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Protein-Mediated Shape-Control of Silver Nanoparticles Indranath Chakraborty, Neus Feliu, Sathi Roy, Kenneth A. Dawson, and Wolfgang J Parak Bioconjugate Chem., Just Accepted Manuscript • DOI: 10.1021/acs.bioconjchem.8b00034 • Publication Date (Web): 20 Feb 2018 Downloaded from http://pubs.acs.org on February 21, 2018

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Bioconjugate Chemistry

Protein-Mediated Shape-Control of Silver Nanoparticles Indranath Chakraborty 1 , 2 , Neus Feliu 2 , 3 , Sathi Roy 1 , 2 , Kenneth Dawson 4 , Wolfgang J. Parak 1, 2 , 5 * 1

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Fachbereich Physik, Philipps Universität Marburg, Germany. Fachbereich Physik und Chemie, and Center for Hybrid Nanostructure (CHyN), Universität Hamburg, Hamburg, Germany. 3 Department of Laboratory Medicine (LABMED), Karolinska Institutet, Stockholm, Sweden. 4 Centre for BioNano Interactions, School of Chemistry and Chemical Biology, University College Dublin, Dublin, Ireland. 5 CIC Biomague, San Sebastian, Spain. * corresponding author: [email protected]

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Abstract Silver nanoparticles were grown in aqueous solution, without the presence of typical surfactant molecules, but under the presence of different proteins. The shape of the resulting silver nanoparticles could be tuned by the selection of the types of proteins. The amount of accessible lysine groups was found to be mainly responsible for the anisotropy in nanoparticle formation. Viability measurements of cells exposed to protein capped spherical or prism-shaped NPs did not reveal differences between both geometries. Thus, in case of protein-only coated Ag NPs, no shapeinduced toxicity was found under the investigated exposure conditions.

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Introduction With the emerging use of nanomaterials in consumer products, particular importance has to be given concerning nano-safety.(1) In the case of colloidal nanoparticles (NPs), modern synthesis protocols allow for an enormous flexibility in obtaining NPs with the desired functional properties, by changing parameters such as material / composition, size, shape, surface-coating, etc.(2) While synthesis can be in this way directed towards best functional performance, potential toxicity may be enhanced. Shape-controlled synthesis of gold NPs and their applications in photothermal therapy is an example in this direction. Concerning the functional performance in photothermal activity, rod-shape NPs beat spherical NPs due to their strong surface plasmon absorption band in the infrared. On the other hand, rod-shaped Au NPs have been reported to be more toxic than spherical Au NPs.(3) For safe-bydesign approaches, improvement in functional properties thus always needs to be analyzed in the context of potential changes in toxicity. While NPs can be synthesized rationally in order to warrant for certain functional properties, despite massive efforts, potential toxicity can still not be predicted straight forward from physicochemical properties. There are generally agreed-on tendencies, for example, that elongated NPs, in general, are better incorporated by cells and are more toxic.(3) However, the key-problem is that different physico-chemical properties of NPs often are entangled. Changes in aspect ratio (e.g. in the direction of spherical to rod-shaped NPs) also influence the volume per NP.(4) Changes in surface coating may change the effective size of NPs, in particular in case of agglomeration. Rod-shaped Au NPs are typically synthesized under the presence of a toxic surfactant, cetyltrimethylammonium bromide (CTAB),(5, 6) whereas spherical Au NPs can be synthesized without typical surfactant, e.g. just under the presence of citric acid salts. Note that surfactants are "surface active agents". As citric acid also adsorbs to the NP surface it also could be termed surfactant. However, in the following the term typical surfactant will be used rather for detergents and not for natural molecules like citric acid which are adsorbed to NP surfaces. At any rate, the higher toxicity of rod-shaped Au NPs in comparison to spherical Au NPs may originate from their elongated shape, but also from their CTABcoating.(7) While attempts have been reported in which the CTAB-coating around rod-shaped Au NPs was removed in a post-synthesis procedure, leading to reduced toxicity,(8) but the exchange in surface coating may not complete.(9) In order to better understand the role of the surface coating on shape-induced toxicity, NPs without the use of typical surfactant in their synthesis would be a helpful model system. Li et al. have demonstrated shape controlling of Pt nanoparticles using specifically designed peptides.(10, 11) We note that without the use of surfactants the surface of the NPs would not be "naked", as in biological media there will be adsorption of proteins to the surface of the NPs.(12) However, adsorption of proteins, e.g. the formation of a protein corona,(13) may colloidally stabilize NPs.(14) In this way, as proteins will be adsorbed at any rate to the surface of NPs in biological environments, protein-mediated synthesis would be an excellent approach to achieve NPs free of typical surfactants. In fact, there are many reports in literature using proteins as reducing agent of metal salts for the synthesis of metal NPs and nanoclusters (NCs),(15) in particular of Au and Ag. Bovine serum albumin (BSA), which is abundant in blood, is most often used as protein for this purpose. However, generally, such synthesis lead to the generation of spherically shaped metal NPs.(16, 17) In the present work, we investigated whether using different proteins allows for synthesis of non-spherical


