Letter pubs.acs.org/JPCL
Streptavidin Inhibits Self-Assembly of CdTe Nanoparticles Azizeh-Mitra Yousefi,†,⊥ Yunlong Zhou,† Ana Querejeta-Fernández,† Kai Sun,‡ and Nicholas A. Kotov*,†,‡,§,∥ †
Department of Chemical Engineering, ‡Department of Material Sciences and Engineering, §Department of Biomedical Engineering, and ∥BioInterface Institute, University of Michigan, Ann Arbor, Michigan 48109, United States S Supporting Information *
ABSTRACT: Nanoparticles (NPs) exhibit strong tendency to self-assemble. It is important to understand how the presence of other macromolecular compounds, affects this ability. The interaction between standard thiol-capped cadmium telluride (CdTe) NPs and streptavidin (STAV)the essential component of many NP applicationswas examined at different molar ratios and pH values. The central observation of this study is that STAV strongly inhibits the self-assembly of CdTe NPs into nanowires. The underlying mechanism of inhibition was attributed to the formation of a STAV corona and surface layer that precludes attachment of NPs to each other. Instead of nanowires, we observed a spectrum of agglomerates containing both CdTe and STAV of different geometries depending on the molar ratios of the reagents in NP synthesis and pH values of the media. SECTION: Physical Processes in Nanomaterials and Nanostructures
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similar to each other and depend on the same media parameters.13 For example, surface charges of both NPs and GPs depend on pH and ionic strength and can influence their binding interactions to cellular membranes. The similarity of the chemical behavior of NPs and GPs seen in a number of selfassembly processes including DNA13 is not accidental but is based on analogous structure as well as thermodynamic and kinetic behavior of such nanoscale structures in aqueous media. Inorganic NPs coated with organic films can display surface chemistries that allow them to function like GPs.13 In addition to the fundamental merits of detailed studies of noncovalent assemblies of NPs and proteins, semiconductor NPs have been the subject of extensive studies as a new class of fluorescent probes for many biological and biomedical applications, including cell imaging, biosensing, and single molecule detection.14−18 There has been a growing interest of utilizing these NPs, for in vivo animal tracking, tumor targeting, and cancer therapy.18−20 Fundamental understanding of the parameters affecting NP−protein interaction can provide insight into designing optimal imaging agents. Streptavidin (STAV) is one of the most common GPs used in imaging, sensing, drug delivery, and general modification of NPs. It is used in combination with NPs very often. Wu et al. used NPs linked to immunoglobulin G (IgG) and STAV to label the breast cancer marker HER2 on the surface of fixed and
aining control over the spatial distribution and architecture of nanoparticle (NP) assemblies for a variety of catalytic, optical, and sensing applications necessitates understanding of their self-organization processes, which can be driven by a variety of forces and result in very diverse products. Recent studies indicate that NPs can self-assemble into complex microscale superstructures such as chains, sheets, and twisted ribbons1−4 and potentially some others. A selflimiting assembly with similarly charged NPs attracted by van der Waals forces leads to supraparticles and is expected to be very versatile in respect to different components.5 Hierarchically organized colloidal crystals of supraparticles and threedimensional (3D) NP systems with continuous crystallinity throughout the assembly facilitating charge transport6 will open the door to simple manufacturing pathways of complex macroscale hybrid materials and devices.5 In this respect, it is essential to understand the factors that both stimulate and inhibit self-assembly processes in NP dispersions. The latter were paid much less attention than the former, although they are as technologically significant and academically interesting. Different compounds capable of noncovalent interactions with NPs, the ionic strength/pH of the NPs solution, the NPs concentration, and their size, are among the parameters that may influence the self-assembly dynamics, but very little is known about it.7−12 This is particularly true with respect to proteins as the essential part of all biological systems and important components of many applications of NPs, from artificial photosynthesis to sensors. It has been reported that the interactions of water-soluble NPs and globular proteins (GPs) with the environment and other soluble molecules are very © 2012 American Chemical Society
