Abstract

Nano-composites of quantum dots (QDs) and gold nanorods (GNRs) or silica-coated GNRs (GNRs_SiO2) were synthesized. The attached GNRs modify the excitation intensity and spontaneous emission of QDs through the surface plasmonic effects. The fluorescence from QDs is enhanced and can be optimized by modifying the thickness of silica coated on GNRs, under both one- and two-photon excitations. The measurements of fluorescence intensity and lifetime demonstrate that the enhancement may be attributed to the matching of the localized surface plasmon resonance of GNR to the excitation wavelength. In addition to enhancing QD-fluorescence in QD-GNR@SiO2, GNRs also present as an effective contrast agent for bio-imaging, through light scattering and or two-photon emission, as well as for photo-thermal therapy. The composite’s multifunctional characteristics are highly valuable and to be exploited in bio-applications.

© 2010 OSA

1. Introduction

Fluorescence-based techniques have emerged as powerful methods in the field of biomedicine, and especially in bio-molecule detection and disease diagnosis [1,2]. Fluorescence enhancement not only is of great interest for improving bio-detective sensitivity but also constitutes an important subject in physics, chemistry, and materials science. Since the pioneering work of Purcell indicated that the lifetime of the excited state and the spontaneous emission can be modified by controlling the external nano-environment [3], numerous studies have emerged to elucidate further the enhancement of emission when a fluorophore is combined with resonant cavities, photonic crystals and metallic structures [4,5]. Metallic structures, which possess particular surface plasmon properties, have been applied to enhance fluorescence from adjacent fluorophores [618]. The surface plasmon on metallic nanoparticles is modified in a manner that depends on the sizes and shapes of such particles, as predicted by Mie theory [19]. This unique characteristic offers a convenient means of generating insights on surface plasmon-induced fluorescence enhancement by modifying the surface plasmon properties by shaping nanoparticles.

In this work, gold nanorods (GNRs) are used as the enhancing metallic nanoparticles to study their effects on the emission of adjacent quantum dots (QDs). A GNR has two localized surface plasmon resonance (LSPR) extinction (longitudinal and transverse) bands. The longitudinal LSPR band can be tuned from visible to near-infrared by adjusting the rod’s aspect ratio (width to length) and is much stronger than the LSPR band of nanosphere structures [20]. The strong LSPR band results in an enhanced electromagnetic field at the surface of the nanoparticle. This unique property makes GNRs excellent candidates for studying surface-enhanced Raman scattering [21], optical antenna, and fluorescence enhancement [6,7]. GNRs also present great potential in bio-applications, because of their favorable properties for scattering and absorption [2224]. Pronounced two-photon absorption and luminescence from GNRs have also been observed. These properties are exploited very effectively in cellular imaging [25,26] and optical recording [27].

The LSPR-induced electromagnetic field from metallic nanostructures affects the photoluminescence of adjacent fluorophores by modifying their radiative and nonradiative decay rates, which compete to determine the emission quantum yield, as well as the excitation intensity. The enhancement factor of the emission can be expressed as γem,

γem=γexcκη=γexcκRradRrad+Rnonrad
where γexc is the enhancement factor of excitation intensity; κ is the light collection efficiency; η is the quantum yield, and Rradand Rnonrad are the radiative and nonradiative decay rates of the luminescence, respectively. The enhancement of excitation intensity and the increase in radiative decay rate strengthen the emission. However, the increase in nonradiative decay rate reduces the emission (quenching effect). As indicated by Eq. (1), the fluorescence enhancement has from two components: excitation enhancement and changes in quantum yield. Few studies have separately discussed these two components of fluorescence enhancement [28,29]. Many works have focused only on the increase in radiative decay rate as a result of the spectral overlapping of the LSPR band of the nanoparticles and the emission spectra of the fluorophores- especially for fluorophores of low internal quantum yield [68,14,15]. However, the excitation enhancement, which is caused by the strong absorption that is the well-known optical antenna effect [16], cannot be easily differentiated from the overall enhancement. Some works have also demonstrated that when the fluorophores are close to metallic nanoparticles, the nonradiative decay rate is increased and the quantum yield is therefore reduced, as revealed by time-resolved fluorescence measurements and theoretical modeling [16,30,31]. To minimize the effect of the increase in the nonradiative decay rate, the spatial separation between the fluorophores and the metal surface is varied. Many works have shown that the separation critically determines whether enhancement or quenching eventually dominates [1013]. Emission quenching of the fluorophores that are close to metallic nanoparticles is regarded as analogous to Förster resonance energy transfer (FRET) and is referred to as surface energy transfer (SET), which is sensitive to the separation between donors (fluorophores) and acceptors (metallic nanoparticles) [32,33]. The SET quenching effect dominates the modification process when the separation is short (usually less than around 10 nm) [3033]. Increasing this distance reduces the nonradiative decay rate, and consequently the quenching efficiency. However, the excitation enhancement and the radiative decay rate are also decreased [16]. Therefore, optimizing the separation to maximize fluorescence enhancement involves a trade-off. Some studies have suggested that the optimal distance is approximately 10 to 20 nm [1013]. Enhancing and quenching of the fluorescence by metal nanoparticles and plasmon becomes a popular topic with many reports [3437].

We described the SET quenching effect of CdSe quantum dots (QDs) with GNRs and polyelectrolytes coated GNRs in a previous work [32]. The conjugation of QDs with GNRs_SiO2(to represent SiO2 over GNRs) enhances their emission by increasing the distance of QDs from the metal surface. Coating silica on GNRs is advantageous for robust bio-applications because it reduces toxicity, improves stability, has good biocompatibility, and offers the convenience of surface functionalization [38]. Silica coatings can reach more than 20 nm thick; such thicknesses cannot be achieved using polymer coatings. Coating with silica to various thicknesses provides a convenient means of studying the distance-dependent enhancement effect of QD-emission with GNRs. Three kinds of GNR with distinct LSPR peaks were used to investigate the effect of LSPR on fluorescence enhancement. The samples were excited under one- and two-photon excitation to study the contribution of such excitation to the enhancement. Fluorescence lifetime imaging microscopy (FLIM) [39,40] was used to examine the change in the lifetime of QD-emission. Fluorescence lifetime is helpful in differentiating the effect of excitation intensity from the effect of changes in emission decay rate, since excitation intensity does not influence the decay rate or the lifetime of the luminescence.

In bio-imaging applications, the large surface area of GNR-composites facilitates surface functionalization for organic or other conjugations. In addition to strengthening fluorescence from GNRs_SiO2-combined QDs, GNRs and GNRs_SiO2 also strongly scatter red light [38,41], unlike cells in dark-field imaging, which scatter white-blue light. Additionally, under two-photon excitation, GNRs emit bright fluorescence with a very short lifetime, which differs from longer lifetime of QD-emission. The strong absorption of GNRs may be applied to heat the composites in cells for photo-thermal therapy in a 3D, highly spatially localized manner. Multifunctional properties make QD-GNR_SiO2 composites effective materials for bio-applications under a broad range of applications settings: one-, two-photon and dark-field imaging, as well as the effect of photo-thermal therapy.

2. Experimental section

2.1 Materials

Cetyltrimethylammonium bromide (CTAB), chloroauric acid (HAuCl4·3H2O), sodium borohydride (NaBH4), silver nitrate (AgNO3), ascorbic acid, anhydrous ethanol and ammonia aqueous were purchased from Sinopharm Chemical Reagent Co., Ltd.. Tetraethylorthosilicate (TEOS) and Dulbecco’s Modified Eagle’s medium (DMEM) were obtained from Sigma-Aldrich. Carboxyl capped CdSe QDs (emission peak 605 nm) were purchased from Invitrogen, Inc. The antibody anti-CEA8 (anti-CEAcam8/CD67) was purchased from Beijing Biosynthesis Biotechnology Co., Ltd.. Deionized (DI) water was used in all experimental steps.

2.2 Synthesis of GNR and GNR_SiO2

To synthesize GNRs with different LSPR peaks, gold nanoparticle seeds were firstly prepared by adding 0.6 ml 0.01 M ice-cold sodium borohydride to a 10 ml stirred solution of 0.1 M CTAB and 0.25 mM chloroauric acid. 80 mM 0.185 mL, 0.18 mL and 0.15 mL ascorbic acid were added into three bottles of 20 mL 0.04 mM, 0.128 mM and 0.14 mM aqueous silver nitrate, and mixed with 0.1 M CTAB and 0.5 mM chloroauric acid, to reduce Au3+ to Au+ and form three growth solutions. After the color of the solutions had turned from orange to colorless, 0.024 mL of gold seed solution was injected into each of the three growth solutions to grow the GNRs with LSPR peaks at 600 nm, 650 nm and 730 nm. To remove excess CTAB in the GNR-solution, centrifugation was carried out at 9,000 rpm for 15 min after the GNRs had grown for 12h. The concentrations of GNRs in the solution are estimated and simulated with reference to their sizes and absorbance optical densities [42]. 1 mL and 1.5 mL of 10 mM TEOS ethanol solutions were added to 8 mL of 10 nM aqueous GNRs at a pH of 9.0 (adjusted by adding aqueous ammonia) to synthesize 8 nm- and 13 nm-thick silica coatings on the GNRs. The reaction lasted for six hours at room temperature. Excess TEOS was removed by centrifuging at 6,500 rpm for 15 min.

