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Cellular effects of manufactured nanoparticles: effect of adsorption ability of nanoparticles

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Abstract

Nanoparticles are important industrial materials. However, many nanoparticles show biological effects, including toxic activity. Metal ion release is the most important factor affecting the biological effects of nanoparticles. In addition, nanoparticles have large adsorption ability. The adsorption ability, in particular protein adsorption to nanoparticles, has an effect on cellular uptake and cellular metabolisms. Moreover, the adsorption ability of nanoparticles causes artificial effects in in vitro systems. Consequently, accurate determination of released or secreted proteins such as lactate dehydrogenase and cytokines adsorbed to nanoparticles is affected. In addition, artificial effects cause overestimation or underestimation of the cytotoxicity of nanoparticles. Therefore, measurement of the protein adsorption of nanoparticles is important. Some methods for the determination of the adsorption to nanoparticles have been suggested. The flow field-flow fractionation method is one of the efficient techniques for determining proteins on the surface of nanoparticles. The cellular effects caused by nanoparticles should be carefully considered.

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References

  • Alarifi S, Ali D, Al Omar Y, Ahamed M, Siddiqui MA, Al-Khedhairy AA (2013) Oxidative stress contributes to cobalt oxide nanoparticles-induced cytotoxicity and DNA damage in human hepatocarcinoma cells. Int J Nanomed 8:17–23

    Article  Google Scholar 

  • Asuri P, Bale SS, Pangule RC, Shah DA, Kane RS, Dordick JS (2007) Structure, function, and stability of enzymes covalently attached to single-walled carbon nanotubes. Langmuir 23:12318–12321

    Article  PubMed  CAS  Google Scholar 

  • Avram L, Cohen Y (2005) Diffusion measurements for molecular capsules: pulse sequences effect on water signal decay. J Am Chem Soc 127:5714–5719

    Article  PubMed  CAS  Google Scholar 

  • Baier G, Costa C, Zeller A, Baumann D, Sayer C, Araujo PH, Mailänder V, Musyanovych A, Landfester K (2011) BSA adsorption on differently charged polystyrene nanoparticles using isothermal titration calorimetry and the influence on cellular uptake. Macromol Biosci 11:628–638

    Article  PubMed  CAS  Google Scholar 

  • Borm PJ, Kreyling W (2004) Toxicological hazards of inhaled nanoparticles-potential implications for drug delivery. J Nanosci Nanotechnol 4:521–531

    Article  PubMed  CAS  Google Scholar 

  • Casey A, Herzog E, Lyng FM, Byrne HJ, Chambers G, Davoren M (2008) Single walled carbon nanotubes induce indirect cytotoxicity by medium depletion in A549 lung cells. Toxicol Lett 179:78–84

    Article  PubMed  CAS  Google Scholar 

  • Cedervall T, Lynch I, Foy M, Berggård T, Donnelly SC, Cagney G, Linse S, Dawson KA (2007a) Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. Angew Chem Int Ed Engl 46:5754–5756

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen A, Shapriro MJ (1998) NOE pumping: a novel NMR technique for identification of compounds with binding affinity to macromolecules. J Am Chem Soc 120:10258–10259

    Article  CAS  Google Scholar 

  • Cronholm P, Karlsson HL, Hedberg J, Lowe TA, Winnberg L, Elihn K, Wallinder IO, Möller L (2013) Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions. Small. doi:10.1002/smll.201201069

  • Deguchi S, Yamazaki T, Mukai SA, Usami R, Horikoshi K (2007) Stabilization of C60 nanoparticles by protein adsorption and its implications for toxicity studies. Chem Res Toxicol 20:854–858

    Article  PubMed  CAS  Google Scholar 

  • Dutta D, Sundaram SK, Teeguarden JG, Riley BJ, Fifield LS, Jacobs JM, Addleman SR, Kaysen GA, Moudgil BM, Weber TJ (2007) Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol Sci 100:303–315

    Article  PubMed  CAS  Google Scholar 

  • Eom HJ, Choi J (2009) Oxidative stress of CeO2 nanoparticles via p38-Nrf-2 signaling pathway in human bronchial epithelial cell, Beas-2B. Toxicol Lett 187:77–83

    Article  PubMed  CAS  Google Scholar 

  • Fröhlich E (2012) The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomed 7:5577–5591