Received: September 18, 2012 Accepted: October 16, 2012 Published: October 16, 2012 3249
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For the first set of experiments, a molar ratio of primary reagents during synthesis, i.e., TGA and cadmium perchlorate, was 1.5; it will be denoted throughout the paper as synthetic molar ratio (SMR), which to determine the relative density of TGA molecules on the surface of NPs. The effect of SMR on the size of the NPs was compensated by different reaction times. The average NP diameter based on the luminescence peak was 3 nm in all experiments (SI). The same diameter determined from transmission electron microscopy (TEM) data was ∼2.5−3 nm, as can be seen in Figure 1a. After
live cancer cells.15 Lai et al.21 demonstrated that STAVfunctionalized silver-NP-enriched carbon nanotube (CNT/Ag NPs) were easily linked to a biotinylated signal antibody for multiplexed immunoassay of tumor markers. Liu et al.22 developed a three-component NP in which up to four biotinylated components were combined via STAV as a linker. It was shown that the presence of STAV permitted the migration to the nucleus of the radiolabeled oligomer within the NP. The noncovalent biotin−STAV bond was found to be essential for adequate delivery of the radiolabeled antisense oligomer to the nucleus of tumor cells. Despite the numerous studies combining NPs with STAV and the commonality of the STAV/NP system, the question of how the presence of this GP affects the ability of NP to assemble was never posed. For these reasons, and considering the widely discussed applications of both STAV and NPs, we decided to investigate how STAV affects the self-organization of prototypical NPs. As a model system, we used well-known water-soluble CdTe NPs; the interaction between these NPs and STAV was investigated at different molar ratios of reagents used in NP synthesis and pH values of the media where the assembly process took place. It was found that STAV strongly inhibits the self-assembly of CdTe NPs into nanowires (NWs). Instead we observed the formation of less regular supraparticle-like structures of different geometry depending on the assembly conditions, attributed to the balance between electrostatic repulsion and noncovalent intermolecular attraction between CdTe and STAV within each superstructure. Assembly of negatively charged semiconductor NPs, cadmium telluride (CdTe), coated with thioglycolic acid (TGA)2 has been used as the key building block for NW formation.23 To initiate the NW formation, the excess stabilizer should be removed through centrifugation. The precipitate is then dispersed in water at pH 9 and aged at room temperature for several days. Over time, the color of the solution gradually turns from orange to dark brown or black. It has been demonstrated that the individual NPs can self-assemble into solid NWs irrespective of the CdTe particle size.24 Using similar approaches, electrostatic or hydrophobic interactions of ligand-stabilized NPs with DNA has enabled the synthesis of long chain-like linear architectures, composed of parallel and branched morphologies of assembled NPs. In the present work, this synthetic procedure has been modified to examine the interactions between semiconductor NPs with STAV aiming at better understanding of how self-assembly tendencies of NPs are affected by the presence of this particular GP. The reason that we chose STAV as an exemplary GP for this study is that it is probably the most common protein in scientific studies. STAV is a tetramer approximately 5.4 × 5.8 × 5.8 nm in size;25,26 it is typically obtained by purification from the bacterium Streptomyces avidini. Its frequent use in molecular biology is attributed to its exceptionally strong bond with biotin; with the aid of the strong STAV−biotin bond, various biomolecules can be attached to one another or onto a solid support.27 STAV has an isoelectric point (IEP) of ∼5−6,28 and therefore, it is negatively charged in a wide range of pH values coinciding with the colloidal stability of NPs. CdTe NPs demonstrate an intrinsic tendency to selfassemble due to a combination of charge, dipolar, hydrophobic, and van der Waals interactions. In this study, TGA-stabilized NPs (TGA−CdTe) were synthesized according to previous publications3,29 in a form of aqueous dispersions with a concentration of 13 μmol/L (see Supporting Information, SI).