2.3 Conjugation of QDs and antibodies with GNR and GNR_SiO2

The QD-GNR and QD-GNR_SiO2 composites were synthesized by mixing 100 μL of 10 nM GNRs and GNR_SiO2 separately with 10 μL of 2 μM carboxyl capped QDs with stirring. The ratio of GNR-number to QD-number in QD-GNR/GNR_SiO2 composites was around 1:20. Anti-CEAcam8/CD67 (carcinoembryonic antigen-related cell adhesion molecule 8) was conjugated with QD-GNR and QD-GNR_SiO2 composites to label HeLa cells. To functionalize anti-CEA8, 100 μL of 10 nM QD-GNR and QD-GNR_SiO2 were separately treated with 10 μL of a mixed solution of 2 μM QDs and 1 μM anti-CEA8. The freshly synthesized anti-CEA8 conjugated composites were immediately added to cell culture solutions for incubation.

2.4 Incubating cells with nanoparticles

Cervical cancer HeLa cells were cultured with DMEM supplemented with 10% fetal bovine serum in a humidified incubator at 37°Cunder 5% CO2. After two days of cell differentiation and proliferation, 50 μL sample-solutions with a particular QD-concentration (20 nM) were introduced into the cells. The endocytic process was performed for two hours. After the nanoparticles had been incubated, the cells on cover slips were rinsed several times using PBS buffer (pH 7.4) and then fixed with DMEM again to be directly observed under a microscope.

2.5 Optical experiments

All samples that were used in the optical experiments were prepared by dispersing 10 μL drops of different sample-solutions and the same concentration of QDs (20 nM) onto clean glass object slides with standard cover-slips. The FLIM system comprises a titanium-sapphire laser (Mira 900, Coherent), a diode laser (LDH-P-C-470, Picoquant), an avalanche photodiode (APD) detector, a scanning confocal microscope (FV-300, Olympus), a spectrometer, and a PC-based time correlated single-photon counting (TCSPC) system (shown in Fig. 1 ). In the single-photon experiments, a diode laser with a wavelength of 470 nm was turned on with an excitation power of 5-500 μW and 480 nm long-pass filters were placed before the detector and the spectrometer. In the two-photon experiments, an fs laser with a wavelength of 750 nm was turned on with a pulse frequency of 76 MHz and a pulse duration of 120 fs. The power used for the two-photon excitation was 10 mW in the experiments without cells, 4 mW in the cell imaging experiments and 6 mW in cell photo-thermal therapy. 680 nm short-pass filters were placed before the detector and the spectrometer; a 600 nm bandpass filter with a bandwidth of 40 nm was introduced before the short-pass filter to eliminate auto-fluorescence in the cell experiments. A 60 × /1.42 oil objective was used in the experiments without cells, whereas both the 20 × /0.4 and the 60 × /1.42 oil objectives were used in the cell experiments.The spectrum and lifetime of fluorescence were measured using the spectrometer and an APD detector, respectively, for each scanning pixel. Lifetime was analyzed using software (SymphoTime, PicoQuant Inc.) based on the measurements of photon count rate and the arrival times made using the APD detector and TCSPC system. The time-resolved fluorescence decay curves were fitted single exponential decay curves and used to calculate the lifetime in single-sample experiments. Double exponential decay curve were fitted to the results of QD-GNR-composites experiments. All measurements were made several times to yield average data. The dark field images were obtained using a phase contrast condenser with a numerical aperture between 0.9 and 1.2 by collecting the strongly scattered light.

 

Fig. 1 Schematic diagram of the FLIM system

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2.6 Characterization

A Shimadzu 2550 UV-vis scanning spectrophotometer was used to measure the extinction spectra of GNRs and GNR_SiO2 within 450 nm-800 nm wavelength region. A JEOL JEM-1200EX transmission electron microscope was used to record TEM imaging for the structures of the nanoparticles.

3. Results and discussion

Figure 2(a) shows the three LSPR spectral bands of synthesized GNRs as solid curves, with peaks at 600 nm, 650 nm and 730 nm. The thickness of silica coating on GNRs was controlled using various concentrations of TEOS [38,43]. Two coatings, with thicknesses of 8 nm and 13 nm, were synthesized on the surface of GNRs [TEM images in Figs. 2(c), 2(d)]. Coating with silica red-shifted the LSPR peak of GNRs_SiO2 from that of the uncoated GNR, by increasing the local refractive index on GNRs. The dashed curves in Fig. 2(a) show a red-shift in the LSPR spectra of about 15-20 nm, corresponding to a coating thickness of 13 nm, for the three GNRs of different aspect ratios [38]. Carboxyl-functionalized CdSe QDs with an emission peak at 605 nm [dotted curve in Fig. 2(a)] were conjugated on the surface of the GNRs and GNRs_SiO2 in coatings of two thicknesses (8 and 13 nm) via the electrostatic interaction. Considering the thickness of carboxyl on QD and CTAB on GNR, the separation between QD and GNR was estimated approximately 3 nm [32]. From the TEM images in Figs. 2(f) and 2(g), the separations between QD and GNRs of various silica-coating-thicknesses are approximately 10 nm and 15 nm, respectively.

 

Fig. 2 (a) UV-visible absorbance spectra of GNRs with LSPR peaks at 600, 650 and 730 nm are shown as solid curves. UV-visible absorbance spectra of GNRs that were coated with 13 nm-thick silica with LSPR peaks at 615 nm, 665 nm, and 750 nm are shown as dashed curves. The emission spectrum of QDs with the peak at 605 nm is shown as a dotted curve. (b)-(d) TEM images of 650 nm-GNRs, 650 nm-GNRs coated with 8 nm silica and 13 nm silica. (e)-(g) TEM images of QDs conjugated with 650 nm-GNRs, 650 nm-GNRs coated with 8 nm silica and 13 nm silica.

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Table 1 presents the measured intensity and lifetime of QD-emission with various thicknesses of coating on the GNRs with LSPR peaks at 650 nm. As demonstrated in a previous work [32], SET quenching dominates the metal modification process when the separation is less than 10 nm. Therefore, a silica coating of thickness 10 nm was considered first. According to the table, the lifetime of QD-emission is reduced as the separation of the two particles is shortened. The detected fluorescence lifetime τ is determined by the radiative and nonradiative decay rate, τ = 1/(Rrad + Rnonrad). The reduction in lifetime results from the increase both in the radiative and the nonradiative decay rates. To differentiate the two different contributions, a method proposed by Wenger et al. [44] is used. In this method, the reduction factor of radiative rate is deduced from the factor of fluorescence enhancement when the the excitation intensity is much larger than the saturation intensity. By increasing the excitation power, different fluorescence intensities and fluorescence enhancement factors are obtained. The fluorescence enhancement factor at saturation of each sample is then calculated through numerical fits [44], and is equal to the reduction factor of radiative decay rate, as listed in Table 1. Note that, GNRs affect light collection efficiencies of the samples, and contribute to the overall fluorescence enhancement. It is difficult to measure the values of the collection efficiencies with high accuracy. Since the high NA objective lens is used here, the collection efficiencies are believed to be the same as those for the samples without GNRs [45]. The radiative decay rate is decreased while the nonradiative decay rate is increased when the distance between two particles shortens. Both rate changes affect negatively to the fluorescence enhancement. Increasing the coating thickness on GNRs would, however, reduce the changes in both the radiative and the nonradiative decay rates, and therefore the change in lifetime. When the separation is around 10 nm, the intensity of QD-emission is slightly quenched, suggesting that the negative effects due to the increase in nonradiative decay rate and the decrease in radiative decay rate are overriding the enhancement in excitation intensity, which comes from the LSPR-enhanced electromagnetic field at the presence of GNRs. A fluorescence enhancement factor of approximately 1.55 was obtained from the QDs that were combined with 15 nm-thick silica-coated GNRs. In this case, the fluorescence lifetime and the radiative decay rate are almost the same as its original value, indicating that the changes in decay rate are negligible and that the enhancement is caused by the excitation enhancement. This effect is also known as optical antenna absorption [46].

Tables Icon

Table 1. Fluorescence intensities, lifetimes and enhancement factors of radiative decay rate of QDs at different separations from GNRs and without GNRs.

Although the excitation wavelength (470 nm) does not match the LSPR peak of 650-GNR, lower enhancement of excitation intensity is still found because GNR also has a weak SP extinction at the off-resonance wavelength- 470 nm as shown in Fig. 2(a). Increasing the coating thickness does not affect the fluorescence lifetime but does reduce the excitation enhancement. Herein, the maximum enhancement is achieved when the separation is around 15 nm or a little less. At this distance, the radiative and nonradiative decay rates are minimally changed from their original values. The excitation enhancement caused by the optical antenna- GNRs dominates the enhancement of fluorescence of adjacent QDs.

