Temperature-Induced Energy Transfer in Dye-Conjugated

Article pubs.acs.org/cm

Temperature-Induced Energy Transfer in Dye-Conjugated Upconverting Nanoparticles: A New Candidate for Nanothermometry Eva Hemmer,* Marta Quintanilla, François Légaré, and Fiorenzo Vetrone* Institut National de la Recherche Scientifique - Énergie, Matériaux et Télécommunications, Université du Québec, 1650 Boulevard Lionel-Boulet, Varennes, Québec J3X 1S2, Canada S Supporting Information *

ABSTRACT: Lanthanide-doped upconverting nanoparticles (UCNPs) are highly promising candidates for bioimaging and for cellular nanothermometry as a novel diagnostic tool. Aiming for the diagnosis of diseases at very early stages in order to optimize therapy and recovery of the patient, it must be taken into account that thermal singularities are often one of the first indicators of a disease. It is therefore our goal to develop a nanothermometer based on UCNPs that is suitable to detect the temperature at a subcellular level in the physiological range. Thus, upconverting NaGdF4:Er3+,Yb3+ nanoparticles that convert near-infrared (NIR) into visible (VIS) light are synthesized by thermal decomposition. Appropriate surface modification with a thermoresponsive polymer pNIPAM (poly(N-isopropylacrylamide)) guarantees dispersibility in aqueous media required for biomedical applications. In a further step, the combination of the obtained UCNPs with an organic dye (FluoProbe532A) provides potential donor-acceptor-pairs allowing for energy transfer processes, whereas the light emitted by the Er3+ ions (donors) is absorbed by the organic dye (acceptor). It has been demonstrated that the dye-conjugated UCNPs undergo a temperature-dependent energy transfer process inducing a temperature-dependent increase in the thermal sensitivity when compared to unlabeled UCNPs. This result indicates the great potential of the presented nanoprobes for applications in nanothermometry.

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INTRODUCTION Thermal changes within a biological cell are indicators for chemical and biophysical interactions during the cell’s life cycle. The intracellular thermogenesis may affect for example the rates of chemical reactions or diffusion processes within the cell which allows for the use of thermal singularities as indicators for subcellular changes.1,2 Moreover, thermal singularities may act as one of the first indicators of diseases such as cancer due to the generally higher temperature of pathological cells3,4 or obesity due to abnormalities in energy expenditure.5 The detection of such thermal irregularities is expected to strongly support the diagnosis of diseases at an earlier stage than it is recently possible with up-to-date diagnostic tools thereby increasing the chances of full recovery of the patient. This leads to the potential use of thermal sensing at the cellular level as a novel diagnostic tool.6 However, the potential use of such nanothermometers is not limited to detection. For example, the efficiency and local specificity of therapies based on thermal processes, such as hyperthermia inducing the death of tumor cells by increasing their temperature up to cytotoxic levels, could be improved by monitoring the temperature of the environment surrounding the tumor such that any healthy cells are not subject to overheating.7,8 Luminescence nanothermometry could strongly support such approaches as temperaturedependent photoluminescence allows for the monitoring of the © XXXX American Chemical Society

temperature of a biosystem and for the deeper understanding of intracellular mechanisms of specific diseases.9 Among potential probes for nanothermometry, organic dyes, quantum dots, and upconverting lanthanide (Ln3+)-based nanoparticles (UCNPs) have been reported.10,11 Particularly, Ln3+-doped nanoparticles have generated increasing interest as promising probes not only for nanothermometry but also for optical bioimaging in general. This trend is due to the outstanding optical properties of Ln3+doped nanoparticles based on the electron configuration of their ions.12 The incomplete 4f shell of Ln3+ ions is located inside the complete 5s2 and 5p6 shells resulting in its shielding, and, therefore, only a small influence of the host lattice on the optical transitions within the 4f configurations is observed. Furthermore, lanthanide ions doped in suitable ceramic host materials show narrow optical absorption and emission bands, high emission efficiency, and long lifetime of the excited states (μs to ms range).13−15 These properties favor excitation in the near-infrared (NIR) region since some of these states can act as population reservoirs enabling the possibility to undergo multiphoton excitation followed by the emission of higher energy light, spanning the UV to the NIR regions, known as Received: October 15, 2014 Revised: December 4, 2014

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dx.doi.org/10.1021/cm503799f | Chem. Mater. XXXX, XXX, XXX−XXX

