Skip to main content
SpringerLink
Log in

Impact of surface coating and food-mimicking media on nanosilver-protein interaction

  • Research Paper
  • Published:
Journal of Nanoparticle Research Aims and scope Submit manuscript

Abstract

The application of silver nanoparticles (AgNPs) in food contact materials has recently become a subject of dispute due to the possible migration of silver in nanoform into foods and beverages. Therefore, the analysis of the interaction of AgNPs with food components, especially proteins, is of high importance in order to increase our knowledge of the behavior of nanoparticles in food matrices. AgPURE™ W10 (20 nm), an industrially applied nanomaterial, was compared with AgNPs of similar size frequently investigated for scientific purposes differing in the surface capping agent (spherical AgNP coated with either PVP or citrate). The interactions of the AgNPs with whey proteins (BSA, α-lactalbumin and β-lactoglobulin) at different pH values (4.2, 7 or 7.4) were investigated using surface plasmon resonance, SDS-PAGE, and asymmetric flow field-flow fractionation. The data obtained by the three different methods correlated well. Besides the nature of the protein and the nanoparticle coating, the environment was shown to affect the interaction significantly. The strongest interaction was obtained with BSA and AgNPs in an acidic environment. Neutral and slightly alkaline conditions however, seemed to prevent the AgNP-protein interaction almost completely. Furthermore, the interaction of whey proteins with AgPURE™ W10 was found to be weaker compared to the interaction with the other two AgNPs under all conditions investigated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alarcon EI, Bueno-Alejo CJ, Noel CW, Stamplecoskie KG, Pacioni NL, Poblete H, Scaiano JC (2013) Human serum albumin as protecting agent of silver nanoparticles: role of the protein conformation and amine groups in the nanoparticle stabilization. J Nanopart Res 15:1374–1377

    Article  Google Scholar 

  • Artiaga G, Ramos K, Ramos L, Cámara C, Gómez-Gómez M (2015) Migration and characterisation of nanosilver from food containers by af4-icp-ms. Food Chem 166:76–85

    Article  Google Scholar 

  • Ashby J, Schachermeyer S, Pan S, Zhong W (2013) Dissociation-based screening of nanoparticle-protein interaction via flow field-flow fractionation. Anal Chem 85:7494–7501

    Article  Google Scholar 

  • Ashkarran AA, Ghavami M, Aghaverdi H, Stroeve P, Mahmoudi M (2012) Bacterial effects and protein corona evaluations: crucial ignored factors in the prediction of bio-efficacy of various forms of silver nanoparticles. Chem Res Toxicol 25:1231–1242

    Article  Google Scholar 

  • Bolea E, Jimenez-Lamana J, Laborda F, Abad-Alvaro I, Blade C, Arola L, Castillo JR (2014) Detection and characterization of silver nanoparticles and dissolved species of silver in culture medium and cells by asflfff-uv-vis-icpms: application to nanotoxicity tests. Anal 139:914–922

    Article  Google Scholar 

  • Bolea E, Jimenez-Lamana J, Laborda F, Castillo JR (2011) Size characterization and quantification of silver nanoparticles by asymmetric flow field-flow fractionation coupled with inductively coupled plasma mass spectrometry. Anal Bioanal Chem 401:2723–2732

    Article  Google Scholar 

  • Botasini S, Méndez E (2013) Silver nanoparticle aggregation not triggered by an ionic strength mechanism. J Nanopart Res 15:1526

    Article  Google Scholar 

  • Bouwmeester H, Brandhoff P, Marvin HJP, Weigel S, Peters RJB (2014) State of the safety assessment and current use of nanomaterials in food and food production. Trends Food Sci Technol 40:200–210

    Article  Google Scholar 

  • Brahma A, Mandal C, Bhattacharyya D (2005) Characterization of a dimeric unfolding intermediate of bovine serum albumin under mildly acidic condition. Biochim Biophys Acta 1751:159–169

    Article  Google Scholar 

  • Brewer SH, Glomm WR, Johnson MC, Knag MK, Franzen S (2005) Probing bsa binding to citrate-coated gold nanoparticles and surfaces. Langmuir 21:9303–9307

