Abstract
When nanoparticles (NPs) come into contact with biological fluids, proteins, and other biomolecules interact with their surface. Upon exposure to biological fluids a layer of proteins adsorbs onto their surface, the so-called protein corona, and interactions of biological systems with NPs are therefore mediated by this corona. Here, interactions of serum albumin with silver and gold NPs were quantitatively investigated using circular dichroism spectroscopy. Moreover, surface enhanced Raman spectroscopy was used for further elucidation of protein binding to silver surfaces. The decisive role of poly(vinylpyrrolidone), coatings on the protein adsorption was quantitatively described for the first time and the influential role of the polymer coatings is discussed. Research in nanotoxicology may benefit from such molecular scale data as well as scientific approaches seeking to improve nanomedical applications by using a wide range of polymer surface coatings to optimize biological transport and medical action of NPs.
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Abbas K, Cydzik I, Del Torchio R, Farina M, Forti E, Gibson N, Holzwarth U, Simonelli F, Kreyling WG (2010) Radiolabelling of TiO2 nanoparticles for radiotracer studies. J Nanopart Res 12:2435–2443
Aggarwal P, Hall JB, McLeland CB, Dobrovolskaia MA, McNeil SE (2009) Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv Drug Delivery Rev 61:428–437
Aubin-Tam M-E, Hamad-Schifferli K (2005) Gold nanoparticle-cytochrome c complexes: the effect of nanoparticle ligand charge on protein structure. Langmuir 21:12080–12084
Bailon P, Won CY (2009) PEG-modified biopharmaceuticals. Expert Opin Drug Del 6:1–16
Boisselier E, Astruc D (2009) Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chem Soc Rev 38:1759–1782
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 USA 104:2050–2055
Cometto FP, Paredes-Olivera P, Macagno VA, Patrito EM (2005) Density functional theory study of the adsorption of alkanethiols on Cu(111), Ag(111), and Au(111) in the low and high coverage regimes. J Phys Chem B 109:21737–21748
De Paoli Lacerda SH, Park JJ, Meuse C, Pristinski D, Becker ML, Karim A, Douglas JFD (2010) Interaction of gold nanoparticles with common human blood proteins. ACS Nano 4:365–379
Des Rieux A, Fievez V, Garinot M, Schneider Y-J, Préat V (2006) Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J Control Release 116:1–27
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
Fass D (2012) Disulfide bonding in protein biophysics. Annu Rev Biophys 41:63–79
Ferrari M (2005) Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer 5:161–171
Galindo-Rodriguez SA, Allemann E, Fessi H, Doelker E (2005) Polymeric nanoparticles for oral delivery of drugs and vaccines: a critical evaluation of in vivo studies. Crit Rev Ther Drug Carr Syst 22:419–464
Gan ZH, Yu D, Zhong Z, Liang Q, Jing X (1999) Enzymatic degradation of poly(ε-caprolactone)/poly(dl-lactide) blends in phosphate buffer solution. Polymer 40:2859–2862
Garrido C, Aliaga AE, Gomez-Jeria JS, Clavijo RE, Campos-Vallette MM, Sanchez-Cortes S (2010) Adsorption of oligopeptides on silver nanoparticles: surface-enhanced Raman scattering and theoretical studies. J Raman Spectrosc 41:1149–1155
Gebauer JS, Treuel L (2011) Influence of individual ionic components on the agglomeration kinetics of silver nanoparticles. J Colloid Interface Sci 354:546–554
Gebauer JS, Malissek M, Simon S, Knauer SK, Maskos M, Stauber RH, Peukert W, Treuel L (2012) Impact of the nanoparticle–protein corona on colloidal stability and protein structure. Langmuir 28:9673–9679
Geiser M, Rothen-Rutishauser B, Kapp N, Schürch S, Kreyling WG, Schulz H, Semmler M, Im Hof V, Heyder J, Gehr P (2005) Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 113:1555–1560
