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Studies on plant cell toxicity of luminescent silica nanoparticles (Cs2[Mo6Br14]@SiO2) and its constitutive components

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Abstract

As part of the risk evaluation before potential applications of nanomaterials, phytotoxicity of newly designed multifunctional silica nanoparticles (CMB@SiO2, average diameter of 47 nm) and their components, i.e., molybdenum octahedral cluster bromide units (CMB, 1 nm) and SiO2 nanoparticles (nSiO2, 29 nm), has been studied using photosynthetic Arabidopsis thaliana cell suspension cultures. CMB clusters presented toxic effects on plant cells, inhibiting cell growth and negatively affecting cell viability and photosynthetic efficiency. Nevertheless, we showed that neither nSiO2 nor CMB@SiO2 have any significant effect on cell growth and viability or photosynthetic efficiency. At least, part of the harmful impact of CMB clusters could be ascribed to their capacity to generate an oxidative stress since lipid peroxidation greatly increased after CMB exposure, which was not the case for nSiO2 or CMB@SiO2 treatments. Exposure of cells to CMB clusters also leads to the induction of several enzymatic antioxidant activities (i.e., superoxide dismutase, guaiacol peroxidase, glutathione peroxidase, glutathione reductase, and glutathione S-transferase activities) compared to control and the other treatments. Finally, using electron microscopy, we showed that Arabidopsis cells internalize CMB clusters and both silica nanoparticles, the latter through, most likely, endocytosis-like pathway as nanoparticles were mainly found incorporated into vesicles.

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References

  • Adams LK, Lyon DY, Alvarez PJJ (2006) Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 40:3527–3532. doi:10.1016/j.watres.2006.08.004

    Article  Google Scholar 

  • Aubert T, Grasset F, Mornet S, Duguet E, Cador O, Cordier S, Molard Y, Demange V, Mortier M, Haneda H (2010) Functional silica nanoparticles synthesized by water-in-oil microemulsion processes. J Colloid Interface Sci 341:201–208. doi:10.1016/j.jcis.2009.09.064

    Article  Google Scholar 

  • Aubert T, Burel A, Esnault M-A, Cordier S, Grasset F, Cabello-Hurtado F (2012) Root uptake and phytotoxicity of nanosized molybdenum octahedral clusters. J Hazard Mater 219–220:111–118. doi:10.1016/j.jhazmat.2012.03.058

    Article  Google Scholar 

  • Aubert T, Cabello-Hurtado F, Esnault M-A, Neaime C, Lebret-Chauvel D, Jeanne S, Pellen P, Roiland C, Le Polles L, Saito N, Kimoto K, Haneda H, Ohashi N, Grasset F, Cordier S (2013) Extended investigations on luminescent Cs2[Mo6Br 14]@SiO2 nanoparticles: physico-structural characterizations and toxicity studies. J Phys Chem C 117:20154–20163. doi:10.1021/jp405836q

    Article  Google Scholar 

  • Axelos M, Curie C, Mazzolini L, Bardet C, Lescure B (1992) A protocol for transient gene expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiol Biochem 30:123–128

    Google Scholar 

  • Baker GL, Ghosh RN, Osborn DJ (2010) Sol–gel encapsulated hexanuclear clusters for oxygen sensing by optical techniques. U.S. Patent 7,858,380

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  Google Scholar 

  • Brown DM, Varet J, Johnston H, Chrystie A, Stone V (2015) Silica nanoparticles and biological dispersants: genotoxic effects on A549 lung epithelial cells. J Nanopart Res 17:1–16. doi:10.1007/s11051-015-3210-3

    Article  Google Scholar 

  • Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2:MR17–MR71. doi:10.1116/1.2815690

    Article  Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzymol 113:484–490

    Article  Google Scholar 

  • Colvin V-L (2003) The potential environmental impact of engineered nanomaterials. Nat Biotechnol 21:1166–1170. doi:10.1038/nbt875

    Article  Google Scholar 

  • Cordier S, Grasset F, Molard Y, Amela-Cortes M, Boukherroub R, Ravaine S, Mortier M, Ohashi N, Saito N, Haneda H (2015) Inorganic molybdenum octahedral nanoclusters, versatile functional building block for nanoarchitectonics. J Inorg Organomet Polym Mater 25:189–204. doi:10.1007/s10904-014-0112-2

    Article  Google Scholar 

  • Debnath N, Das S, Chandra DSR, Bhattacharya SCh, Goswami A (2011) Entomotoxic effect of silica nanoparticles against Sitophilus oryzae (L.). J Pest Sci 84:99–105. doi:10.1007/s10340-010-0332-3

    Article  Google Scholar 

  • Doyle SM, Diamond M, McCabe PF (2010) Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures. J Exp Bot 61:473–482. doi:10.1093/jxb/erp320

    Article  Google Scholar 

  • Fan L, Li R, Pan J, Ding Z, Lin J (2015) Endocytosis and its regulation in plants. Trends Plant Sci 20:388–397. doi:10.1016/j.tplants.2015.03.014

