Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-25T19:19:05.470Z Has data issue: false hasContentIssue false
  • English
  • Français

Antibacterial properties and in vivo studies of tannic acid-stabilized silver–halloysite nanomaterials

Published online by Cambridge University Press:  23 June 2020

Anna Stavitskaya ,
Christina Shakhbazova ,
Yulia Cherednichenko ,
Läysän Nigamatzyanova ,
Gölnur Fakhrullina ,
Nail Khaertdinov ,
Galiya Kuralbayeva ,
Alla Filimonova ,
Vladimir Vinokurov  and
Rawil Fakhrullin Open the ORCID record for Rawil Fakhrullin [Opens in a new window]
Anna Stavitskaya
Affiliation:
Gubkin University, Functional Aluminosilicate Nanomaterials Lab, 119991Moscow, Russia
Christina Shakhbazova
Affiliation:
Gubkin University, Functional Aluminosilicate Nanomaterials Lab, 119991Moscow, Russia
Yulia Cherednichenko
Affiliation:
Kazan Federal University, Institute of Fundamental Medicine and Biology, Bionanotechnology Lab, 420008Kazan, Republic of Tatarstan, Russia
Läysän Nigamatzyanova
Affiliation:
Kazan Federal University, Institute of Fundamental Medicine and Biology, Bionanotechnology Lab, 420008Kazan, Republic of Tatarstan, Russia
Gölnur Fakhrullina
Affiliation:
Gubkin University, Functional Aluminosilicate Nanomaterials Lab, 119991Moscow, Russia Kazan Federal University, Institute of Fundamental Medicine and Biology, Bionanotechnology Lab, 420008Kazan, Republic of Tatarstan, Russia
Nail Khaertdinov
Affiliation:
Kazan Federal University, Institute of Fundamental Medicine and Biology, Bionanotechnology Lab, 420008Kazan, Republic of Tatarstan, Russia
Galiya Kuralbayeva
Affiliation:
National University of Science and Technology ‘MISIS’, College of New Materials and Nanotechnologies, 119049Moscow, Russia
Alla Filimonova
Affiliation:
Gubkin University, Functional Aluminosilicate Nanomaterials Lab, 119991Moscow, Russia
Vladimir Vinokurov
Affiliation:
Gubkin University, Functional Aluminosilicate Nanomaterials Lab, 119991Moscow, Russia
Rawil Fakhrullin*
Affiliation:
Gubkin University, Functional Aluminosilicate Nanomaterials Lab, 119991Moscow, Russia Kazan Federal University, Institute of Fundamental Medicine and Biology, Bionanotechnology Lab, 420008Kazan, Republic of Tatarstan, Russia
*
*E-mail: kazanbio@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Tannic acid-stabilized silver nanoparticles were synthesized in situ on halloysite clay nanotubes. The synthesis strategy included simple steps of tannic acid adsorption on clay nanotubes and further particle formation from silver salt solution. Pristine halloysite nanotubes as well as amino-modified clays were used for silver stabilization in water or ethanol. The materials were tested for antibacterial performance using three different methods. All of the materials produced showed antimicrobial activity. The pristine halloysite-based material with ~5 nm particles produced using ethanol as the solvent and tannic acid as the reducing agent showed the greatest antibacterial activity against Serratia marcescens. The materials were tested in vivo on Caenorhabditis elegans nematodes to ensure their safety, and they showed no negative effects on nematode growth and life expectancy.

Keywords

antibacterialCaenorhabditis elegansclay nanotubeshalloysiteSerratia marcescenssilver nanoparticles
Type
Article
Information
Clay Minerals , Volume 55 , Issue 2 , June 2020 , pp. 112 - 119
Copyright
Copyright © The Mineralogical Society of Great Britain and Ireland, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Miroslav Pospíšil

