Demir (III) oksit (Fe2O3) nanopartiküllerinin genotoksisitesinin Drosophila hemositlerinde KOMET yöntemi ile araştırılması
Yıl 2021,
Cilt: 11 Sayı: 3, 643 - 652, 15.07.2021
Burcin Yalcin
,
Merve Güneş
,
İbrahim Hakkı Ciğerci
,
Bülent Kaya
Öz
Nanopartikül (NP) kaynaklı ürünlerin giderek çeşitlenmesi ve bu ürünlerin ekonomik, çevresel ve insan sağlığı yararına fayda sağlaması nedeni ile NP’lerin kullanımı yaygınlaşmıştır. Ancak bu yoğun kullanım beraberinde bazı endişelerin oluşmasına da yol açmıştır. NP’ler kimyasal bileşimlerine, yapılarına, partikül büyüklüklerine, yüzey alanlarına ve şekillerine göre farklı toksik etkiler gösterebilmektedir. Şekilleri ve boyutları NP’lerin hücresel alımları ve potansiyel toksisitesinde önemli belirleyicilerdir. Demir (III) oksit (Fe2O3) NP’leri, manyetik rezonans görüntülemede, ilaç dağıtımında, biyolojik sıvıların detoksifikasyonu gibi birçok biyomedikal ve biyomühendislik alanlarında kullanıma sahiptir. Bu çalışmada Fe2O3 NP’lerinin genotoksisitesinin partikül boyutu ve şekli ile ilişkisini belirlemek amacıyla Drosophila hemositleri ile KOMET (alkali tek hücre jel elektroforez) analizi gerçekleştirilmiştir. KOMET sonucuna göre, <50 nm boyutlu ve küre forma sahip Fe2O3 NP’leri ile <100 nm boyutlu ve çubuk forma sahip Fe2O3 NP’lerinin genotoksik etkileri karşılaştırıldığında istatistiksel olarak anlamlı bir farklılık bulunmamıştır. Ancak her iki Fe2O3 NP uygulamasında da çalışılan 3 farklı dozdan (1, 2 ve 5 mM) sadece 1 mM’lık uygulamada kontrol grubu distile suya göre istatistiksel olarak anlamlı düzeyde genoksisitenin indüklendiği belirlenmiştir.
Destekleyen Kurum
Akdeniz Üniversitesi / Afyon Kocatepe Üniversitesi
Proje Numarası
FBG-2019-4977 / 13.FENBİL.22
Teşekkür
Bu çalışma FBG-2019-4977 proje numarası ile Akdeniz Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi tarafından desteklenmiştir. Ayrıca çalışmada kullanılan Fe2O3 NP’leri Afyon Kocatepe Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi tarafından desteklenen 13.FENBİL.22 numaralı projeden temin edilmiştir.
Kaynakça
- Abakumov, M.A., Semkina, A.S., Skorikov, A.S., Vishnevskiy, D.A., Ivanova, A.V., Mironova, E., Davydova, G.A., Majouga, A.G. and Chekhonin, V.P. (2018). Toxicity of iron oxide nanoparticles: Size and coating effects. Journal of Biochemical and Molecular Toxicology, 32(12), e22225. https://doi.org/10.1002/jbt.22225.
- Alaraby, M., Annangi, B., Marcos, R. and Hernández, A. (2016). Drosophila melanogaster as a suitable in vivo model to determine potential side effects of nanomaterials: A review. Journal of Toxicology and Environmental Health, Part B. 19(2), 65-104. https://doi.org/10.1080/10937404.2016.1166466.
- Alarifi, S., Ali, D., Alkahtani, S. and Alhaber, M.S. (2014). Iron oxide nanoparticles induce oxidative stress, DNA damage, and caspase activation in the human breast cancer cell line. Biological Trace Element Research, 159, 416-424. https://doi.org/10.1007/s12011-014-9972-0.