    Article  Google Scholar 

  • Fukui H, Horie M, Endoh S, Kato H, Fujita K, Nishio K, Komaba LK, Maru J, Miyauhi A, Nakamura A, Kinugasa S, Yoshida Y, Hagihara Y, Iwahashi H (2012) Association of zinc ion release and oxidative stress induced by intratracheal instillation of ZnO nanoparticles to rat lung. Chem Biol Interact 198:29–37

    Article  PubMed  CAS  Google Scholar 

  • Gojova A, Guo B, Kota RS, Rutledge JC, Kennedy IM, Barakat AI (2007) Induction of inflammation in vascular endothelial cells by metal oxide nanoparticles: effect of particle composition. Environ Health Perspect 115:403–409

    Article  PubMed  CAS  Google Scholar 

  • Heng BC, Zhao X, Tan EC, Khamis N, Assodani A, Xiong S, Ruedl C, Ng KW, Loo JS (2011) Evaluation of the cytotoxic and inflammatory potential of differentially shaped zinc oxide nanoparticles. Arch Toxicol 85:1517–1528

    Article  PubMed  CAS  Google Scholar 

  • Hirano A, Uda K, Maeda Y, Akasaka T, Shiraki K (2010) One-dimensional protein-based nanoparticles induce lipid bilayer disruption: carbon nanotube conjugates and amyloid fibrils. Langmuir 26:17256–17259

    Article  PubMed  CAS  Google Scholar 

  • Hirsch V, Kinnear C, Moniatte M, Rothen-Rutishauser B, Clift MJ, Fink A (2013) Surface charge of polymer coated SPIONs influences the serum protein adsorption, colloidal stability and subsequent cell interaction in vitro. Nanoscale. doi:10.1039/C2NR33134A

  • Horie M, Nishio K, Fujita K, Endoh S, Miyauchi A, Saito Y, Iwahashi H, Yamamoto K, Murayama H, Nakano H, Nanashima N, Niki E, Yoshida Y (2009a) Protein adsorption of ultrafine metal oxide and its influence on cytotoxicity toward cultured cells. Chem Res Toxicol 22:543–553

    Article  PubMed  CAS  Google Scholar 

  • Horie M, Nishio K, Fujita K, Kato H, Nakamura A, Kinugasa S, Endoh S, Miyauchi A, Yamamoto K, Murayama H, Niki E, Iwahashi H, Yoshida Y, Nakanishi J (2009b) Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chem Res Toxicol 222:1415–1426

    Article  Google Scholar 

  • Horie M, Nishio K, Fujita K, Kato H, Endoh S, Suzuki M, Nakamura A, Miyauchi A, Kinugasa S, Yamamoto K, Iwahashi H, Murayama H, Niki E, Yoshida Y (2010) Cellular responses by stable and uniform ultrafine titanium dioxide particles in culture-medium dispersions when secondary particle size was 100 nm or less. Toxicol In Vitro 24:1629–1638

    Article  PubMed  CAS  Google Scholar 

  • Horie M, Fukui H, Nishio K, Endoh S, Kato H, Fujita K, Miyauchi A, Nakamura A, Shichiri M, Ishida N, Kinugasa S, Morimoto Y, Niki E, Yoshida Y, Iwahashi H (2011a) Evaluation of acute oxidative stress induced by NiO nanoparticles in vivo and in vitro. J Occup Health 53:64–74

    Article  PubMed  CAS  Google Scholar 

  • Horie M, Nishio K, Kato H, Fujita K, Endoh S, Nakamura A, Miyauchi A, Kinugasa S, Yamamoto K, Niki E, Yoshida Y, Hagihara Y, Iwahashi H (2011b) Cellular responses induced by cerium oxide nanoparticles: induction of intracellular calcium level and oxidative stress on culture cells. J Biochem 150:461–471

    Article  PubMed  CAS  Google Scholar 

  • Horie M, Fujita K, Kato H, Endoh S, Nishio K, Komaba LK, Nakamura A, Miyauchi A, Kinugasa S, Hagihara Y, Niki E, Yoshida Y, Iwahashi H (2012a) Association of the physical and chemical properties and the cytotoxicity of metal oxide nanoparticles: metal ion release, adsorption ability and specific surface area. Metallomics 4:350–360

    Article  PubMed  CAS  Google Scholar 

  • Horie M, Kato H, Fujita K, Endoh S, Iwahashi H (2012b) In vitro evaluation of cellular response induced by manufactured nanoparticles. Chem Res Toxicol 25:605–619

