Nanotechnologies in Russia

, Volume 6, Issue 3–4, pp 244–255 | Cite as

Acute toxicity analysis of polyelectrolyte microcapsules with zinc oxide nanoparticles and microcapsule shell components using aquatic organisms

  • T. A. Kolesnikova
  • I. A. Fedorova
  • A. A. Gusev
  • D. A. Gorin


Nanocomposite microcapsules with zinc oxide nanoparticles in their shells were fabricated using layer-by-layer assembly. An investigation of the toxic effect of microcapsules and their constituent components was performed for four types of test objects (ceriodaphnids (Ceriodaphnia affinis Lilljeborg), the Ekolyum biosensor (a culture of fluorescent genetically engineered Escherichia coli M-17 bacteria), midge larvae (Chironomus riparius Meigen), and aquarium fish (Brachydanio rerio)). It was established that, for each test object, the poly(allylamine hydrochloride) solution (PAH) used as a constituent component for the microcapsule shell formation has the maximal toxicity. The poly(sodium styrene sulfonate) solution (PSS) and a sample of microcapsules with a shell structure of (PAH/PSS)2(ZnO/PSS)3(PAH/PSS) have the least toxicity among the tested samples. At the same time, a significant decrease in the acute toxicity effect for the suspension of the microcapsules in comparison with their constituent components was detected. In the future, our results can be used in the development of a complex methodology for determining the toxicity parameters of a microcapsule, as well as the polyelectrolytes and inorganic nanoparticle colloids used as the initial material for the fabrication of nanocomposite microcontainers.


Test Object Zinc Oxide Nanoparticles Hazard Class Chironomus Riparius Sodium Styrene Sulfonate 
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  1. 1.
    G. A. Ozin, A. C. Arsenault, and L. Cademartiri, Nanochemistry: A Chemical Approach to Nanomaterials (RSC Publishing, Cambridge, 2009).Google Scholar
  2. 2.
    N. G. Khlebtsov and L. A. Dykman, “Optical Properties and Biomedical Applications of Plasmonic Nanoparticles,” J. Quant. Spectrosc. Radiat. Transfer 111, 1–35 (2010).CrossRefGoogle Scholar
  3. 3.
    L. A. Dykman, V. A. Bogatyrev, S. Yu. Shchegolev, and N. G. Khlebtsov, Gold Nanoparticles: Synthesis, Properties, and Biomedical Applications (Nauka, Moscow, 2008) [in Russian].Google Scholar
  4. 4.
    D. R. Picot and S. B. Ross-Murphy, Polymer Gels and Networks, Ed. by Y. Osada Y. and A. R. Khokhlov (Marcel Dekker, New York, 2002).Google Scholar
  5. 5.
    A. A. Askadskii and A. R. Khokhlov, Introduction to Physico-Chemistry of Polymers (Nauchnyi Mir, Moscow, 2009) [in Russian].Google Scholar
  6. 6.
    M. A. C. Stuart, W. T. S. Huck, J. Genzer, M. Müller, C. Ober, M. Stamm, G. B. Sukhorukov, I. Szleifer, V. V. Tsukruk, M. Urban, F. Winnik, S. Zauscher, I. Luzinov, and S. Minko, “Emerging Applications of Stimuli-Responsive Polymer Materials,” Nat. Mater. 9, 101–113 (2010).CrossRefGoogle Scholar
  7. 7.
    E. Donath, G. B. Sukhorukov, F. Caruso, S. A. Davis, and H. Möhwald, “Novel Hollow Polymer Shells by Colloid-Templated Assembly of Polyelectrolytes,” Angew. Chem., Int. Ed. 37, 2201–2205 (1998).CrossRefGoogle Scholar
  8. 8.
    S. A. Portnov, O. A. Inozemtseva, D. A. Gorin, and T. A. Kolesnikova, “Formation and Physicochemical Properties of Polyelectrolytic Nanocomposite Microcapsules,” Ross. Nanotekhnol. 2(9–10), 68–80 (2007).Google Scholar
  9. 9.
    G. B. Sukhorukov, A. Fery, M. Brumen, and H. Möhwald, “Physical Chemistry of Encapsulation and Release,” Phys. Chem. Chem. Phys. 6, 4078–4089 (2004).CrossRefGoogle Scholar
  10. 10.