- Bai, C. and Tang, M. (2020). Toxicological study of metal and metal oxide nanoparticles in zebrafish. Journal of Applied Toxicology, 40(1), 37–63. https://doi.org/10.1002/jat.3910.
- Carmona, E.R., Inostroza-Blancheteau, C., Rubio, L. and Marcos, R. (2015). Genotoxic effects of copper oxide nanoparticles in Drosophila melanogaster. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 791, 1-11. https://doi.org/10.1016/j.mrgentox.2015.07.006.
- Carmona, E.R., Inostroza-Blancheteau, C., Rubio, L. and Marcos, R. (2016). Genotoxic and oxidative stres potential of nanosized and bulk zinc oxide particles in Drosophila melanogaster. Toxicology and Industrial Health, 32(12), 1987-2001. https://doi.org/10.1177/0748233715599472.
- Caro, C., Egea-Benavente, D., Polvillo, R., Royo, J.L., Leal, M.P. and Garcia-Martin, M.L. (2019). Comprehensive toxicity assessment of PEGylated magnetic nanoparticles for in vivo applications. Colloids and Surfaces B: Biointerfaces, 177, 253–259. https://doi.org/10.1016/j.colsurfb.2019.01.051.
- Dahman, Y. (2019). Biomaterials science and technology fundamentals and developments (Vol. 1). Boca Raton:CRC Press.
- Demir, E., Aksakal, S., Turna, F., Kaya, B. and Marcos, R. (2015). In vivo genotoxic effects of four different nano-sizes forms of silica nanoparticles in Drosophila melanogaster. Journal of Hazardous Materials, 283, 260-266. https://doi.org/10.1016/j.jhazmat.2014.09.029.
- Dlugosz, O., Szostak, K., Staron, A., Pulit-Prociak, J. and Banach, M. (2020). Methods for reducing the toxicity of metal and metal oxide NPs as biomedicine. Materials, 13(2), 279. https://doi.org/10.3390/ma13020279.
- Dong, L., Tang, S., Deng, F., Gong, Y., Zhao, K., Zhou, J., Liang, D., Fang, J., Hecker, M., Giesy, J.P., Bai, X. and Zhang, H. (2019). Shape-dependent toxicity of alumina nanoparticles in rat astrocytes. Science of the Total Environment, 690, 158–166. https://doi.org/10.1016/j.scitotenv.2019.06.532.
- Gaharwar, U.S. and Paulraj, R. (2015). Iron oxide nanoparticles induced oxidative damage in peripheral blood cells of rat. Journal of Biomedical Science and Engineering, 8(4), 274-286. https://doi.org/10.4236/jbise.2015.84026.
- Güneş, M., Yalçın, B., Ertuğrul, H. and Kaya, B. (2018). Ascorbic acid ameliorates genotoxic effects of cobalt nanoparticles and cobalt chloride in in vivo Drosophila assays. Fresenius Environmental Bulletin, 27, 2380-2391.
- Ertuğrul, H., Yalçın, B., Güneş, M. and Kaya, B. (2020). Ameliorative effects of melatonin against nano and ionic cobalt induced genotoxicity in two in vivo Drosophila assays. Drug and Chemical Toxicology, 43(3), 279-286. https://doi.org/10.1080/01480545.2019.1585444.
- Honary, S. and Zahir, H. (2013). Effect of zeta potential on the properties of nano-drug delivery systems-a review (Part 2). Tropical Journal of Pharmaceutical Research, 12(2), 265-273. https://doi.org/10.4314/tjpr.v12i2.20.
- Horie, M., Fujita, K., Kato, H., Endoh, S., Nishio, K., Komaba, L.K., Nakamura, A., Miyauchi, A., Kinugasa, S., Hagihara, Y., Niki, E., Yoshida, Y. and Iwahashi, H. (2012). Association of the physical and chemical properties and the cytotoxicity of metal oxide nanoparticles: metal ion release, adsorption ability and specific surface areaw. Metallomics, 4(4), 350–360. https://doi.org/10.1039/c2mt20016c.
