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Surface capping and size-dependent toxicity of gold nanoparticles on different trophic levels

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Abstract

In the present study, the toxicity of gold nanoparticles (Au NPs) was evaluated on various trophic organisms. Bacteria, algae, cell line, and mice were used as models representing different trophic levels. Two different sizes (CIT30 and CIT40) and surface-capped (CIT30–polyvinyl pyrrolidone (PVP)-capped) Au NPs were selected. CIT30 Au NP aggregated more rapidly than CIT40 Au NP, while an additional capping of PVP (CIT30–PVP capped Au NP) was found to enhance its stability in sterile lake water medium. Interestingly, all the forms of NPs evaluated were stable in the cell culture medium during the exposure period. Size- and dose-dependent cytotoxicities were observed in both bacteria and algae, with a strong dependence on reactive oxygen species (ROS) generation and lactate dehydrogenase (LDH) release. CIT30–PVP capped Au NP showed a significant decrease in toxicity compared to CIT30 Au NP in bacteria and algae. In the SiHa cell line, dose- and exposure-dependent decline in cell viability were noted for all three types of Au NPs. In mice, the induction of DNA damage was size and dose dependent, and surface functionalization with PVP reduced the toxic effects of CIT30 Au NP. The exposure to CIT30, CIT40, and CIT30–PVP capped Au NPs caused an alteration of the oxidative stress-related endpoints in mice hepatocytes. The toxic effects of the gold nanoparticles were found to vary in diverse test systems, accentuating the importance of size and surface functionalization at different trophic levels.

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References

  • Abei H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  Google Scholar 

  • Alkilany AM, Murphy CJ (2010) Toxicity and cellular uptake of gold nanoparticles: what we have learned so far? J Nanoparticle Res 12:2313–2333

    Article  CAS  Google Scholar 

  • Anker JN, Hall WP, Lyandres O, Shah NC, Zhao J, Van Duyne RP (2008) Biosensing with plasmonic nanosensors. Nat Mater 7:442–453

    Article  CAS  Google Scholar 

  • Aruoja V, Dubourguier H, Kasemets K, Kahru A (2009) Toxicity of NPs of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ 407(4):1461–1468

    Article  CAS  Google Scholar 

  • Behra R, Wagner B, Sgier L, Kistler D (2015) Colloidal stability and toxicity of gold nanoparticles and gold chloride on Chlamydomonas reinhardtii. Aquat Geochem 21(2-4):331–342

    Article  CAS  Google Scholar 

  • Bozich JS, Lohse SE, Torelli MD, Murphy CJ, Hamers RJ, Klaper RD (2014) Surface chemistry, charge and ligand type impact the toxicity of gold nanoparticles to Daphnia magna. Environ Sci Nano 1(3):260–270

    Article  CAS  Google Scholar 

  • 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  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–311

    Article  CAS  Google Scholar 

  • Cedervall T, Lynch I, Lindman S, Berggård T, Thulin E, Nilsson H, Dawson KA, Linse S (2007) Understanding the nanoparticle–protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci U S A 104(7):2050–2055

    Article  CAS  Google Scholar 

  • Chen H, Dorrigan A, Saad S, Hare DJ, Cortie MB, Valenzuela S (2013) In vivo study of spherical gold nanoparticles: Inflammatory effects and distribution in mice. PLoS ONE 8(2):e58208. doi:10.1371/journal.pone.0058208

    Article  CAS  Google Scholar 

  • Cho WS, Cho M, Jeong J, Choi M, Cho HY, Han BS, Kim SH, Kim HO, Lim YT, Chung BH, Jeong J (2009) Acute toxicity and pharmacokinetics of 13 nm-sized PEG-coated gold nanoparticles. Toxicol Appl Pharmacol 236:16–24

    Article  CAS  Google Scholar 

  • Chuang S, Lee Y, Liang R, Roam G, Zeng Z, Tu H, Wang S, Chueh P (2013) Extensive evaluations of the cytotoxic effects of gold nanoparticles. Biochim Biophys Acta 1830:4960–4973

