Abstract
Copper indium gallium diselenide (CIGS) and cadmium sulfide (CdS) nanoparticles (NP) are next generation semiconductors used in photovoltaic cells (PV). They possess high quantum efficiency, absorption coefficient, and cheaper manufacturing costs compared to silicon. Due to their potential for an industrial development and the lack of information about the risk associated in their use, we investigated the influence of the physicochemical characteristics of CIGS (9 nm) and CdS (20 nm) in relation to the induction of cytotoxicity in human alveolar A549 cells through ROS generation and mitochondrial dysfunction. CIGS induced cytotoxicity in a dose dependent manner in lower concentrations than CdS; both NP were able to induce ROS in A549. Moreover, CIGS interact directly with mitochondria inducing depolarization that leads to the induction of apoptosis compared to CdS. Antioxidant pretreatment significantly prevented the loss of mitochondrial membrane potential and cytotoxicity, suggesting ROS generation as the main cytotoxic mechanism. These results demonstrate that semiconductor characteristics of NP are crucial for the type and intensity of the cytotoxic effects. Our work provides relevant information that may help guide the production of a safer NP-based PV technologies, and would be a valuable resource on future risk assessment for a safer use of nanotechnology in the development of clean sources of renewable energy.
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References
Bagnall DM, Boreland M (2008) Photovoltaic technologies. Energy Policy 36:4390–4396. doi:10.1016/j.enpol.2008.09.070
Burello E, Worth AP (2011) A theoretical framework for predicting the oxidative stress potential of oxide nanoparticles. Nanotoxicology 5:228–235. doi:10.3109/17435390.2010.502980
Cho AK, Sioutas C, Miguel AH, Kumagai Y, Schmitz DA, Singh M, Eiguren-Fernandez A, Froines JR (2005) Redox activity of airborne particulate matter at different sites in the Los Angeles Basin. Environ Res 99:40–47
De Vizcaya-Ruiz A, Gutiérrez-Castillo ME, Uribe-Ramirez M, Cebrián ME, Mugica-Alvarez V, Sepúlveda J, Rosas I, Salinas E, Garcia-Cuéllar C, Martínez F (2006) Characterization and in vitro biological effects of concentrated particulate matter from Mexico City. Atmos Environ 40:583–592. doi:10.1016/j.atmosenv.2005.12.073
Dhere NG (2007) Toward GW/year of CIGS production within the next decade. Sol Energy Mater Sol Cells 91:1376–1382. doi:10.1016/j.solmat.2007.04.003
Dreher KL (2004) Health and environmental impact of nanotechnology: toxicological assessment of manufactured nanoparticles. Toxicol Sci 77:3–5. doi:10.1093/toxsci/kfh041
Eisenberg DA, Yu M, Lam CW, Ogunseitan OA, Schoenung JM (2013) Comparative alternative materials assessment to screen toxicity hazards in the life cycle of CIGS thin film photovoltaics. J Hazard Mater 260:534–542. doi:10.1016/j.jhazmat.2013.06.007
Escamilla-Rivera V, Uribe-Ramírez M, González-Pozos S, Lozano O, Lucas S, De Vizcaya-Ruiz A (2016) Protein corona acts as a protective shield against Fe3O4-PEG inflammation and ROS-induced toxicity in human macrophages. Toxicol Lett 240:172–184. doi:10.1016/j.toxlet.2015.10.018
European Commission (2011) Commission Recommendation of 18 October 2011 on the definition of nanomaterial. Off J Eur Union 50:38–40
Forrest VJ, Kang YH, McClain DE, Robinson DH, Ramakrishnan N (1994) Oxidative stress-induced apoptosis prevented by Trolox. Free Radic Biol Med 16(6):675–684