    Article  Google Scholar 

  • Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V (2010) Time evolution of the nanoparticle protein corona. ACS Nano 4:3623–3632

    Article  Google Scholar 

  • Cedervall T et al (2007a) Detailed identification of plasma proteins adsorbed on copolymer nanoparticles. Angew Chem Int Ed 46:5754–5756

    Article  Google Scholar 

  • Cedervall T et al (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  Google Scholar 

  • Chakraborty S, Joshi P, Shanker V, Ansari ZA, Singh SP, Chakrabarti P (2011) Contrasting effect of gold nanoparticles and nanorods with different surface modifications on the structure and activity of bovine serum albumin. Langmuir 27:7722–7731

    Article  Google Scholar 

  • Cukalevski R, Lundqvist M, Oslakovic C, Dahlbäck B, Linse S, Cedervall T (2011) Structural changes in apolipoproteins bound to nanoparticles. Langmuir 27:14360–14369

    Article  Google Scholar 

  • De M, You CC, Srivastava S, Rotello VM (2007) Biomimetic interactions of proteins with functionalized nanoparticles: a thermodynamic study. J Am Chem Soc 129:10747–10753

    Article  Google Scholar 

  • Delay M, Dolt T, Woellhaf A, Sembritzki R, Frimmel FH (2011) Interactions and stability of silver nanoparticles in the aqueous phase: influence of natural organic matter (nom) and ionic strength. J Chromatogr A 1218:4206–4212

    Article  Google Scholar 

  • Echegoyen Y, Nerin C (2013) Nanoparticle release from nano-silver antimicrobial food containers. Food Chem Toxicol 62:16–22

    Article  Google Scholar 

  • Feng M, Morales AB, Poot A, Beugeling T, Bantjes A (1995) Effects of tween 20 on the desorption of proteins from polymer surfaces. J Biomater Sci Polym Ed 7:415–424

    Article  Google Scholar 

  • Gebregeorgis A, Bhan C, Wilson O, Raghavan D (2013) Characterization of silver/bovine serum albumin (Ag/BSA) nanoparticles structure: morphological, compositional, and interaction studies. J Colloid Interface Sci 389:31–41

    Article  Google Scholar 

  • Geranio L, Heuberger M, Nowack B (2009) The behavior of silver nanotextiles during washing. Environ Sci Technol 43:8113–8118

    Article  Google Scholar 

  • Gigault J, Pettibone JM, Schmitt C, Hackley VA (2014) Rational strategy for characterization of nanoscale particles by asymmetric-flow field flow fractionation: a tutorial. Anal Chim Acta 809:9–24

    Article  Google Scholar 

  • Gnanadhas DP, Ben Thomas M, Thomas R, Raichur AM, Chakravortty D (2013) Interaction of silver nanoparticles with serum proteins affects their antimicrobial activity in vivo. Antimicrob Agents Chemother 57:4945–4955

    Article  Google Scholar 

  • Hadrup N, Lam HR (2014) Oral toxicity of silver ions, silver nanoparticles and colloidal silver—a review. Regul Toxicol Pharmacol 68:1–7

    Article  Google Scholar 

  • Hakansson A, Magnusson E, Bergenstahl B, Nilsson L (2012) Hydrodynamic radius determination with asymmetrical flow field-flow fractionation using decaying cross-flows. Part I. A theoretical approach. J Chromatogr A 1253:120–126

    Article  Google Scholar 

  • Haynes CL (2001) Nanosphere lithography: a versatile nanofabrication tool for studies of size-dependent nanoparticle optics. J Phys Chem B 105:5599–5611

    Article  Google Scholar 

  • Hellstrand E et al (2009) Complete high-density lipoproteins in nanoparticle corona. FEBS J 276:3372–3381

    Article  Google Scholar 

  • Huhn D et al (2013) Polymer-coated nanoparticles interacting with proteins and cells: focusing on the sign of the net charge. ACS Nano 7:3253–3263