References

Akhatova, F., Fakhrullina, G., Khakimova, E. & Fakhrullin, R. (2018) Atomic force microscopy for imaging and nanomechanical characterisation of live nematode epicuticle: a comparative Caenorhabditis elegans and Turbatrix aceti study. Ultramicroscopy, 194, 40–47.CrossRefGoogle ScholarPubMed
Bastús, N.G., Merkoçi, F., Piella, J. & Puntes, V. (2014) Synthesis of highly monodisperse citrate-stabilized silver nanoparticles of up to 200 nm: kinetic control and catalytic properties. Chemistry of Materials, 26, 2836–2846.10.1021/cm500316kCrossRefGoogle Scholar
Bulut O'acar, E. (2009) Facile synthesis of silver nanostructure using hydrolysable tannin. Industrial & Engineering Chemistry Research, 48, 5686–5690.10.1021/ie801779fCrossRefGoogle Scholar
Cao, Y., Zheng, R., Ji, X., Liu, H., Xie, R. & Yang, W. (2014) Syntheses and characterization of nearly monodispersed, size-tunable silver nanoparticles over a wide size range of 7–200 nm by tannic acid reduction. Langmuir, 30, 3876–3882.CrossRefGoogle Scholar
Cervini-Silva, J., Camacho, A.N., Palacios, E., del Angel, P., Pentrak, M., Pentrakova, L. et al. (2016) Anti-inflammatory, antibacterial, and cytotoxic activity by natural matrices of nano-iron(hydr)oxide/halloysite. Applied Clay Science, 120, 101–110.CrossRefGoogle Scholar
Cristina, M.L., Sartini, M. & Spagnolo, A.M. (2019) Serratia marcescens infections in neonatal intensive care units (NICUs). International Journal of Environmental Research and Public Health, 16, 610.CrossRefGoogle Scholar
Dadosh, T. (2009) Synthesis of uniform silver nanoparticles with a controllable size. Materials Letters, 63, 2236–2238.CrossRefGoogle Scholar
Drits, V.A., Sakharov, B.A. & Hillier, S. (2018) Phase and structural features of tubular halloysite (7 Å). Clay Minerals, 53, 691–720.CrossRefGoogle Scholar
Fakhrullina, G., Akhatova, F.S., Kibardina, M., Fokin, D. & Fakhrullin, R. (2017). Nanoscale imaging and characterisation of Caenorhabditis elegans epicuticle using atomic force microscopy. Nanomedicine, 13, 483–491.CrossRefGoogle Scholar
Fakhrullina, G.I., Akhatova, F.S., Lvov, Y.M. & Fakhrullin, R.F. (2015) Toxicity of halloysite clay nanotubes in vivo: a Caenorhabditis elegans study. Environmental Science: Nano, 2, 54–59.Google Scholar
Fakhrullina, G., Khakimova, E., Akhatova, F., Lazzara, G., Parisi, F. & Fakhrullin, R. (2019). Selective antimicrobial effects of curcumin@halloysite nanoformulation: a Caenorhabditis elegans study. ACS Applied Materials & Interfaces, 11, 23050–23064.CrossRefGoogle ScholarPubMed
Fix, D., Andreeva, D.V., Lvov, Y.M., Shchukin, D.G. & Mohwald, H. (2009) Application of inhibitor-loaded halloysite nanotubes in active anti-corrosive coatings. Advanced Functional Materials, 19, 1720–1727.CrossRefGoogle Scholar
Hagerman, A.E., Riedl, K.M., Jones, G.A., Sovik, K.N., Ritchard, N.T., Hartzfeld, P.W. & Riechel, T.L. (1998) High molecular weight plant polyphenolics (tannins) as biological antioxidants. Journal of Agricultural and Food Chemistry, 46, 1887–1892.CrossRefGoogle ScholarPubMed
Hong, H., Xiao, W., Lazarus, H.M., Good, C.E., Maitta, R.W. & Jacobs, M.R. (2016) Detection of septic transfusion reactions to platelet transfusions by active and passive surveillance. Blood, 127, 496–502.CrossRefGoogle ScholarPubMed
Horváth, E., Kristóf, J., Kurdi, R., Makó, É. & Khunová, V. (2011) Study of urea intercalation into halloysite by thermoanalytical and spectroscopic techniques. Journal of Thermal Analysis and Calorimetry, 105, 53–59.CrossRefGoogle Scholar
Huang, X., Wu, H., Liao, X.P. & Shi, B. (2010) One-step, size-controlled synthesis of gold nanoparticles at room temperature using plant tannin. Green Chemistry, 12, 395–399.10.1039/B918176HCrossRefGoogle Scholar
Jana, S., Kondakova, A.V., Shevchenko, S.N., Sheval, E.V., Gonchar, K.A., Timoshenko, V.Y. & Vasiliev, A.N. (2017) Halloysite nanotubes with immobilized silver nanoparticles for anti-bacterial application. Colloids and Surfaces B: Biointerfaces, 151, 249–254.10.1016/j.colsurfb.2016.12.017CrossRefGoogle ScholarPubMed