Chemistry of Materials

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few reports have been recently published: Complexes formed between pNIPAM and Eu3+ as well as Tb3+ were shown to exhibit temperature-dependent emission intensities with a significant increase upon heating to temperatures above the transition temperature.52 A similar trend was reported for NaYF4:Eu3+/pNIPAM hydrogels.53 Besides the decreasing of their emission intensity with increasing temperature, the thermosensitive energy level splitting of 4F7/2 → 4I15/2 of Er3+ was observed for YF3:Yb3+,Er3+ nanoparticles embedded in pNIPAM-based nanogels.54 This concept of pNIPAM supported temperature measurement can be applied to LRET systems, and it had been successfully implemented in several studies including thermo-, light-, and glucose-sensitive pNIPAM microgels covalently incorporated with organic donor and acceptor dyes.55,56 Herein, the temperature induced collapse of the polymer chains results in closer spatial proximity of the donor and acceptor moiety and therefore in increased energy transfer efficiency between the two organic dyes. Further, it has been demonstrated that the change of the local environment by passing the transition temperature (LCST, lower critical solution temperature) of pNIPAM grafted on iron oxide nanoparticles and modified with a fluorescent label allows simultaneous induction of localized heating and noninvasive monitoring of the temperature, which makes those nanoparticles very attractive for biomedical applications.57,58 Kusolkamabot et al. developed a chemical nose for protein detection based on the quenching of the fluorescence of a fluorophore by pNIPAM modified Au nanoparticles.59 Very recently Xiao et al. presented a thermoresponsive LRET system based on NaLuF4:Mn2+/Ln3+ UCNPs (Ln3+ = Yb3+, Er3+, Tm3+) as energy donors and gold nanoparticles as acceptors.60 Those studies clearly reveal the high potential of LRET pairs in combination with pNIPAM for nanothermometry applications. Yet, the reported donor and acceptor pairs are based on either organic molecules or on oxides as well as UCNPs and non-luminescent gold nanoparticles as quenchers, while to the best of our knowledge, a temperature dependent LRET process between donor UCNPs and acceptor fluorophores that are linked by thermoresponsive pNIPAM has not been reported until now. Thus, with the goal to develop a LRET system that will be applicable in upconversion-based bioimaging and in nanothermometry, here we present the fabrication and characterization of a novel NaGdF4:Er3+,Yb3+-pNIPAM-FluoProbe532A system and evaluate its suitability as a thermosensitive LRET probe.

upconversion. The use of NIR light is of particular interest for bioimaging as absorption by hemoglobin and scattering is reduced resulting in the increased transparency of biological tissue, as heat transfer from the laser to the biological tissue along the excitation path can be minimized, and as the image contrast can be improved due to a lack of autofluorescence.16−19 The ability of the UCNPs to act as thermal probes can be based on temperature-sensitive changes of the spectral shape,20,21 on changes of the luminescence intensity ratio (LIR),22,23 or the lifetime of the excited states of the Ln3+ ions.24 Yet, currently, we are facing the need to develop more reliable and faster techniques for the investigation of biological processes, the sensing of biochemical compounds and eventual diagnosis of diseases at the earliest stage possible. In this context, it is possible to exploit LRET (luminescence resonant energy transfer), known as a sensitive and reliable analytical technique that is widely used in bioassays, biosensing, and bioimaging.25,26 LRET is a process in which energy is transferred from an excited donor to an acceptor, both exhibiting a spectral overlap.27 This nonradiative transfer leads to a decrease, or quenching, of the donor’s emission and/or lifetime as well as an increase of the acceptor’s emission intensities. Thus, we are aiming for the development of a novel temperature-sensitive system by combining the outstanding optical properties of UCNPs and the great analytical possibilities of LRET, hereby seeking for an increased thermal sensitivity of the energy transfer processes between the donor UCNP and the acceptor moiety. Recently, LRET systems involving Ln3+-doped nanoparticles have been developed combining UCNPs as donors and various fluorescent acceptors such as organic dyes28−36 and quantum dots37−39 as well as non-luminescent quenchers such as gold nanoparticles.40,41 While all these reported systems focus on the detection of specific molecules or cells, the application of UCNPs in LRET systems for temperature measurements is a barely reported approach42 requiring the introduction of an additional, namely temperature-sensitive, component to the system. It is well-known that the efficiency of the LRET process is strongly dependent on the distance between the donor and the acceptor moieties.43−45 Thus, the linkage of a donor and an acceptor united by a temperature sensitive linker is expected to yield a LRET system where the energy transfer efficiency is sensitive to changes of the thermal environment. In this context, stimuli (e.g., temperature or pH) responsive polymers that were modified with a fluorophore have been reported as promising candidates for fluorescent nanothermometry.46 For instance, Chen et al. developed a temperature sensor based on dye-labeled poly(N-isopropylacrylamide) (pNIPAM).47 Gota et al. reported the suitability of pNIPAM in combination with a water-sensitive fluorophore for intracellular thermometry.48 Those strategies are based on the fact that the thermoresponsive polymer pNIPAM exhibits a discontinuous change of its chain length in dependence of the temperature, whereas the polymer chains are stretched at low temperatures while they collapse when the temperature increases.49 This leads for example to the release of water molecules from the polymeric network and therefore from the surroundings of the attached fluorophore resulting in increased emission.48 For biomedical applications, this temperaturedriven conformational change of the polymer is ideally in the range of the body temperature, as it is in the case of pNIPAM.50,51 Focusing on lanthanide-based systems, only a

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EXPERIMENTAL PROCEDURES

Materials Synthesis. Starting materials such as lanthanide oxides (Gd2O3, REacton, 99.999%, < 10 Micron Powder; Yb2O3, REacton, 99.998%, Powder; Er2O3, REacton, 99.99%, Powder, Alfa Aesar, Ward Hill, USA), sodium trifluoroacetate (CF3COONa, 98%, Sigma-Aldrich, St. Louis, USA), trifluoroacetic acid (CF3COOH, 99%, Alfa Aesar, Ward Hill, USA), 1-octadecene (CH3(CH2)15CHCH2, tech. 90%, Alfa Aesar, Ward Hill, USA), oleic acid (CH3(CH2)7CHCH(CH2)7COOH, tech. 90%, Alfa Aesar, Ward Hill, USA), HOOCpNIPAM-SH (α-carboxy ω-thiol terminated poly(N-isopropylacrylamide, Mn = 10,000, Mw = 14,000, Polymer Source Inc., Montreal, Canada), FluoProbe532A-maleimde (Interchim, Montluçon Cedex, France), and hydrochloric acid (HCl, Reagent A.C.S., Fisher Scientific, Nepean, Canada) were used without further purification. The synthesis of the UCNPs was carried out in a well-ventilated fume hood as described previously.61,62 B



