Novel type of fluorescent silica nanoparticles: towards ultrabright. silica nanoparticles**
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1 Novel type of fluorescent silica nanoparticles: towards ultrabright silica nanoparticles** I. Sokolov 1,2.3.*, S. Naik 1 1 Department of Physics, 2 Department of Chemistry, 3 Center for Advanced Material processing (CAMP), Clarkson University, Potsdam, NY , USA * Corresponding author: Igor Sokolov, Dept. of Physics, 8 Clarkson Ave., Clarkson University, Potsdam, NY , USA; tel: , fax: ; e- mail: sokolov@clarkson.edu ** This work was supported by the US Army Research Office grant W911NF Recently we have reported on a novel type of fluorescent material, meso(nano)porous silica micron-size particles, in which organic fluorescent dyes were non-covalently entrapped inside self-sealed silica nanochannels. Here we present an attempt to scale down the size of those particles by quenching the synthesis at its early stage. In this way, we obtain a new class of silica fluorescent nanoparticles (~30 nm in diameter). We found the dyes can be packed inside the nanoparticles without quenching fluorescence ~250x denser than in aqueous solution. We demonstrate compatibility of the synthesized particles with labeling biological cells, and measure photostability of the particles directly inside the cells. Keywords: self-assembly; mesoporous silica particles; fluorescent silica particles; encapsulated fluorescent dyes. 1
2 Fluorescent nanoparticles (FNP) are of considerable interest nowadays as labels, tracers, sensors, and photon sources. Probably the largest areas of their application are nanobiotechnology and bioinformatics. Both areas require biocompatible nontoxic FNP. Silica FNP satisfy both requirements. Brightness of the particles is desired because it improves the signal-to-noise ratio when measuring florescent signals. An example of such bright commercially available FNP is well know quantum dots (QD), several nanometers semiconductor crystals. QD are brighter and typically more photostable than organic fluorescent dyes even when used in aqueous media [1, 2]. However, its use in many applications is still restricted because of their toxicity [3, 4]. Organic fluorescent dyes encapsulated in silica [5-7] have presented a promising alternative to quantum dots. Because of large variety of available fluorescent dyes, it is plausible to expect creation of FNP with more versatile fluorescent properties than fluorescence of quantum dots. Recently a synthesis of a new type of fluorescent material has been reported [8]. Dyes were non-covalently (physically) encapsulated in self-sealed nanosize channels inside micron size silica particles in high concentrations. Self-sealed topology of the channels manifested itself in virtually no leakage of the dyes out of the particles. Moreover, just physical confinement of the dye molecules resulted in no detectable decrease of the fluorescence quantum yield. Finally, a specific one-dimensional entrapment of the dye molecules inside silica nanochannels resulted in attaining much higher concentrations of the dye molecules inside the channels without quenching fluorescence. Up to four orders of magnitude higher concentration of the dyes can be [8, 9] reached inside the tubes without dimerization (i.e., quenching the fluorescence) compared to that in water (~4µM for rhodamine 6G dye). This made those particles times brighter than the particles of the same size made of QD encapsulated in polymeric matrix [10]. It would 2
3 definitely be a serious breakthrough in labeling technology if one would be able to synthesize nanosize silica particles with similar properties. Here we report on an attempt to do the above, to decrease the size of the ultra-bright fluorescent silica particles to nano dimensions. The main idea of the synthesis described here comes from the results of refs. [11, 12], in which it was shown that the nanoporous shapes were passing through a stage of seed formation. Here the nanosize particles are synthesized using a method based on origami type of templated sol gel synthesis [13, 14] with modification of ref. [8]. The synthesis is quenched at an early stage. Specifically, silica comes from hydrolysis and condensation of different water soluble organic silica precursors (organosiloxanes) in acidic conditions in presence of formamide. To synthesize the silica FNP, the origami synthesis [8] with rhodamine 6G fluorescent dye was stopped after approximately 4 hours. Atomic Force Microscopy (AFM, show in Fig.1) and Dynamic Light Scattering (DLS, shown in Fig.2b) indicate presence of ~30 nm nanoparticles in the synthesizing sol. A small percentage of micron size particles can also be seen, which are however can be easily separated by either filtration or centrifugation. The sol was neutralized with an alkaline solution, e.g., sodium hydroxide, or just diluted by a 5-10 fold with deionized water (MilliQ water). The solution was then dialyzed in quiescent conditions against ultrapure water for up to one week (fluorescence of the FNP solution should remain constant after that period of time). Aqueous solution of the particles was further passed through a 100nm syringe filter, and/or centrifuged to remove possible agglomerates (supernatant was collected). Fig.1 shows an AFM image of air dried FNP on a graphite slide. Particle-size analysis, Fig.2 a, shows that we are dealing with particle diameter averaged at ~31nm with 9 nm standard deviation (was found using SPIP 4 software, version 4; the diameter was estimated after taking 3
4 into account the AFM tip convolution). DLS data, Fig.2 b, shows a quite narrow size distribution centered at 30 nm. One can see a very good agreement with the AFM data. It was difficult however to obtain the TEM image of the particles. The particles tend to agglomerate and form almost continuous films when placed on a TEM film grid from aqueous environment. Separate particles were seen only as attached to the edge of those films. TEM data show a nanostructure of the particles with periodicity ca. 4nm, Fig.3, which is in agreement with the lattice constant of the origami structure [8, 13, 14]. It is interesting to note that some smaller particles (~10-20nm) observed with TEM showed the ordered structure only partially (Fig. 3 b). This observation is in agreement with other TEM observations of the initial stage of growth of mesoporous material [11, 15, 16]. Fig.1 Atomic force microscopy image of the nanoparticles dispersed on a graphite surface. 4
5 Fig.2. Particle size distributions obtained from AFM (a) and DLS (b). After stopping the synthesis, the sol contains mostly nanoparticles with some percentage of large particles as seen in (b). After filtration and centrifugation as described in the text, only nanoparticles are left. Fig.3. Transmission electron microscopy images showing nanoporosity of the particles. Scale bars are 20 (left) and 10 nm (right). 5
6 Fig.4 shows 3D fluorescent spectra of the synthesized FNP in water, Fig. 4 (a). For comparison, the spectra of the same dye in water (and the maximum non-dimerized concentration, 4µM) are shown, Fig. 4 (b). One can see virtually the same spectra for both free non-dimerized dye and the FNP (except the straight line corresponding to the direct scattering of excitation light by the nanoparticles). This indicates that the dye molecules inside the FNP are not dimerized. This is important fact because the lack of dimerization of the dye inside the particles was one of the reasons for ultra-bright fluorescence. Spectrum of the synthesizing sol (with no silica precursor, TEOS) is also presented. One can see much broader excitation range in the sol (as well as a red shift of the fluorescent maximum), which means that the dye in the sol is heavily dimerized. Absorbance (extinction) spectra of free dye and the FNP with the encapsulated dye are also almost identical near the region of maximum absorbance, Fig.4 (d). For shorter wavelengths there is a considerable deviation in the absorbance spectra due to the known phenomenon of light scattering (extinction) by nanosized particles. 6
7 Fig.4. Fluorescence spectra of the synthesized nanoparticles (a) and free dye in water (b). Spectrum of the synthesizing sol (with no silica precursor, TEOS) is shown in (c). All spectra are normalized on 100 au fluorescence for better comparison. (d) Absorbance/ extinction spectra of the free dye and the FNP with the encapsulated dye. High resolution spectra of the FNP, free dye, and ultra-bright origami micron size particles [8] are shown in Fig.5. For comparison, we also added a spectrum of 60 nm solid silica particles electrostatically coated with R6G ( colloidal silica was put in aqueous dye solution for overnight, then washed with buffer by centrifugation for ~5-7 times until supernatant gets clear). 7