    Article  Google Scholar 

  • Iosin M, Canpean V, Astilean S (2011) Spectroscopic studies on pH- and thermally induced conformational changes of bovine serum albumin adsorbed onto gold nanoparticles. J Photochem Photobiol A 217:395–401

    Article  Google Scholar 

  • Jara FL, Carrera Sánchez C, Rodríguez Patino JM, Pilosof AMR (2014) Competitive adsorption behavior of β-lactoglobulin, α-lactalbumin, bovin serum albumin in presence of hydroxypropylmethylcellulose. Influence of pH. Food Hydrocoll 35:189–197

    Article  Google Scholar 

  • Khot LR, Sankaran S, Maja JM, Ehsani R, Schuster EW (2012) Applications of nanomaterials in agricultural production and crop protection: a review. Crop Prot 35:64–70

    Article  Google Scholar 

  • Klein CL et al. (2011) Nm-300 silver characterisation, stability, homogeneity. Publications Office of the European Union EUR 24693 EN:1-84

  • Kreibig U, Genzel L (1985) Optical absorption of small metallic particles. Surf Sci 156:678–700

    Article  Google Scholar 

  • Kurylowicz M, Paulin H, Mogyoros J, Giuliani M, Dutcher JR (2014) The effect of nanoscale surface curvature on the oligomerization of surface-bound proteins. J R Soc Interface 11:20130818

    Article  Google Scholar 

  • Ledwith DM, Whelan AM, Kelly JM (2007) A rapid, straight-forward method for controlling the morphology of stable silver nanoparticles. J Mater Chem 17:2459–2464

    Article  Google Scholar 

  • Lehner R, Wang X, Marsch S, Hunziker P (2013) Intelligent nanomaterials for medicine: carrier platforms and targeting strategies in the context of clinical application. Nanomedicine 9:742–757

    Article  Google Scholar 

  • Liu J, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175

    Article  Google Scholar 

  • Liu W, Rose J, Plantevin S, Auffan M, Bottero JY, Vidaud C (2013) Protein corona formation for nanomaterials and proteins of a similar size: hard or soft corona? Nanoscale 5:1658–1668

    Article  Google Scholar 

  • Loeschner K et al (2013) Optimization and evaluation of asymmetric flow field-flow fractionation of silver nanoparticles. J Chromatogr A 1272:116–125

    Article  Google Scholar 

  • Lozano O, Mejia J, Tabarrant T, Masereel B, Dogne JM, Toussaint O, Lucas S (2012) Quantification of nanoparticles in aqueous food matrices using particle-induced x-ray emission. Anal Bioanal Chem 403:2835–2841

    Article  Google Scholar 

  • Lundqvist M, Sethson I, Jonsson BH (2004) Protein adsorption onto silica nanoparticles: conformational changes depend on the particles’ curvature and the protein stability. Langmuir 20:10639–10647

    Article  Google Scholar 

  • Lundqvist M et al (2011) The evolution of the protein corona around nanoparticles: a test study. ACS Nano 5:7503–7509

    Article  Google Scholar 

  • Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA (2008) Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc Natl Acad Sci USA 105:14265–14270

    Article  Google Scholar 

  • Lynch I, Dawson KA (2008) Protein-nanoparticle interactions. Nano Today 3:40–47

    Article  Google Scholar 

  • MacCuspie RI (2011) Colloidal stability of silver nanoparticles in biologically relevant conditions. J Nanopart Res 13:2893–2908

    Article  Google Scholar 

  • Maffre P, Nienhaus K, Amin F, Parak WJ, Nienhaus GU (2011) Characterization of protein adsorption onto FePt nanoparticles using dual-focus fluorescence correlation spectroscopy. Beilstein J Nanotechnol 2:374–383

    Article  Google Scholar 

  • Mahmoudi M, Lynch I, Ejtehadi MR, Monopoli MP, Bombelli FB, Laurent S (2011) Protein-nanoparticle interactions: opportunities and challenges. Chem Rev 111:5610–5637