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Preparation of Lanthanide Trifluoroacetate Precursors. In a typical precursor synthesis 0.975 mmol of Gd2O3 (353.4 mg), 0.25 mmol of Yb2O3 (98.5 mg, 20 mol % doping rate), and 0.025 mmol of Er2O3 (9.6 mg, 2 mol % doping rate) were mixed with 5 mL of distilled water and 5 mL of trifluoroacetic acid in a 50 mL three-neck round-bottom flask. The mixture was refluxed under magnetic stirring at 80 °C until a clear solution was obtained. The temperature was then lowered to 60 °C to slowly evaporate residual water and trifluoroacetic acid. The precursor was obtained as a white solid. Synthesis of NaGdF4:Er3+,Yb3+ Nanoparticles (UCNPs). For the preparation of NaGdF4 nanoparticles doped with 2 mol % Er3+ and 20 mol % Yb3+, 12.5 mL each of the high boiling solvent 1-octadecene and of the coordinating oleic acid were mixed in the reaction vessel (100 mL three-neck round-bottom flask) and degassed for 30 min at 150 °C under vacuum and magnetic stirring. Meanwhile, 2.5 mmol of sodium trifluoroacetate (340 mg) as well as 7.5 mL each of 1octadecene and oleic acid were added to the as-prepared precursor. The mixture was degassed at 125 °C under vacuum and magnetic stirring. Subsequently, the reaction vessel containing the degassed 1octadecene and oleic acid was heated to 315 °C under gentle argon flow. The hot precursor solution was then added dropwise to the reaction vessel using a syringe and pump system (Harvard Apparatus, Pump 11 Elite, injection rate: 1.5 mL min−1). Following injection, the solution was maintained at 315 °C and stirred for further 60 min under argon flow. The solution was then allowed to cool to room temperature. The obtained nanoparticles were precipitated by addition of ethanol and recovered by centrifugation at 5500 rpm for 10 min. The obtained white powder was washed twice with a mixture of hexane and ethanol (1:4 v/v) followed by centrifugation. The resultant oleate-capped NaGdF4:Er3+,Yb3+ nanoparticles were finally redispersed in hexane for storage. Surface Modification (UCNPs-pNIPAM) and Dye-Conjugation (UCNPs-pNIPAM-dye). Ligand-free lanthanide-doped nanoparticles were obtained following a procedure previously described in the literature.61 Therefore, 60 mg of oleate-capped nanoparticles were dispersed in 5 mL of hexane, and 5 mL of an aqueous solution of HCl (pH adjusted to 4) were added. The mixture was kept stirring at room temperature for 3 h, followed by separation of the aqueous phase containing the nanoparticles by use of a separation funnel. Acetone was added for precipitation, and the nanoparticles were collected by centrifugation (5500 rpm, 15 min). Subsequently, the obtained particles were stirred for further 2 h in a 5 mL aqueous solution maintaining the pH at 4. After the reaction protonating the carboxylate groups of the oleate ligand was completed, ligand-free nanoparticles were recuperated by centrifugation (5500 rpm, 15 min) after precipitation with acetone and finally redispersed in distilled water. For modification with HOOC-pNIPAM-SH, 300 μL of the ligand-free particles dispersed in water (c ∼ 10 wt %) were added to a solution of 100 mg of HOOC-pNIPM-SH dissolved in 3 mL of water and magnetically stirred at room temperature for 48 h. Herein, the surface modification was achieved through electrostatical coordination between the carboxylate groups at one end of the pNIPAM chain and the positively charged lanthanide ions on the surface of the nanoparticles. The modified nanoparticles were precipitated with acetone, washed twice with water, recuperated by centrifugation (8000 rpm, 20 min), and redispersed in 1 mL of distilled water. The obtained dispersion was split into two equal parts, whereas one part was kept as a dye-free control sample (UCNPs-pNIPAM), while the other part was used for conjugation with the organic dye FluoProbe532A-maleimide (UCNPs-pNIPAM-dye). The coupling reaction of the maleimide group of the organic dye with the free thiol group of the polymer is allowed by adding 30 μL of an aqueous solution of the dye (c = 0.5 g L−1) diluted in further 500 μL of water to 500 μL of the dispersion of pNIPAM-modified nanoparticles. The mixture was gently stirred at room temperature for 1 h, followed by stirring in a refrigerator (T = 4 °C) overnight. The conjugated particles were washed with water until the supernatant was colorless, recuperated by centrifugation (8000 rpm, 20 min) after precipitation with acetone, and finally redispersed in 500 μL of distilled water.