    M. F. Bédard, A. Muñz-Javier, R. Mueller, P. del Pino, A. Fery, W. J. Parak, A. G. Skirtach, and G. B. Sukhorukov, “On the Mechanical Stability of Polymeric Microcontainers Functionalized with Nanoparticles,” Soft Matter 5, 148–155 (2009).CrossRefGoogle Scholar
  11. 11.
    T. A. Kolesnikova, D. A. Gorin, P. Fernandes, S. Kessel, G. B. Khomutov, A. Fery, D. G. Shchukin, and H. Möhwald, “Nanocomposite Microcontainers with High Ultrasound Sensitivity,” Adv. Funct. Mater. 20, 1189–1195 (2010).CrossRefGoogle Scholar
  12. 12.
    S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human Skin Penetration of Sunscreen Nanoparticles: In-Vitro Assessment of a Novel Micronized Zinc Oxide Formulation,” Skin Pharmacol. Physiol. 20, 148–154 (2007).CrossRefGoogle Scholar
  13. 13.
    N. Lü, X. Lü, X. Jin, and C. Lü, “Preparation and Characterization of UV-Curable ZnO/Polymer Nanocomposite Films,” Polym. Int. 56, 138–143 (2007).CrossRefGoogle Scholar
  14. 14.
    S. C. Tjong and G. D. Liang, “Electrical Properties of Low-Density Polyethylene/ZnO Nanocomposites,” Mater. Chem. Phys. 100, 1–5 (2006).CrossRefGoogle Scholar
  15. 15.
    D. Yeom, K. Keem, J. Kang, D.-Y. Jeong, C. Yoon, D. Kim, and S. Kim, “NOT and NAND Logic Circuits Composed of Top-Gate ZnO Nanowire Field-Effect Transistors with High-k Al2O3 Gate Layers,” Nanotechnology 19, 265 202 (2008).Google Scholar
  16. 16.
    M.-H. Zhao, Z.-L. Wang, and S. X. Mao, “Piezoelectric Characterization of Individual Zinc Oxide Nanobelt Probed by Piezoresponse Force Microscope,” Nano Lett. 4(4), 587–590 (2004).CrossRefGoogle Scholar
  17. 17.
    M. Wang, Y. Lian, and X. Wang, “PPV/PVA/ZnO Nanocomposite Prepared by Complex Precursor Method and Its Photovoltaic Application,” Curr. Appl. Phys. 9, 189–194 (2009).CrossRefGoogle Scholar
  18. 18.
    G. S. Terentyuk, G. N. Maslyakova, L. V. Suleymanova, B. N. Khlebtsov, B. Ya. Kogan, G. G. Akchurin, A. V. Shantrocha, I. L. Maksimova, N. G. Khlebtsov, and V. V. Tuchin, “Circulation and Distribution of Gold Nanoparticles and Induced Alterations of Tissue Morphology at Intravenous Particle Delivery,” J. Biophoton. 2(5), 292–302 (2009).CrossRefGoogle Scholar
  19. 19.
    W. Jiang, B. Y. S. Kim, J. T. Rutka, and W. C. W. Chan, “Nanoparticle-Mediated Cellular Response Is Size-Dependent,” Nat. Nanotechnol. 3, 145–150 (2008).CrossRefGoogle Scholar
  20. 20.
    C. Hanley, J. Layne, A. Punnoose, K. M. Reddy, I. Coombs, A. Coombs, K. Feris, and D. Wingett, “Preferential Killing of Cancer Cells and Activated Human T Cells Using ZnO Nanoparticles,” Nanotechnology 19, 295 103 (2008).CrossRefGoogle Scholar
  21. 21.
    K. M. Reddy, K. Feris, J. Bell, D. Wingett, C. Hanley, and A. Punnoose, “Selective Toxicity of Zinc Oxide Nanoparticles to Prokaryotic and Eukaryotic Systems,” Appl. Phys. Lett. 90, 213 902-1–213 902-3 (2007).Google Scholar
  22. 22.
    R. Brayner, R. Ferrari-Iliou, N. Brivois, S. Djediat, M. F. Benedetti, and F. Fievet, “Toxicological Impact Studies Based on Escherichia coli Bacteria in Ultrafine ZnO Nanoparticles Colloidal Medium,” Nano Lett. 6(4), 866–870 (2006).CrossRefGoogle Scholar
  23. 23.