Gessner A, Waicz R, Lieske A, Paulke B, Mäder K, Müller RH (2000) Nanoparticles with decreasing surface hydrophobicities: influence on plasma protein adsorption. Int J Pharmaceut 196:245–249
Ghosh P, Han G, De M, Kim CK, Rotello VM (2008) Gold nanoparticles in delivery applications. Adv Drug Deliv Rev 60:1307–1315
Goodman CM, McCusker CD, Yilmaz T, Rotello VM (2004) Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjug Chem 15:897–900
Gref R, Lück M, Quellec P, Marchand M, Dellacherie E, Harnisch S, Blunk T, Müller RH (2000) ‘Stealth’ corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloid Surface B 18:301–3013
Greulich C, Kittler S, Epple M, Muhr G, Köller M (2009) Studies on the biocompatibility and the interaction of silver nanoparticles with human mesenchymal stem cells (hMSCs). Langenbecks Arch Surg 394:495–502
Hamman JH, Enslin GM, Kotzé AF (2005) Oral delivery of peptide drugs: barriers and developments. BioDrugs 19:165–177
Han G, Chari NS, Verma A, Hong R, Martin CT, Rotello VM (2005) Controlled recovery of the transcription of nanoparticle-bound DNA by intracellular concentrations of glutathione. Bioconjugate Chem 16:1356–1359
Harris JM, Martin NE, Modi M (2001) Pegylation: a novel process for modifying pharmacokinetics. Clin Pharmacokinet 40:539–551
He XM, Carter DC (1992) Atomic structure and chemistry of human serum albumin. Nature 358:209–214
Hellstrand E, Lynch I, Andersson A, Drakenberg T, Dahlbäck B, Dawson KA, Linse S, Cedervall T (2009) Complete high-density lipoproteins in nanoparticle corona. FEBS J 276:3372–3381
Hogg PJ (2003) Disulfide bonds as switches for protein function. Trends Biochem Sci 28:210–214
Huang X, El-Sayed IH, Qian W, El-Sayed MA (2006) Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J Am Chem Soc 128:2115–2120
Jiang X, Jiang J, Jin Y, Wang E, Dong S (2005) Effect of colloidal gold size on the conformational changes of adsorbed cytochrome c: probing by circular dichroism, UV-visible, and infrared spectroscopy. Biomacromolecules 6:46–53
Jiang X, Weise S, Hafner M, Röcker C, Zhang F, Parak WJ, Nienhaus GU (2010) Quantitative analysis of the protein corona on FePt nanoparticles formed by transferrin binding. J R Soc Interface 7:S5–S13
Kah JCY, Wong KY, Neoh KG, Song JH, Fu JWP, Mhaisalkar S, Olivo M, Sheppard CJR (2009) Critical parameters in the pegylation of gold nanoshells for biomedical applications: an in vitro macrophage study. J Drug Targeting 17:181–193
Kim HR, Andrieux K, Delomenie C, Chacun H, Appel M, Desmaële D, Taran F, Georgin D, Couvreur P, Taverna M (2007a) Analysis of plasma protein adsorption onto PEGylated nanoparticles by complementary methods: 2-DE, CE and protein Lab-on-chip® system. Electrophoresis 28:2252–2261
Kim HR, Andrieux K, Gil S, Taverna M, Chacun H, Desmaële D, Taran F, Georgin D, Couvreur P (2007b) Translocation of poly(ethylene glycol-co-hexadecyl)cyanoacrylate nanoparticles into rat brain endothelial cells: role of apolipoproteins in receptor-mediated endocytosis. Biomacromolecules 8:793–799
Kittler S, Greulich C, Diendorf J, Köller M, Epple M (2010a) Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem Mater 22:4548–4554
Kittler S, Greulich C, Gebauer JS, Diendorf J, Treuel L, Ruiz L, Gonzalez-Calbet JM, Vallet-Regi M, Zellner R, Köller M, Epple M (2010b) The influence of proteins on the dispersability and cell-biological activity of silver nanoparticles. J Mater Chem 20:512–518
Klein J (2007) Probing the interactions of proteins and nanoparticles. Proc Natl Acad Sci USA 104:2029–2030
Kostarelos K, Bianco A, Prato M (2009) Promises, facts and challenges for carbon nanotubes in imaging and therapeutics. Nat Nanotechnol 4:627–633
Kreyling WG, Semmler M, Moller W (2004) Dosimetry and toxicology of ultrafine particles. J Aerosol Med 17:140–152