If not otherwise mentioned in the text, UCNPs refers to NaGdF4:Er3+,Yb3+ nanoparticles, UCNPs-pNIPAM refers to nanoparticles modified with the thermoresponsive polymer poly(Nisopropylacrylamide) (pNIPAM), and UCNPs-pNIPAM-dye refers to the nanoparticles that are labeled with the organic dye FluoProbe532A subsequent to pNIPAM-modification. Morphological and Structural Characterization. The crystalline phase of the samples was determined by powder X-ray diffraction (XRD) with a Bruker D8 Advance Diffractometer using CuKα radiation. The morphology and size distribution of the obtained powders was investigated by transmission electron microscopy (TEM) (Philips CM200 High-Resolution TEM). For Fourier transform infrared (FTIR) spectroscopy of the oleate-capped and ligand-free UCNPs, dried samples were mixed with potassium bromide (KBr, FTIR grade, Alfa Aesar, Ward Hill, USA), and the spectra of the powders were recorded using a Nicolet 6700 FTIR spectrometer from Thermo Electron Corporation. In the case of UCNPs-pNIPAM, UCNPs-pNIPAM-dye, HOOC-pNIPAM-SH and FluoProbe532A-maleimide aqueous solutions were dropped on Real Crystal NaCl IR cards (9.5 mm aperture, International Crystal Laboratories), and spectra were recorded after drying by use of a Spectrum Two FTIR spectrometer by PerkinElmer. The transition temperature of the thermoresponsive polymer was estimated from DLS (dynamic light scattering) measurements using a Brookheaven 90Plus Particle Size Analyzer. Pure HOOC-pNIPAM-SH was dissolved in distilled water (1 g L−1, filtered with Milex-HA 0.45 μm filter), and the effective size was measured as a function of the temperature in the range from 25 to 45 °C (temperature step: 1°, measuring time per temperature step: 5 min). Optical Characterization. Absorption spectra of the organic fluorophore were recorded with a UV−vis-NIR (ultraviolet−visiblenear-infrared) spectrophotometer Cary 5000 by Varian. For upconversion emission measurements, dispersions of the nanoparticles were transferred into glass cuvettes and placed into a temperaturecontrolled cuvette holder (qpod 2e by Quantum Northwest, Washington, USA) allowing for wireless temperature control through USB using the Q-Blue software (Quantum Northwest). Spectra were recorded under 980 nm excitation using a Thorlabs fiber-coupled laser diode (maximum power 330 mW). The laser was focused on the sample using a lens to obtain a spot with a Gaussian intensity distribution with a 0.4 mm diameter. The emitted light was collected by a lens in a 90° configuration and then transferred to a spectrophotometer (Avaspec -2048L - USB2) by use of an optical fiber. For measurements as a function of temperature, the nanoparticle dispersion was kept under stirring (200 rpm) until the set temperature was reached in order to guarantee a homogeneous temperature distribution. After a period of at least 10 min that was given to allow the temperature to stabilize, the stirrer was turned off in order to eliminate any influence of the stirring on the luminescence characteristics. Subsequently emission spectra were recorded, immediately after stopping the stirrer and in further steps of approximately 10 s each.

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RESULTS AND DISCUSSION Preparation and Characterization of Upconverting Nanoparticles (UCNPs). Oleate-capped UCNPs of NaGdF4 doped with 2 mol % Er3+ and codoped with 20 mol % Yb3+ were synthesized by thermal decomposition as previously described in the literature.63,64 The X-ray diffraction pattern recorded on the as-prepared UCNPs revealed that the particles crystallized in the hexagonal β-phase (Figure 1a), which is believed to be the more efficient phase for upconversion emission for the NaGdF4 host material. As one can see from the TEM micrograph shown in Figure 1b, the obtained oleatecapped nanoparticles exhibit faceted, mainly hexagon-shaped, morphology with an average particle size of 26 nm in diameter. Because of the oleate-capping, the as-prepared UCNPs are hydrophobic and therefore are dispersible only in nonpolar C



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the two chromophores, whereas the Er3+ ions act as donors and the organic dye as the acceptor. Generally, the efficiency of the LRET process strongly depends on the spatial distance between the donor and the acceptor.44,45 In order to control the distance between the acceptor and the donor as a function of temperature, we introduced the thermoresponsive polymer, namely pNIPAM poly(N-isopropylacrylamide), as a linker between the UCNPs and the FluoProbe. Preparation and Characterization of pNIPAM-Modified (UCNPs-pNIPAM) and Dye-Conjugated (UCNPspNIPAM-dye) Upconverting Nanoparticles. pNIPAMmodified UCNPs (UCNPs-pNIPAM) were prepared by surface grafting of α-carboxy, ω-thiol terminated pNIPAM onto the ligand-free UCNPs, whereas the modification is based on the electrostatic adsorption of the COOH group of the polymer on the positively charged surface of the bare UCNPs. For further functionalization of the UCNPs-pNIPAM with an organic dye, maleimide-labeled FluoProbe532A was chosen due to its absorption band that overlaps with the green emission of the Er3+-doped UCNPs. The maleimide group of the organic dye allows the reaction with the thiol group at the free end of the pNIPAM chain grafted to the nanoparticle surface resulting in the final dye-labeled pNIPAM-coated UCNPs (UCNPspNIPAM-dye).65 These now modified and conjugated nanoparticles are hydrophilic and water-dispersible. The functionalization of the UCNPs was analyzed by FTIR spectroscopy, and data as well as discussion are provided as Supporting Information (Figure S1b and c). Again, thermoresponsive polymers such as pNIPAM change their physical properties as a function of temperature. Here, we are using pNIPAM as a spacer molecule in order to control the distance between the donor and the acceptor moieties and hence the efficiency of the energy transfer between the UCNP and the organic dye. Thus, the change of the polymer chain length as a function of the temperature is of fundamental interest. Generally, pNIPAM is well-known for the collapsing of its chains when a specific transition temperature is exceeded. Hereby, the molecular weight of the polymer and the functionalization of the pNIPAM backbone with various functional groups such as carboxyl or thiol units may influence the exact transition point.51 Temperature-dependent dynamic light scattering (DLS) measurements were performed in order to analyze the aggregation behavior of HOOC-pNIPAM-SH in aqueous solution used in this work.66 In fact, the change of the measured effective diameter in dependence of the temperature is used to estimate the transition temperature. As seen in Figure 3, the effective diameter determined from an aqueous solution of HOOC-pNIPAM-SH increases sharply between 30 and 35 °C, resulting in an estimated transition temperature of approximately 33 °C. The collapsing of the polymer chains in this temperature range results in a reduced solubility of the polymer, which is also obvious from the fact that the solution becomes cloudy once the transition temperature is exceeded (photograph in Figure 3 inset). This could also explain the seemingly decrease of the effective diameter after passing the transition temperature as the high opacity of the solution results in a saturation of the current count rate during the DLS measurement potentially affecting the accuracy of the obtained values. Based on those findings, we expect a change in the energy transfer efficiency of the dye-conjugated sample (UCNPs-pNIPAM-dye) at a temperature of approximately 35 °C.