Figure 1. TEM images of (a) CdTe NPs (day 1) and (b,c) selfassembled CdTe (diluted - day 5); SEM images of (d) self-assembled CdTe (diluted - day 5), (e) CdTe nanowire formation (nondiluted day 7), and (f) dendritic crystallites predominantly observed for solutions of STAV without NPs. SMR = 1.5 (pH 9).
removing the excess stabilizer through centrifugation, the precipitate was dispersed in water at different pH in order to investigate the effect of charges on the interactions between CdTe and STAV. The different CdTe/STAV molar ratios considered in this study are summarized in Table 1. Due to the low solubility of STAV (0.1 mg/mL H2O), all the solutions were diluted (≥6 times). Formulations containing pure CdTe and pure STAV were also prepared for comparison (controls). Unless otherwise indicated, the scanning electron microscopy (SEM) and TEM images correspond to diluted formulations 5 days after preparing the samples to provide an adequate benchmark visualizing potential agglomeration/ assembly process in these systems. The orange color of the solutions containing CdTe turned brown in ∼3−4 days of the assembly process in all cases. TEM and SEM of the dispersions of CdTe NPs without STAV indicated the presence of self3250
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Table 1. CdTe/STAV Molar Ratios and Water pH for the Different Formulations formulation
molar ratio
pH (water)
1 2 3 4 5 6 7 8 9 10 11 12
1 2 6 13 1 2 6 13 1 2 6 13
9
7
5
assembled networks (day 5) as shown in Figure 1b to 1d. Examination of the dispersions in the absence of STAV using SEM revealed the formation of NWs (Figure 1e) for a nondiluted solution (day 7); the redispersion of CdTe in water (pH 9) after centrifugation was performed as reported elsewhere.20 At the same time, SEM of the samples produced from pure STAV solution showed a dendritic crystallites (Figure 1f). STAV crystallizes readily in two-dimensions,30 under a wide range of concentrations and temperatures.31 It has been reported that the impurities in commercially available STAV is responsible for the dendritic growth of H- and Xshaped crystals,32 at length scales similar to the one shown in the SEM image (Figure 1f). The effect of STAV on the assembly of NPs was studied for different concentrations of STAV and at different pH values. Figure 2a,c shows the TEM images of the formulation with CdTe/STAV at a molar ratio of 1 (pH 7). The darker parts in these images correspond to domains primarily made of CdTe NPs. The lighter regions are associated with the STAV-rich domains surrounded with the NPs, which are more transparent to electron beam than inorganic NPs. Overall, no formation of CdTe NWs could be observed in the presence of STAV similar to those in Figure 1e. The effect of STAV on CdTe NP assembly is very obvious: a strong suppression of linear assemblies of NPs, which would lead to the formation of NWs in the absence of STAV. Instead of the NWs, for CdTe/STAV = 1 at pH 7 we see the formation of small clusters similar to those observed before with amyloid peptides.33 The TEM and SEM images show the presence of both CdTe and STAV within these structures and suggests a size of ∼100 nm for these clusters (Figure 2c,e). Although, some tendency of NPs to self-assemble into chains within these clusters could be observed, further recrystallization into NWs and the formation of extended chain networks is inhibited compared to NP dispersions without STAV. This indicates the formation of STAV “coronas” around NPs34,35 and adsorption of STAV on NP surface36,37 is believed to prevent the merger of crystalline cores into CdTe NWs. These clusters are irregular and do not have the well-defined shape but they still show fairly narrow size distribution (Figure 2e). They could be conceptually similar to CdSe, CdS, and other supraparticles observed before5 with the difference that they are made from inorganic and organic components. Figure 2b,d,f gives the TEM and SEM images of the formulation with greater concentration of NPs, i.e., with CdTe/STAV at a molar ratio of 6 and pH 7. Large aggregates and networks made with a large content of CdTe NPs were formed in this case, indicating
Figure 2. (a) TEM image of the system for CdTe/STAV=1, pH 7; (c) lower magnification TEM image revealing clusters of CdTe/STAV ∼100 nm in size (marked) within which the NP form chains; (e) SEM image showing the presence of sporadically distributed particles (clusters) of the same size formed under the same conditions. (b,d,f) Corresponding results for the formulation with CdTe/STAV = 6, pH 7 revealing the NP-STAV networks. SMR = 1.5.