Leroueil-Le Verger M, Fluckiger L, Kim YI, Hoffman M, Maincent P (1998) Preparation and characterization of nanoparticles containing an antihypertensive agent. Eur J Pharm Biopharm 46:137–143
Li Y, He W, Tian J, Tang J, Hu Z, Chen X (2005) The effect of Berberine on the secondary structure of human serum albumin. J Mol Struct 743:79–84
Li D, Teoh WY, Selomulya C, Woodward RC, Amal R, Rosche B (2006) Flame-sprayed superparamagnetic bare and silica-coated maghemite nanoparticles: synthesis, characterization, and protein adsorption-desorption. Chem Mater 18:6403–6413
Linse S, Cabaleiro-Lago C, Xue W-F, Lynch I, Lindman S, Thulin E, Radford SE, Dawson KA (2007) Nucleation of protein fibrillation by nanoparticles. Proc Natl Acad Sci USA 104:8691–8696
Lipka J, Semmler-Behnke M, Sperling RA, Wenk A, Takenaka S, Schleh C, Kissel T, Parak WJ, Kreyling WG (2010) Biodistribution of PEG-modified gold nanoparticles following intratracheal instillation and intravenous injection. Biomaterials 31:6574–6581
Liu Z, Wu G (2006) The electro-oxidative activity of cysteine on the Au electrode as evidenced by surface enhanced Raman scattering. Spectrochim Acta A 64:251–254
Lu ZX, Cui T, Shi QL (1987) Application of circular dichroism and optical rotatory dispersion in molecular biology. Science press, Beijing
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
Lynch I (2006) Are there generic mechanisms governing interactions between nanoparticles and cells? Epitope mapping the outer layer of the protein-material interface. Phys A 373:511–520
Lynch I, Dawson KA, Linse S (2006) Detecting cryptic epitopes created by nanoparticles. Sci STKE 2006:14
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 2:374–383374
Mahl D, Greulich C, Meyer-Zaika W, Köller M, Epple M (2010) Gold nanoparticles: dispersability in biological media and cell-biological effect. J Mater Chem 20:6176–6181
Mahl D, Diendorf J, Meyer-Zaika W, Epple M (2011) Possibilities and limitations of different analytical methods for the size determination of a bimodal dispersion of metallic nanoparticles. Colloid Surface A 377:386–392
Marambio-Jones C, Hoek EMV (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12:1531–1551
Martínez-Castañón G, Niño-Martínez N, Martínez-Gutierrez F, Martínez-Mendoza J, Ruiz F (2008) Synthesis and antibacterial activity of silver nanoparticles with different sizes. J Nanopart Res 10:1343–1348
Maynard AD, Aitken RJ, Butz T, Colvin V, Donaldson K, Oberdörster G, Philbert MA, Ryan J, Seaton A, Stone V, Tinkle SS, Tran L, Walker NJ, Warheit DB (2006) Safe handling of nanotechnology. Nature 444:267–269
Medintz IL, Konnert JH, Clapp AR, Stanish I, Twigg ME, Mattoussi H, Mauro JM, Deschamps JR (2004) A fluorescence resonance energy transfer-derived structure of a quantum dot-protein bioconjugate nanoassembly. Proc Natl Acad Sci USA 101:9612–9617
Monopoli MP, Baldelli Bombelli F, Dawson KA (2011a) Nanobiotechnology: nanoparticle coronas take shape. Nat Nanotechnol 6:11–12
Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Bombelli FB, Dawson KA (2011b) Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 133:2525–2534
Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627
Nel AE, Mädler L, Velegol D, Xia T, Hoek EMV, Somasundaran P, Klaessig F, Castranova V, Thompson M (2009) Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 8:543–557
Niidome T, Yamagata M, Okamoto Y, Akiyama Y, Takahashi H, Kawano T, Y. K, Niidome Y (2006) PEG-modified gold nanorods with a stealth character for in vivo applications. J Control Release 114:343–347
Nogami N, Sugeta H, Miyazawa T (1975) C–S stretching vibrations and molecular conformations of isobutyl methyl sulfide and related alkyl sulfides. Bull Chem Soc Jpn 48:2417–2420
Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839
Oberdörster G, Maynard A, Donaldson K, Castranova V, Fitzpatrick J, Ausman K, Carter J, Karn B, Kreyling WG, Lai D, Olin S, Monteiro-Riviere N, Warheit D, Yang H (2007) Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy. Part Fibre Toxicol 2:1–35
Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium escherichia coli. Appl Environ Microbiol 73:1712–1720
Peng ZG, Hidajat K, Uddin MS (2004) Adsorption and desorption of lysozyme on nano-sized magnetic particles and its conformational changes. Colloid Surf B 35:169–174
Perracchia M, Harnisch S, Pinto-Alphandary H, Gulik A, Dedieu J, Desmaële D, d′Angelo J, Müller RH, Couvreur P (1999) Visualization of in vitro protein-rejecting properties of PEGylated stealth® polycyanoacrylate nanoparticles. Biomaterials 20:1269–1275
Podstawka E, Ozaki Y, Proniewicz LM (2004) Adsorption of S–S containing proteins on a colloidal silver surface studied by surface-enhanced Raman spectroscopy. Appl Spectrosc 58:1147–1156
Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WAH, Seaton A, Stone V, Brown S, MacNee W, Donaldson K (2008) Carbon nanotubes introduced into the abdominal cavity ofmice show asbestoslike pathogenicity in a pilot study. Nature 3:423–428
Roach P, Farrar D, Perry CC (2006) Surface tailoring for controlled protein adsorption: effect of topography at the nanometer scale and chemistry. J Am Chem Soc 128:3939–3945
Röcker C, Pötzl M, Zhang F, Parak WJ, Nienhaus GU (2009) A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat Nanotechnol 4:577–580
Rodriguez CE, Fukuto JM, Taguchi JM, Froines J, Cho AK (2005) The interactions of 9,10-phenanthrenequinone with glyceraldehyde-3-phosphate dehydrogenase (GAPDH), a potential site for toxic actions. Chem Biol Interact 155:97–110
Rostek A, Mahl D, Epple M (2011) Chemical composition of surface-functionalized gold nanoparticles. J Nanopart Res 13:4809–4814
Rothen-Rutishauser B, Kiama SG, Gehr P (2005) A three-dimensional cellular model of the human respiratory tract to study the interaction with particles. Am J Respir Cell Mol Biol 32:281–289
Schlücker S, Liang C, Strehle KR, DiGiovanna JJ, Kraemer KH, Levin IW (2006) Conformational differences in protein disulfide linkages between normal hair and hair from subjects with trichothiodystrophy: a quantitative analysis by Raman microspectroscopy. Biopolymers 82:615–622
Seil J, Webster T (2012) Antimicrobial applications of nanotechnology: methods and literature. Int J Nanomed 7:2767–2781
Semmler-Behnke M, Takenaka S, Fertsch S, Wenk A, Seitz J, Mayer P, Oberdörster G, Kreyling WG (2007) Efficient elimination of inhaled nanoparticles from the alveolar region: evidence for interstitial uptake and subsequent reentrainment onto airways epithelium. Environ Health Perspect 115:728–733
Shang L, Wang Y, Jiang J, Dong S (2007) pH-dependent protein conformational changes in albumin: gold nanoparticle bioconjugates: a spectroscopic study. Langmuir 23:2714–2721
Shang L, Dong SJ, Nienhaus GU (2011a) Ultra-small fluorescent metal nanoclusters: synthesis and biological applications. Nano Today 6:401–418
Shang L, Dörlich RM, Brandholt S, Schneider R, Trouillet V, Bruns M, Gerthsen D, Nienhaus GU (2011b) Facile preparation of water-soluble fluorescent gold nanoclusters for cellular imaging applications. Nanoscale 3:2009–2014
Shang L, Brandholt S, Stockmar F, Trouillet V, Bruns M, Nienhaus GU (2012) Effect of protein adsorption on the fluorescence of ultrasmall gold nanoclusters. Small 8:661–665
Sharma B, Frontiera RR, Henry A-I, Ringe E, Van Duyne RP (2012) SERS: materials, applications, and the future. Mater Today 15:16–25
Stewart S, Fredericks PM (1999) Surface-enhanced Raman spectroscopy of amino acids adsorbed on an electrochemically prepared silver surface. Spectrochim Acta A 55:1641–1660