Figure 1. a) XRD pattern recorded on as-prepared oleate-capped UCNPs. Reference file: β-NaGdF4 [00-027-0699]. b) TEM image of as-prepared oleate-capped NaGdF4:Er3+,Yb3+ upconverting nanoparticles.

solvents such as hexane. Yet, for biomedical applications and for the surface modification with a thermoresponsive polymer as well as subsequent conjugation of the organic dye reported here, water dispersibility is essential. Thus, the UCNPs were rendered water dispersible by utilizing an easy approach reported in the literature, where the oleate chains are protonated and removed from the nanoparticle surface creating hydrophilic UCNPs whose surface charge keeps them from agglomerating.61 The successful removal of the oleate-capping agent was confirmed by Fourier transform infrared (FTIR) spectroscopy. The FTIR spectra recorded on the as-prepared oleate-capped and ligand-free UCNPs as well as their discussion are provided as Supporting Information (Figure S1a). The upconversion luminescence spectrum recorded following 980 nm excitation (Figure 2, green graph) of the ligand-free

Figure 2. Upconversion emission spectrum (green graph) recorded on ligand-free UCNPs dispersed in water and UV−vis absorption spectrum recorded on FluoProbe532A-maleimide (red graph).

UCNPs dispersed in water showed sharp emission peaks in the green (550 nm) and in the red (670 nm) regions of the visible spectrum. These characteristic peaks of the Er3+ ions can be assigned to the 2H11/2 → 4I15/2 (520 nm), 4S3/2 → 4I15/2 (540 nm), and 4F9/2 → 4I15/2 (655 nm) f-f transitions. Figure 2 further shows that the absorption band of the organic dye FluoProbe532A-maleimide (red graph) matches very well with the green 2H11/2 → 4I15/2 transition and partially matches with the 4S3/2 → 4I15/2 emission from the Er3+ and Yb3+ codoped UCNPs. Therefore, the combination of the obtained UCNPs with this organic dye provides a potential donor-acceptor-pair. In fact, an energy transfer (LRET) process is expected between D



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particularly when the dispersion is allowed to stabilize for 50 s after stopping the stirrer (Figure 4a2). In contrast, the equilibration period had no significant effect on the temperature-depending emission characteristics of bare UCNPs or UCNPs-pNIPAM (Figure 4b and c). This may be assigned to subsequent quenching of the upconversion emission by the organic dye only present in UCNPspNIPAM-dye when the temperature is increasing. As shown by UV−vis absorption spectroscopy, FluoProbe532A exhibits a maximum absorption at 532 nm, which matches with the green emission from the Er3+/Yb3+ codoped nanoparticles. The maximum emission from FluoProbe532A is expected to be seen at 553 nm. However, no additional peak was observed at this wavelength, as it may be overlaid by the stronger 4S3/2 → 4I15/2 emission band of the Er3+ ion. In order to rule out any concentration or power density effect, which may affect the absolute emission intensity, we further analyzed the temperature-dependent changes in the luminescence intensity ratio (LIR) Igreen/Itotal of UCNPs-pNIPAM-dye as well as control samples UCNPs and UCNPs-pNIPAM. Figure 5a shows the ratio between the green emission (Igreen, determined by integration of the peak area in a wavelength range from 496 to 580 nm) and the total (Itotal, λ = 300 to 840 nm) emission intensities as a function of the temperature. As expected, the relative green emission, expressed by the ratio Igreen/Itotal, is constant over the observed temperature range in the case of the control samples not containing any fluorophore (UCNPs and UCNPs-pNIPAM). In contrast, the data obtained for the dyelabeled system UCNPs-pNIPAM-dye exhibit a drop of the relative green emission when the temperature exceeds 35 °C. In other words, the temperature increase results in a more pronounced decrease of the emission intensity in the green wavelength range when compared to the overall emission. This indicates a specific quenching of the green emission by an energy transfer from the donor-UCNP to the acceptor-dye as a function of temperature. It must be further mentioned that the critical temperature at which this increased energy transfer process is observed, namely at 35 °C, is in good agreement with the transition temperature of the thermoresponsive polymer used as a linker between the donor (UCNP) and the acceptor (dye). Thus, with the increase of the temperature, the collapse of the pNIPAM polymer chains lead to closer proximity between the UCNP/FluoProbe pair that will eventually result in the decrease of the green emission intensity due to more effective energy transfer process. Preliminary lifetime measurements (using a specific band-pass filter for the green UCNP emission) on UCNPs-pNIPAM-dye show a shortening of the

Figure 3. Estimation of the transition temperature of the thermoresponsive polymer pNIPAM by DLS measurements: Effective diameter of pure COOH-pNIPAM-SH as a function of temperature. Inset: Photograph of COOH-pNIPAM-SH solutions at room temperature and after heating to 45 °C.