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Ag NPs. With such protein-coated Ag NPs, the influence of NP shape on NP toxicity could be investigated without the complication of contribution of surface chemistries to toxicity. Results and Discussion For the synthesis of Ag NPs, first small Ag clusters were synthesized from Ag+ upon reduction with citric acid salt. Citric acid occurs in the metabolism of all aerobic organisms (citric acid cycle = tricarboxylic acid cycle = Krebs cycle) and thus is considered as natural compound. Citric acid salt is commonly used for the synthesis of Ag or Au NPs,(18) it only weakly coordinates to the NP surface,(19) and is not a toxic surfactant. The Ag clusters were then used as seeds for the growth of Ag NPs (several control experiments are described in the supporting information, section 2). For this purpose different proteins were added to the Ag clusters, see Figure 1A. The formation of Ag NPs can be conveniently followed, as they exhibit a surface plasmon resonance (SPR) band in their absorption spectrum.(20) In Figure 1B spectra after the addition of bovine serum albumin (BSA) and lysozyme (Lyz) are shown. In both spectra a characteristic peak corresponding to SPR is present, verifying the presence of Ag NPs. The Ag NPs synthesized under the presence of lysozyme show the typical SPR peak of spherical Ag NPs.(21) However, in the case of BSA, a shift of the SPR band to higher wavelength is observed, which is associated to non-spherical Ag NPs.(22) In fact, these data indicate that the shape of Ag NPs can be controlled by just using different proteins as capping agent, without the presence of quaternary ammonium surfactant, and with fully natural and biocompatible coatings.

Figure 1: A) Scheme of the synthesis. B) Absorption spectra A(λ) of Ag NPs synthesized under the presence of bovine serum albumin (BSA) or lysozyme (Lyz). Based on these first findings, a larger set of proteins was screened to unravel the mechanism on which this shape-controlled growth of Ag NPs may be based. In Figure 2 results for 8 different proteins are shown. Transmission electron microscopy (TEM) images of the different Ag NPs indicate again that the shape of the Ag NPs is determined by the type of protein used for synthesis (Figure 2 and supporting information, section 3). In the case of lysozyme, 100% of the resulting Ag NPs have spherical shape, whereas with most other proteins also other shapes, in particular, prisms were observed. Ag prisms have been synthesized before by others upon using typical surfactants,(22) and seem to be a preferential shape of Ag NPs. The highest fraction of prisms was observed upon using catalase. The kinetics of the development of the different shapes could be observed by recording time resolve absorption spectra of the solutions during reaction. In Figure 2 contour plots of such ACS Paragon Plus Environment

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A(λ,t) graphs are shown, whereby the red color corresponds to maximum absorption (i.e. the SPR peak), and the blue color to zero absorption. In the case of lysozyme, the SPR peak remains constant around 408 nm over time, which corresponds to spherical shape. In contrast, for catalase, a shift of SPR peak to higher wavelength over time can be seen, which indicates the formation of prisms. The kinetics of the NP formation does not follow any specific trend. Avidin and β-lactoglobulin were found to have the fastest and slowest NP formation kinetics, respectively.