that the tendency of NPs to self-assemble is still retained when the STAV coating on them is thinner and has smaller interference with the interparticle forces. The relatively high negative charge producing inter-NP electrostatic repulsion facilitates colloidal stability of aqueous NPs.38 Lowering pH decreases the ionization of terminal groups and leads to the decreased electrostatic repulsion and finally results in the aggregation of NPs. However, the change of pH also affects the manifold of attractive interactions between the constitutive elements of the assembled superstructure with STAV by altering the surface charges. Aggregation of the NPs due to the formation of STAV layers on the surface can also be prevented similarly to their selfassembly. Therefore, the overall effect of pH on the morphology and dimensions of the hybrid STAV-NP systems could be rather unpredictable and dependent on CdTe/STAV ratio. It should be noted that the charge on the surface of a protein is a complex function of the distribution of amino acid residues in the protein molecule, and is unevenly distributed over its surface.39 In addition, this charge depends on the medium surrounding the protein molecule. The interaction of a charged surface (e.g., NPs) with the protein changes the zeta potential (ζ) of the particle, where the maximum alteration has been observed near the IEP of the protein.40 Moreover, it has been shown that an increase in particle size from 6 to 104 nm (TiO2) can reduce the IEP of the NP from 6 to 3.8, which may in turn influence the NP interactions with the biomolecule.41 While biomolecules may promote NP aggregation, this phenomenon is mediated by protein−protein interaction occurring at a high 3251
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Figure 3. (a,b) TEM and (c) SEM images of the aggregates found in the dispersion with CdTe/STAV = 13 pH 9; (d,e) TEM and (f) SEM images for CdTe/STAV = 13 pH 5; (g,h) TEM and (i) SEM images for CdTe/STAV=2 pH 5. SMR = 1.5.
Figure 4. XPS spectra for CdTe/STAV = 1 pH 7; SMR = 1.5.
eliminate it completely and scrambles the linear patterns typical for them. This observation can be confirmed by the data in Figure 3c,f. At lower pH, the SEM image suggests the formation of sporadically distributed aggregates composed of CdTe NPs. As one can possibly expect already, changing the molar ratio to CdTe/STAV = 2 leads to drastic decrease of diameter of NP agglomerates to 30 nm (Figure 3g,h) and affects the overall size of the clusters (Figure 3i). The reduction of the cluster size compared to Figure 2 and between pH 9 versus pH 5 is likely to correspond not to the increase of electrostatic repulsion within the CdTe-STAV but rather to the decrease of attractive forces at pH 5, for instance hydrogen
protein concentration. It has been reported that protein molecules can form bridges between NPs in certain cases.39 Dispersions with high CdTe/STAV ratios were used to further investigate STAV-inhibited linear assembly of NPs. The TEM and SEM images for pH 9 indicate the formation of aggregates and linear chains at a CdTe/STAV = 13 (Figure 3a− c). However, the corresponding images at pH 5 for the same molar ratio appear to have platelet-like geometry (Figure 3d− f). We see again the same trend that increase of the relative content of CdTe regardless of pH results in larger agglomerates and linear modes of association of NPs in them. Therefore, while inhibiting the NP assembly process, STAV cannot 3252
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bonding. The pKa of STAV is between 5 and 6,42 so at pH 5 the STAV becomes protonated43 and attracts the negatively charged CdTe NPs. The overall concentration of negative charges residing on TGA-CdTe NPs decreases with a decrease in pH.44 The pHsensitive photoluminescence (PL) behavior of as-prepared aqueous TGA-CdTe NPs has been studied by Xu et al.45 For TGA ligands, the negatively charged terminal groups (COO−) transform to the uncharged form (COOH) upon reducing the pH. Enhanced PL of NPs at a lower pH was attributed to the decreased electrostatic repulsion of NPs and, in turn, adsorption/diffusion of stabilizers to NPs. However, when the solution pH drops below 6, the hydrodynamic diameter of NPs increases dramatically and adversely affects the PL intensity.45 In this study, the PL intensity at different pH indicated a similar trend for CdTe after 4 days of assembly, when compared to asprepared NPs. For the formulations containing a small concentration of STAV (CdTe/STAV = 13), the observed peak intensity at pH 5 was greater that the corresponding value at pH 9 (see the Supporting Information, SI). This suggests the absence of dramatic increase in hydrodynamic diameter of the clusters at pH 5 in the presence of STAV. The composition of the dispersions was determined from Xray photoelectron spectroscopy (XPS) spectra. The presence of STAV was demonstrated by the appearance