    Article  PubMed  CAS  Google Scholar 

  • Horie M, Komaba LK, Kato H, Nakamura A, Yamamoto K, Endoh S, Fujita K, Kinugasa S, Mizuno K, Hagihara Y, Yoshida Y, Iwahashi H (2012c) Evaluation of cellular influences induced by stable nanodiamond dispersion; the cellular influences of nanodiamond are small. Diam Relat Mater 24:15–24

    Article  CAS  Google Scholar 

  • Horie M, Nishio K, Endoh S, Kato H, Fujita K, Miyauchi A, Nakamura A, Kinugasa S, Yamamoto K, Niki E, Yoshida Y, Iwahashi H (2013a) Chromium(III) oxide nanoparticles induced remarkable oxidative stress and apoptosis on culture cells. Environ Toxicol 28:61–75

    Article  PubMed  CAS  Google Scholar 

  • Horie M, Stowe M, Tabei M, Kato H, Nakamura A, Endoh S, Morimoto Y, Fujita K (2013b) Dispersant affects the cellular influences of single-wall carbon nanotube: the role of CNT as carrier of dispersants. Toxicol Mech Methods. doi:10.3109/15376516.2012.755595

  • Jia G, Wang H, Yan L, Wang X, Pei R, Yan T, Zhao Y, Guo X (2005) Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ Sci Technol 39:1378–1383

    Article  PubMed  CAS  Google Scholar 

  • Karlsson HL, Cronholm P, Gustafsson J, Möller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–1732

    Article  PubMed  CAS  Google Scholar 

  • Kato H, Takahashi K, Saito T, Kinugasa S (2008) Characterization of nanoparticles in an aqueous solution with bound water molecules using pulsed field gradient nuclear magnetic resonance spectroscopy. Chem Lett 37:1128–1129

    Article  CAS  Google Scholar 

  • Kato H, Mizuno K, Shimada M, Nakamura A, Takahashi K, Hata K, Kinugasa S (2009a) Observations of bound Tween80 surfactant molecules on single-walled carbon nanotubes in an aqueous solution. Carbon 47:3434–3440

    Article  CAS  Google Scholar 

  • Kato H, Nakamura A, Takahashi K, Kinugasa S (2009b) Size effect on UV–Vis absorption properties of colloidal C(60) particles in water. Phys Chem Chem Phys 11:4946–4948

    Article  PubMed  CAS  Google Scholar 

  • Kato H, Fujita K, Horie M, Suzuki M, Nakamura A, Endoh S, Yoshida Y, Iwahashi H, Takahashi K, Kinugasa S (2010a) Dispersion characteristics of various metal oxide secondary nanoparticles in culture medium for in vitro toxicology assessment. Toxicol In Vitro 24:1009–1018

    Article  PubMed  CAS  Google Scholar 

  • Kato H, Shinohara N, Nakamura A, Horie M, Fujita K, Takahashi K, Iwahashi H, Endoh S, Kinugasa S (2010b) Characterization of fullerene colloidal suspension in a cell culture medium for in vitro toxicity assessment. Mol BioSyst 6:1238–1246

    Article  PubMed  CAS  Google Scholar 

  • Kato H, Nakamura A, Horie M, Endoh S, Fujita K, Iwahashi H, Kinugasa S (2011) Preparation and characterization of stable dispersions of carbon black and nanodiamond in culture medium for in vitro toxicity assessment. Carbon 49:3989–3997

    Article  CAS  Google Scholar 

  • Kermanizadeh A, Pojana G, Gaiser BK, Birkedal R, Bilaničová D, Wallin H, Jensen KA, Sellergren B, Hutchison GR, Marcomini A, Stone V (2012) In vitro assessment of engineered nanomaterials using a hepatocyte cell line: cytotoxicity, pro-inflammatory cytokines and functional markers. Nanotoxicology. doi:10.3109/17435390.2011.653416

  • Klinger A, Steinberg D, Kohavi D, Sela MN (1997) Mechanism of adsorption of human albumin to titanium in vitro. J Biomed Mater Res 36:387–392

    Article  PubMed  CAS  Google Scholar 

  • Kroll A, Pillukat MH, Hahn D, Schnekenburger J (2012) Interference of engineered nanoparticles with in vitro toxicity assays. Arch Toxicol 86:1123–1136

    Article  PubMed  CAS  Google Scholar 

  • Lesniak A, Fenaroli F, Monopoli MP, Åberg C, Dawson KA, Salvati A (2012) Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6:5845–5857