Next, the spectral correlation among GNR-LSPR, QD-emission, and excitation wavelength is further investigated to elucidate the enhancement effect. Since the resonance between the emission transition and the surface plasmon oscillation is essential to emission modification, the overlap of the spectra between GNR-LSPR and QD-emission is required to modify the emission decay rate and, consequently, the SET quenching effect. As shown in Fig. 3(a) , the intensity of QD-emission from QD-GNR composites is most quenched when the GNR-LSPR and QD-emission spectra are matched. Better overlapping of the LSPR and emission spectra results in greater quenching, which is consistent with the conclusions of our previous work [32]. Figure 3(b) plots the fluorescence lifetimes of QDs when combined with the GNRs with three LSPR peaks. QD-emission with greater quenching (when LSPR and emission spectra are better matched) exhibits a shorter lifetime, because the nonradiative decay rate is higher. For QD-GNR_SiO2 composites, as shown in Fig. 3(b), the fluorescence lifetimes of QDs with different GNRs are almost equal to the original lifetime of QD-emission without GNRs. Increasing the overlapping of LSPR and emission spectra only minimally reduces the lifetime. This phenomenon is attributable to the increase in nonradiative decay rate, just like the change in the lifetime of QDs with uncoated GNRs. However, the emission intensities of QDs are not quenched but enhanced, because the increasing of nonradiative decay rate is weakened and the excitation intensity is still enhanced. As shown in Fig. 3(b), the enhancement factors are approximately the same for the three QD-GNR composites with different LSPR peaks. The three LSPR spectra do not differ at 470 nm (as no matched resonance peaks are present around the excitation wavelength from any of the three GNRs), so just low intensity enhancement factors are obtained.

 

Fig. 3 (a) Fluorescence lifetimes of QDs conjugated with 600, 650, and 730 nm-GNRs (square) and GNR_SiO2 (triangle), with corresponding LSPR peaks at 615, 665 and 750 nm under single-photon excitation at 470nm. (b) Ratios of fluorescence intensities (I) of QDs conjugated with GNRs (solid) and GNR_SiO2 (shadow) with corresponding LSPR peaks to original intensity (I0) of QDs without GNRs-conjugation under single-photon excitation at 470 nm.

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Two-photon excitation at a wavelength of 750 nm was adopted to examine further the mechanism of excitation enhancement. Prominent emission from GNRs with a spectral range of about 400 nm to 600 nm was also observed under two-photon excitation, which complicated the study of QD-enhancement. Such emission has a very short lifetime, which cannot be easily differentiated from the system impulse response function (IRF, less than 0.2 ns) [Fig. 4(A) ]. The QD-emission from QD-GNR composites can hardly be seen [Fig. 4(B)]. This means the fluorescence of QDs is also quenched under two-photon excitation. The FRET-like quenching effect, which is induced by the modification of the decay rate, occurs in the emission process and is independent of the type of excitation. Additionally, the emission from GNRs is a completely different process, which can only be excited by multi-photon absorption and therefore may not be influenced by the energy transfer from QDs to GNRs. The possible FRET from GNRs to QDs is also taken into account. However, no appreciable change (either in intensity or lifetime) was observed in the GNR-emission from QD-GNR composites by comparison with GNRs alone (data not shown). The fast decay rate of GNR-emission differs markedly from the slow FRET decay rate [47]. Apparently, the FRET (from GNRs to QDs is negligible. The modification of emission of QDs by GNRs and the self-emission of GNRs can be regarded as two unrelated processes in this experiment. The decay curve of QD-GNR emission comprises two distinct parts -fast decay associated with GNR-emission and slow decay (the tail in the decay curve) associated with QD-emission [Fig. 4(A)]. The fitted curve for QDs (fitting curve in the tail part) in QD-GNR composites [inset in Fig. 4(A)] reveals faster decay and a shorter lifetime than the emission decay curve of QDs without GNRs shows. The results are consistent with the measurements under one-photon excitation, in which the increase in nonradiative decay rate shortens the fluorescence lifetime. For QD-GNR_SiO2 composites, the fitting curve for QDs (the tail part) is similar to that for the QDs without GNRs [inset in Fig. 4(A)]. Hence the changes in lifetime of QD-emission from QD-GNR_SiO2 are too small to influence the emission intensity. Fluorescence enhancements are made in all three QD-GNRs_SiO2 composites. 615 nm-GNR_SiO2 and 665 nm-GNR_SiO2 conjugated QDs exhibit the same fluorescence enhancement (data not shown). From Fig. 4(B), the 750 nm- GNR_SiO2 greatly increases QD-emission, such that the intensity of the highest emission peak at 605 nm is several times of the intensity of emission from QDs with unconjugated GNRs. This remarkable increase in excitation is attributed to the matching resonance of the excitation wavelength with the LSPR peak at 750 nm. A higher GNR-emission intensity is also observed when the GNR-LSPR is matched with the excitation peak [48].

 

Fig. 4 (A) Normalized fluorescence decay curves of QDs, 650 nm-GNRs, QDs-650 nm-GNRs and QDs-665 nm-GNR_SiO2 under two-photon excitation at 750 nm; inset shows magnified fitting decay curves. (B) Emission spectra of QD-650 nm-GNRs, 650 nm-GNRs to which are added QD-emission spectra, QD-665 nm-GNR_SiO2, and QD-750 nm-GNR_SiO2 (from a to d) under two-photon excitation at 750 nm.

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The intensity and lifetime measurements of the fluorescence from QDs that are combined with GNRs and GNRs_SiO2 with different LSPR peaks demonstrated that excitation enhancement dominates the increase in emission, and the passive quenching modifies the decay rate when separation between QDs and GNRs is small. The enhancement factor is maximal when the separation is around 15 nm, at which the change in the lifetime of QD-emission is very small. These findings demonstrate that reducing modifications in the decay rate is critical to maximizing the enhancement. This fact may be attributable to the fact that the absorption dominates in GNR-LSPR extinction (just with a smaller scattering cross section) [49], increasing the nonradiative decay rate, such that it dominates the overall change in the decay rate, even when the change is reduced by increasing the separation. GNRs therefore do not help to promote the emission of adjacent fluorophores by modifying their decay rates, as determined comparison with other metallic nanostructures such as nanoshells [7]. However, the magnified local electromagnetic field close to the GNRs causes the increase in excitation intensity to dominate the fluorescence enhancement when the excitation wavelength is matched with the LSPR spectrum. Accordingly, in the QD-GNR_SiO2 composites, the fluorescence of QDs is strongly enhanced by the excitation enhancement. These QD-GNR_SiO2 composites with enhanced QD-emission are applied for bio-imaging.

As Scheme 1 shows, GNRs and GNRs_SiO2 are conjugated with both QDs and anti-CEA8 via electrostatic interaction. HeLa cells with over-expressed CEA8 can take up these composites efficiently. Figure 5 displays FLIM images of HeLa cells that have been treated with these composites. A control experiment using QDs mixed with anti-CEA8 is performed, as shown in Figs. 5(a), 5(b) and 5(c). The carboxyl group on the QDs prevents the negatively charged anti-CEA8 from being conjugated with the QDs. QDs cannot label the HeLa cells without efficient uptake, and so no fluorescence is observed upon one- or two-photon excitation when only QDs are mixed with the antibody. The advantages of surface functionalization make GNRs and GNRs_SiO2 convenient vehicles for bio-applications, including cell uptake, for delivering small molecules [50] and particles. Conjugated with GNRs and GNRs_SiO2, QD-composites are efficiently functionalized with anti-CEA8 and can be easily taken up by cancer cells. For QD-GNR composites, GNRs quench the fluorescence of QDs. Therefore, Figs. 5(e) and 5(f) present only weak fluorescence with a long lifetime (red signal in the figure). Figure 5(f) displays two-photon emission of the GNRs, which is indicated on the cells. Figure 5(h) displays enhanced fluorescence of QDs in QD-GNR_SiO2 composites under one-photon excitation; Fig. 5(i) displays enhanced fluorescence under two-photon excitation. Two-photon emission of GNRs_SiO2, with a green color and short lifetime, is also observed in Fig. 5(i) at the same positions as the QD-emission. This finding demonstrates that the QD-GNR_SiO2 emits both GNR-emission and QD-emission under two-photon excitation. GNR_SiO2 drives the QDs onto cells and enhances QD-emission under both one- and two-photon excitation; it can also scatter light as revealed by dark-field imaging and exploitable in photo-thermal therapy in bio- applications.

 

Scheme 1 GNR, silica coated on GNR using TEOS, and both GNR and GNR_SiO2 conjugated with QDs and anti-CEAcam8.

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Fig. 5 Images made by transmitted light (left), one-photon (middle) and two-photon FLIM images (right) of HeLa cells treated with (a)-(c) QDs and anti-CEA8, (d)-(f) QD-750 nm-GNR composites functionalized with anti-CEA8, (g)-(i) QD-GNR_SiO2 composites functionalized with anti-CEA8. Color bar shows different colors, used in the images to represent varying fluorescence lifetime.