of the signals in the XPS spectra between 400 and 550 eV for O and N. As nitrogen is a main constituent of peptides, a peak at ∼400 eV is expected for N1s signal, as shown in Figure 4.46 Considering different forces, stabilizers play a significant role in the balance of forces between constitutive parts of NP agglomerates. The effect of TGA concentration during synthesis, and therefore, the relative density of ionizable −COOH groups at the NP−water interface in the resulting NPs, on the interactions between CdTe NPs and STAV was investigated by increasing the SMR from 1.5, as in the previous experimental sets, to 2.4 (see the SI). The CdTe/STAV molar ratios considered for this series of experiments were chosen to be 1, 2, and 6 at pH 7, which are comparable to the case of CdTe−STAV dispersions in Figure 2 and other dispersions investigated above (Table 1). Figure 5a,b shows the TEM images of the formulation with CdTe/STAV = 1, pH 7, where we can clearly see the formation of NP sheets comprised from both NP and STAV. Given the pKa value of STAV (5−6),42 the formation of NP sheets indicates stronger attractive forces associated with greater density of TGA on NP surface. The nature of these forces can be debated and requires extended further studies. It is conceivable that TGA is involved extensively in hydrogen bonds with STAV. A parallel with previous studies of self-organization of 2-(dimethylamino)ethanethiol (DMAET)-stabilized CdTe is probably appropriate: the relative increase of attractive interactions stimulated extended two-dimensional structures of NPs.1 One additional point to be made here is that while inhibiting the assembly of NP into NWs, STAV apparently can facilitate other types of assemblies. The preferential pattern of such assemblies is difficult to predict at the moment due to the complexity of the interactions involved and the multitude of effects that adsorption of GPs, and STAV in particular, on NPs can infer. Some information about the forces acting between the assembling blocks in these dispersions and the reasons for inhibition of NW self-organization can be obtained from the measurements of zeta potential, ξ.47 They were performed for the dispersions with SMR = 2.4 so as to investigate the role of
Figure 5. (a,b) TEM images of dispersions with CdTe/STAV = 1 pH 7; (c-d) corresponding SEM images at different magnifications; SMR= 2.4.
surface charges on the two-dimensional structures of NPs observed in Figure 5. The zeta potential shows an average value below −70 mV after 24 h (Figure 6a), which reflects stable NPs at the early stage of the dispersion. Then, it gradually becomes more positive and finally stabilizes between −15 to −12 mV (after 72 h) for all the different ratios of CdTe/STAV (Figure 6b,c). It has been shown that the adsorbed proteins change the zeta potentials and the IEP of NPs (e.g., oxide particles with diameters 73−271 nm),40,48 and therefore the IEP of the suspension shifts toward the corresponding IEP of the added protein. The reported zeta potential for as-prepared TGACdTe NPs at pH 7 is ξ = −35 mV.30 Since STAV has an IEP between 5−6,28 at pH 7 it carries a negative charge, for which the estimated zeta potential is ξ = −10 mV.49 This explains the multiple peaks observed after 24 h for CdTe/STAV = 1 at pH 7 and indicates the presence of constituents with different surface charges (Figure 6a). The overall trend of zeta potential during the formation of CdTe/STAV aggregates is shown in Figure 6c and indicates the formation of structures with the same surface charge after 72 h (Figure 6b). The corresponding data for CdTe, without STAV, shows a zeta potential of −36 mV after 72 h (Figure 6d). In light of this, the observed value for CdTe/STAV after 72 h (−15 to −12 mV) might be due to the shift of IEP of the dispersion toward the IEP of STAV.40 This could be a potential driving force for the formation of NP-STAV agglomerates and a strong confirmation for the reasons of NW assembly inhibition due to the attachment of STAV to CdTe NPs (Figure 5). The same conclusion can be reached from the trend reflected by the zeta potential of the dispersions50−52 after 72 h (approaching zero). Biomolecule−NP assemblies have been widely used in bioanalytical applications and for the fabrication of bioelectronic devices.53 Biological molecules are used for functionalization of NPs through a variety of techniques, including physical adsorption, electrostatic binding, specific recognition, and covalent coupling.53−55 The NP−protein conjugates can be prepared through the interaction between the NPs and the mercapto and amino groups of proteins. 56 STAV is 3253
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Figure 6. Zeta potential for the CdTe/STAV = 1, pH 7 (a) 24 h and (b) 72 h after preparation; (c) the overall trend for the CdTe/STAV ratios of 1, 2, and 6 at pH 7; (d) CdTe without STAV at pH 7 after 72 h; SMR = 2.4.