- Irving, P., Ubeda, J.M., Doucet, D., Troxler, L., Lagueux, M., Zachary, D., Hoffmann, J.A., Hetru, C. and Meister, M. (2005). New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cellular Microbiology, 7(3), 335-350. https://doi.org/10.1111/j.1462-5822.2004.00462.x.
- Johnston, B.D., Scown, T.M., Morger, J., Cumberland, S.A., Baalousha, M., Linge, K., van Aerle, R., Jarvis, K., Lead, J.R. and Tyler, C.R. (2010). Bioavailability of nanoscale metal oxides TiO2, CeO2, and ZnO to fish. Environmental Science and Technology, 44(3), 1144–1151. https://doi.org/10.1021/es901971a.
- Ju-Nam, Y. and Lead, J.R. (2008). Manufactured nanoparticles: An overview of their chemistry, interactions and potential environmental implications. Science of The Total Enviroment, 400(1-3), 396–414. https://doi.org/10.1016/j.scitotenv.2008.06.042.
- Karlsson, H.L., Di Bucchianico, S., Collins, A.R. and Dusinska, M. (2015). Can the comet assay be used reliably to detect nanoparticle-induced genotoxicity? Environmental and Molecular Mutagenesis, 56(2), 82-96. https://doi.org/10.1002/em.21933.
- Karlsson, H.L. (2010). The comet assay in nanotoxicology research. Analytical and Bioanalytical Chemistry, 398(2), 651-666. https://doi.org/10.1007/s00216-010-3977-0.
- Katz, E. (2019). Synthesis, properties and applications of magnetic nanoparticles and nanowires—A brief introduction. Magnetochemistry, 5(4), 61. https://doi.org/10.3390/magnetochemistry5040061.
- Kumari, M., Kumari, S.I. and Grover, P. (2014). Genotoxicity analysis of cerium oxide micro and nanoparticles in Wistar rats after 28 days of repeated oral administration. Mutagenesis, 29(6), 467–479. https://doi.org/10.1093/mutage/geu038.
- Ma, H., Diamond, S., Hinkley, G. and Roberts, S.M. (2015). Nanotoxicology. Roberts, S.M., James, R.C., Williams, P.L. (Ed.), Principles of Toxicology Environmental and Industrial Applications (s. 359-372)., Canada: John Wiley and Sons.
- PubMed. (2020, 31 Ekim). Iron oxide nanoparticle, Results by year. https://www.ncbi.nlm.nih.gov/pubmed/?term=iron+oxide+nanoparticles.
- Reiter, L.T., Potocki, L., Chien, S., Gribskov, M. and Bier, E. (2001). A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Research, 11(6), 1114-1125. https://doi.org/10.1101/gr.169101.
- Rosenkranz, P., Fernández-Cruz, M.L., Conde, E., Ramírezfernández, M.B., Flores, J.C., Fernández, M. and Navas, J.M. (2012). Effects of cerium oxide nanoparticles to fish and mammalian cell lines: Anassessment of cytotoxicity and methodology. Toxicology in vitro, 26(6), 888–896. https://doi.org/10.1016/j.tiv.2012.04.019.
- Sadeghi, L., Tanwir, F. and Babadi, V.Y. (2015a). In vitro toxicity of iron oxide nanoparticle: Oxidative damages on HepG2 cells. Experimental and Toxicologic Pathology, 67(2), 197-203. https://doi.org/10.1016/j.etp.2014.11.010.
- Sadeghi, L., Yousefi Babadi, V. and Espanani, H.R. (2015b). Toxic effects of the Fe2O3 nanoparticles on the liver and lung tissue. Bratislavske Lekarske Listy, 116(6), 373 – 378. https://doi.org/10.4149/BLL_2015_071.