    Article  Google Scholar 

  • Floh L, Günzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–121

    Article  Google Scholar 

  • Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21. doi:10.1016/j.phytochem.2014.07.020

    Article  Google Scholar 

  • Fruijtier-Pölloth C (2012) The toxicological mode of action and the safety of synthetic amorphous silica-A nanostructured material. Toxicology 294:61–79. doi:10.1016/j.tox.2012.02.001

    Article  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. doi:10.1016/j.plaphy.2010.08.016

    Article  Google Scholar 

  • Gogos A, Knauer K, Bucheli TD (2012) Nanomaterials in plant protection and fertilization: current state, foreseen applications, and research priorities. J Agric Food Chem 60:9781–9792. doi:10.1021/jf302154y

    Article  Google Scholar 

  • González-Pérez S, Gutiérrez J, García-García F, Osuna D, Dopazo J, Lorenzo O, Revuelta JL, Arellano JB (2011) Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions. Plant Physiol 156:1439–1456. doi:10.1104/pp.111.177766

    Article  Google Scholar 

  • Grasset F, Labhsetwar N, Li D, Park DC, Saito N, Haneda H, Cador O, Roisnel T, Mornet S, Duguet E, Portier J, Etourneau J (2002) Synthesis and magnetic characterization of zinc ferrite nanoparticles with different environments: powder, colloidal solution and zinc ferrite-silica core-shell nanoparticles. Langmuir 18:8209–8216. doi:10.1021/la020322b

    Article  Google Scholar 

  • Grasset F, Dorson F, Cordier S, Molard Y, Perrin C, Marie AM, Sasaki T, Haneda H, Bando Y, Mortier M (2008) Water-in-oil microemulsion preparation and characterization of Cs2Mo6X14@SiO2 phosphor nanoparticles based on transition metal clusters (X = Cl, Br, and I). Adv Mater 20:143–148. doi:10.1002/adma.200701686

    Article  Google Scholar 

  • Guarnieri D, Malvindi MA, Belli V, Pompa PP, Netti P (2014) Effect of silica nanoparticles with variable size and surface functionalization on human endothelial cell viability and angiogenic activity. J Nanopart Res 16:1–14. doi:10.1007/s11051-013-2229-6

    Google Scholar 

  • Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione-S-transferases. Methods Enzymol 77:398–405

    Article  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611. doi:10.1007/s004250050524

    Article  Google Scholar 

  • Jouanneau JP, Péaud-Lenoël C (1967) Growth and synthesis of proteins in cell suspensions of a kinetin dependent tobacco. Physiol Plant 20:834–850

    Article  Google Scholar 

  • Le V, Rui Y, Gui X, Li X, Liu S, Han Y (2014) Uptake, transport, distribution and bio-effects of SiO2 nanoparticles in Bt-transgenic cotton. J Nanobiotechnol 12:50. doi:10.1186/s12951-014-0050-8

    Article  Google Scholar 

  • Lee SW, Kim SM, Choi J (2009) Genotoxicity and ecotoxicity assays using the freshwater crustacean Daphnia magna and the larva of the aquatic midge Chironomus riparius to screen the ecological risks of nanoparticle exposure. Environ Toxicol Pharmacol 28:86–91. doi:10.1016/j.etap.2009.03.001

    Article  Google Scholar 

  • Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J, Alvarez PJ (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem 29:669–675. doi:10.1002/etc.58

    Article  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophyll a and b of leaf extract in different solvents. Biochem Soc Trans 11:591–592

    Article  Google Scholar 

  • Lin BS, Diao SQ, Li CH, Fang LJ, Qiao SC, Yu M (2004) Effect of TMS (nanostructured silicon dioxide) on growth of Changbai larch seedlings. J For Res 15:138–140. doi:10.1007/BF02856749

    Article  Google Scholar 

  • Long JR, Xheng X, Holm RH, Yu S-B, Droege M, Sanderson WA (1998) Contrast agents. U.S. Patent 5,804,161

  • Menges M, Hennig L, Gruissem W, Murray JAH (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol 53:423–442. doi:10.1023/B:PLAN.0000019059.56489.ca

    Article  Google Scholar 

  • Minibayeva F, Beckett RP, Ilse K (2015) Roles of apoplastic peroxidases in plant response to wounding. Phytochemistry 112:122–129. doi:10.1016/j.phytochem.2014.06.008

    Article  Google Scholar 

  • Nair R, Poulose A, Nagaoka Y, Yoshida Y, Maekawa T, Kumar DS (2011) Uptake of FITC labeled silica nanoparticles and quantum dots by rice seedlings: effects on seed germination and their potential as biolabels for plants. J Fluoresc 21:2057–2068. doi:10.1007/s10895-011-0904-5