Luminescence Quenching of the Upconversion Emission by the Conjugated Fluorophore. In order to demonstrate the suitability of the prepared UCNPs-pNIPAMdye as a temperature sensitive probe (Scheme 1), the emission spectra of the functionalized particles dispersed in water and excited at 980 nm were recorded as a function of temperature. The nanoparticle dispersion was kept under stirring until the set temperature was reached in order to guarantee a homogeneous temperature distribution. In order to study a potential effect of the time given to the dispersion to equilibrate after stopping the stirrer, spectra were recorded for each temperature immediately after stopping the stirrer (equilibration time ∼10 s) and in further steps of approximately 10 s each up to an equilibration time of 90 s. Figure 4 shows the upconversion emission spectra obtained in a temperature range from 20 to 50 °C for UCNPs-pNIPAM-dye (a1) immediately after (t ∼ 10 s) and (a2) 50 s after stopping the stirrer. For comparison, temperature dependent spectra are also shown for ligand-free UCNPs and UCNPs-pNIPAM (Figure 4b and c). With the increase of temperature from 20 to 50 °C, the overall emission intensity decreases prominently for all samples, which can be explained by the partial quenching of the upconversion luminescence through multiphononic processes that are increasing with increasing temperature. Yet, interestingly, the rate at which the emission intensity is decreasing is higher for the dye-labeled nanoparticles (UCNPspNIPAM-dye) than for ligand-free UCNPs or UCNPs-pNIPAM,

Scheme 1. Scheme of the LRET System Based on Er3+/Yb3+ Co-Doped NaGdF4 Upconverting Nanoparticles, Thermoresponsive Polymer pNIPAM and Organic Dye FluoProbe532A

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Figure 4. Temperature-dependent emission spectra recorded on UCNPs-pNIPAM-dye dispersed in water 10 s (a1), respectively 50 s (a2) after turning off the stirrer. Reference emission spectra: b) ligand-free UCNPs, c) UCNPs-pNIPAM.

donor lifetime indicating that nonradiative LRET was present. While this does not rule out the possibility of radiative emission and reabsorption processes, it provides a clear hint that LRET is present. A full kinetic study has been initiated and will be the subject of a future manuscript. Generally speaking, the energy transfer probability, WTr, between the donor and the acceptor depends on the distance RDA between them in such a manner that WTr ∼ RDA−6,26 whereas RDA is decreasing as a function of the temperature in the system presented here. A second important parameter influencing whether efficient energy transfer can happen or not is the overlap integral J(λ) described by the spectral overlap between the donor emission and the acceptor absorption spectrum.26 Thus, in a simplified way, the probability that energy transfer will take place between the donor UCNPs and the acceptor dye follows the dependency given by eq 1:

WTr ∝

1 × J (λ , T ) RDA(T )6

(1)

One must also take into account that the distribution of the population of the two green-emitting energy levels in close proximity of the Er3+ ions, namely 2H11/2 and 4S3/2, changes with the temperature. Figure 5b shows the ratio between the emission intensity originating from the 2H11/2 level (I(2H11/2), determined by integration of the peak area in a wavelength range from 510 to 533 nm) and the residual emission intensity (Iresidual = Itotal − I(2H11/2)) as a function of the temperature. In the case of dye-free samples UCNPs and UCNPs-pNIPAM (orange and blue graphs) I(2H11/2)/Iresidual increases with increasing temperature indicating a shift toward the higher energy level 2H11/2. As it is shown in Figure 2, the acceptor dye applied here exhibits a better spectral overlap with the UCNP emission originating from this 2H11/2 level. As the 2H11/2 F



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Figure 5. a) Relative green emission Igreen/Itotal (LIRUCNPs‑pNIPAM‑dye) as a function of temperature and b) temperature dependence of the ratio I(2H11/2)/Iresidual for UCNPs-pNIPAM-dye as well as control samples. Time dependence of the relative green emission from c) UCNPs-pNIPAM-dye as well as d) control samples UCNPs and UCNPs-pNIPAM.

transition temperature. Further, due to the lack of an appropriate acceptor moiety, no time-dependent change of Igreen/Itotal was observed in the case of the control samples (Figure 5d). The observed effect of the equilibration time given to the system after stopping the stirrer suggest a hindering effect of the stirring on the energy transfer process that may be explained as follows. Taking into account that the polymer chains providing the linking unit between the nanoparticle and the dye molecules are not rigid, the forced and directed movement of the nanoparticle through the stirrer may imply some stretching force on the polymer chains, pulling them behind the nanoparticle. This may then avoid the unhindered and sufficient collapsing of the chains and therewith close enough spatial approach of the acceptor dye molecule to the donor UCNP for efficient energy transfer. On the other side, by stopping of the stirrer, this pulling force will be released, the polymer chains can collapse above the critical transition temperature, and the energy transfer process takes place once the organic dye and the UCNP are in close enough distance. The thermal reversibility of the UCNPs-pNIPAM-dye was evaluated by monitoring the relative green emission Igreen/Itotal after repetitive heating and cooling. Figure S2 (see the Supporting Information) shows that after 5 heating cycles a decreasing trend of the LIRUCNPs‑pNIPAM‑dye after passing the polymer’s transition temperature is still observed. However, the decrease becomes much less pronounced. As in the case of

emission is favored for higher temperatures, we then assume that the overlap integral J(λ) is increasing with increasing temperature. In the case of UCNPs-pNIPAM-dye, I(2H11/2)/Iresidual follows the same trend as for the dye-free reference samples (Figure 5b, green graph) until reaching the transition temperature of pNIPAM. However, when reaching the transition temperature, I(2H11/2)/Iresidual decreases. The ongoing decrease of the ratio I(2H11/2)/Iresidual as well as the ratio Igreen/Itotal (Figure 5a) may be explained by the temperature dependence of the probability for energy transfer. Following eq 1, the probability of energy transfer from the UCNP to the dye increases with increasing temperature as, first, the distance RDA is decreasing at the transition temperature, and second, the overlap integral S is continuously increasing within the observed temperature range, eventually resulting in the efficient quenching of the green emission through the organic dye. Moreover, the efficiency of the energy transfer increases when the system is allowed to stabilize after turning off the stirrer as obvious from the sharp drop of Igreen/Itotal measured after 50 s without stirring (Figure 5c). As expected, the timedependent data obtained for UCNPs-pNIPAM-dye reveal that Igreen/Itotal remains constant over time when the temperature of the system is below the pNIPAM transition temperature, yet the efficiency of the energy transfer significantly increases with increasing stabilization time for temperatures higher than the G