- Scherer, M.D., Sposito, J.C.V., Falco, W.F., Grisolia, A.B., Andrade, L.H.C., Lima, S.M., Machado, G., Nascimento, V.A., Gonçalves, D.A., Wender, H., Oliveira, S.L. and Caires, A.R.L. (2019). Cytotoxic and genotoxic effects of silver nanoparticles on meristematic cells of Allium cepa roots: A close analysis of particle size dependence. Science of the Total Environment, 660, 459–467. https://doi.org/10.1016/j.scitotenv.2018.12.444.
- Sukhanova, A., Bozrova, S., Sokolov, P., Berestovoy, M., Karaulov, A. and Nabiev, I. (2018). Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Research Letters, 13(1), 44. https://doi.org/10.1186/s11671-018-2457-x.
- Shukla, A.K., Pragya, P. and Chowdhuri, D. (2011). A modified alkaline Comet assay for in vivo detection of oxidative DNA damage in Drosophila melanogaster. Mutation Research, 726(2), 222-226. https://doi.org/10.1016/j.mrgentox.2011.09.017.
- Singh, A.K. (2016a). Structure, synthesis, and application of nanoparticles. Singh, A.K. (Ed.), Engineered Nanoparticles Structure-Properties and Mechanisms of Toxicity (s. 19-76). USA: Elsevier. https://doi.org/10.1016/B978-0-12-801406-6.00002-9.
- Singh, A.K. (2016b). Mechanisms of nanoparticle toxicity. Singh, A.K. (Ed.), Engineered Nanoparticles Structure-Properties and Mechanisms of Toxicity (s. 295-341). USA: Elsevier. https://doi.org/10.1016/B978-0-12-801406-6.00007-8.
- Singh, N., Manshian, B., Jenkins, G.J.S., Griffiths, S.M., Williams, P.M., Maffeis, T.G.G, Wright, C.J. and Doak, S.H. (2009). NanoGenotoxicology: The DNA damaging potential of engineered nanomaterials. Biomaterials, 30(23-24), 3891–3914. https://doi.org/10.1016/j.biomaterials.2009.04.009.
- Singh, S.P., Rahman, M.F., Murty, U.S.N. and Grover, P. (2013). Comparative study of genotoxicity and tissue distribution of nano and micron sized iron oxide in rats after acute oral treatment. Toxicology and Applied Pharmacology, 266(1), 56–66. https://doi.org/10.1016/j.taap.2012.10.016.
- Wang, L., Wang, L., Ding, W. and Zhang, F. (2010). Acute toxicity of ferric oxide and zinc oxide nanoparticles in rats. Journal of Nanoscience and Nanotechnology, 10(12), 8617–8624. https://doi.org/10.1166/jnn.2010.2483.
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Investigation of genotoxicity of iron (III) oxide (Fe2O3) nanoparticles in Drosophila hemocytes by COMET method
Yıl 2021,
Cilt: 11 Sayı: 3, 643 - 652, 15.07.2021
Burcin Yalcin
,
Merve Güneş
,
İbrahim Hakkı Ciğerci
,
Bülent Kaya
Öz
The use of nanoparticles (NPs) has become widespread due to the increasing diversification of products from NP and the benefit of these products for economic, environmental and human health. However, this overutilize has also led to some concerns. NPs can show different toxic effects depending on their chemical composition, structure, particle size, surface area and shape. Their shape and size are important determinants in the cellular uptake and potential toxicity of NPs. Iron (III) oxide (Fe2O3) NPs are used in many biomedical and bioengineering fields such as magnetic resonance imaging, drug delivery, detoxification of biological fluids. In this study, COMET (alkaline single cell gel electrophoresis) analysis was performed with Drosophila hemocytes to determine the relationship between the genotoxicity of Fe2O3 NPs and particle size and shape. According to the result of COMET, no statistically significant difference was found in terms of genotoxicity when Fe2O3 NPs with of <50 nm and sphere form and Fe2O3 NPs with of <100 nm and rod form were compared. However, in both Fe2O3 NP treatments, it was determined that only 1 mM dose (between 1, 2 and 5 mM) was induced statistically significant level of genoxicity compared to the control group distilled water.