    Article  Google Scholar 

  • Napierska D, Thomassen LC, Lison D, Martens JA, Hoet PH (2010) The nanosilica hazard: another variable entity. Part Fibre Toxicol 7:39. doi:10.1186/1743-8977-7-39

    Article  Google Scholar 

  • Parveen A, Rizvi SHM, Mahdi F, Tripathi S, Ahmad I, Shukla RK, Khanna VK, Singh R, Patel DK, Mahdi AA (2014) Silica nanoparticles mediated neuronal cell death in corpus striatum of rat brain: implication of mitochondrial, endoplasmic reticulum and oxidative stress. J Nanopart Res 16:1–15. doi:10.1007/s11051-014-2664-z

    Google Scholar 

  • Ruban AV (2015) Evolution under the sun: optimizing light harvesting in photosynthesis. J Exp Bot 66:7–23. doi:10.1093/jxb/eru400

    Article  Google Scholar 

  • Selvan ST, Tan TT, Yi DK, Jana NR (2010) Functional and multifunctional nanoparticles for bioimaging and biosensing. Langmuir 26:11631–11641. doi:10.1021/la903512m

    Article  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH (2014) Role of nano-SiO2 in germination of tomato (Lycopersicum esculentum seeds Mill.). Saudi J Biol Sci 21:13–17. doi:10.1016/j.sjbs.2013.04.005

    Article  Google Scholar 

  • Slomberg DL, Schoenfisch MH (2012) Silica nanoparticle phytotoxicity to Arabidopsis thaliana. Environ Sci Technol 46:10247–10254. doi:10.1021/es300949f

    Google Scholar 

  • Srivastava OP, van Huystee RB (1977) IAA oxidase and polyphenol oxidase activities of peanut peroxidase isoenzymes. Phytochemistry 16:1527–1530

    Article  Google Scholar 

  • Torney F, Trewyn BG, Lin VS-Y, Wang K (2007) Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotech 2:295–300. doi:10.1038/nnano.2007.108

    Article  Google Scholar 

  • Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968. doi:10.1104/pp.108.125690

    Article  Google Scholar 

  • van Hoecke K, de Schamphelaere KAC, Ramirez-Garcia S, van der Meeren P, Smagghe G, Janssen CR (2011) Influence of alumina coating on characteristics and effects of SiO2 nanoparticles in algal growth inhibition assays at various pH and organic matter contents. Environ Int 37:1118–1125. doi:10.1016/j.envint.2011.02.009

    Article  Google Scholar 

  • Vivero-Escoto JL, Huxford-Phillips RC, Lin W (2012) Silica-based nanoprobes for biomedical imaging and theranostic applications. Chem Soc Rev 41:2673–2685. doi:10.1039/C2CS15229K

    Article  Google Scholar 

  • Zhang X, Wollenweber B, Jiang D, Liu F, Zhao J (2008) Water deficits and heat shock effects on photosynthesis of a transgenic Arabidopsis thaliana constitutively expressing ABP9, a bZIP transcription factor. J Exp Bot 59:839–848. doi:10.1093/jxb/erm364

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the French National Research Agency (Project CLUSTOP 2011 BS0801301). Authors thank Marie Thérèse Lavault for technical assistance (MRic, UR 1), Juan B. Arellano for kindly providing Arabidopsis cells (IRNASA-CSIC), and Vincent Dorcet for nanoparticle TEM microcraphs (Plateforme THEMIS, UR1).

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Authors and Affiliations

  1. UMR UR1-CNRS 6553 ECOBIO, Mechanisms at the Origin of Biodiversity Team, University of Rennes 1, 263 av. du Général Leclerc, 35042, Rennes, France

    Francisco Cabello-Hurtado & María Dolores Lozano-Baena

  2. Solid State Chemistry and Materials Group, UMR UR1-CNRS 6226 Institut des Sciences Chimiques de Rennes, University of Rennes 1, 263 av. du Général Leclerc, 35042, Rennes, France

    Chrystelle Neaime, Sylvie Jeanne, Pascal Pellen-Mussi, Stéphane Cordier & Fabien Grasset

  3. Electronic Microscopy Department, University of Rennes 1, 2 av. du Professeur Léon-Bernard, Campus de Villejean, 35043, Rennes, France

    Agnès Burel

  4. CNRS-Saint Gobain, UMI 3629, Laboratory for Innovative Key Materials and Structures-Link, National Institute of Material Science (NIMS), GREEN/MANA Room 512, 1-1 Namiki, Tsukuba, 305-0044, Japan

    Fabien Grasset

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  1. Francisco Cabello-Hurtado
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  2. María Dolores Lozano-Baena
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Correspondence to Francisco Cabello-Hurtado.

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Cabello-Hurtado, F., Lozano-Baena, M.D., Neaime, C. et al. Studies on plant cell toxicity of luminescent silica nanoparticles (Cs2[Mo6Br14]@SiO2) and its constitutive components. J Nanopart Res 18, 69 (2016). https://doi.org/10.1007/s11051-016-3381-6

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