    M. Semmling, O. Kreft, A. Muñoz-Javier, G. B. Sukhorukov, J. Käs, and W. J. Parak, “A Novel Flow-Cytometry-Based Assay for Cellular Uptake Studies of Polyelectrolyte Microcapsules,” Small 4(10), 1763–1768 (2008).CrossRefGoogle Scholar
  24. 24.
    S. Faraasen, J. Vörös, G. Csúcs, M. Textor, H. P. Merkle, and E. Walter, “Ligand-Specific Targeting of Microspheres to Phagocytes by Surface Modification with Poly(L-Lysine)-Grafted Poly(Ethylene Glycol) Conju gate,” Pharm. Res. 20(2), 235–243 (2003).CrossRefGoogle Scholar
  25. 25.
    A. Muñoz-Javier, O. Kreft, M. Semmling, S. Kempter, A. G. Skirtach, O. T. Bruns, P. del Pino, M. F. Bedard, J. Radler, J. Käs, C. Plank, G. B. Sukhorukov, and W. J. Parak, “Uptake of Colloidal Polyelectrolyte-Coated Particles and Polyelectrolyte Multilayer Capsules by Living Cells,” Adv. Mater. (Weinheim) 20, 4281–4287 (2008).CrossRefGoogle Scholar
  26. 26.
    J. A. Champion and S. Mitragotri, “Role of Target Geometry in Phagocytosis,” Proc. Natl. Acad. Sci. USA 103, 4930–4934 (2006).CrossRefGoogle Scholar
  27. 27.
    U. Wattendorf, O. Kreft, M. Textor, G. B. Sukhorukov, and H. P. Merkle, “Stable Stealth Function for Hollow Polyelectrolyte Microcapsules through a Poly(Ethylene Glycol) Grafted Polyelectrolyte Adlayer,” Biomacromolecules 9, 100–108 (2008).CrossRefGoogle Scholar
  28. 28.
    B. G. De Geest, R. E. Vandenbroucke, A. M. Guenther, G. B. Sukhorukov, W. E. Hennink, N. N. Sanders, J. Demeester, and S. C. De Smedt, “Intracellularly Degradable Polyelectrolyte Microcapsules,” Adv. Mater. (Weinheim) 18(8), 1005–1009 (2006).CrossRefGoogle Scholar
  29. 29.
    N. M. Franklin, N. J. Rogers, S. C. Apte, G. E. Batley, G. E. Gadd, and P. S. Casey, “Comparative Toxicity of Nanoparticulate ZnO, Bulk ZnO, and ZnCl2 to a Freshwater Microalga (Pseudokirchneriella subcapitata): The Importance of Particle Solubility,” Environ. Sci. Technol. 41(24), 8484–8490 (2007).CrossRefGoogle Scholar
  30. 30.
    D. Lin and B. Xing, “Root Uptake and Phytotoxicity of ZnO Nanoparticles,” Environ. Sci. Technol. 42(15), 5580–5585 (2008).CrossRefGoogle Scholar
  31. 31.
    R. Brayner, S. A. Dahoumane, C. Yéprémian, C. Djediat, M. Meyer, A. Couté, and F. Fiévet, “ZnO Nanoparticles: Synthesis, Characterization, and Ecotoxicological Studies,” Langmuir 26(9), 6522–6528 (2010).CrossRefGoogle Scholar
  32. 32.
    J. D. Fortner, D. Y. Lyon, C. M. Sayes, A. M. Boyd, J. C. Falkner, E. M. Hotze, L. B. Alemany, Y. J. Tao, W. Guo, K. D. Ausman, V. L. Colvin, and J. B. Hughes, “C60 in Water: Nanocrystal Formation and Microbial Response,” Environ. Sci. Technol. 39, 4307–4316 (2005).CrossRefGoogle Scholar
  33. 33.
    D. Y. Lyon, J. D. Fortner, C. M. Sayes, V. L. Colvin, and J. B. Hughes, “Bacterial Cell Association and Antimicrobial Activity of a C60 Water Suspension,” Environ. Toxicol. Chem. 24, 2757–2762 (2005).CrossRefGoogle Scholar
  34. 34.