    Article  CAS  Google Scholar 

  • Chueh P, Liang R, Lee Y, Zeng Z, Chuang S (2014) Differential cytotoxic effects of gold nanoparticles in different mammalian cell lines. J Hazard Mater 264:303–312

    Article  CAS  Google Scholar 

  • Cooper GM. (2000) Cell walls and the extracellular matrix. In: The cell: a molecular approach. 2nd edn. Sinauer Associates, Sunderland (MA). Available from: http://www.ncbi.nlm.nih.gov/books/NBK9874/. Accessed 22 September 2015

  • Coradeghini R, Gioria S, García CP, Nativo P, Franchini F, Gilliland D, Ponti J, Rossi F (2013) Size-dependent toxicity and cell interaction mechanisms of gold nanoparticles on mouse fibroblasts. Toxicol Lett 217:205–216

    Article  CAS  Google Scholar 

  • Cumberland SA, Lead JR (2009) Particle size distribution of silver nanoparticles at environmentally relevant conditions. J Chromatogr A 1216:7

    Article  Google Scholar 

  • Dalai S, Pakrashi S, Suresh Kumar RS, Chandrasekaran N, Mukherjee A (2012) A comparative cytotoxicity study of TiO2 nanoparticles under light and dark conditions at low exposure concentrations. Toxicol Res 1(2):116–130

    Article  CAS  Google Scholar 

  • Dhawan A, Sharma V (2010) Toxicity assessment of nanomaterials: methods and challenges. Anal Bioanal Chem 398:3996

    Article  Google Scholar 

  • Diegoli S, Manciulea AL, Begum S, Jones IP, Lead JR, Preece JA (2008) Interaction between manufactured gold nanoparticles and naturally occurring organic macromolecules. Sci Total Environ 402:51–61

    Article  CAS  Google Scholar 

  • Eustis S, El-Sayed MA (2006) Why gold nanoparticles are more precious than pretty gold: noble metal surface plasmon resonance and its enhancement of the radiative and nonradiative properties of nanocrystals of different shapes. Chem Soc Rev 35:209–217

    Article  CAS  Google Scholar 

  • Freese C, Uboldi C, Gibson MI, Unger TE, Weksler BB, Romero IA, Couraud PO, Kirkpatrck JC (2012) Uptake and cytotoxicity of citrate-coated gold nanospheres: comparative studies on human endothelial and epithelial cells. Part Fibre Toxicol 9:23–32

    Article  CAS  Google Scholar 

  • Gao W, Xu K, Ji L, Tang B (2011) Effect of gold nanoparticles on glutathione depletion induced hydrogen peroxide generation and apoptosis in HL7702 cells. Toxicol Lett 205:86–95

    Article  CAS  Google Scholar 

  • Gao J, Huang X, Liu H, Zan F, Ren J (2012) Colloidal stability of gold nanoparticles modified with thiol compounds: bioconjugation and application in cancer cell imaging. Langmuir 28(9):4464–4471

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WD (1974) Glutathione S-transferases, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Herrmann M, Lorenz HM, Voll R, Grunke M, Woith W, Kalden JR (1994) A rapid and simple method for the isolation of apoptotic DNA fragments. Nucleic Acids Res 22:5506–5507

    Article  CAS  Google Scholar 

  • Hoecke KV, De Schamphelaere KAC, Ali Z, Zhang F, Elsaesser A, Rivera-Gil P, Parak WJ, Smagghe G, Howard CV, Janssen CR (2013) Ecotoxicity and uptake of polymer coated gold nanoparticles. Nanotoxicology 7(1):37–47

    Article  Google Scholar 

  • Hwang JH, Kim SJ, Kim YH, Noh JR, Gang GT, Chung BH, Song NW, Lee CH (2012) Susceptibility to gold nanoparticle-induced hepatotoxicity is enhanced in a mouse model of nonalcoholic steatohepatitis. Toxicology 294:27–35