Figure 2: Results for the growth of Ag NPs under the presence of different proteins. From the transmission electron microscopy (TEM) images the respected percentage of different shapes is determined. The scale bars correspond to 100 nm. The time-resolve absorption spectra A(λ,t) were obtained from absorption spectra A(λ), such as the ones shown in Figure 1B, at different time points t. The white dotted line corresponds to the time needed to complete the growth, i.e. the reaction time after which the SPR peak stays at fixed wavelength. Here contour plots are shown, in which the normalized absorption is color coded. For each protein, also the molar mass Mw, the pH at which the isoelectric point is reached pI, the number of amino acids per protein Namino acids, and the zeta potentials (ξ) are given. Note, that while some proteins may be similar in some properties, they may have significant differences in others. For example BSA and Ova vary strongly in Namino acids. While presence of different proteins present during NP growth lead to distinct NP geometries, a correlation of anisotropic growth to different proteins properties such as molecular weight or zeta potential was not straight forward. We thus decided to start investigating the role of the individual building blocks of proteins, i.e. amino acids. In order to investigate the role of the individual amino acids, synthesis of the Ag NPs was also carried out under the presence of different amino acids, and the kinetics of NP growth was recorded with absorption spectroscopy in the form of A(λ,t) contour plots (Supporting Information, section 9). Data demonstrate that amino acids such as Ala, Gly, Ile, Ser, Thr, and Val led to the formation of anisotropic NPs, whereas Lys, Cys produced spherical NPs


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with broad size distribution. The rest of the amino acids lead to reaction products with in-significant optical features. However, none of this amino acid protected NPs were chemically stable except lysine (Figure S32). Most of them were completely degraded within 2 hours leading to featureless spectra as seen in Figure S32. Lysine has a primary amine group in its side chain, which may form strong bonds with silver.(23) Moreover, a strong role of lysine in stabilizing silver NPs has been reported, and in all the cases lysine-capped NPs appeared with spherical shape.(24) As control water soluble PEG-NH2 was also used to mimic the role of lysine in proteins. In this case, the NPs showed anisotropic features but again they were not chemically stable (cf. Figure S33) suggesting multiple coordinations (e.g. attachment of several amines in the form of chains of amino acids i.e. proteins) are indeed needed to get sufficient stability. Lysines thus seem to promote growth of Ag NPs, though for colloidally stable NPs individual amino-terminated ligands are not sufficient. Proteins comprising multiple lysine residues on the other hand warrant for stable NPs. It needs to be noted that in protein structure only the primary amine located at the side chain of lysine is available for coordination with silver. Thus, the coordination of silver with free lysine and lysine in proteins might be different, which then can influence anisotropy. To further investigate the mechanism for protein-directed anisotropy, control experiments were done with highly similar but chemically modified proteins, for which the number of lysine residues was modified (see the Supporting Information, section 8). Succinylation and amination were carried out on BSA and catalase to confirm the role of lysine in dictating particle anisotropy. Succinylation blocks the amine groups of lysine and introduces a carboxyl functionalities (see Figure S24), whereas amination increases the number of free primary amine groups in the proteins (see Figure S24). Both methods may affect protein structure, but the hydrodynamic diameter of the modified proteins remained similar (Figure S24). The results for both proteins, BSA, and catalase, showed that succinylation lead to spherical NPs, whereas amination lead to anisotropic NPs (Supporting information, Figure S25 and Figure S28). In the case of the avidin family, streptavidin (number of lysines NK =12) has lower number of lysine as compared to avidin (NK =28) or neutravidin (NK =28) which was the reason for its isotropic particle formation (see Figure S22). A high number of (accessible) lysines thus seems to promote anisotropy in NP growth. Also, the pH during the synthesis plays a role, as investigated by modifying the pH of the reaction mixture for different proteins (see Supporting Information, section 5). At pH = 13, all the NPs were spheres, which could be due to several reasons: i) at high concentration of OH-, a layer of AgOH may form on the Ag seed NPs. Such AgOH layer has been reported to promote isotropic growth, leading to spherical shape.(25) ii) at high pH, the protein structure may become unfolded, which could also lead to NP growth with different morphology. Differences in protein structure might affect how strongly the proteins stabilize the ions to be reduced, thus affecting both reaction kinetics and NP surface energy. iii) upon raising the pH, more amino groups (e.g. from lysine residues) become deprotonated (-NH3+ → -NH2) and coordination of deprotonated amines to silver is assumed to be different than protonated one which can lead to isotropic growth. Thus, according to the above hypothesis about the influence of accessible lysines at high pH, the NPs would grow to isotropic shape. The effect of different proteins on dictating the anisotropy of NPs as reported here seems to be specific to silver. Gold NPs did not show similar diversity in NP morphologies upon being synthesized under the presence of different proteins (Supporting Information section 11). ACS Paragon Plus Environment