    S. B. Lovern and R. Kapler, “Daphnia Magna Mortality When Exposed to Titanium Dioxide and Fullerene (C60) Nanoparticles,” Environ. Toxicol. Chem. 25, 1132–1137 (2006).CrossRefGoogle Scholar
  35. 35.
    E. Oberdörster, “Manufactured Nanomaterials (Fullerenes, C60) Induce Oxidative Stress in the Brain of Juvenile Largemouth Bass,” Environ. Health Perspect. 112 1058–1062 (2004).CrossRefGoogle Scholar
  36. 36.
    G. Andrievsky, V. Klochkov, and L. Derevyanchenko, “Is the C60 Fullerene Molecule Toxic?!” Fullerenes, Nanotubes, Carbon Nanostruct. 13, 363–376 (2005).CrossRefGoogle Scholar
  37. 37.
    L. B. Piotrovskii, “Fullerenes in the Design of Medicinal Preparations,” Ross. Nanotekhnol. 2(7–8), 6–16 (2007).Google Scholar
  38. 38.
    K. E. Biesinger, A. E. Lemke, W. E. Smith, and R. Tyo, “Comparative Toxicity of Polyelectrolytes to Selected Aquatic Animals,” J. Water Pollut. Control Fed. 48(1), 183–187 (1976).Google Scholar
  39. 39.
    K. E. Biesinger and G. N. Stokes, “Effects of Synthetic Polyelectrolytes on Selected Aquatic Organisms,” J. Water Pollut. Control Fed. 58(3), 207–213 (1986).Google Scholar
  40. 40.
    T. I. Moiseenko, “Ecotoxicological Approach to the Evaluation of the Quality of Water,” Vodn. Resur. 32(2), 184–195 (2005).Google Scholar
  41. 41.
    RD 52.24.635-2002. Methodological Instructive Regulations. Verification of Observations for the Assessment of the Level of Toxic Pollution of Bottom Sediments by Means of Biotesting. Methods for Toxicological Evaluation of the Pollution of Freshwater Ecosystems (Rosgidromet, Moscow, 2002) [in Russian].Google Scholar
  42. 42.
    Yu. V. Novikov, K. S. Lastochkina, and Z. N. Boldina, Methods of Investigation the Quality of Reservoir Water (Meditsina, Moscow, 1990) [in Russian].Google Scholar
  43. 43.
    Instruction on the Hydrobiological Monitoring of Freshwater Ecosystems (Gidrometeoizdat, St. Petersburg, 1992) [in Russian].Google Scholar
  44. 44.
    Treatise on the Methods of Hydrobiological Analysis of Surface Waters and Bottom Sediments, Ed. by V. A. Abakumov (Gidrometeoizdat, Leningrad, 1983) [in Russian].Google Scholar
  45. 45.
    Technique for Determination of the Toxicity of Water and Aqueous Extracts from Soils, Sewage Sludges, and Waste against the Lethality Characteristics and Variations in the Fecundity of Ceriodaphni. Federal Requirements of Current Environmental Regulations (Toxicological Methods of Control) PND F T 14.1:2:3:4.8-02; 16.1:2.3:3.5-02 (Ministry of Natural Resources of the Russian Federation, Moscow, 2002) [in Russian].Google Scholar
  46. 46.
    Technique for Determination of the Toxicity of Water and Aqueous Extracts from Soils, Sewage Sludges, and Waste against the Variations in the Intensity of Bacterial Bioluminescence by the Test System “Ecolum.” Federal Requirements of Current Environmental Regulations (Toxicological Methods of Control) (PND F T) 14.1:2:3:4.11-04, Federal Requirements of Current Environmental Regulations (Toxicological Methods of Control) (PND F) 16.1:2.3:3.8-04 (Scientific Center Ecological Perspective, Perm, 2004) [in Russian].Google Scholar
  47. 47.
    “Criteria for Assignment of Hazardous Waste Products to the Hazard Classes by Degree of Impact on the Environment,” Resolution of the Ministry of Natural Resources of the Russian Federation No. 511 (June 15, 2001).Google Scholar
  48. 48.