    Article  CAS  Google Scholar 

  • Iswarya V, Bhuvaneshwari M, Alex SA, Iyer S, Chaudhuri G, Chandrasekaran PT, Bhalerao GM, Chakravarty S, Raichur AM, Chandrasekaran N, Mukherjee A (2015) Combined toxicity of two crystalline phases (anatase and rutile) of Titania nanoparticles towards freshwater microalgae: Chlorella sp. Aquat Toxicol 161:154–169

    Article  CAS  Google Scholar 

  • Jain PK, El-Sayed IH, El-Sayed MA (2007) Au nanoparticles target cancer. Nano Today 2:18–29

    Article  Google Scholar 

  • Jans H, Liu X, Austin L, Maes G, Huo Q (2009) Dynamic light scattering as a powerful tool for gold nanoparticle bioconjugation and biomolecular binding studies. Anal Chem 81:9425–9432

    Article  CAS  Google Scholar 

  • Keel T, Holliday R, Harper T (2010) Gold for good—gold and nanotechnology in the age of innovation. World Gold Counc. 1e20

  • Khan MS, Vishakante GD, Siddaramaiah H (2013) Gold nanoparticles: a paradigm shift in biomedical applications. Adv Colloid Interf Sci 199-200:44-58

  • Kim KT, Zaikova T, Hutchison JE, Tanguay RL (2013) Gold nanoparticles disrupt zebrafish eye development and pigmentation. Toxicol Sci 133(2):275–288

    Article  CAS  Google Scholar 

  • Kumar S, Gandhi KS, Kumar R (2006) Modeling of formation of gold nanoparticles by citrate method. Ind Eng Chem Res 46:3128–3136

    Article  Google Scholar 

  • Kumar A, Boruah BM, Liang XJ (2011) Gold nanoparticles: promising nanomaterials for the diagnosis of cancer and HIV/AIDS. J Nanomater 2011:22

    Google Scholar 

  • Kumar D, Kumari J, Pakrashi S, Dalai S, Raichur AM, Sastry TP, Mandal AB, Chandrasekaran N, Mukherjee A (2014) Qualitative toxicity assessment of AgNPs on the fresh water bacterial isolates and consortium at low level of exposure concentration. Ecotoxicol Environ Saf 108:152–160

    Article  CAS  Google Scholar 

  • Kumaravel TS, Jha AN (2006) Reliable comet assay measurements for detecting DNA damage induced by ionizing radiation and chemicals. Mutat Res 605:7–16

    Article  CAS  Google Scholar 

  • Lasagna-Reeves C, Gonzalez-Romero D, Barria MA, Olmedo I, Clos A, Ramanujam VMS, Urayama A, Vergara L, Kogan MJ, Soto C (2010) Bioaccumulation and toxicity of gold nanoparticles after repeated administration in mice. Biochem Biophys Res Commun 393:649–655

    Article  CAS  Google Scholar 

  • Leonard K, Ahmmad B, Okamura H, Kurawaki J (2011) In situ green synthesis of biocompatible ginseng capped gold nanoparticles with remarkable stability. Colloids Surf B: Biointerfaces 82(2):391–396

    Article  CAS  Google Scholar 

  • Li JJ, Hartono D, Ong CN, Bay BH, Yung LYL (2010) Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 31:5996–6003

    Article  CAS  Google Scholar 

  • Manivannan J, Sinha S, Ghosh M, Mukherjee A (2013) Evaluation of multi-endpoint assay to detect genotoxicity and oxidative stress in mice exposed to sodium fluoride. Mutat Res 751:59–65

    Article  Google Scholar 

  • Mossman T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assays. J Immunol Methods 65:55–63

    Article  Google Scholar 

  • Nur Y (2013) Gold nanoparticles: synthesis, characterisation and their effect on Pseudomonas flourescens. Doctoral dissertation, University of Birmingham

  • Organisation for Economic Cooperation and Development (OECD) (2011) Freshwater alga and cyanobacteria, growth inhibition test. OECD Guidelines for the Testing of Chemicals, Test No. 201. OECD Publishing, Paris, France. DOI: 10.1787/9789264069923-en

  • Osler GHR, Sommerkorn M (2007) Toward a complete soil C and N cycle: incorporating the soil fauna. Ecology 88(7):1611–1621