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Figure 6(a) shows the dark-field image of HeLa cells that were treated with QD-GNR_SiO2. Red spots of light scattered by GNRs_SiO2 in the cells (which themselves scatter white-blue light) are seen. Figure 6(b) shows the fluorescence image in the same field as Fig. 6(a) shows. QD-emission is enhanced where the scattering signals of GNRs_SiO2 are observed. This spatial matching indicates that both red light scattering and fluorescence arise from QD-GNR_SiO2 in the cells. A control experiment using QD-GNR composites is carried out. Dark-field imaging of the QD-GNR in the cells is the same performance as that of QD-GNR_SiO2 [Fig. 6(c)], because the scattering properties of GNRs and GNRs_SiO2 are very similar. However, for QD-GNR, QD-emission is not enhanced but quenched, so the fluorescence image in Fig. 6(d) shows hardly any emission. Photo-thermal therapy is another bio-application of QD-GNR_SiO2. GNRs generate a very large amount of localized heat to kill tumor cells as they absorb strongly when they are excited at the wavelength of the LSPR peak. The results of thermal treatment with rods will be shown elsewhere. Besides its usefulness in diagnosing cancer using various imaging methods, QD-GNR_SiO2 has promising clinical treatment applications.

 

Fig. 6 Dark-field images (left) and one-photon fluorescence images (right) of HeLa cells treated with (a),(b) QD-GNR_SiO2 composites and (c),(d) QD-GNR composites that had been functionalized with anti-CEA8.

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4. Conclusions

In conclusion, this work demonstrates the enhancement of fluorescence from QDs by adjacent GNRs. The strong absorption of GNRs is such that the modification of decay rate by GNRs to dominate the quenching of QD-emission. Excitation intensity is increased near the GNRs by the optical antenna effect because of the presence of a magnified local electromagnetic field. QD-emission is maximally enhanced when the QD-GNR separation is around 15 nm, balancing the reduction in the quenching effect with the excitation enhancement, and when the excitation wavelength is matched with the GNR-LSPR (maximizing the excitation enhancement). The QD-GNR_SiO2 composites exhibit enhanced QD-emission under both one- and two-photon excitation. This composite promotes surface functionalization and is useful in the diagnosis of cancer cells by a wide range of imaging methods. Photo-thermal therapy is another important bio-application of this multifunctional hybrid composite.

Acknowledgments

The authors would like to thank the Swedish Foundation for Strategic Research (SSF), the National Science Council of the Republic of China, Taiwan (NSC 97-3112-B-010-006, NSC 96-2112-M-010-001, and NSC98-2112-M-010-001-MY3), as well as the Ministry of Education of the Republic of China, Taiwan under the “Aim for Top University“ project, and Dr. Vladimir Ghukasyan for assisting in preparation of the cell culture. Ted Knoy is appreciated for his editorial assistance.

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8. Y. P. Hsieh, C. T. Liang, Y. F. Chen, C. W. Lai, and P. T. Chou, “Mechanism of giant enhancement of light emission from Au/CdSe nanocomposites,” Nanotechnology 18(41), 415707 (2007). [CrossRef]  

9. Y. S. Chi, H. R. Byon, B. S. Lee, B. Kong, H. C. Choi, and I. S. Choi, “Polymeric Rulers: Distance-Dependent Emission Behaviors of Fluorophores on Flat Gold Surfaces and Bioassay Platforms Using Plasmonic Fluorescence Enhancement,” Adv. Funct. Mater. 18(21), 3395–3402 (2008). [CrossRef]  

10. O. Kulakovich, N. Strekal, A. Yaroshevich, S. Maskevich, S. Gaponenko, I. Nabiev, U. Woggon, and M. Artemyev, “Enhanced luminescence of CdSe quantum dots on gold colloids,” Nano Lett. 2(12), 1449–1452 (2002). [CrossRef]  

11. P. Anger, P. Bharadwaj, and L. Novotny, “Enhancement and quenching of single-molecule fluorescence,” Phys. Rev. Lett. 96(11), 113002 (2006). [CrossRef]   [PubMed]  

12. P. Bharadwaj and L. Novotny, “Spectral dependence of single molecule fluorescence enhancement,” Opt. Express 15(21), 14266–14274 (2007). [CrossRef]   [PubMed]  

13. J. Zhang and J. R. Lakowicz, “Metal-enhanced fluorescence of an organic fluorophore using gold particles,” Opt. Express 15(5), 2598–2606 (2007). [CrossRef]   [PubMed]  

14. J. C. Ostrowski, A. Mikhailovsky, D. A. Bussian, M. A. Summers, S. K. Buratto, and G. C. Bazan, “Enhancement of phosphorescence by surface-plasmon resonances in colloidal metal nanoparticles: The role of aggregates,” Adv. Funct. Mater. 16(9), 1221–1227 (2006). [CrossRef]  

15. F. Tam, G. P. Goodrich, B. R. Johnson, and N. J. Halas, “Plasmonic enhancement of molecular fluorescence,” Nano Lett. 7(2), 496–501 (2007). [CrossRef]   [PubMed]  

16. S. Kühn, U. Håkanson, L. Rogobete, and V. Sandoghdar, “Enhancement of single-molecule fluorescence using a gold nanoparticle as an optical nanoantenna,” Phys. Rev. Lett. 97(1), 017402 (2006). [CrossRef]   [PubMed]  

17. M. Thomas, J. J. Greffet, R. Carminati, and J. R. Arias-Gonzalez, “Single-molecule spontaneous emission close to absorbing nanostructures,” Appl. Phys. Lett. 85(17), 3863 (2004). [CrossRef]  

18. V. K. Komarala, Y. P. Rakovich, A. L. Bradley, S. J. Byrne, Y. K. Gun’ko, N. Gaponik, and A. Eychmüller, “Off-resonance surface plasmon enhanced spontaneous emission from CdTe quantum dots,” Appl. Phys. Lett. 89(25), 253118 (2006). [CrossRef]  

19. H. C. Van de Hulst, “Light scattering by small particles,” Wiley-Interscience, New York (1957).

20. S. Link, M. B. Mohamed, and M. A. El-Sayed, “Simulation of the optical absorption spectra of gold nanorods as a function of their aspect ratio and the effect of the medium dielectric constant,” J. Phys. Chem. B 103(16), 3073–3077 (1999). [CrossRef]  

21. B. Nikoobakht and M. A. El-Sayed, “Surface-enhanced Raman scattering studies on aggregated gold nanorods,” J. Phys. Chem. A 107(18), 3372–3378 (2003). [CrossRef]  

22. X. Li, J. Qian, and S. He, “Impact of the self-assembly of multilayer polyelectrolyte functionalized gold nanorods and its application to biosensing,” Nanotechnology 19(35), 355501 (2008). [CrossRef]   [PubMed]  

23. R. S. Norman, J. W. Stone, A. Gole, C. J. Murphy, and T. L. Sabo-Attwood, “Targeted photothermal lysis of the pathogenic bacteria, Pseudomonas aeruginosa, with gold nanorods,” Nano Lett. 8(1), 302–306 (2008). [CrossRef]  

24. X. Huang, I. H. El-Sayed, W. Qian, and M. A. El-Sayed, “Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods,” J. Am. Chem. Soc. 128(6), 2115–2120 (2006). [CrossRef]   [PubMed]  

25. N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007). [CrossRef]   [PubMed]  

26. X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008). [CrossRef]   [PubMed]  

27. P. Zijlstra, J. W. M. Chon, and M. Gu, “Five-dimensional optical recording mediated by surface plasmons in gold nanorods,” Nature 459(7245), 410–413 (2009). [CrossRef]   [PubMed]  

28. Y. Chen, K. Munechika, and D. S. Ginger, “Dependence of fluorescence intensity on the spectral overlap between fluorophores and plasmon resonant single silver nanoparticles,” Nano Lett. 7(3), 690–696 (2007). [CrossRef]   [PubMed]  

29. Y. Chen, K. Munechika, I. Jen-La Plante, A. M. Munro, S. E. Skrabalak, Y. Xia, and D. S. Ginger, “Excitation enhancement of CdSe quantum dots by single metal nanoparticles,” Appl. Phys. Lett. 93(5), 053106 (2008). [CrossRef]  

30. E. Dulkeith, A. C. Morteani, T. Niedereichholz, T. A. Klar, J. Feldmann, S. A. Levi, F. C. J. M. van Veggel, D. N. Reinhoudt, M. Möller, and D. I. Gittins, “Fluorescence quenching of dye molecules near gold nanoparticles: radiative and nonradiative effects,” Phys. Rev. Lett. 89(20), 203002 (2002). [CrossRef]   [PubMed]  

31. T. Soller, M. Ringler, M. Wunderlich, T. A. Klar, J. Feldmann, H. P. Josel, Y. Markert, A. Nichtl, and K. Kürzinger, “Radiative and nonradiative rates of phosphors attached to gold nanoparticles,” Nano Lett. 7(7), 1941–1946 (2007). [CrossRef]  

32. X. Li, J. Qian, L. Jiang, and S. He, “Fluorescence quenching of quantum dots by gold nanorods and its application to DNA detection,” Appl. Phys. Lett. 94(6), 063111 (2009). [CrossRef]  