    N. B. Il’inskaya and M. S. Iordan, “Technique for Determination of the Stage of Physiological Maturity of Chironomid Larvae of the Age IV from the Structure and Size of Embryonic Discs,” in Proceedings of the First (IX) Workshop of the Working Group on Project No. 18 “Species and Its Productivity in Area,” Vilnius, 1975, pp. 17–22.Google Scholar
  49. 49.
    I. A. Fedorova, “Methodological Approaches to the Analysis of Toxicological and Cytogenetic Effects of Cholinotropic Preparations on Chironomus (Diptera) Larvae In Vivo Acute Experiment,” Biomed. Radioelektron., No. 12, 58–65 (2009).Google Scholar
  50. 50.
    Evaluation of the Safety of Nano materials In Vitro and In Vivo Model Systems: Methodological Recommendations (MR 1.2.2566-09) (Federal Center of Hygiene and Epidemiology of Rospotrebnadzor, Moscow, 2009) [in Russian].Google Scholar
  51. 51.
    A. V. Korosov and N. M. Kalinkina, Quantitative Methods of Ecological Toxicology (Petrozavodsk State University, Petrozavodsk, 2003) [in Russian].Google Scholar
  52. 52.
    G. T. Frumin, “Rapid Method for Determination of Effective and Lethal Doses (Concentrations),” Khim.-Farm. Zh., No. 6, 15–18 (1991).Google Scholar
  53. 53.
    H. Selye, “The Concept of Stress as We Understand in 1976,” in New about Hormones and Mechanisms of Their Action (Naukova Dumka, Kiev, 1977), pp. 27–51 [in Russian].Google Scholar
  54. 54.
    B. G. De Geest, S. De Koker, G. B. Sukhorukov, O. Kreft, W. J. Parak, A. G. Skirtach, J. Demeester, S. C. De Smedt, and W. E. Hennink, “Polyelectrolyte Microcapsules for Biomedical Applications,” Soft Matter 5, 282–291 (2009).CrossRefGoogle Scholar
  55. 55.
    M. Bartneck, H. A. Keul, G. Zwadlo-Klarwasser, and J. Groll, “Phagocytosis Independent Extracellular Nanoparticle Clearance by Human Immune Cells,” Nano Lett. 10, 59–63 (2010).CrossRefGoogle Scholar
  56. 56.
    K. Köhler and G. B. Sukhorukov, “Heat Treatment of Polyelectrolyte Multilayer Capsules: A Versatile Method for Encapsulation,” Adv. Funct. Mater. 17(13), 2053–2061 (2007).CrossRefGoogle Scholar
  57. 57.
    Z. Tang, Y. Wang, P. Podsiadlo, and N. A. Kotov, “Biomedical Applications of Layer-By-Layer Assembly: From Biomimetics to Tissue Engineering” Adv. Mater. (Weinheim) 18, 3203–3224 (2006).CrossRefGoogle Scholar
  58. 58.
    A. S. Shcherbachenko, R. Sh. Al’myashev, I. A. Fedorova, and N. V. Polukonova, “Analysis for Toxicity of the Raw Extract of the Hybrid Species of Maize Zea mays L on Chironomids Chironomus plumosus and Fishes Danio rerio,” in Proceedings of the International Scientific and Practical Conference “Bekker Readings,” Volgograd State University, Volgograd, Russia, 2010 (Volgograd State University, Volgograd, 2010), pp. 25–30.Google Scholar
  59. 59.
    N. V. Polukonova, N. A. Durnova, S. V. Raikova, I. A. Fedorova, K. A. Razuvaeva, A. S. Shcherbachenko, and R. Sh. Al’myashev, “Analysis of the Chemical Composition and Biological Properties of the Alcoholic Extract of the Hybrid Species of Maize Zea mays L,” in Proceedings of the Fourth All-Russian Workshop with the International Participation of the Scientific and Methodological Conference “Farmobrazovanie 2010,” Voronezh, Russia, 2010, pp. 306–311.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • T. A. Kolesnikova
    • 1
    • 2
  • I. A. Fedorova
    • 3
  • A. A. Gusev
    • 4
  • D. A. Gorin
    • 1
    • 2
  1. 1.Saratov State UniversitySaratovRussia
  2. 2.Max Planck Institute of Colloids and InterfacesPotsdamGermany
  3. 3.Saratov State Medical UniversitySaratovRussia
  4. 4.Tambov State UniversityTambovRussia

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