    Article  Google Scholar 

  • Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, Schmid G, Brandau W, Jahnen-Dechent W (2007) Size-dependent cytotoxicity of gold nanoparticles. Small 3:1941–1949

    Article  CAS  Google Scholar 

  • Pillai ZS, Kamat PV (2004) What factors control the size and shape of silver nanoparticles in the citrate ion reduction method? J Phys Chem B 108:945–951

    Article  CAS  Google Scholar 

  • Powers K, Brown S, Krishna V, Wasdo S, Moudgil B, Roberts S (2006) Research strategies for safety evaluation of nanomaterials. Part VI. Characterization of nanoscale particles for toxicological evaluation. Toxicol Sci 90:296–303

    Article  CAS  Google Scholar 

  • Remade J (1990) The cell wall and metal binding. In: Biosorption of heavy metals. CRC Press Boca Raton. 83-92

  • Renault S, Baudrimont M, Mesmer-Dudons N, Gonzalez P, Mornet S, Brisson A (2008) Impacts of gold nanoparticle exposure on two freshwater species: a phytoplanktonic alga (Scenedesmus subspicatus) and a benthic bivalve (Corbicula fluminea). Gold Bull 41:116–26

    Article  CAS  Google Scholar 

  • Rohiman A, Anshori I, Surawijaya A, Idris I (2011) Study of colloidal gold synthesis using Turkevich method. AIP Conf Proc 1415:39–42

    Article  CAS  Google Scholar 

  • Römer I, White TA, Baalousha M, Chipman K, Viant MR, Lead JR (2011) Aggregation and dispersion of silver nanoparticles in exposure media for aquatic toxicity tests. J Chromatogr A 1218(27):4226–4233

    Article  Google Scholar 

  • Sathishkumar M, Pavagadhi S, Mahadevan A, Balasubramanian R (2014) Biosynthesis of gold nanoparticles and related cytotoxicity evaluation using A549 cells. Ecotoxicol Environ Saf 114:232–40

    Article  Google Scholar 

  • Sayes CM, Marchione AA, Reed KL, Warheit DB (2007) Comparative pulmonary toxicity assessments of C60 water suspensions in rats: few differences in fullerene toxicity in vivo in contrast to in vitro profiles. Nano Lett 7:2399–2406

    Article  CAS  Google Scholar 

  • Schaechter M, Ingraham JL, Neidhardt FC (2006) Microbe. ASM Press, Washington, DC

    Book  Google Scholar 

  • Schipper M, Nakayama-Ratchford N, Davis CR, Kam NWS, Chu P, Liu Z, Sun X, Dai H, Gambhir SS (2008) A pilot toxicology study of single-walled carbon nanotubes in a small sample of mice. Nat Nanotechnol 3:216–221

    Article  CAS  Google Scholar 

  • Schulz M, Ma-Hock L, Brill S, Strauss V, Treumann S, Gröters S, Ravenzwaay BV, Landsiedel R (2012) Investigation on the genotoxicity of different sizes of gold nanoparticles administered to the lungs of rats. Mutat Res 745:51–57

    Article  CAS  Google Scholar 

  • Sedlak J, Lindsay RN (1968) Estimation of total protein bound and non-protein sulphydryl groups in tissue with Ellman reagent. Anal Biochem 25:192–1005

    Article  CAS  Google Scholar 

  • Simpson CA, Salleng KJ, Cliffel DE, Feldheim DL (2013) In vivo toxicity, biodistribution, and clearance of glutathione-coated gold nanoparticles. Nanomedicine 9:257–263

    Article  CAS  Google Scholar 

  • Sokolov K, Follen M, Aaron J, Pavlova I, Malpica A, Lotan R, Richartz-Kortum R (2003) Real-time vital optical imaging of precancer using anti-epidermal growth factor receptor antibodies conjugated to gold nanoparticles. Cancer Res 63:1999–2004

    CAS  Google Scholar 

  • Stankus DP, Lohse SE, Hutchison JE, Nason JA (2011) Interactions between natural organic matter and gold nanoparticles stabilized with different organic capping agents. Environ Sci Technol 45(8):3238–44