33. C. S. Yun, A. Javier, T. Jennings, M. Fisher, S. Hira, S. Peterson, B. Hopkins, N. O. Reich, and G. F. Strouse, “Nanometal surface energy transfer in optical rulers, breaking the FRET barrier,” J. Am. Chem. Soc. 127(9), 3115–3119 (2005). [CrossRef]   [PubMed]  

34. J. Lee, A. O. Govorov, J. Dulka, and N. A. Kotov, “Bioconjugates of CdTe nanowires and Au nanoparticles: Plasmon-excition interactions, luminescence enhancement, and collective effects,” Nano Lett. 4(12), 2323–2330 (2004). [CrossRef]  

35. A. O. Govorov, J. Lee, and N. A. Kotov, “Theory of plasmon-enhanced Forster energy transfer in optically excited semiconductor and metal nanoparitcles,” Phys. Rev. B 76(12), 125308 (2007). [CrossRef]  

36. G. L. Liu, Y. T. Long, Y. Choi, T. Kang, and L. P. Lee, “Quantized plasmon quenching dips nanospectroscopy via plasmon resonance energy transfer,” Nat. Methods 4(12), 1015–1017 (2007). [CrossRef]   [PubMed]  

37. P. Viste, J. Plain, R. Jaffiol, A. Vial, P. M. Adam, and P. Royer, “Enhancement and quenching regimes in metal-semiconductor hybrid optical nanosources,” ACS Nano 4(2), 759–764 (2010). [CrossRef]   [PubMed]  

38. Q. Q. Zhan, J. Qian, X. Li, and S. He, “A study of mesoporous silica-encapsulated gold nanorods as enhanced light scattering probes for cancer cell imaging,” Nanotechnology 21(5), 055704 (2010). [CrossRef]  

39. V. Ghukasyan, Y. Y. Hsu, S. H. Kung, and F. J. Kao, “Application of fluorescence resonance energy transfer resolved by fluorescence lifetime imaging microscopy for the detection of enterovirus 71 infection in cells,” J. Biomed. Opt. 12(2), 024016 (2007). [CrossRef]   [PubMed]  

40. V. Ghukasyan and F. J. Kao, “Monitoring Cellular Metabolism with Fluorescence Lifetime of Reduced Nicotinamide Adenine Dinucleotide,” J. Phys. Chem. C 113(27), 11532–11540 (2009). [CrossRef]  

41. R. Hu, K. T. Yong, I. Roy, H. Ding, S. He, and P. N. Prasad, “Metallic Nanostructures as Localized Plasmon Resonance Enhanced Scattering Probes for Multiplex Dark-Field Targeted Imaging of Cancer Cells,” J. Phys. Chem. C 113(7), 2676–2684 (2009). [CrossRef]  

42. B. Nikoobakht, J. Wang, and M. A. El-Sayed, “Surface-enhanced Raman scattering of molecules adsorbed on gold nanorods: off-surface plasmon resonance condition,” Chem. Phys. Lett. 366(1-2), 17–23 (2002). [CrossRef]  

43. C. Wang, Z. Ma, T. Wang, and Z. Su, “Synthesis, assembly, and biofunctionalization of silica-coated gold nanorods for colorimetric biosensing,” Adv. Funct. Mater. 16(13), 1673–1678 (2006). [CrossRef]  

44. J. Wenger, D. Gérard, J. Dintinger, O. Mahboub, N. Bonod, E. Popov, T. W. Ebbesen, and H. Rigneault, “Emission and excitation contributions to enhanced single molecule fluorescence by gold nanometric apertures,” Opt. Express 16(5), 3008–3020 (2008). [CrossRef]   [PubMed]  

45. T. H. Taminiau, F. D. Stefani, and N. F. van Hulst, “Single emitters coupled to plasmonic nano-antennas: angular emission and collection efficiency,” N. J. Phys. 10(10), 105005 (2008). [CrossRef]  

46. S. He, Y. Cui, Y. Ye, P. Zhang, and Y. Jin, “Optical nano-antennas and metamaterials,” Mater. Today 12(12), 16–24 (2009). [CrossRef]  

47. A. R. Clapp, I. L. Medintz, B. R. Fisher, G. P. Anderson, and H. Mattoussi, “Can luminescent quantum dots be efficient energy acceptors with organic dye donors?” J. Am. Chem. Soc. 127(4), 1242–1250 (2005). [CrossRef]   [PubMed]  

48. O. P. Varnavski, M. B. Mohamed, M. A. El-Sayed, and T. Goodson, “Relative enhancement of ultrafast emission in gold nanorods,” J. Phys. Chem. B 107(14), 3101–3104 (2003). [CrossRef]  

49. P. K. Jain, K. S. Lee, I. H. El-Sayed, and M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006). [CrossRef]   [PubMed]  

50. C. C. Chen, Y. P. Lin, C. W. Wang, H. C. Tzeng, C. H. Wu, Y. C. Chen, C. P. Chen, L. C. Chen, and Y. C. Wu, “DNA-gold nanorod conjugates for remote control of localized gene expression by near infrared irradiation,” J. Am. Chem. Soc. 128(11), 3709–3715 (2006). [CrossRef]   [PubMed]  