Proje Numarası
FBG-2019-4977 / 13.FENBİL.22
Kaynakça
- Abakumov, M.A., Semkina, A.S., Skorikov, A.S., Vishnevskiy, D.A., Ivanova, A.V., Mironova, E., Davydova, G.A., Majouga, A.G. and Chekhonin, V.P. (2018). Toxicity of iron oxide nanoparticles: Size and coating effects. Journal of Biochemical and Molecular Toxicology, 32(12), e22225. https://doi.org/10.1002/jbt.22225.
- Alaraby, M., Annangi, B., Marcos, R. and Hernández, A. (2016). Drosophila melanogaster as a suitable in vivo model to determine potential side effects of nanomaterials: A review. Journal of Toxicology and Environmental Health, Part B. 19(2), 65-104. https://doi.org/10.1080/10937404.2016.1166466.
- Alarifi, S., Ali, D., Alkahtani, S. and Alhaber, M.S. (2014). Iron oxide nanoparticles induce oxidative stress, DNA damage, and caspase activation in the human breast cancer cell line. Biological Trace Element Research, 159, 416-424. https://doi.org/10.1007/s12011-014-9972-0.
- Bai, C. and Tang, M. (2020). Toxicological study of metal and metal oxide nanoparticles in zebrafish. Journal of Applied Toxicology, 40(1), 37–63. https://doi.org/10.1002/jat.3910.
- Carmona, E.R., Inostroza-Blancheteau, C., Rubio, L. and Marcos, R. (2015). Genotoxic effects of copper oxide nanoparticles in Drosophila melanogaster. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 791, 1-11. https://doi.org/10.1016/j.mrgentox.2015.07.006.
- Carmona, E.R., Inostroza-Blancheteau, C., Rubio, L. and Marcos, R. (2016). Genotoxic and oxidative stres potential of nanosized and bulk zinc oxide particles in Drosophila melanogaster. Toxicology and Industrial Health, 32(12), 1987-2001. https://doi.org/10.1177/0748233715599472.
- Caro, C., Egea-Benavente, D., Polvillo, R., Royo, J.L., Leal, M.P. and Garcia-Martin, M.L. (2019). Comprehensive toxicity assessment of PEGylated magnetic nanoparticles for in vivo applications. Colloids and Surfaces B: Biointerfaces, 177, 253–259. https://doi.org/10.1016/j.colsurfb.2019.01.051.
- Dahman, Y. (2019). Biomaterials science and technology fundamentals and developments (Vol. 1). Boca Raton:CRC Press.
- Demir, E., Aksakal, S., Turna, F., Kaya, B. and Marcos, R. (2015). In vivo genotoxic effects of four different nano-sizes forms of silica nanoparticles in Drosophila melanogaster. Journal of Hazardous Materials, 283, 260-266. https://doi.org/10.1016/j.jhazmat.2014.09.029.
- Dlugosz, O., Szostak, K., Staron, A., Pulit-Prociak, J. and Banach, M. (2020). Methods for reducing the toxicity of metal and metal oxide NPs as biomedicine. Materials, 13(2), 279. https://doi.org/10.3390/ma13020279.
- Dong, L., Tang, S., Deng, F., Gong, Y., Zhao, K., Zhou, J., Liang, D., Fang, J., Hecker, M., Giesy, J.P., Bai, X. and Zhang, H. (2019). Shape-dependent toxicity of alumina nanoparticles in rat astrocytes. Science of the Total Environment, 690, 158–166. https://doi.org/10.1016/j.scitotenv.2019.06.532.