8 One can see that the maximum of the origami is blue shifted relative to the free dye maximum. FNP spectrum is only slightly blue shifted with respect to the free dye. The FNP maximum is red shifted with respect to the origami maximum, and lies in-between the origami and the dye adhered on solid silica particles. This fact presumably means that some of the dye molecules are located inside the nanochannels while the other are electrostatically attached to the silica matrix. Fig.5. High resolution spectra of the FNP, free dye, ultra-bright origami micron size particles, and the dye electrostatically attached to 60nm solid silica particles. Quantum efficiency of the encapsulated dye was measured following a standard method which relates fluorescence and absorbance at low concentrations using R6G dye as a reference dye [17]. Using 488nm excitation, within the error of measurement we did not found the change of quantum efficiency of the dye inside of the particles vs water solution. To estimate the concentration of the dye inside nanoparticles, we weighted the nanoparticles by using a quartz microbalance (QCM). Four microliters of the particles in DI water was dried in a vacuum desiccator for 1 hour. The experiment was repeated three times 8
9 with two different Quartz crystals. The average mass of the precipitant, nanoparticles was found to be 6.9(±1.2) 10-7 g. Assuming the mass density of the nanoparticles equal to the density of large origami particles [8], ca.1.6g/cm 3, one can get % for the volume concentration of the nanoparticles in water. Extracting the dyes from the particles as described in ref. [8], and using the Beer s law, we found that the nanoparticles retain ~1.0mM of R6G dye (0.31mg of the dye per 1 g of the particles). This corresponds to approximately 8 molecules of R6G dye per FNP. It is interesting to compare fluorescent brightness of these particles with QD. Because each QD is approximately 20 times brighter than a single R6G molecule [10], brightness of each silica FNP can be estimated as 0.4 (8molecules/FNP *20) of the brightness of a single QD. The used here synthesis is capable of assembly of considerably brighter micron size particles. Therefore, we can hope that the reported here brightness is not the top limit of this method. We will work on the increase of brightness of silica FNP in the future. To find the relative brightness of the FNP with another independent method, we compared the FNP fluorescent brightness to the maximum brightness of water solution of pure R6G dye (observed for concentrations ca. 4µM; further increase of the concentration results in saturation of the fluorescent brightness due to dimerization). Because both spectra have maxima at ca. 555 nm, we compared the fluorescence at that wavelength. For the above estimated concentration of nanoparticles ( %) the brightness was 21 vs. 830 (measured in arbitral units) for the dye solution in water at 4µM concentration. To find the relative brightness, one needs obviously to compare the amount of fluorescence coming from the same volume of the particle s material and the dye solution. As a result, one gets that the FNP are 230 times (=21/830*100%/ %) brighter than the same volume of the dye water solution at its maximum non-dimerized concentration, 4µM. 9
10 Let us now show that the calculated above ratio of brightnesses is in quantitative agreement with the estimated dye concentration inside of the particles. Taking into account the concentration of the dye in water, 4µM, and comparing it to the concentration of the dye inside the particles, ~1.0mM, one can find that the particles should be 250 times brighter than the similar volume of the dye at its maximum non-dimerized concentration. The estimated ratio of 230 is slightly below that. This small difference can presumably be explained by some scattering of the excitation 488nm light by the silica surface of the nanoparticles. Because of biological compatibility of silica FNT, the synthesized nanoparticles can be applied for the labeling of viable biological cells without the need to fix the cells. Here we use human epithelial cervical cell model to demonstrate it. We also study photobleaching of the particles while inside the cells. This is not entirely quantitative approach but it gives a good feeling about how long the cells labeled with such nanoparticles can be imaged in a fluorescent microscope. To make this to some extend quantitative, we compare the bleaching of particles with photobleaching of pure dyes accumulated inside the cells, as well as photobleaching of a reference fluorescein dye. We also compare it to the photobleaching of 60 nm solid silica particles electrostatically coated with R6G, the same as we used for the fluorescence analysis shown in Fig.5. Primary culture of viable human cervical epithelial cells in growth medium was prepared as described in [18, 19]. The cells were washed with PBS buffer two times, and immediately immersed in PBS buffers containing approximately similar optical density solutions of the nanoparticles and dyes for ~5 minutes. Subsequently, the cells were washed twice with clear PBS buffer, and were imaged being immersed in PBS buffer with the help of a confocal microscope (Nikon C1, 10mW 488nm argon and 514 nm semiconductor lasers, 100x CFI VC 10