    Article  CAS  Google Scholar 

  • Tedesco S, Doyle H, Blasco J, Redmond G, Sheehan D (2010) Oxidative stress and toxicity of gold nanoparticles in Mytilus edulis. Aquat Toxicol 100:178–186

    Article  CAS  Google Scholar 

  • Tejamaya M, Römer I, Merrifield RC, Lead JR (2012) Stability of citrate, PVP, and PEG coated silver nanoparticles in ecotoxicology media. Environ Sci Technol 46(13):7011–7

    Article  CAS  Google Scholar 

  • Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu C, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221

    Article  CAS  Google Scholar 

  • Tolaymat TM, El Badawy AM, Genaidy A, Scheckel KG, Luxton TP, Suidan M (2010) An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer reviewed scientific papers. Sci Total Environ 408(5):999–1006

    Article  CAS  Google Scholar 

  • Turkevich J, Stevenson PC, Hillier J (1953) The formation of colloidal gold. J Phys Chem 57:670

    Article  CAS  Google Scholar 

  • Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using micro plate reader. Free Radic Biol Med 27(5):612–616

    Article  CAS  Google Scholar 

  • Wang S, Lawson R, Ray PC, Yu H (2011) Toxic effects of gold nanoparticles on Salmonella typhimurium bacteria. Toxicol Ind Health 27(6):547–554

    Article  CAS  Google Scholar 

  • Wu D, Zhang XD, Liu PX, Zhang LA, Fan FY, Guo ML (2011) Gold nanostructure: fabrication, surface modification, targeting imaging, and enhanced radiotherapy. Curr Nanosci 7:110–118

    Article  CAS  Google Scholar 

  • Yah CS (2013) The toxicity of gold nanoparticles in relation to their physiochemical properties. Biomed Res 24(3):400–413

    CAS  Google Scholar 

  • Yang H, Du L, Tian X, Fan Z, Sun C, Liu Y, Keelan JA, Nie G (2014) Effects of nanoparticle size and gestational age on maternal biodistribution and toxicity of gold nanoparticles in pregnant mice. Toxicol Lett 230:10–18

    Article  CAS  Google Scholar 

  • Zeng S, Cai M, Liang H, Hao J (2012) Size-dependent colorimetric visual detection of melamine in milk at 10 ppb level by citrate-stabilized Au nanoparticles. Anal Methods 4:2499

    Article  CAS  Google Scholar 

  • Zhang G, Yang Z, Lu W, Zhang R, Huang Q, Tian M, Li L, Liang D, Li C (2009) Influence of anchoring ligands and particle size on the colloidal stability and in vivo biodistribution of polyethylene glycol-coated gold nanoparticles in tumor-xenografted mice. Biomaterials 30(10):1928–36

    Article  CAS  Google Scholar 

  • Zhang X, Wu D, Shen X, Liu P, Yang N, Zhao B, Zhang H, Sun Y, Zhang L, Fan F (2011) Size-dependent in vivo toxicity of PEG-coated gold nanoparticles. Int J Nanomedicine 6:2071–2081

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank the Advanced Facility for Microscopy and Microanalysis (AFMM), Indian Institute of Science, Bangalore, for the transmission electron microscopy facility and the Center for Research in Nanoscience and Nanotechnology (CRNN), University of Calcutta, for the instrumentation facilities.

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Correspondence to Anita Mukherjee or Amitava Mukherjee.

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For the mice model study, the ethical clearance for the use of animals in the study was obtained from the institutional animal ethics committee.

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Responsible editor: Philippe Garrigues

V. Iswarya and Arpita De contributed equally to this work.

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A detailed description about the methodology of oxidative stress assays have been provided in the supplementary information (DOCX 21 kb)

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Iswarya, V., Manivannan, J., De, A. et al. Surface capping and size-dependent toxicity of gold nanoparticles on different trophic levels. Environ Sci Pollut Res 23, 4844–4858 (2016). https://doi.org/10.1007/s11356-015-5683-0

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