- Gaharwar, U.S. and Paulraj, R. (2015). Iron oxide nanoparticles induced oxidative damage in peripheral blood cells of rat. Journal of Biomedical Science and Engineering, 8(4), 274-286. https://doi.org/10.4236/jbise.2015.84026.
- Güneş, M., Yalçın, B., Ertuğrul, H. and Kaya, B. (2018). Ascorbic acid ameliorates genotoxic effects of cobalt nanoparticles and cobalt chloride in in vivo Drosophila assays. Fresenius Environmental Bulletin, 27, 2380-2391.
- Ertuğrul, H., Yalçın, B., Güneş, M. and Kaya, B. (2020). Ameliorative effects of melatonin against nano and ionic cobalt induced genotoxicity in two in vivo Drosophila assays. Drug and Chemical Toxicology, 43(3), 279-286. https://doi.org/10.1080/01480545.2019.1585444.
- Honary, S. and Zahir, H. (2013). Effect of zeta potential on the properties of nano-drug delivery systems-a review (Part 2). Tropical Journal of Pharmaceutical Research, 12(2), 265-273. https://doi.org/10.4314/tjpr.v12i2.20.
- Horie, M., Fujita, K., Kato, H., Endoh, S., Nishio, K., Komaba, L.K., Nakamura, A., Miyauchi, A., Kinugasa, S., Hagihara, Y., Niki, E., Yoshida, Y. and Iwahashi, H. (2012). Association of the physical and chemical properties and the cytotoxicity of metal oxide nanoparticles: metal ion release, adsorption ability and specific surface areaw. Metallomics, 4(4), 350–360. https://doi.org/10.1039/c2mt20016c.
- Irving, P., Ubeda, J.M., Doucet, D., Troxler, L., Lagueux, M., Zachary, D., Hoffmann, J.A., Hetru, C. and Meister, M. (2005). New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cellular Microbiology, 7(3), 335-350. https://doi.org/10.1111/j.1462-5822.2004.00462.x.
- Johnston, B.D., Scown, T.M., Morger, J., Cumberland, S.A., Baalousha, M., Linge, K., van Aerle, R., Jarvis, K., Lead, J.R. and Tyler, C.R. (2010). Bioavailability of nanoscale metal oxides TiO2, CeO2, and ZnO to fish. Environmental Science and Technology, 44(3), 1144–1151. https://doi.org/10.1021/es901971a.
- Ju-Nam, Y. and Lead, J.R. (2008). Manufactured nanoparticles: An overview of their chemistry, interactions and potential environmental implications. Science of The Total Enviroment, 400(1-3), 396–414. https://doi.org/10.1016/j.scitotenv.2008.06.042.
- Karlsson, H.L., Di Bucchianico, S., Collins, A.R. and Dusinska, M. (2015). Can the comet assay be used reliably to detect nanoparticle-induced genotoxicity? Environmental and Molecular Mutagenesis, 56(2), 82-96. https://doi.org/10.1002/em.21933.
- Karlsson, H.L. (2010). The comet assay in nanotoxicology research. Analytical and Bioanalytical Chemistry, 398(2), 651-666. https://doi.org/10.1007/s00216-010-3977-0.
- Katz, E. (2019). Synthesis, properties and applications of magnetic nanoparticles and nanowires—A brief introduction. Magnetochemistry, 5(4), 61. https://doi.org/10.3390/magnetochemistry5040061.
- Kumari, M., Kumari, S.I. and Grover, P. (2014). Genotoxicity analysis of cerium oxide micro and nanoparticles in Wistar rats after 28 days of repeated oral administration. Mutagenesis, 29(6), 467–479. https://doi.org/10.1093/mutage/geu038.
- Ma, H., Diamond, S., Hinkley, G. and Roberts, S.M. (2015). Nanotoxicology. Roberts, S.M., James, R.C., Williams, P.L. (Ed.), Principles of Toxicology Environmental and Industrial Applications (s. 359-372)., Canada: John Wiley and Sons.