Freyre-Fonseca V, Delgado-Buenrostro NL, Gutierrez-Cirlos EB, Calderon-Torres CM, Cabellos-Avelar T, Sanchez-Perez Y, Pinzon E, Torres I, Molina-Jijon E, Zazueta C, Pedraza-Chaverri J, Garcia-Cuellar CM, Chirino YI (2011) Titanium dioxide nanoparticles impair lung mitochondrial function. Toxicol Lett 202:111–119. doi:10.1016/j.toxlet.2011.01.025
Frick R, Müller-Edenborn B, Schlicker A, Rothen-Rutishauser B, Raemy DO, Günther D, Hattendorf B, Stark W, Beck-Schimmer B (2011) Comparison of manganese oxide nanoparticles and manganese sulfate with regard to oxidative stress, uptake and apoptosis in alveolar epithelial cells. Toxicol Lett 205:163–172. doi:10.1016/j.toxlet.2011.05.1037
Fthenakis V (2009) Sustainability of photovoltaics: the case for thin-film solar cells. Renew Sustain Energy Rev 13:2746–2750
Fthenakis V, Moskowitz PD (2000) Photovoltaics: environmental, health and safety issues and perspectives. Prog Photovoltaics Res Appl 8:27–38. doi:10.1002/(sici)1099-159x(200001/02)8:1<27:aid-pip296>3.0.co;2-8
George S, Pokhrel S, Ji Z, Henderson BL, Xia T, Li L, Zink JI, Nel AE, Mädler L (2011) Role of Fe doping in tuning the band gap of TiO2 for the photo-oxidation-induced cytotoxicity paradigm. J Am Chem Soc 133:11270–11278. doi:10.1021/ja202836s
Ghiazza M, Alloa E, Oliaro-Bosso S, Viola F, Livraghi S, Rembges D, Capomaccio R, Rossi F, Ponti J, Fenoglio I (2014) Inhibition of the ROS-mediated cytotoxicity and genotoxicity of nano-TiO2 toward human keratinocyte cells by iron doping. J Nanopart Res 16:1–17. doi:10.1007/s11051-014-2263-z
Hardman R (2006) A toxicologic review of quantum dots: toxicity depends on physicochemical and environmental factors. Environ Health Perspect 114:165–172
Hoffmann MR, Martin ST, Choi W, Bahnemann DW (1995) Environmental applications of semiconductor photocatalysis. Chem Rev 95:69–96. doi:10.1021/cr00033a004
Huang C, Aronstam R, Chen R, Huang W (2010) Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol in vitro 24:45–55. doi:10.1016/j.tiv.2009.09.00
Izyumov DS, Domnina LV, Nepryakhina OK, Avetisyan AV, Golyshev SA, Ivanova OY, Korotetskaya MV, Lyamzaev KG, Pletjushkina OY, Popova EN, Chernyak BV (2010) Mitochondria as source of reactive oxygen species under oxidative stress. Study with novel mitochondria-targeted antioxidants — the “Skulachev-ion” derivatives. Biochem Moscow 75:123–129
Jackson P, Hariskos D, Lotter E, Paetel S, Wuerz R, Menner R, Wischmann W, Powalla M (2011) New world record efficiency for Cu(In, Ga)Se2 thin-film solar cells beyond 20%. Prog Photovoltaics Res Appl 19:894–897. doi:10.1002/pip.1078
Jiang J, Oberdörster G, Biswas P (2008) Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies. J Nanopart Res 11:77–89. doi:10.1007/s11051-008-9446-4
Kamp DW, Panduri VA, Weitzman S, Chandel N (2002) Asbestos-induced alveolar epithelial cell apoptosis: role of mitochondrial dysfunction caused by iron-derived free radicals. Mol Cell Biochem 234–235:153–160
Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE (2009) Mitochondria and reactive oxygen species. Free Radic Biol Med 47:333–343. doi:10.1016/j.freeradbiomed.2009.05.004
Kumagai Y, Koide S, Taguchi K, Endo A, Nakai Y, Yoshikawa T, Shimojo N (2002) Oxidation of proximal protein sulfhydryls by phenanthraquinone, a component of diesel exhaust particles. Chem Res Toxicol 15:483–489. doi:10.1021/tx0100993
Liu C-J, Burghaus U, Besenbacher F, Wang ZL (2010) Preparation and characterization of nanomaterials for sustainable energy production. ACS Nano 4:5517–5526. doi:10.1021/nn102420c
Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192:1–15
Maynard AD (2007) Nanotechnology: the next big thing, or much ado about nothing? Ann Occup Hyg 51:1–12. doi:10.1093/annhyg/mel071