Article

applying the basic definition of S as the thermal derivative of the LIR

most organic dyes, the acceptor dye may suffer and be partially damaged by the repetitive heating and laser radiation resulting in reduced sensing ability. Estimation of the Thermal Sensitivity. The LIR (luminescence intensity ratio) technique is a straightforward tool to calculate the thermal sensitivity S of a luminescent material having two closely spaced energy levels whose temperature governed population is following Boltzmann’s distribution.23 Under such conditions, which also apply for Er3+/Yb3+ codoped NaGdF4 upconverting nanoparticles, LIR is given by23 LIR =

⎛ ΔE ⎞ I1 = B × exp⎜ − ⎟ I2 ⎝ kBT ⎠

S=

⎛ ΔE ⎞ ∂(LIR) ⎟ = LIR × ⎜ 2 ∂T ⎝ kBT ⎠

(4)

where LIR is redefined as the ratio between the green and total luminescence intensities (Igreen/Itotal) as presented in Figure 5a. The experimental data for Igreen/Itotal as a function of the temperature can be fitted by a polynomial function (graph given in Supporting Information, Figure S5) LIR =

(2)

Igreen Itotal

= T0 + B1·T + B2 ·T 2 + B3 ·T 3

(5)

With the intercept T0 = 0.78 ± 0.06, B1 = 0.03 ± 0.01, B2 = 9.75 · 10−4 ± 1.63 · 10−4, and B3 = 1.15 · 10−5 ± 1.55 · 10−6, and from which the thermal sensitivity S of UCNPs-pNIPAMdye can be obtained as

where ΔE is the energy gap between the emitting levels in close proximity I1 and I2, and B is a constant that depends on the experimental system and the intrinsic spectroscopic parameters of the dopant/host pair. T is given in Kelvin. kB is the Boltzmann factor. ΔE and B can be obtained from the leastsquares fitting of the linear dependence of ln(LIR) versus the reciprocal absolute temperature, so-called Boltzmann’s plot. Considering the green emitting levels of the Er3+ ions (2H11/2 and 4S3/2) in the UCNPs presented here, the obtained Boltzmann’s plots for ligand-free UCNPs and UCNPs-pNIPAM have been determined and are given in the Supporting Information (Figure S3). Based on the obtained Boltzmann’s plots, the thermal sensitivity S as a function of the temperature can be determined for the presented UCNPs and UCNPspNIPAM (Figure S4 in the Supporting Information and Figure 6) as S is defined by23 S=

∂(LIR) ∂T

S=

∂(LIR) = |B1 + 2B2 ·T + 3B3 ·T 2| ∂T

(6)

As B1, B2, and B3 are given through the fitting parameters (eq 5), the thermal sensitivity of UCNPs-pNIPAM-dye can be plotted as a function of T, and the resultant graph is presented in Figure 6. As it can be deduced from the graphs in Figure 6 and Figure S4, the thermal sensitivities of ligand-free UCNPs and UCNPs-pNIPAM are following a linear trend within the observed temperature range exhibiting values in the physiological temperature range between 3.3 and 3.9 · 10−3 °C−1 (Table 1). Those values are in a comparable range with previously published data for Er3+-doped host materials (Table 1 and69). In contrast to the linear development of S in the case of the UCNPs and UCNPs-pNIPAM, UCNPs-pNIPAM-dye exhibit an increase of their thermal sensitivity. Below the transition temperature of the thermoresponsive polymer, the estimated sensitivities are lower than of those determined for the control samples (S35 °C = 0.9 · 10−3 °C−1). Yet, with increasing temperature and the therewith collapsing of the polymer chains allowing an energy transfer between the nanoparticle and the fluorophore, the thermal sensitivity SUCNPs‑pNIPAM‑dye drastically increases reaching a more than twice as high value at 45 °C (S45 °C = 8.9 · 10−3 °C−1) and a four times higher sensitivity at 50 °C (S50 °C = 15.5 · 10−3 °C−1) when compared to the unlabeled control samples (UCNPs: S45 °C = 3.9 · 10−3 °C−1, S50 °C = 4.0 · 10−3 °C−1; UCNPspNIPAM: S45 °C = 3.5 · 10−3 °C−1, S50 °C = 3.6 · 10−3 °C−1). Generally, the transition temperature of a thermoresponsive polymer is known to be tunable through the careful choice of the polymer’s backbone length, potential introduction of side chains as well as functional groups.51 Taking this into account, the linkage of donor UCNPs with acceptor dyes by a tailored thermoresponsive polymer exhibiting a slightly lower transition temperature than that used here pNIPAM is expected to result in a shift of the high thermal sensitivity to lower temperatures and therewith toward the more physiologically interesting temperature range making the system presented here a highly promising candidate for biomedical nanothermometry.