- PubMed. (2020, 31 Ekim). Iron oxide nanoparticle, Results by year. https://www.ncbi.nlm.nih.gov/pubmed/?term=iron+oxide+nanoparticles.
- Reiter, L.T., Potocki, L., Chien, S., Gribskov, M. and Bier, E. (2001). A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Research, 11(6), 1114-1125. https://doi.org/10.1101/gr.169101.
- Rosenkranz, P., Fernández-Cruz, M.L., Conde, E., Ramírezfernández, M.B., Flores, J.C., Fernández, M. and Navas, J.M. (2012). Effects of cerium oxide nanoparticles to fish and mammalian cell lines: Anassessment of cytotoxicity and methodology. Toxicology in vitro, 26(6), 888–896. https://doi.org/10.1016/j.tiv.2012.04.019.
- Sadeghi, L., Tanwir, F. and Babadi, V.Y. (2015a). In vitro toxicity of iron oxide nanoparticle: Oxidative damages on HepG2 cells. Experimental and Toxicologic Pathology, 67(2), 197-203. https://doi.org/10.1016/j.etp.2014.11.010.
- Sadeghi, L., Yousefi Babadi, V. and Espanani, H.R. (2015b). Toxic effects of the Fe2O3 nanoparticles on the liver and lung tissue. Bratislavske Lekarske Listy, 116(6), 373 – 378. https://doi.org/10.4149/BLL_2015_071.
- Scherer, M.D., Sposito, J.C.V., Falco, W.F., Grisolia, A.B., Andrade, L.H.C., Lima, S.M., Machado, G., Nascimento, V.A., Gonçalves, D.A., Wender, H., Oliveira, S.L. and Caires, A.R.L. (2019). Cytotoxic and genotoxic effects of silver nanoparticles on meristematic cells of Allium cepa roots: A close analysis of particle size dependence. Science of the Total Environment, 660, 459–467. https://doi.org/10.1016/j.scitotenv.2018.12.444.
- Sukhanova, A., Bozrova, S., Sokolov, P., Berestovoy, M., Karaulov, A. and Nabiev, I. (2018). Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Research Letters, 13(1), 44. https://doi.org/10.1186/s11671-018-2457-x.
- Shukla, A.K., Pragya, P. and Chowdhuri, D. (2011). A modified alkaline Comet assay for in vivo detection of oxidative DNA damage in Drosophila melanogaster. Mutation Research, 726(2), 222-226. https://doi.org/10.1016/j.mrgentox.2011.09.017.
- Singh, A.K. (2016a). Structure, synthesis, and application of nanoparticles. Singh, A.K. (Ed.), Engineered Nanoparticles Structure-Properties and Mechanisms of Toxicity (s. 19-76). USA: Elsevier. https://doi.org/10.1016/B978-0-12-801406-6.00002-9.
- Singh, A.K. (2016b). Mechanisms of nanoparticle toxicity. Singh, A.K. (Ed.), Engineered Nanoparticles Structure-Properties and Mechanisms of Toxicity (s. 295-341). USA: Elsevier. https://doi.org/10.1016/B978-0-12-801406-6.00007-8.
- Singh, N., Manshian, B., Jenkins, G.J.S., Griffiths, S.M., Williams, P.M., Maffeis, T.G.G, Wright, C.J. and Doak, S.H. (2009). NanoGenotoxicology: The DNA damaging potential of engineered nanomaterials. Biomaterials, 30(23-24), 3891–3914. https://doi.org/10.1016/j.biomaterials.2009.04.009.
- Singh, S.P., Rahman, M.F., Murty, U.S.N. and Grover, P. (2013). Comparative study of genotoxicity and tissue distribution of nano and micron sized iron oxide in rats after acute oral treatment. Toxicology and Applied Pharmacology, 266(1), 56–66. https://doi.org/10.1016/j.taap.2012.10.016.
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