    Article  PubMed  CAS  Google Scholar 

  • Lesniak A, Salvati A, Santos-Martinez MJ, Radomski MW, Dawson KA, Aberg C (2013) Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. J Am Chem Soc 135:1438–1444

    Article  PubMed  CAS  Google Scholar 

  • Lin W, Huang YW, Zhou XD, Ma Y (2006) Toxicity of cerium oxide nanoparticles in human lung cancer cells. Int J Toxicol 25:451–457

    Article  PubMed  CAS  Google Scholar 

  • Lindman S, Lynch I, Thulin E, Nilsson H, Dawson KA, Linse S (2007) Systematic investigation of the thermodynamics of HSA adsorption to N-iso-propylacrylamide/N-tert-butylacrylamide copolymer nanoparticles. Effects of particle size and hydrophobicity. Nano Lett 7:914–920

    Article  PubMed  CAS  Google Scholar 

  • Lundqvist M, Stigler J, Cedervall T, Berggård T, Flanagan MB, Lynch I, Elia G, Dawson K (2011) The evolution of the protein corona around nanoparticles: a test study. ACS Nano 5:7503–7509

    Article  PubMed  CAS  Google Scholar 

  • Matsuura K, Saito T, Okazaki T, Ohshima S, Yumura M, Iijima S (2006) Selectivity of water-soluble proteins in single-walled carbon nanotube dispersions. Chem Phys Lett 429:497–502

    Article  CAS  Google Scholar 

  • Monteiro-Riviere NA, Inman AO, Zhang LW (2009) Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 234:222–235

    Article  PubMed  CAS  Google Scholar 

  • Morishige T, Yoshioka Y, Tanabe A, Yao X, Tsunoda S, Tsutsumi Y, Mukai Y, Okada N, Nakagawa S (2010) Titanium dioxide induces different levels of IL-1beta production dependent on its particle characteristics through caspase-1 activation mediated by reactive oxygen species and cathepsin B. Biochem Biophys Res Commun 392:160–165

    Article  PubMed  CAS  Google Scholar 

  • Norde W, Giacomelli CE (2000) BSA structural changes during homomolecular exchange between the adsorbed and the dissolved states. J Biotechnol 79:259–268

    Article  PubMed  CAS  Google Scholar 

  • Pagliari F, Mandoli C, Forte G, Magnani E, Pagliari S, Nardone G, Licoccia S, Minieri M, Di Nardo P, Traversa E (2012) Cerium oxide nanoparticles protect cardiac progenitor cells from oxidative stress. ACS Nano 6:3767–3775

    Article  PubMed  CAS  Google Scholar 

  • Park EJ, Park K (2009) Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol Lett 184:18–25

    Article  PubMed  CAS  Google Scholar 

  • Park EJ, Yi J, Chung KH, Ryu DY, Choi J, Park K (2008) Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells. Toxicol Lett 180:222–229

    Article  PubMed  CAS  Google Scholar 

  • Patil S, Sandberg A, Heckert E, Self W, Seal S (2007) Protein adsorption and cellular uptake of cerium oxide nanoparticles as a function of zeta potential. Biomaterials 28:4600–4607

    Article  PubMed  CAS  Google Scholar 

  • Rahman Q, Lohani M, Dopp E, Pemsel H, Jonas L, Weiss DG, Schiffmann D (2002) Evidence that ultrafine titanium dioxide induces micronuclei and apoptosis in Syrian hamster embryo fibroblasts. Environ Health Perspect 110:797–800

    Article  PubMed  CAS  Google Scholar 

  • Sabatino P, Casella L, Granata A, Iafisco M, Lesci IG, Monzani E, Roveri N (2007) Synthetic chrysotile nanocrystals as a reference standard to investigate surface-induced serum albumin structural modifications. J Colloid Interface Sci 314:389–397

    Article  PubMed  CAS  Google Scholar 

  • Schimpf M, Caldwell K, Giddings JC (2000) Field-flow fractionation handbook. Wiley, Hoboken

    Google Scholar 

  • Schubert D, Dargusch R, Raitano J, Chan SW (2006) Cerium and yttrium oxide nanoparticles are neuroprotective. Biochem Biophys Res Commun 342:86–91