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63. doi:10.1016/0022-1759(83)90303-4
Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627. doi:10.1126/science.1114397
Oberdörster G (2010) Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J Intern Med 267:89–105. doi:10.1111/j.1365-2796.2009.02187.x
Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183. doi:10.1146/annurev.pharmtox.47.120505.105122
Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913–922
Pal AK, Bello D, Budhlall B, Rogers E, Milton DK (2011) Screening for oxidative stress elicited by engineered nanomaterials: evaluation of acellular DCFH assay. Dose-Response 1:1–23. doi:10.2203/dose-response.10-036.Pal
Reinhard P, Buecheler S, Tiwari AN (2013) Technological status of Cu(In, Ga)(Se, S)2-based photovoltaics. Sol Energy Mater Sol Cells 119:287–290. doi:10.1016/j.solmat.2013.08.030
Reyes P, Velumani S (2012) Structural and optical characterization of mechanochemically synthesized copper doped CdS nanopowders. Mater Sci Eng B-Adv Funct Solid-State Mater 177:1452–1459. doi:10.1016/j.mseb.2012.03.002
Sauvain J-J, Deslarzes S, Riediker M (2008) Nanoparticle reactivity toward dithiothreitol. Nanotoxicology 2:121–129
Tedja R, Marquis C, Lim M, Amal R (2011) Biological impacts of TiO2 on human lung cell lines A549 and H1299: particle size distribution effects. J Nanopart Res 13:3801–3813. doi:10.1007/s11051-011-0302-6
Teodoro JS, Simoes AM, Duarte FV, Rolo AP, Murdoch RC, Hussain SM, Palmeira CM (2011) Assessment of the toxicity of silver nanoparticles in vitro: a mitochondrial perspective. Toxicol In Vitro 25:664–670. doi:10.1016/j.tiv.2011.01.004
Unfried K, Albrecht C, Klotz LO, Von Mikecz A, Grether-Beck S, Schins RPF (2007) Cellular responses to nanoparticles: target structures and mechanisms. Nanotoxicology 1:52–71
Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84
Vidhya B, Velumani S, Arenas-Alatorre JA, Morales-Acevedo A, Asomoza R, Chavez-Carvayar JA (2010). Structural studies of mechano-chemically synthesized CuIn1− x Ga x Se2 nanoparticles. Mater Sci Eng B 174: 216–221. doi:10.1016/j.mseb.2010.03.014
Wang L, Pal AK, Isaacs JA, Bello D, Carrier RL (2014) Nanomaterial induction of oxidative stress in lung epithelial cells and macrophages. J Nanopart Res 16:1–14. doi:10.1007/s11051-014-2591-z
Xia T, Kovochich M, Brant J, Hotze M, Sempf J, Oberley T, Sioutas C, Yeh J, Wiesner M, Nel A (2006) Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett 6:1794–1807. doi:10.1021/nl061025k
Xia T, Kovochich M, Liong M, Ma dler L, Gilbert B, Shi H, Yeh JI, Zink JI, Nel A (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2:2121–2134 doi:10.1021/nn800511k
Zhang H, Ji Z, Xia T, Meng H, Low-Kam C, Liu R, Pokhrel S, Lin S, Wang X, Liao Y-P, Wang M, Li L, Rallo R, Damoiseaux R, Telesca D, Mädler L, Cohen Y, Zink JI, Nel A (2012) Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano 6:4349–4368. doi:10.1021/nn3010087
Zorov DB, Filburn CR, Klotz L-O, Zweier JL, Sollott SJ (2000) Reactive oxygen species (ROS-induced) ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192(7):1001–1014
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This research project was supported partially by Project No. ICyT-DF 396/10.
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Escamilla-Rivera, V., Uribe-Ramirez, M., Gonzalez-Pozos, S. et al. Cytotoxicity of semiconductor nanoparticles in A549 cells is attributable to their intrinsic oxidant activity. J Nanopart Res 18, 85 (2016). https://doi.org/10.1007/s11051-016-3391-4
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DOI: https://doi.org/10.1007/s11051-016-3391-4