014;35:1597–1607. doi: 10.1016/j.biomaterials.2013.11.020. PubMed DOI

Sonnemann K.J., Bement W.M. Wound repair: Toward understanding and integration of single-cell and multicellular wound responses. Annu. Rev. Cell. Dev. Biol. 2011;27:237–263. doi: 10.1146/annurev-cellbio-092910-154251. PubMed DOI PMC

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