References

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  7. R. Bardhan, N. K. Grady, J. R. Cole, A. Joshi, and N. J. Halas, “Fluorescence enhancement by Au nanostructures: nanoshells and nanorods,” ACS Nano 3(3), 744–752 (2009).
    [CrossRef] [PubMed]
  8. Y. P. Hsieh, C. T. Liang, Y. F. Chen, C. W. Lai, and P. T. Chou, “Mechanism of giant enhancement of light emission from Au/CdSe nanocomposites,” Nanotechnology 18(41), 415707 (2007).
    [CrossRef]
  9. Y. S. Chi, H. R. Byon, B. S. Lee, B. Kong, H. C. Choi, and I. S. Choi, “Polymeric Rulers: Distance-Dependent Emission Behaviors of Fluorophores on Flat Gold Surfaces and Bioassay Platforms Using Plasmonic Fluorescence Enhancement,” Adv. Funct. Mater. 18(21), 3395–3402 (2008).
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  10. O. Kulakovich, N. Strekal, A. Yaroshevich, S. Maskevich, S. Gaponenko, I. Nabiev, U. Woggon, and M. Artemyev, “Enhanced luminescence of CdSe quantum dots on gold colloids,” Nano Lett. 2(12), 1449–1452 (2002).
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    [CrossRef] [PubMed]
  13. J. Zhang and J. R. Lakowicz, “Metal-enhanced fluorescence of an organic fluorophore using gold particles,” Opt. Express 15(5), 2598–2606 (2007).
    [CrossRef] [PubMed]
  14. J. C. Ostrowski, A. Mikhailovsky, D. A. Bussian, M. A. Summers, S. K. Buratto, and G. C. Bazan, “Enhancement of phosphorescence by surface-plasmon resonances in colloidal metal nanoparticles: The role of aggregates,” Adv. Funct. Mater. 16(9), 1221–1227 (2006).
    [CrossRef]
  15. F. Tam, G. P. Goodrich, B. R. Johnson, and N. J. Halas, “Plasmonic enhancement of molecular fluorescence,” Nano Lett. 7(2), 496–501 (2007).
    [CrossRef] [PubMed]
  16. S. Kühn, U. Håkanson, L. Rogobete, and V. Sandoghdar, “Enhancement of single-molecule fluorescence using a gold nanoparticle as an optical nanoantenna,” Phys. Rev. Lett. 97(1), 017402 (2006).
    [CrossRef] [PubMed]
  17. M. Thomas, J. J. Greffet, R. Carminati, and J. R. Arias-Gonzalez, “Single-molecule spontaneous emission close to absorbing nanostructures,” Appl. Phys. Lett. 85(17), 3863 (2004).
    [CrossRef]
  18. V. K. Komarala, Y. P. Rakovich, A. L. Bradley, S. J. Byrne, Y. K. Gun’ko, N. Gaponik, and A. Eychmüller, “Off-resonance surface plasmon enhanced spontaneous emission from CdTe quantum dots,” Appl. Phys. Lett. 89(25), 253118 (2006).
    [CrossRef]
  19. H. C. Van de Hulst, Light scattering by small particles, (Wiley-Interscience, New York, 1957).
  20. S. Link, M. B. Mohamed, and M. A. El-Sayed, “Simulation of the optical absorption spectra of gold nanorods as a function of their aspect ratio and the effect of the medium dielectric constant,” J. Phys. Chem. B 103(16), 3073–3077 (1999).
    [CrossRef]
  21. B. Nikoobakht and M. A. El-Sayed, “Surface-enhanced Raman scattering studies on aggregated gold nanorods,” J. Phys. Chem. A 107(18), 3372–3378 (2003).
    [CrossRef]
  22. X. Li, J. Qian, and S. He, “Impact of the self-assembly of multilayer polyelectrolyte functionalized gold nanorods and its application to biosensing,” Nanotechnology 19(35), 355501 (2008).
    [CrossRef] [PubMed]
  23. R. S. Norman, J. W. Stone, A. Gole, C. J. Murphy, and T. L. Sabo-Attwood, “Targeted photothermal lysis of the pathogenic bacteria, Pseudomonas aeruginosa, with gold nanorods,” Nano Lett. 8(1), 302–306 (2008).
    [CrossRef]
  24. X. Huang, I. H. El-Sayed, W. Qian, and M. A. El-Sayed, “Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods,” J. Am. Chem. Soc. 128(6), 2115–2120 (2006).
    [CrossRef] [PubMed]
  25. N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007).
    [CrossRef] [PubMed]
  26. X. Qu, J. Wang, Z. Zhang, N. Koop, R. Rahmanzadeh, and G. Hüttmann, “Imaging of cancer cells by multiphoton microscopy using gold nanoparticles and fluorescent dyes,” J. Biomed. Opt. 13(3), 031217 (2008).
    [CrossRef] [PubMed]
  27. P. Zijlstra, J. W. M. Chon, and M. Gu, “Five-dimensional optical recording mediated by surface plasmons in gold nanorods,” Nature 459(7245), 410–413 (2009).
    [CrossRef] [PubMed]
  28. Y. Chen, K. Munechika, and D. S. Ginger, “Dependence of fluorescence intensity on the spectral overlap between fluorophores and plasmon resonant single silver nanoparticles,” Nano Lett. 7(3), 690–696 (2007).
    [CrossRef] [PubMed]
  29. Y. Chen, K. Munechika, I. Jen-La Plante, A. M. Munro, S. E. Skrabalak, Y. Xia, and D. S. Ginger, “Excitation enhancement of CdSe quantum dots by single metal nanoparticles,” Appl. Phys. Lett. 93(5), 053106 (2008).
    [CrossRef]
  30. E. Dulkeith, A. C. Morteani, T. Niedereichholz, T. A. Klar, J. Feldmann, S. A. Levi, F. C. J. M. van Veggel, D. N. Reinhoudt, M. Möller, and D. I. Gittins, “Fluorescence quenching of dye molecules near gold nanoparticles: radiative and nonradiative effects,” Phys. Rev. Lett. 89(20), 203002 (2002).
    [CrossRef] [PubMed]
  31. T. Soller, M. Ringler, M. Wunderlich, T. A. Klar, J. Feldmann, H. P. Josel, Y. Markert, A. Nichtl, and K. Kürzinger, “Radiative and nonradiative rates of phosphors attached to gold nanoparticles,” Nano Lett. 7(7), 1941–1946 (2007).
    [CrossRef]
  32. X. Li, J. Qian, L. Jiang, and S. He, “Fluorescence quenching of quantum dots by gold nanorods and its application to DNA detection,” Appl. Phys. Lett. 94(6), 063111 (2009).
    [CrossRef]
  33. C. S. Yun, A. Javier, T. Jennings, M. Fisher, S. Hira, S. Peterson, B. Hopkins, N. O. Reich, and G. F. Strouse, “Nanometal surface energy transfer in optical rulers, breaking the FRET barrier,” J. Am. Chem. Soc. 127(9), 3115–3119 (2005).
    [CrossRef] [PubMed]
  34. J. Lee, A. O. Govorov, J. Dulka, and N. A. Kotov, “Bioconjugates of CdTe nanowires and Au nanoparticles: Plasmon-excition interactions, luminescence enhancement, and collective effects,” Nano Lett. 4(12), 2323–2330 (2004).
    [CrossRef]
  35. A. O. Govorov, J. Lee, and N. A. Kotov, “Theory of plasmon-enhanced Forster energy transfer in optically excited semiconductor and metal nanoparitcles,” Phys. Rev. B 76(12), 125308 (2007).
    [CrossRef]
  36. G. L. Liu, Y. T. Long, Y. Choi, T. Kang, and L. P. Lee, “Quantized plasmon quenching dips nanospectroscopy via plasmon resonance energy transfer,” Nat. Methods 4(12), 1015–1017 (2007).
    [CrossRef] [PubMed]
  37. P. Viste, J. Plain, R. Jaffiol, A. Vial, P. M. Adam, and P. Royer, “Enhancement and quenching regimes in metal-semiconductor hybrid optical nanosources,” ACS Nano 4(2), 759–764 (2010).
    [CrossRef] [PubMed]
  38. Q. Q. Zhan, J. Qian, X. Li, and S. He, “A study of mesoporous silica-encapsulated gold nanorods as enhanced light scattering probes for cancer cell imaging,” Nanotechnology 21(5), 055704 (2010).
    [CrossRef]
  39. V. Ghukasyan, Y. Y. Hsu, S. H. Kung, and F. J. Kao, “Application of fluorescence resonance energy transfer resolved by fluorescence lifetime imaging microscopy for the detection of enterovirus 71 infection in cells,” J. Biomed. Opt. 12(2), 024016 (2007).
    [CrossRef] [PubMed]
  40. V. Ghukasyan and F. J. Kao, “Monitoring Cellular Metabolism with Fluorescence Lifetime of Reduced Nicotinamide Adenine Dinucleotide,” J. Phys. Chem. C 113(27), 11532–11540 (2009).
    [CrossRef]
  41. R. Hu, K. T. Yong, I. Roy, H. Ding, S. He, and P. N. Prasad, “Metallic Nanostructures as Localized Plasmon Resonance Enhanced Scattering Probes for Multiplex Dark-Field Targeted Imaging of Cancer Cells,” J. Phys. Chem. C 113(7), 2676–2684 (2009).
    [CrossRef]
  42. B. Nikoobakht, J. Wang, and M. A. El-Sayed, “Surface-enhanced Raman scattering of molecules adsorbed on gold nanorods: off-surface plasmon resonance condition,” Chem. Phys. Lett. 366(1-2), 17–23 (2002).
    [CrossRef]
  43. C. Wang, Z. Ma, T. Wang, and Z. Su, “Synthesis, assembly, and biofunctionalization of silica-coated gold nanorods for colorimetric biosensing,” Adv. Funct. Mater. 16(13), 1673–1678 (2006).
    [CrossRef]
  44. J. Wenger, D. Gérard, J. Dintinger, O. Mahboub, N. Bonod, E. Popov, T. W. Ebbesen, and H. Rigneault, “Emission and excitation contributions to enhanced single molecule fluorescence by gold nanometric apertures,” Opt. Express 16(5), 3008–3020 (2008).
    [CrossRef] [PubMed]
  45. T. H. Taminiau, F. D. Stefani, and N. F. van Hulst, “Single emitters coupled to plasmonic nano-antennas: angular emission and collection efficiency,” N. J. Phys. 10(10), 105005 (2008).
    [CrossRef]
  46. S. He, Y. Cui, Y. Ye, P. Zhang, and Y. Jin, “Optical nano-antennas and metamaterials,” Mater. Today 12(12), 16–24 (2009).
    [CrossRef]
  47. A. R. Clapp, I. L. Medintz, B. R. Fisher, G. P. Anderson, and H. Mattoussi, “Can luminescent quantum dots be efficient energy acceptors with organic dye donors?” J. Am. Chem. Soc. 127(4), 1242–1250 (2005).
    [CrossRef] [PubMed]
  48. O. P. Varnavski, M. B. Mohamed, M. A. El-Sayed, and T. Goodson, “Relative enhancement of ultrafast emission in gold nanorods,” J. Phys. Chem. B 107(14), 3101–3104 (2003).
    [CrossRef]
  49. P. K. Jain, K. S. Lee, I. H. El-Sayed, and M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006).
    [CrossRef] [PubMed]
  50. C. C. Chen, Y. P. Lin, C. W. Wang, H. C. Tzeng, C. H. Wu, Y. C. Chen, C. P. Chen, L. C. Chen, and Y. C. Wu, “DNA-gold nanorod conjugates for remote control of localized gene expression by near infrared irradiation,” J. Am. Chem. Soc. 128(11), 3709–3715 (2006).
    [CrossRef] [PubMed]

2010

P. Viste, J. Plain, R. Jaffiol, A. Vial, P. M. Adam, and P. Royer, “Enhancement and quenching regimes in metal-semiconductor hybrid optical nanosources,” ACS Nano 4(2), 759–764 (2010).
[CrossRef] [PubMed]

Q. Q. Zhan, J. Qian, X. Li, and S. He, “A study of mesoporous silica-encapsulated gold nanorods as enhanced light scattering probes for cancer cell imaging,” Nanotechnology 21(5), 055704 (2010).
[CrossRef]

2009

V. Ghukasyan and F. J. Kao, “Monitoring Cellular Metabolism with Fluorescence Lifetime of Reduced Nicotinamide Adenine Dinucleotide,” J. Phys. Chem. C 113(27), 11532–11540 (2009).
[CrossRef]

R. Hu, K. T. Yong, I. Roy, H. Ding, S. He, and P. N. Prasad, “Metallic Nanostructures as Localized Plasmon Resonance Enhanced Scattering Probes for Multiplex Dark-Field Targeted Imaging of Cancer Cells,” J. Phys. Chem. C 113(7), 2676–2684 (2009).
[CrossRef]