(3)

Figure 6. Estimated thermal sensitivities for UCNPs-pNIPAM-dye as well as control samples UCNPs and UCNPs-pNIPAM.

where LIR = I(2H11/2)/I(4S3/2) is determined by integration of the emission peaks, and ΔE/kB is given by the slope of the Boltzmann’s plot. However, in the case of the dye-labeled system UCNPspNIPAM-dye the interaction of the acceptor dye with the donor UCNP does not allow an estimation of S by the same approach. Due to the partial quenching of the green emission from the UCNPs by the organic dye, one cannot assume here Boltzmann’s distribution between the 2H11/2 and 4S3/2 levels. Yet, one can still estimate S of the dye-labeled system by

■

CONCLUSION In summary, upconverting NaGdF4:Er3+,Yb3+ nanoparticles were prepared by the thermal decomposition of trifluoroacetate precursors, followed by surface modification with the H



Article

Table 1. Thermal Sensitivities of UCNPs for Optical Thermometry material

preparation

T (°C)

S (10−3 °C−1)

β-NaGdF4:Er ,Yb (UCNPs, 26 nm) β-NaGdF4:Er3+,Yb3+ (UCNPs, 26 nm) β-NaGdF4:Er3+,Yb3+ (UCNPs, 26 nm) pNIPAM-modified β-NaGdF4:Er3+,Yb3+ (UCNPs-pNIPAM) pNIPAM-modified β-NaGdF4:Er3+,Yb3+ (UCNPs-pNIPAM) pNIPAM-modified β-NaGdF4:Er3+,Yb3+ (UCNPs-pNIPAM) dye-labeled β-NaGdF4:Er3+,Yb3+ (UCNPs-pNIPAM-dye) dye-labeled β-NaGdF4:Er3+,Yb3+ (UCNPs-pNIPAM-dye) dye-labeled β-NaGdF4:Er3+,Yb3+ (UCNPs-pNIPAM-dye) α-NaYF4:Er3+,Yb3+ (18 nm particle size) Gd2O3:Er3+,Yb3+ (17−50 nm crystallite size) Y2O3:Ho3+,Tm3+,Yb3+ (43 nm crystallite size) LiNbO3: Er3+,Yb3+ (160 nm particle size)

thermal decomposition thermal decomposition thermal decomposition thermal decomposition thermal decomposition thermal decomposition thermal decomposition thermal decomposition thermal decomposition solvothermal process solution combustion process combustion process milling technique

35 40 45 35 40 45 35 40 45 37 37 30 37

3.6 3.8 3.9 3.3 3.4 3.5 0.9 4.1 8.9 2.2 2.7 6.9 7.5

3+

3+

Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS The authors thank Timothy Mack (McGill University, Montreal, Canada) for provision of the DLS equipment and Petr Fiurasek (McGill University, Montreal, Canada) for experimental support with the FTIR measurements. Profs. F. Vetrone and F. Légaré are grateful for financial support from the Natural Sciences and Engineering Research Council (NSERC) of Canada, the Canadian Institute for Photonic Innovations (CIPI), the Fonds de Recherche du Québec − Nature et Technologies (FRQNT), and NanoQuébec for supporting their research. E. Hemmer is thankful to the Alexander von Humboldt Foundation for financial support in the frame of the Feodor Lynen Research Fellowship. M. Quintanilla would like to thank Fundación Ramón Areces for financially supporting her through their granting program for Life and Matter Sciences.

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REFERENCES

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ASSOCIATED CONTENT

S Supporting Information *

FTIR spectra of as-prepared, ligand-free, pNIPAM-modified, and dye-conjugated UCNPs; reversibility of the system: LIRUCNPs‑pNIPAM‑dye as a function of the temperature after five repetitive heating cycles; Boltzmann’s plots and thermal sensitivities of ligand-free and pNIPAM-modified UCNPs; fitting parameters for the LIR of dye-conjugated UCNPs. This material is available free of charge via the Internet at http:// pubs.acs.org.

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work work work work work work work work work

*E-mail: [email protected].

thermoresponsive polymer pNIPAM and subsequent conjugation of the organic dye FluoProbe532A. The suitability of the synthesized NaGdF4:Er3+,Yb3+-pNIPAM-FluoProbe532A system as a temperature-sensitive probe was investigated. The obtained results clearly reflect that NaGdF4:Er3+,Yb3+ upconverting nanoparticles are suitable donors for efficient energy transfer to the organic dye FluoProbe532A. Most importantly, the use of the thermoresponsive polymer pNIPAM as the linker between the donor and acceptor introduce an additional functionality, namely temperature-sensitivity. It was shown that the efficiency of the energy transfer between the donor UCNP and the acceptor dye can be controlled by the spatial distance between the donor and the acceptor moieties which is itself controlled by the temperature-depending collapsing or stretching of the pNIPAM chains. It was found that the efficiency significantly increased when reaching the transition temperature of 35 °C, which is in close proximity to a temperature range of biological interest. The estimation of the thermal sensitivity of the presented system revealed a strong increase for temperatures higher than the polymer’s transition temperature (T > 40 °C) when compared to control samples without organic dye as acceptor moiety. It is expected that the use of a thermoresponsive polymer with a tailored transition temperature below 35 °C would induce a shift of the observed high thermal sensitivities toward lower temperatures, reaching the physiologically highly interesting range of ∼37 °C. Thus, the developed UCNP-based system opens new possibilities for the measurement of the temperature using a nanoscale probe, and we expect the reported system to be a promising candidate for the implementation in the field of, e.g. subcellular, nanothermometry.

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ref this this this this this this this this this 22 67 68 23

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. I



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Temperature-Induced Energy Transfer in Dye-Conjugated

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