    Article  PubMed  CAS  Google Scholar 

  • Seki H, Sei Y, Shikii K, Shimotakahara S, Utsumi H, Yamaguchi K, Tashiro M (2004) Application of difference NOE-pumping NMR technique and cold-spray ionization mass spectrometry to identify a ligand binding with a protein receptor. Anal Sci 20:1467–1470

    Article  PubMed  CAS  Google Scholar 

  • Selim ME, Hendi AA (2012) Gold nanoparticles induce apoptosis in MCF-7 human breast cancer cells. Asian Pac J Cancer Prev 13:1617–1620

    Article  PubMed  Google Scholar 

  • Shen XC, Liou XY, Ye LP, Liang H, Wang ZY (2007) Spectroscopic studies on the interaction between human hemoglobin and CdS quantum dots. J Colloid Interface Sci 311:400–406

    Article  PubMed  CAS  Google Scholar 

  • Srivastava R, Rahman Q, Kashyap M, Singh A, Jain G, Jahan S, Lohani M, Lantow M, Pant A (2013) Nano-titanium dioxide induces genotoxicity and apoptosis in human lung cancer cell line, A549. Hum Exp Toxicol 32:153–166

    Article  PubMed  CAS  Google Scholar 

  • Suresh AK, Pelletier DA, Wang W, Morrell-Falvey JL, Gu B, Doktycz MJ (2012) Cytotoxicity induced by engineered silver nanocrystallites is dependent on surface coatings and cell types. Langmuir 28:2727–2735

    Article  PubMed  CAS  Google Scholar 

  • Tedja R, Lim M, Amal R, Marquis C (2012) Effects of serum adsorption on cellular uptake profile and consequent impact of titanium dioxide nanoparticles on human lung cell lines. ACS Nano 6:4083–4093

    Article  PubMed  CAS  Google Scholar 

  • Toduka Y, Toyooka T, Ibuki Y (2012) Flow cytometric evaluation of nanoparticles using side-scattered light and reactive oxygen species-mediated fluorescence-correlation with genotoxicity. Environ Sci Technol 46:7629–7636

    Article  PubMed  CAS  Google Scholar 

  • Tsou TC, Yeh SC, Tsai FY, Lin HJ, Cheng TJ, Chao HR, Tai LA (2010) Zinc oxide particles induce inflammatory responses in vascular endothelial cells via NF-κB signaling. J Hazard Mater 183:182–188

    Article  PubMed  CAS  Google Scholar 

  • Veranth JM, Kaser EG, Veranth MM, Koch M, Yost GS (2007) Cytokine responses of human lung cells (BEAS-2B) treated with micron-sized and nanoparticles of metal oxides compared to soil dusts. Part Fibre Toxicol 4:2

    Article  PubMed  Google Scholar 

  • Wassell DT, Embery G (1996) Adsorption of bovine serum albumin on to titanium powder. Biomaterials 17:859–864

    Article  PubMed  CAS  Google Scholar 

  • Xia T, Kovochich M, Liong M, Mädler L, Gilbert B, Shi H, Yeh JI, Zink JI, Nel AE (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2:2121–2134

    Article  PubMed  CAS  Google Scholar 

  • Zaqout MS, Sumizawa T, Igisu H, Wilson D, Myojo T, Ueno S (2012) Binding of titanium dioxide nanoparticles to lactate dehydrogenase. Environ Health Prev Med 17:341–345

    Article  PubMed  CAS  Google Scholar 

  • Zhu X, Zhou J, Cai Z (2011) TiO2 nanoparticles in the marine environment: impact on the toxicity of tributyltin to abalone (Haliotis diversicolor supertexta) embryos. Environ Sci Technol 45:3753–3758

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Kazuhiro Yamamoto of Research Institute of Instrumentation Frontier, AIST, for kindly supplying the images of TEM observations.

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Authors and Affiliations

  1. Institute of Industrial Ecological Sciences, University of Occupational and Environmental Health, Japan, Kitakyushu, Fukuoka, Japan

    Masanori Horie

  2. National Metrology Institute of Japan (NMIJ), National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan

    Haruhisa Kato

  3. Faculty of Applied Biological Sciences, Gifu University, Gifu, Japan

    Hitoshi Iwahashi

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  1. Masanori Horie
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  2. Haruhisa Kato
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Correspondence to Masanori Horie.

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Horie, M., Kato, H. & Iwahashi, H. Cellular effects of manufactured nanoparticles: effect of adsorption ability of nanoparticles. Arch Toxicol 87, 771–781 (2013). https://doi.org/10.1007/s00204-013-1033-5

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