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Being able to perform protein-mediated shape control toxicity of differently shaped Ag NPs was investigated. As control spherical Ag NPs synthesized with CTAB only and prism-shaped Ag NPs as synthesized with citrate were used. A standard resazurin-based viability assays was carried out to probe toxicity of the Ag NPs. In fact, Ag prisms with CTAB coating were found to have toxicity (Figure 3A,B and Supporting Information Figure S40). However, in the case of protein-coated Ag prisms in the investigated concentration range no reduction in cell viability was found, as in the case of all the spherical NPs. This indicates that shape alone may not be the dominant parameter in case toxicity of non-spherical NPs is reported, but that in fact, the surface coating may bear the key responsibility. In order to probe whether toxicity was correlated with enhanced NP internalization, uptake studies performed by elemental analysis (using the inductively coupled plasma mass spectrometry; ICP-MS) were carried out, see Figure 3C,D and Supporting Information Figure S41. Data indicate that Ag@CTAB NPs, the most toxic NPs, did not enter most to cells. Ag@Lyz NPs were most found inside cells, which may be due to reduced colloidal stability (see the Supporting Information section 13). Experiments under serum-supplemented conditions lead to the same results (see the Supporting Information sections 14 and 15).

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Figure 3. Biocompatibility studies of differently shaped Ag NPs. (A-B) Cell viability studies. HeLa cells were exposed to various concentrations of Ag NPs (CAg) in serum-supplemented media for A) 24 h and B) 48 h. AgNO3 was used as reference control. Results are presented as percent of cell viability V [%] (mean value) from four independent experiments. (C-D). Uptake studies. HeLa cells were exposed to different concentrations of Ag NPs and AgNO3 (CAg) for A) 24 h and B) 48h. Uptake was assessed using elemental analysis (ICP-MS). Results are presented as mass of silver per cell mAg/cell from three to


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four independent experiments. Due to their toxicity uptake data with Ag@CTAB NPs could be only recorded for low exposure concentrations