Joussein, E., Petit, S., Churchman, J., Theng, B., Righi, D. & Delvaux, B. (2005) Halloysite clay minerals: a review. Clay Minerals, 40, 383–426.10.1180/0009855054040180CrossRefGoogle Scholar
Karthikeyan, P., Mitu, L., Pandian, K., Anbarasu, G. & Rajavel, R. (2017) Electrochemical deposition of a Zn-HNT/p(EDOT-co-EDOP) nanocomposite on LN SS for anti-bacterial and anti-corrosive applications. New Journal of Chemistry, 41, 4758–4762.CrossRefGoogle Scholar
Keeling, J. (2015) The mineralogy, geology and occurrences of halloysite. Pp. 96–115 in: Natural Mineral Nanotubes: Properties and Applications (Pasbakhsh, P. and Churchman, G.J., editors). Apple Academic Press, Palm Bay, FL, USA.Google Scholar
Kumar, A., Vemula, P.K., Ajayan, P.M. & John, G. (2008) Silver-nanoparticle-embedded antimicrobial paints based on vegetable oil. Nature Materials, 7, 236–241.CrossRefGoogle ScholarPubMed
Liong, M., France, B., Bradley, K.A. & Zink, J.I. (2009) Antimicrobial activity of silver nanocrystals encapsulated in mesoporous silica nanoparticles. Advanced Materials, 21, 1684–1689.CrossRefGoogle Scholar
Luo, J., Lai, J., Zhang, N., Liu, Y., Liu, R. & Liu, X. (2016) Tannic acid induced self-assembly of three-dimensional graphene with good adsorption and antibacterial properties. ACS Sustainable Chemistry & Engineering, 4, 1404–1413.10.1021/acssuschemeng.5b01407CrossRefGoogle Scholar
Luo, J., Zhang, N., Lai, J., Liu, R. & Liu, X. (2015) Tannic acid functionalized graphene hydrogel for entrapping gold nanoparticles with high catalytic performance toward dye reduction. Journal of Hazardous Materials, 300, 615–623.10.1016/j.jhazmat.2015.07.079CrossRefGoogle ScholarPubMed
Lv, M., Su, S., He, Y., Huang, Q., Hu, W., Li, D. et al. (2010) Long-term antimicrobial effect of silicon nanowires decorated with silver nanoparticles. Advanced Materials, 22, 5463–5467.CrossRefGoogle ScholarPubMed
Lvov, Y.M., Panchal, A., Fu, Y., Fakhrullin, R., Kryuchkova, M., Batasheva, S. et al. (2019) Interfacial self-assembly in halloysite nanotube composites. Langmuir, 35, 8646–8657.CrossRefGoogle ScholarPubMed
Lvov, Y.M., Shchukin, D.G., Mohwald, H. & Price, R.R. (2008) Halloysite clay nanotubes for controlled release of protective agents. ACS Nano, 2, 814–820.10.1021/nn800259qCrossRefGoogle ScholarPubMed
Lvov, Y.M., Wang, W.C., Zhang, L.Q. & Fakhrullin, R. (2016) Halloysite clay nanotubes for loading and sustained release of functional compounds. Advanced Materials, 28, 1227–1250.CrossRefGoogle ScholarPubMed
Mallakpour, S. & Hatami, M. (2018) Green and eco-friendly route for the synthesis of Ag@vitamin B9-LDH hybrid and its chitosan nanocomposites: characterization and antibacterial activity. Polymer, 154, 188–199.CrossRefGoogle Scholar
Moran, A., Israela, B. & Meital, Z. (2007) Gentamicin-loaded bioresorbable films for prevention of bacterial infections associated with orthopedic implants. Journal of Biomedical Materials Research Part A, 83, 10–19.Google Scholar
Ouyang, J., Guo, B., Fu, L., Yang, H., Hu, Y., Tang, A. et al. (2016) Radical guided selective loading of silver nanoparticles at interior lumen and out surface of halloysite nanotubes. Materials & Design, 110, 169–178.CrossRefGoogle Scholar
Price, R., Gaber, B. & Lvov, Y. (2001) Release characteristics of tetracycline, khellin and NAD from halloysite: a cylindrical mineral for delivery of biologically active agents. Journal of Microencapsulation, 18, 713–723.Google Scholar
Ramstedt, M., Cheng, N., Azzaroni, O., Mossialos, D., Mathieu, H.J. & Huck, W.T.S. (2007) Synthesis and characterization of poly(3-sulfopropylmethacrylate) brushes for potential antibacterial applications. Langmuir, 23, 3314–3321.CrossRefGoogle ScholarPubMed
Sagbas, S., Aktas, N. & Sahiner, N. (2015) Modified biofunctional p(tannic acid) microgels and their antimicrobial activity. Applied Surface Science, 354, 306–313.CrossRefGoogle Scholar