Sugeta H, Go A, Miyazawa T (1972) S–S and C–S streching vibrations and molecular conformations of dialkyl disulfides and cystine. Chem Lett 1:83–86
Tasis D, Tagmatarchis N, Bianco A, Prato M (2006) Chemistry of carbon nanotubes. Chem Rev 106:1105–1136
Tenzer S, Docter D, Rosfa S, Wlodarski A, Kuharev J, Rekik A, Knauer SK, Bantz C, Nawroth T, Bier C, Sirirattanapan J, Mann W, Treuel L, Zellner R, Maskos M, Schild H, Stauber RH (2011) Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis. ACS Nano 5:7155–7167
Thode K, Lück M, Semmler W, Müller RH, Kresse M (1997) Determination of plasma protein adsorption on magnetic iron oxides: sample preparation. Pharm Res 14:905–910
Treuel L, Malissek M (2012) Interaction of nanoparticles with proteins-determination of equilibrium constants (accepted). In: Weissig V (ed) Cellular and sub-cellular nanotechnology: methods and protocols. Springer, New York
Treuel L, Nienhaus G (2012) Toward a molecular understanding of nanoparticle–protein interactions. Biophys Rev 4:137–147
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
Turkevich J, Stevenson PC, Hillier J (1951) A study of the nucleation and growth processes in the synthesis of colloidal gold. Faraday Discuss 11:55–75
Verma A, Rotello VM (2005) Surface recognition of biomacromolecules using nanoparticle receptors. Chem Commun 303–312
Vertegel AA, Siegel RW, Dordick JS (2004) Silica nanoparticle size influences the structure and enzymatic activity of adsorbed lysozyme. Langmuir 20:6800–6807
Villalonga R, Cao R, Gragoso A (2007) Supramolecular chemistry of cyclodextrins in enzyme technology. Chem Rev 107:3088–3116
Wang Y, Sun HF, Wang HF, Liu YF (2001) In vitro interaction of nicotine and hemoglobin under liver cell metabolizing condition. Chinese Chem Lett 12:449–452
Wang H, Qiao X, Chen J, Ding S (2005) Preparation of silver nanoparticles by chemical reduction method. Colloid Surf A 256:111–115
Watanabe T, Maeda H (1989) Adsorption-controlled redox activity. Surface-enhanced Raman investigation of cystine versus cysteine on silver electrodes. J Phys Chem 93:3258–3260
Wedemeyer WJ, Welker E, Narayan M, Scheraga HA (2000) Disulfide bonds and protein folding. Biochemistry 39:7032
Xiao Q, Huang S, Liu Y, Tian F, Zhu J (2009) Thermodynamics, conformation and active sites of the binding of Zn–Nd hetero-bimetallic schiff base to bovine serum albumin. J Fluoresc 19:317–326
Xiu Z-m, Zhang Q-b, Puppala HL, Colvin VL, Alvarez PJJ (2012) Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett. doi:10.1021/nl301934w
Yeh HC, Ho Y-P, Wang TH (2005) Quantum dot-mediated biosensing assays for specific nucleic acid detection. Nanomed 1:115–121
Zhou HS, Aoki S, Honma I, Hirasawa M, Nagamune T, Komiyama H (1997) Conformational change of protein cytochrome b-562 adsorbed oncolloidal gold particles; absorption band shift. Chem Commun 605–606
Acknowledgments
The authors acknowledge the support of this study by the Deutsche Forschungsgemeinschaft (DFG) within the priority programme “Bio-Nano-Responses” (SPP1313). The authors thank R. Zellner for valuable discussions and S. Boukercha for assistance with SEM-measurements. LT acknowledges support by a Young Scientists Grant of the UDE, by a research grant of the Centre for Water and Environmental Science (CWE) and by the Bruno-Werdelmann Foundation.
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Treuel, L., Malissek, M., Grass, S. et al. Quantifying the influence of polymer coatings on the serum albumin corona formation around silver and gold nanoparticles. J Nanopart Res 14, 1102 (2012). https://doi.org/10.1007/s11051-012-1102-3
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DOI: https://doi.org/10.1007/s11051-012-1102-3