    Article  Google Scholar 

  • Mahmoudi M, Sheibani S, Milani AS, Rezaee F, Gauberti M, Dinarvand R, Vali H (2015) Crucial role of the protein corona for the specific targeting of nanoparticles. Nanomedicine (Lond) 10:215–226

    Article  Google Scholar 

  • Maiorano G, Sabella S, Sorce B, Brunetti V, Malvindi MA, Cingolani R, Pompa PP (2010) Effects of cell culture media on the dynamic formation of protein- nanoparticle complexes and influence on the cellular response. ACS Nano 4:7481–7491

    Article  Google Scholar 

  • Majhi PR, Ganta RR, Vanam RP, Seyrek E, Giger K, Dubin PL (2006) Electrostatically driven protein aggregation: beta-lactoglobulin at low ionic strength. Langmuir 22:9150–9159

    Article  Google Scholar 

  • Martirosyan A, Schneider YJ (2014) Engineered nanomaterials in food: implications for food safety and consumer health. Int J Environ Res Public Health 11:5720–5750

    Article  Google Scholar 

  • Miclaus T, Bochenkov VE, Ogaki R, Howard KA, Sutherland DS (2014) Spatial mapping and quantification of soft and hard protein coronas at silver nanocubes. Nano Lett 14:2086–2093

    Article  Google Scholar 

  • Mitrano DM, Ranville JF, Bednar A, Kazor K, Hering AS, Higgins CP (2014) Tracking dissolution of silver nanoparticles at environmentally relevant concentrations in laboratory, natural, and processed waters using single particle ICP-MS (spICP-MS). Environ Sci Nano 1:248–259

    Article  Google Scholar 

  • Noh H, Vogler EA (2007) Volumetric interpretation of protein adsorption: competition from mixtures and the Vroman effect. Biomaterials 28:405–422

    Article  Google Scholar 

  • Pfeiffer C et al (2014) Interaction of colloidal nanoparticles with their local environment: the (ionic) nanoenvironment around nanoparticles is different from bulk and determines the physico-chemical properties of the nanoparticles. J R Soc Interface 11:20130931

    Article  Google Scholar 

  • Podila R, Chen R, Ke PC, Brown JM, Rao AM (2012) Effects of surface functional groups on the formation of nanoparticle-protein corona. Appl Phys Lett 101:263701–263701–263704

    Google Scholar 

  • Raj S, Jose S, Sumod US, Sabitha M (2012) Nanotechnology in cosmetics: opportunities and challenges. J Pharm Bioallied Sci 4:186–193

    Article  Google Scholar 

  • Ranjan S, Dasgupta N, Chakraborty AR, Melvin Samuel S, Ramalingam C, Shanker R, Kumar A (2014) Nanoscience and nanotechnologies in food industries: opportunities and research trends. J Nanopart Res 16:2464

    Article  Google Scholar 

  • Ravindran A, Singh A, Raichur AM, Chandrasekaran N, Mukherjee A (2010) Studies on interaction of colloidal Ag nanoparticles with bovine serum albumin (BSA). Colloids Surf B 76:32–37

    Article  Google Scholar 

  • Raza S, Yan W, Stenger N, Wubs M, Mortensen NA (2013) Blueshift of the surface plasmon resonance in silver nanoparticles: substrate effects. Opt Express 21:27344–27355

    Article  Google Scholar 

  • Rezwan K, Studart AR, Vörös J, Gauckler LJ (2005) Change of ζ potential of biocompatible colloidal oxide particles upon adsorption of bovine serum albumin and lysozyme. J Phys Chem B 109:14469–14474

    Article  Google Scholar 

  • RIKILT, JRC (2014) Inventory of nanotechnology applications in the agricultural, feed and food sector. EFSA supporting publication, EN-621:1–125

  • Rostek A, Mahl D, Epple M (2011) Chemical composition of surface-functionalized gold nanoparticles. J Nanopart Res 13:4809–4814

    Article  Google Scholar 

  • Ruh H, Kuhl B, Brenner-Weiss G, Hopf C, Diabate S, Weiss C (2012) Identification of serum proteins bound to industrial nanomaterials. Toxicol Lett 208:41–50