R. Bardhan, N. K. Grady, J. R. Cole, A. Joshi, and N. J. Halas, “Fluorescence enhancement by Au nanostructures: nanoshells and nanorods,” ACS Nano 3(3), 744–752 (2009).
[CrossRef] [PubMed]

P. Zijlstra, J. W. M. Chon, and M. Gu, “Five-dimensional optical recording mediated by surface plasmons in gold nanorods,” Nature 459(7245), 410–413 (2009).
[CrossRef] [PubMed]

X. Li, J. Qian, L. Jiang, and S. He, “Fluorescence quenching of quantum dots by gold nanorods and its application to DNA detection,” Appl. Phys. Lett. 94(6), 063111 (2009).
[CrossRef]

S. He, Y. Cui, Y. Ye, P. Zhang, and Y. Jin, “Optical nano-antennas and metamaterials,” Mater. Today 12(12), 16–24 (2009).
[CrossRef]

2008

Y. S. Chi, H. R. Byon, B. S. Lee, B. Kong, H. C. Choi, and I. S. Choi, “Polymeric Rulers: Distance-Dependent Emission Behaviors of Fluorophores on Flat Gold Surfaces and Bioassay Platforms Using Plasmonic Fluorescence Enhancement,” Adv. Funct. Mater. 18(21), 3395–3402 (2008).
[CrossRef]

T. H. Taminiau, F. D. Stefani, and N. F. van Hulst, “Single emitters coupled to plasmonic nano-antennas: angular emission and collection efficiency,” N. J. Phys. 10(10), 105005 (2008).
[CrossRef]

J. Wenger, D. Gérard, J. Dintinger, O. Mahboub, N. Bonod, E. Popov, T. W. Ebbesen, and H. Rigneault, “Emission and excitation contributions to enhanced single molecule fluorescence by gold nanometric apertures,” Opt. Express 16(5), 3008–3020 (2008).
[CrossRef] [PubMed]

Y. Chen, K. Munechika, I. Jen-La Plante, A. M. Munro, S. E. Skrabalak, Y. Xia, and D. S. Ginger, “Excitation enhancement of CdSe quantum dots by single metal nanoparticles,” Appl. Phys. Lett. 93(5), 053106 (2008).
[CrossRef]

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2007

Y. P. Hsieh, C. T. Liang, Y. F. Chen, C. W. Lai, and P. T. Chou, “Mechanism of giant enhancement of light emission from Au/CdSe nanocomposites,” Nanotechnology 18(41), 415707 (2007).
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V. Ghukasyan, Y. Y. Hsu, S. H. Kung, and F. J. Kao, “Application of fluorescence resonance energy transfer resolved by fluorescence lifetime imaging microscopy for the detection of enterovirus 71 infection in cells,” J. Biomed. Opt. 12(2), 024016 (2007).
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A. O. Govorov, J. Lee, and N. A. Kotov, “Theory of plasmon-enhanced Forster energy transfer in optically excited semiconductor and metal nanoparitcles,” Phys. Rev. B 76(12), 125308 (2007).
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G. L. Liu, Y. T. Long, Y. Choi, T. Kang, and L. P. Lee, “Quantized plasmon quenching dips nanospectroscopy via plasmon resonance energy transfer,” Nat. Methods 4(12), 1015–1017 (2007).
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Y. Chen, K. Munechika, and D. S. Ginger, “Dependence of fluorescence intensity on the spectral overlap between fluorophores and plasmon resonant single silver nanoparticles,” Nano Lett. 7(3), 690–696 (2007).
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P. Bharadwaj and L. Novotny, “Spectral dependence of single molecule fluorescence enhancement,” Opt. Express 15(21), 14266–14274 (2007).
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2006

P. Anger, P. Bharadwaj, and L. Novotny, “Enhancement and quenching of single-molecule fluorescence,” Phys. Rev. Lett. 96(11), 113002 (2006).
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P. K. Jain, K. S. Lee, I. H. El-Sayed, and M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006).
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2005

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A. R. Clapp, I. L. Medintz, B. R. Fisher, G. P. Anderson, and H. Mattoussi, “Can luminescent quantum dots be efficient energy acceptors with organic dye donors?” J. Am. Chem. Soc. 127(4), 1242–1250 (2005).
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2004

J. Lee, A. O. Govorov, J. Dulka, and N. A. Kotov, “Bioconjugates of CdTe nanowires and Au nanoparticles: Plasmon-excition interactions, luminescence enhancement, and collective effects,” Nano Lett. 4(12), 2323–2330 (2004).
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M. Thomas, J. J. Greffet, R. Carminati, and J. R. Arias-Gonzalez, “Single-molecule spontaneous emission close to absorbing nanostructures,” Appl. Phys. Lett. 85(17), 3863 (2004).
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2003

B. Nikoobakht and M. A. El-Sayed, “Surface-enhanced Raman scattering studies on aggregated gold nanorods,” J. Phys. Chem. A 107(18), 3372–3378 (2003).
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O. P. Varnavski, M. B. Mohamed, M. A. El-Sayed, and T. Goodson, “Relative enhancement of ultrafast emission in gold nanorods,” J. Phys. Chem. B 107(14), 3101–3104 (2003).
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2002

O. Kulakovich, N. Strekal, A. Yaroshevich, S. Maskevich, S. Gaponenko, I. Nabiev, U. Woggon, and M. Artemyev, “Enhanced luminescence of CdSe quantum dots on gold colloids,” Nano Lett. 2(12), 1449–1452 (2002).
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B. Nikoobakht, J. Wang, and M. A. El-Sayed, “Surface-enhanced Raman scattering of molecules adsorbed on gold nanorods: off-surface plasmon resonance condition,” Chem. Phys. Lett. 366(1-2), 17–23 (2002).
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S. Link, M. B. Mohamed, and M. A. El-Sayed, “Simulation of the optical absorption spectra of gold nanorods as a function of their aspect ratio and the effect of the medium dielectric constant,” J. Phys. Chem. B 103(16), 3073–3077 (1999).
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1998

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A. R. Clapp, I. L. Medintz, B. R. Fisher, G. P. Anderson, and H. Mattoussi, “Can luminescent quantum dots be efficient energy acceptors with organic dye donors?” J. Am. Chem. Soc. 127(4), 1242–1250 (2005).
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P. Bharadwaj and L. Novotny, “Spectral dependence of single molecule fluorescence enhancement,” Opt. Express 15(21), 14266–14274 (2007).
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J. C. Ostrowski, A. Mikhailovsky, D. A. Bussian, M. A. Summers, S. K. Buratto, and G. C. Bazan, “Enhancement of phosphorescence by surface-plasmon resonances in colloidal metal nanoparticles: The role of aggregates,” Adv. Funct. Mater. 16(9), 1221–1227 (2006).
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Y. S. Chi, H. R. Byon, B. S. Lee, B. Kong, H. C. Choi, and I. S. Choi, “Polymeric Rulers: Distance-Dependent Emission Behaviors of Fluorophores on Flat Gold Surfaces and Bioassay Platforms Using Plasmonic Fluorescence Enhancement,” Adv. Funct. Mater. 18(21), 3395–3402 (2008).
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V. K. Komarala, Y. P. Rakovich, A. L. Bradley, S. J. Byrne, Y. K. Gun’ko, N. Gaponik, and A. Eychmüller, “Off-resonance surface plasmon enhanced spontaneous emission from CdTe quantum dots,” Appl. Phys. Lett. 89(25), 253118 (2006).
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M. Thomas, J. J. Greffet, R. Carminati, and J. R. Arias-Gonzalez, “Single-molecule spontaneous emission close to absorbing nanostructures,” Appl. Phys. Lett. 85(17), 3863 (2004).
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C. C. Chen, Y. P. Lin, C. W. Wang, H. C. Tzeng, C. H. Wu, Y. C. Chen, C. P. Chen, L. C. Chen, and Y. C. Wu, “DNA-gold nanorod conjugates for remote control of localized gene expression by near infrared irradiation,” J. Am. Chem. Soc. 128(11), 3709–3715 (2006).
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C. C. Chen, Y. P. Lin, C. W. Wang, H. C. Tzeng, C. H. Wu, Y. C. Chen, C. P. Chen, L. C. Chen, and Y. C. Wu, “DNA-gold nanorod conjugates for remote control of localized gene expression by near infrared irradiation,” J. Am. Chem. Soc. 128(11), 3709–3715 (2006).
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Chen, Y. F.

Y. P. Hsieh, C. T. Liang, Y. F. Chen, C. W. Lai, and P. T. Chou, “Mechanism of giant enhancement of light emission from Au/CdSe nanocomposites,” Nanotechnology 18(41), 415707 (2007).
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Y. S. Chi, H. R. Byon, B. S. Lee, B. Kong, H. C. Choi, and I. S. Choi, “Polymeric Rulers: Distance-Dependent Emission Behaviors of Fluorophores on Flat Gold Surfaces and Bioassay Platforms Using Plasmonic Fluorescence Enhancement,” Adv. Funct. Mater. 18(21), 3395–3402 (2008).
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Choi, H. C.