characterized by four high-affinity (Ka > 1014 M−1) binding sites for biotin. Therefore, by the appropriate functionalization of NPs with biotin units, 3D NP aggregates can be generated.53,57 Sönnichsen et al.56 used aqueous solutions of gold and silver NPs with STAV-T50 buffer solution, which were allowed to react in the presence of NaHCO3. The same concept was used by Lai et al.21 to prepare STAV-functionalized CNT/Ag NPs. In this study we explored a self-assembly route to produce NP conjugates of STAV. Understanding the mechanism of the interactions between CdTe and STAV can provide insight into intrinsic interactions between NPs and biomolecules. The formation of clusters composed of both CdTe and STAV examined in this work suggests the possibility of producing selfassembled structures from inorganic NPs and organic proteins. The supraparticle-like agglomerates containing both CdTe and STAV were attributed to the compensation between the electrostatic repulsion of the particles and attractive forces between NPs and STAV. From this perspective, Lu et al.18 examined the interactions of surface-immobilized NPs with proteins and reported an electrostatic attraction nature. A mechanism involving protein surface charge distribution and its molecular size was elucidated to explain the NP−protein interaction. The key insight presented in this study was the ability of STAV in inhibiting the self-assembly of CdTe NPs, depending on the molar ratios of the reagents in NP synthesis and pH values of the media. It was inferred that the adsorption of STAV on an NP surface prevented the merger of crystalline cores into CdTe NWs. However, the presence of large aggregates at higher concentrations of CdTe NPs indicated that the tendency of NPs to self-assemble was still retained when the STAV coating on them was thinner. Knowing that NP binding may change the protein structure and affect its function, the structure alteration should be investigated in
future studies. In addition, in some biomedical applications, protein adsorption on NP surfaces can make NPs lose specificity and reduce fluorescent efficiency.14 Therefore, fundamental understanding of the parameters for NP-protein interaction and the underlying mechanism can provide insight into designing optimal systems for biomedical applications.
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ASSOCIATED CONTENT
S Supporting Information *
Experimental details, UV−vis/PL spectra, and concentration calculation of NPs are available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Present Address ⊥
Associate Professor, Bioengineering/Chemical and Paper Engineering Department, Miami University, Oxford, OH 45056 (on sabbatical leave at the University of Michigan). Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The sabbatical leave for Prof. Azizeh-Mitra (Amy) Yousefi was supported by Miami University. Amy Yousefi thanks Prof. Nicholas Kotov for her research stay at the University of Michigan. The authors thank the University of Michigan’s EMAL for its assistance with electron microscopy and for the NSF grant #DMR-9871177 for funding for the JEOL l electron microscope used in this work. We also acknowledge the technical assistance of Yingyue Zhu, John Mansfield, Ying Qi, Wei Liu, and Yongan Tang. This paper is based upon work 3254
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partially supported by the Center for Solar and Thermal Energy Conversion, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Award Number #DE-SC0000957 used to purchase materials for CdTe synthesis as well as STAV. This work was also in part supported by the Center for Photonic and Multiscale Nanomaterials (C-PHOM) funded by the National Science Foundation Materials Research Science and Engineering Center program DMR 1120923 used for the student support. We acknowledge support from NSF under grants ECS-0601345; EFRI-BSBA 0938019; CBET 0933384; CBET 0932823; and CBET 1036672, which were used to maintain the instruments utilized in this project, such as luminescence spectrometer and to pay the electron microscopy user fees.
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