    Article  Google Scholar 

  • Ruiz-Pena M, Oropesa-Nunez R, Pons T, Louro SR, Perez-Gramatges A (2010) Physico-chemical studies of molecular interactions between non-ionic surfactants and bovine serum albumin. Colloids Surf B 75:282–289

    Article  Google Scholar 

  • Sakulkhu U, Mahmoudi M, Maurizi L, Salaklang J, Hofmann H (2014) Protein corona composition of superparamagnetic iron oxide nanoparticles with various physico-chemical properties and coatings. Sci Rep 4:5020

    Article  Google Scholar 

  • Schachermeyer S, Ashby J, Kwon M, Zhong W (2012) Impact of carrier fluid composition on recovery of nanoparticles and proteins in flow field flow fractionation. J Chromatogr A 1264:72–79

    Article  Google Scholar 

  • Shannahan JH, Lai X, Ke PC, Podila R, Brown JM, Witzmann FA (2013) Silver nanoparticle protein corona composition in cell culture media. PLoS One 8:e74001

    Article  Google Scholar 

  • Shannahan JH et al (2015) Formation of a protein corona on silver nanoparticles mediates cellular toxicity via scavenger receptors. Toxicol Sci 143:136–146

    Article  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 46:7011–7017

    Article  Google Scholar 

  • Treuel L, Malissek M, Gebauer JS, Zellner R (2010) The influence of surface composition of nanoparticles on their interactions with serum albumin. ChemPhysChem 11:3093–3099

    Article  Google Scholar 

  • Treuel L, Malissek M, Grass S, Diendorf J, Mahl D, Meyer-Zaika W, Epple M (2012) Quantifying the influence of polymer coatings on the serum albumin corona formation around silver and gold nanoparticles. J Nanopart Res 14:1–12

    Article  Google Scholar 

  • Uvex-safety http://www.Uvex-safety.com/en/products/protective-clothing/disposable-coveralls/technology-disposable-coveralls. Accessed 02 April 2015

  • von der Kammer F, Legros S, Larsen EH, Loeschner K, Hofmann T (2011) Separation and characterization of nanoparticles in complex food and environmental samples by field-flow fractionation. Trends Anal Chem 30:425–436

    Article  Google Scholar 

  • von Goetz N, Fabricius L, Glaus R, Weitbrecht V, Gunther D, Hungerbuhler K (2013) Migration of silver from commercial plastic food containers and implications for consumer exposure assessment. Food Addit Contam Part A 30:612–620

    Article  Google Scholar 

  • Wimuktiwan P, Shiowatana J, Siripinyanond A (2015) Investigation of silver nanoparticles and plasma protein association using flow field-flow fractionation coupled with inductively coupled plasma mass spectrometry (FLFFF-ICP-MS). J Anal At Spectrom 30:245–253

    Article  Google Scholar 

  • Winuprasith T, Suphantharika M, McClements DJ, He LL (2014) Spectroscopic studies of conformational changes of beta-lactoglobulin adsorbed on gold nanoparticle surfaces. J Colloid Interface Sci 416:184–189

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank A. Lauckner-Tessin, I. Ebert, A. Tauer, and F. Mohr for their excellent technical assistance, Dr. D. Behsnilian for SEM analysis, and Dr. K. Oehlke for valuable discussions during preparation of the manuscript.

Author information

Authors and Affiliations

  1. Department of Food Technology and Bioprocess Engineering, Max Rubner-Institute, Haid-und-Neu-Str. 9, 76131, Karlsruhe, Germany

    Anna Burcza, Volker Gräf, Elke Walz & Ralf Greiner

Authors
  1. Anna Burcza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Volker Gräf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elke Walz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ralf Greiner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna Burcza.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Burcza, A., Gräf, V., Walz, E. et al. Impact of surface coating and food-mimicking media on nanosilver-protein interaction. J Nanopart Res 17, 428 (2015). https://doi.org/10.1007/s11051-015-3235-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11051-015-3235-7

Keywords

Search

Navigation