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Conclusions

Silver NPs can be synthesized via wet-chemistry routes with proteins. Different shapes can be synthesized just by using different proteins. The accessible lysine side chains in proteins have a strong role in dictating the shape of the NPs. A high number of accessible lysines seem to promote anisotropic growth. Monodispersity of silver nanoparticles using proteins remains a big challenge, but rather than developing a new synthesis line the aim of the study was to get a better understanding on how different proteins may affect growth. A deeper structural understanding of protein-NP interface would also help in the development of better controlled protein-mediated syntheses in the future. Inorganic NPs dispersed in biological media are complex entities, comprising at least the inorganic core and an organic surface coating. As shape-controlled synthesis typically requires different surface coatings, it is complicated to deconvolute shape from surface effects concerning the interaction of these NPs with cells. In fact, in case toxic surfactant molecules have been used to create anisotropic shapes, rather the surface coating than the anisotropic shape may be responsible for changes in NP toxicity. Protein-protected anisotropic Ag NPs did not lead to higher toxicity than protein-protected isotropic Ag NPs. Associated Content Details of synthesis of nanoparticles, protein information tables, pH dependent kinetics, structural information, control experiments, protein modification, synthesis of NPs with amino acids, silver ion release study, stability in different media, similar NP growth experiments with gold instead of silver, toxicity and uptake experiments. This material is available free of charge via the Internet at http://pubs.acs.org. Acknowledgements This work was supported by the European Commission (grant FutureNanoNeeds) and by the German Research Foundation (grant DFG PA 794/28-1). I.C. was supported by an Alexander von Humboldt fellowship. N.F acknowledges funding from the Swedish Governmental Agency for Innovation Systems (Vinnova). S.R has received a Ph.D. student fellowship by the Fazit foundation. The authors are grateful to Mrs. Marta Gallego (CIC Biomagune) for the TEM images and Ms. Yunhuan Yuan for the help in protein information. Ms. Yu-Hsin Chang, Ms. Yuan Zeng, and Mr. Shoaib Azeem helped in additional control experiments.

References (1) (2) (3)

Nel, A., Xia, T., Mädler, L., and Li, N. (2006) Toxic Potential of Materials at the Nanolevel. Science 311, 622-627. Parak, W. J. (2011) Complex Colloidal Assembly. Science 334, 1359-1360. Alkilany, A. M., Nagaria, P. K., Hexel, C. R., Shaw, T. J., Murphy, C. J., and Wyatt, M. D. (2009) Cellular Uptake and Cytotoxicity of Gold Nanorods: Molecular Origin of Cytotoxicity and Surface Effects. Small 5, 701-708.


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(4)

(5) (6) (7) (8)

(9) (10) (11) (12)

(13)

(14)

(15) (16)

(17)

(18) (19)

(20) (21) (22)

(23)