11 objective was used). Fig.6 shows typical confocal images of cells with nanoparticles, R6G dye, R6G on 60 nm solid silica particles. It is interesting to note that because of different chemistries and sizes, all these three tags demonstrate different intake. Free dye, having the highest mobility and positive charge, moves in the cells faster. This manifests in higher dye intake. The 60 nm dye coated silica nanoparticles show lesser intake than free dye, but higher than our FNP. This is presumably due to the fact that 60nm particles can easily release the dye, which is only electrostatically attached to the particle s surface. Moreover, the surface of the coated particles should be close to neutral, which helps for the intake [20] compared to more negative silica FNP. Compared with the intake of water-soluble QD, the above intake is rather fast. In general it is on the faster end when comparing with typical labeling dyes. 11
12 Fig.6. Labeling of viable human epithelial cervical cells with A) synthesized here silica nanoparticles, B) R6G free dye, C) R6G dye electrostatically bound to 60 nm monolithic silica particles. Horizontal scale of the images is 120 µm. To study photobleaching, the area of confocal imaging was decreased to 15x15 µm 2, with the collection time of 9 µs per pixel. The photo bleaching was studied for 20 seconds. Figure 7 shows a relative decrease of brightness averaged over several areas inside the cells. 12
13 Figure 7. A relative decrease will brightness of different fluorescent substances inside cells. One can see that the fluorescence of the silica FNP is the most stable as compared to both free R6G and R6G dye electrostatically bound to monolithic silica nanoparticles. This is not surprising because of known prolonged photostability of the dyes encapsulated in silica zerogel matrixes [21]. Photobleaching of fluorescein is shown as a reference. It is useful to compare the described synthesis with the other methods of synthesis of silica FNP. Briefly, the existing methods of making silica FNP are based on modification of the classical Stäber method (hydrolysis and condensation of a silica alkoxide precursors) in presence of fluorescence dyes [6, 7, 22-27]. This is done either in solution or in water-in-oil reverse microemulsion. To keep the dye inside silica matrix, it is either covalently coupled to silica or stay inside due to hydrophobic interactions (water insoluble dyes). The main difference from those methods is that the dye is non-covalently entrapped inside micelle channels of mesoporous 13
14 silica matrix. This implies that the synthesis can easily be adapted to virtually any dye without chemical modification of the dye molecules. To conclude, we were able to synthesize nanoparticles following the same route as was used for synthesis of ultra bright fluorescent micron particles. We showed that the dye molecules are physically encapsulated inside nanosize channels/tubes inside FNP, while some dye molecules are presumably electrostatically bound to the silica matrix of FNP. Stable (no-leakage) concentration of the dye inside the particles is 0.31mg per 1 g of the particles. This corresponds to approximately 8 molecules of R6G dye per single nanoparticle. It brings approximately 230 times brighter fluorescence than the maximum emission from the aqueous dye solution of the same volume. It is still only 0.4 of brightness of a single quantum dot, but still can successfully be applied for bio-labeling. Comparing with the potential of the approach [8], we foresee synthesizing silica FNP brighter than quantum dots. The synthesized particles are biocompatible, and can easily permeate the cell membrane to be used for cell labeling. Photostability of the particles measured directly inside cells is higher compared to the stability of free dye and the dye electrostatically bound to the monolithic silica nanoparticles. Large number of available organic fluorescent dyes compatible with the described synthesis makes the developed particles useful for a diverse range of biological and analytical applications. 14
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