Y. S. Chi, H. R. Byon, B. S. Lee, B. Kong, H. C. Choi, and I. S. Choi, “Polymeric Rulers: Distance-Dependent Emission Behaviors of Fluorophores on Flat Gold Surfaces and Bioassay Platforms Using Plasmonic Fluorescence Enhancement,” Adv. Funct. Mater. 18(21), 3395–3402 (2008).
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Y. S. Chi, H. R. Byon, B. S. Lee, B. Kong, H. C. Choi, and I. S. Choi, “Polymeric Rulers: Distance-Dependent Emission Behaviors of Fluorophores on Flat Gold Surfaces and Bioassay Platforms Using Plasmonic Fluorescence Enhancement,” Adv. Funct. Mater. 18(21), 3395–3402 (2008).
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Choi, Y.

G. L. Liu, Y. T. Long, Y. Choi, T. Kang, and L. P. Lee, “Quantized plasmon quenching dips nanospectroscopy via plasmon resonance energy transfer,” Nat. Methods 4(12), 1015–1017 (2007).
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A. R. Clapp, I. L. Medintz, B. R. Fisher, G. P. Anderson, and H. Mattoussi, “Can luminescent quantum dots be efficient energy acceptors with organic dye donors?” J. Am. Chem. Soc. 127(4), 1242–1250 (2005).
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Cole, J. R.

R. Bardhan, N. K. Grady, J. R. Cole, A. Joshi, and N. J. Halas, “Fluorescence enhancement by Au nanostructures: nanoshells and nanorods,” ACS Nano 3(3), 744–752 (2009).
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J. Lee, A. O. Govorov, J. Dulka, and N. A. Kotov, “Bioconjugates of CdTe nanowires and Au nanoparticles: Plasmon-excition interactions, luminescence enhancement, and collective effects,” Nano Lett. 4(12), 2323–2330 (2004).
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E. Dulkeith, A. C. Morteani, T. Niedereichholz, T. A. Klar, J. Feldmann, S. A. Levi, F. C. J. M. van Veggel, D. N. Reinhoudt, M. Möller, and D. I. Gittins, “Fluorescence quenching of dye molecules near gold nanoparticles: radiative and nonradiative effects,” Phys. Rev. Lett. 89(20), 203002 (2002).
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N. J. Durr, T. Larson, D. K. Smith, B. A. Korgel, K. Sokolov, and A. Ben-Yakar, “Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods,” Nano Lett. 7(4), 941–945 (2007).
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El-Sayed, I. H.

P. K. Jain, K. S. Lee, I. H. El-Sayed, and M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006).
[CrossRef] [PubMed]

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X. Huang, I. H. El-Sayed, W. Qian, and M. A. El-Sayed, “Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods,” J. Am. Chem. Soc. 128(6), 2115–2120 (2006).
[CrossRef] [PubMed]

P. K. Jain, K. S. Lee, I. H. El-Sayed, and M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110(14), 7238–7248 (2006).
[CrossRef] [PubMed]

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[CrossRef]

B. Nikoobakht and M. A. El-Sayed, “Surface-enhanced Raman scattering studies on aggregated gold nanorods,” J. Phys. Chem. A 107(18), 3372–3378 (2003).
[CrossRef]

B. Nikoobakht, J. Wang, and M. A. El-Sayed, “Surface-enhanced Raman scattering of molecules adsorbed on gold nanorods: off-surface plasmon resonance condition,” Chem. Phys. Lett. 366(1-2), 17–23 (2002).
[CrossRef]

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V. K. Komarala, Y. P. Rakovich, A. L. Bradley, S. J. Byrne, Y. K. Gun’ko, N. Gaponik, and A. Eychmüller, “Off-resonance surface plasmon enhanced spontaneous emission from CdTe quantum dots,” Appl. Phys. Lett. 89(25), 253118 (2006).
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T. Soller, M. Ringler, M. Wunderlich, T. A. Klar, J. Feldmann, H. P. Josel, Y. Markert, A. Nichtl, and K. Kürzinger, “Radiative and nonradiative rates of phosphors attached to gold nanoparticles,” Nano Lett. 7(7), 1941–1946 (2007).
[CrossRef]

E. Dulkeith, A. C. Morteani, T. Niedereichholz, T. A. Klar, J. Feldmann, S. A. Levi, F. C. J. M. van Veggel, D. N. Reinhoudt, M. Möller, and D. I. Gittins, “Fluorescence quenching of dye molecules near gold nanoparticles: radiative and nonradiative effects,” Phys. Rev. Lett. 89(20), 203002 (2002).
[CrossRef] [PubMed]

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A. R. Clapp, I. L. Medintz, B. R. Fisher, G. P. Anderson, and H. Mattoussi, “Can luminescent quantum dots be efficient energy acceptors with organic dye donors?” J. Am. Chem. Soc. 127(4), 1242–1250 (2005).
[CrossRef] [PubMed]

Fisher, M.

C. S. Yun, A. Javier, T. Jennings, M. Fisher, S. Hira, S. Peterson, B. Hopkins, N. O. Reich, and G. F. Strouse, “Nanometal surface energy transfer in optical rulers, breaking the FRET barrier,” J. Am. Chem. Soc. 127(9), 3115–3119 (2005).
[CrossRef] [PubMed]

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O. Kulakovich, N. Strekal, A. Yaroshevich, S. Maskevich, S. Gaponenko, I. Nabiev, U. Woggon, and M. Artemyev, “Enhanced luminescence of CdSe quantum dots on gold colloids,” Nano Lett. 2(12), 1449–1452 (2002).
[CrossRef]

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V. K. Komarala, Y. P. Rakovich, A. L. Bradley, S. J. Byrne, Y. K. Gun’ko, N. Gaponik, and A. Eychmüller, “Off-resonance surface plasmon enhanced spontaneous emission from CdTe quantum dots,” Appl. Phys. Lett. 89(25), 253118 (2006).
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[CrossRef] [PubMed]

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M. Bruchez, M. Moronne, P. Gin, S. Weiss, and A. P. Alivisatos, “Semiconductor nanocrystals as fluorescent biological labels,” Science 281(5385), 2013–2016 (1998).
[CrossRef] [PubMed]

Ginger, D. S.

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Figures (7)

Fig. 1
Fig. 1

Schematic diagram of the FLIM system

Fig. 2
Fig. 2

(a) UV-visible absorbance spectra of GNRs with LSPR peaks at 600, 650 and 730 nm are shown as solid curves. UV-visible absorbance spectra of GNRs that were coated with 13 nm-thick silica with LSPR peaks at 615 nm, 665 nm, and 750 nm are shown as dashed curves. The emission spectrum of QDs with the peak at 605 nm is shown as a dotted curve. (b)-(d) TEM images of 650 nm-GNRs, 650 nm-GNRs coated with 8 nm silica and 13 nm silica. (e)-(g) TEM images of QDs conjugated with 650 nm-GNRs, 650 nm-GNRs coated with 8 nm silica and 13 nm silica.

Fig. 3
Fig. 3

(a) Fluorescence lifetimes of QDs conjugated with 600, 650, and 730 nm-GNRs (square) and GNR_SiO2 (triangle), with corresponding LSPR peaks at 615, 665 and 750 nm under single-photon excitation at 470nm. (b) Ratios of fluorescence intensities (I) of QDs conjugated with GNRs (solid) and GNR_SiO2 (shadow) with corresponding LSPR peaks to original intensity (I0) of QDs without GNRs-conjugation under single-photon excitation at 470 nm.

Fig. 4
Fig. 4

(A) Normalized fluorescence decay curves of QDs, 650 nm-GNRs, QDs-650 nm-GNRs and QDs-665 nm-GNR_SiO2 under two-photon excitation at 750 nm; inset shows magnified fitting decay curves. (B) Emission spectra of QD-650 nm-GNRs, 650 nm-GNRs to which are added QD-emission spectra, QD-665 nm-GNR_SiO2, and QD-750 nm-GNR_SiO2 (from a to d) under two-photon excitation at 750 nm.

Scheme 1
Scheme 1

GNR, silica coated on GNR using TEOS, and both GNR and GNR_SiO2 conjugated with QDs and anti-CEAcam8.

Fig. 5
Fig. 5

Images made by transmitted light (left), one-photon (middle) and two-photon FLIM images (right) of HeLa cells treated with (a)-(c) QDs and anti-CEA8, (d)-(f) QD-750 nm-GNR composites functionalized with anti-CEA8, (g)-(i) QD-GNR_SiO2 composites functionalized with anti-CEA8. Color bar shows different colors, used in the images to represent varying fluorescence lifetime.

Fig. 6
Fig. 6

Dark-field images (left) and one-photon fluorescence images (right) of HeLa cells treated with (a),(b) QD-GNR_SiO2 composites and (c),(d) QD-GNR composites that had been functionalized with anti-CEA8.

Tables (1)

Tables Icon

Table 1 Fluorescence intensities, lifetimes and enhancement factors of radiative decay rate of QDs at different separations from GNRs and without GNRs.

Equations (1)

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γ e m = γ e x c κ η = γ e x c κ R r a d R r a d + R n o n r a d

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