Feliu, N., Hühn, J., Zyuzin, M. V., Ashraf, S., Valdeperez, D., Masood, A., Said, A. H., Escudero, A., Pelaz, B., Gonzalez, E., et. al. (2016) Quantitative uptake of colloidal particles by cell cultures. Sci. Tot. Environ. 568, 819-828. Gole, A., and Murphy, C. J. (2004) Seed-Mediated Synthesis of Gold Nanorods: Role of the Size and Nature of the Seed. Chem. Mater. 16, 3633-3640. Nikoobakht, B., and El-Sayed, M. A. (2003) Preparation and Growth Mechanism of Gold Nanorods (NRs) Using Seed-Mediated Growth Method. Chem. Mater. 15, 1957-1962. Huff, T. B., Hansen, M. N., Zhao, Y., Cheng, J.-X., and Wei, A. (2007) Controlling the Cellular Uptake of Gold Nanorods. Langmuir 23, 1596-1599. Soliman, M. G., Pelaz, B., Parak, W. J., and del Pino, P. (2015) Phase Transfer and Polymer Coating Methods toward Improving the Stability of Metallic Nanoparticles for Biological Applications. Chem. Mater. 27, 990-997. Liao, H., and Hafner, J. H. (2005) Gold Nanorod Bioconjugates. Chem. Mater. 17, 4636-4641. Li, Y., and Huang, Y. (2010) Morphology-Controlled Synthesis of Platinum Nanocrystals with Specific Peptides. Adv. Mater. 22, 1921-1925. Li, Y., Whyburn, G. P., and Huang, Y. (2009) Specific Peptide Regulated Synthesis of Ultrasmall Platinum Nanocrystals. J. Am. Chem. Soc. 131, 15998-15999. Rivera-Gil, P., Jimenez De Aberasturi, D., Wulf, V., Pelaz, B., Del Pino, P., Zhao, Y., De La Fuente, J. M., Ruiz De Larramendi, I., Rojo, T., et al. (2013) The Challenge To Relate the Physicochemical Properties of Colloidal Nanoparticles to Their Cytotoxicity. Acc. Chem. Res. 46, 743-749. Cedervall, T., Lynch, I., Foy, M., Berggård, T., Donnelly, S. C., Cagney, G., Linse, S., and Dawson, K. A. (2007) Detailed Identification of Plasma Proteins Adsorbed on Copolymer Nanoparticles. Angew. Chem. Int. Ed. 46, 5754-5756. Rehbock, C., Merk, V., Gamrad, L., Streubel, R., and Barcikowski, S. (2013) Size control of laser-fabricated surfactant-free gold nanoparticles with highly diluted electrolytes and their subsequent bioconjugation. Phys. Chem. Chem. Phys. 15, 3057-3067. Chakraborty, I., and Pradeep, T. (2017) Atomically Precise Clusters of Noble Metals: Emerging Link between Atoms and Nanoparticles. Chem. Rev. 117, 8208-8271. Yang, X.-H., Ling, J., Peng, J., Cao, Q.-E., Wang, L., Ding, Z.-T., and Xiong, J. (2013) Catalytic formation of silver nanoparticles by bovine serum albumin protected-silver nanoclusters and its application for colorimetric detection of ascorbic acid. Spectrochimica Acta Part A: Molecul. Biomolecul. Spectroscopy 106, 224-230. Meziani, M. J., Rollins, H. W., Allard, L. F., and Sun, Y.-P. (2002) Protein-Protected Nanoparticles from Rapid Expansion of Supercritical Solution into Aqueous Solution. J. Phys. Chem. B 106, 11178-11182. Turkevich, J., Stevenson, P. C., and Hillier, J. (1951) A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss. Faraday Soc. 11, 55-75. Park, J.-W., and Shumaker-Parry, J. S. (2014) Structural Study of Citrate Layers on Gold Nanoparticles: Role of Intermolecular Interactions in Stabilizing Nanoparticles. J. Am. Chem. Soc. 136, 1907-1921. Khlebtsov, N. G., and Dykman, L. A. (2010) Optical properties and biomedical applications of plasmonic nanoparticles. J. Quantitative Spectroscopy and Radiative Transfer 111, 1-35. Pyatenko, A., Yamaguchi, M., and Suzuki, M. (2007) Synthesis of Spherical Silver Nanoparticles with Controllable Sizes in Aqueous Solutions. J. Phys. Chem. C 111, 7910-7917. Jin, R., Charles Cao, Y., Hao, E., Metraux, G. S., Schatz, G. C., and Mirkin, C. A. (2003) Controlling anisotropic nanoparticle growth through plasmon excitation. Nature 425, 487490. Shoeib, T., Siu, K. W. M., and Hopkinson, A. C. (2002) Silver Ion Binding Energies of Amino Acids: Use of Theory to Assess the Validity of Experimental Silver Ion Basicities Obtained from the Kinetic Method. J. Phys. Chem. A 106, 6121-6128.


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(25)

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Poblete, H., Agarwal, A., Thomas, S. S., Bohne, C., Ravichandran, R., Phopase, J., Comer, J., and Alarcon, E. I. (2016) New Insights into Peptide–Silver Nanoparticle Interaction: Deciphering the Role of Cysteine and Lysine in the Peptide Sequence. Langmuir 32, 265-273. Le Beulze, A., Duguet, E., Mornet, S., Majimel, J., Tréguer-Delapierre, M., Ravaine, S., Florea, I., and Ersen, O. (2014) New Insights into the Side-Face Structure, Growth Aspects, and Reactivity of Agn Nanoprisms. Langmuir 30, 1424-1434.


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