Sahiner, N., Sagbas, S. & Aktas, N. (2015) Very fast catalytic reduction of 4-nitrophenol, methylene blue and eosin Y in natural waters using green chemistry: p(tannic acid)-Cu ionic liquid composites. RSC Advances, 5, 18183–18195.CrossRefGoogle Scholar
Shchukin, D.G. & Mohwald, H. (2007) Surface-engineered nanocontainers for entrapment of corrosion inhibitors. Advanced Functional Materials, 17, 1451–1458.CrossRefGoogle Scholar
Shu, Z., Zhang, Y., Yang, Q. & Yang, H. (2017) Halloysite nanotubes supported Ag and ZnO nanoparticles with synergistically enhanced antibacterial activity. Nanoscale Research Letters, 12, 135–142.CrossRefGoogle ScholarPubMed
Song, S., Zhao, T., Qiu, F., Zhu, W., Wu, Y., Ju, Y. & Dong, L. (2019) Silver nanoparticle decorated halloysite nanotube for efficient antibacterial application. Chemical Physics, 521, 51–54.10.1016/j.chemphys.2019.01.020CrossRefGoogle Scholar
Stavitskaya, A.V., Batasheva, S., Vinokurov, V., Fakhrullina, G., Sangarov, V., Lvov, Y. & Fakhrullin, R. (2019) Antimicrobial applications of clay nanotube-based composites. Nanomaterials, 9, 708.CrossRefGoogle ScholarPubMed
Stavitskaya, A.V., Novikov, A.A., Kotelev, M.S., Kopitsyn, D.S., Rozhina, E.V., Ishmukhametov, I.R. et al. (2018) Fluorescence and cytotoxicity of cadmium sulfide quantum dots stabilized on clay nanotubes. Nanomaterials, 8, 391.CrossRefGoogle ScholarPubMed
Suner, S.S., Sahiner, M., Akcali, A. & Sahiner, N. (2020) Functionalization of halloysite nanotubes with polyethyleneimine and various ionic liquid forms with antimicrobial activity. Journal of Applied Polymer Science, 137, 48352.CrossRefGoogle Scholar
Tari, G., Bobos, I., Gomes, C. & Ferreira, J. (1999) Modification of surface charge properties during kaolinate to halloysite-7Å transformation. Journal of Colloid and Interface Science, 210, 360–369.CrossRefGoogle ScholarPubMed
Veerabadran, N.G., Mongayt, D., Torchilin, V., Price, R.R. & Lvov, Y.M. (2009) Organized shells on clay nanotubes for controlled release of macromolecules. Macromolecular Rapid Communications, 30, 99–103.CrossRefGoogle ScholarPubMed
Vinokurov, V.A., Stavitskaya, A.V., Chudakov, Y.A., Glotov, A.P., Ivanov, E.V., Gushchin, P.A. et al. (2018) Core–shell nanoarchitecture: Schiff-base assisted synthesis of ruthenium in clay nanotubes. Pure and Applied Chemistry, 90, 825.CrossRefGoogle Scholar
Wei, C., Lin, W.Y., Zainal, Z., Williams, N.E., Zhu, K., Kruzic, A.P. et al. (2002) Bactericidal activity of TiO2 photocatalyst in aqueous media: toward a solar-assisted water disinfection system. Environmental Science & Technology, 28, 934–938.CrossRefGoogle Scholar
Yang, T.T., Du, M.L., Zhang, M., Zhu, H., Wang, P. & Zou, M.L. (2015) Synthesis and immobilization of Pt nanoparticles on amino-functionalized halloysite nanotubes toward highly active catalysts. Nanomaterials and Nanotechnology, 5, 9.CrossRefGoogle Scholar
Yuan, P., Southon, P.D., Liu, Z., Green, M.E., Hook, J.M., Antill, S.J. & Kepert, C.J. (2008) Functionalization of halloysite clay nanotubes by grafting with γ-aminopropyltriethoxysilane. Journal of Physical Chemistry C, 112, 15742–15751.CrossRefGoogle Scholar
Zhang, J., Zhang, Y., Chen, Y., Du, L., Zhang, B., Zhang, H. et al. (2012) Preparation and characterization of novel polyethersulfone hybrid ultrafiltration membranes bending with modified halloysite nanotubes loaded with silver nanoparticles. Industrial & Engineering Chemistry Research, 51, 3081–3090.CrossRefGoogle Scholar
Zhang, Y., Chen, Y., Zhang, H., Zhang, B. & Liu, J. (2013) Potent antibacterial activity of a novel silver nanoparticle–halloysite nanotube nanocomposite powder. Journal of Inorganic Biochemistry, 118, 59–64.CrossRefGoogle ScholarPubMed
Zhao, L., Wang, H., Huo, K., Cui, L., Zhang, W., Ni, H. et al. (2011) Antibacterial nano-structured titania coating incorporated with silver nanoparticles. Biomaterials, 24, 5706–5716.CrossRefGoogle Scholar