Dual red-NIR luminescent EuYb heterolanthanide nanoparticles as promising basis for cellular imaging and sensing

Materials Science & Engineering C 105 (2019) 110057

Contents lists available at ScienceDirect

Materials Science & Engineering C journal homepage: www.elsevier.com/locate/msec

Dual red-NIR luminescent EueYb heterolanthanide nanoparticles as promising basis for cellular imaging and sensing

T

⁎

Rustem R. Zairova,b, , Alexey P. Dovzhenkob, Anastasiia S. Sapunovaa, Alexandra D. Voloshinaa, Dmitry A. Tatarinova, Irek R. Nizameeva,c, Aidar T. Gubaidullina, Konstantin A. Petrova, Francesco Enrichid, Alberto Vomierod,e, Asiya R. Mustafinaa a

Arbuzov Institute of Organic and Physical Chemistry, FRC Kazan Scientific Center, Russian Academy of Sciences, Arbuzov str., 8, 420088 Kazan, Russian Federation Kazan (Volga region) Federal University, Kremlyovskaya str., 18, 420008 Kazan, Russian Federation c Kazan National Research Technical University named after A.N. Tupolev - KAI, 10, K. Marx str., Kazan 420111, Russian Federation d Division of Materials Science, Department of Engineering Sciences and Mathematics, Luleå University of Technology, SE-971 87 Luleå, Sweden e Department of Molecular Sciences and Nanosystems, Ca' Foscari University of Venice, via Torino 155, 30172 Venezia-Mestre, Italy b

A R T I C LE I N FO

A B S T R A C T

Keywords: Mixed ligand complexes Heterolanthanide nanoparticles Dual luminescence Energy transfer Cellular imaging Sensors Fluoroquinolones

The present work introduces ternary Ln(III) (Ln = Eu, Yb, Lu) complexes with thenoyltriflouro1,3-diketonate (TTA−) and phosphine oxide derivative (PhO) as building blocks for core-shell nanoparticles with both Eu(III)or Yb(III)-centered luminescence and the dual Eu(III)-Yb(III)-centered luminescence. Solvent-mediated self-assembly of the complexes is presented herein as the procedure for formation of EueLu, EueYb and YbeLu heterometallic or homometallic cores coated by hydrophilic polystyrenesulfonate-based shells. Steady state and time resolved Eu-centered luminescence in homolanthanide and heterolanthanide EueLu and EueYb cores is affected by Eu → Eu and Eu → Yb energy transfer due to a close proximity of the lanthanide blocks within the core of nanoparticles. The Eu → Yb energy transfer is highlighted to be the reason for the enhancement of the NIR Yb-centered luminescence. Efficient cellular uptake, low cytotoxicity towards normal and cancer cells, and sensing ability of EueYb nanoparticles on lomefloxacin additives via both red and NIR channels make them promising as cellular imaging agents and sensors.

1. Introduction Nanoparticles emitting in red and near infra-red (NIR) spectral range have gained great attention in recent decades due to fitting of red or NIR emission to the so-called biological window [1–5]. Literature data introduce fine examples of fluorescent polymeric organic nanoparticles exhibiting high cellular uptake behavior and low cytotoxicity. However, unique photophysical characteristics of lanthanide-centered luminescence exemplified by large Stokes shift, narrow intensive bands, long lifetimes of excited states provide very poor interference with fluorescence of biological background [6,7]. This, in turn, provides great advantage of lanthanide-centered luminescence versus organic fluorescence in cellular imaging and sensing of some biochemical processes in intra- or inter-cellular space [7–10]. It is also worth noting that factors controlling the intensity and wavelengths of lanthanide-centered luminescence are significantly different from those guiding the organic fluorescence [6,7]. It is, in particular, well-known that

wavelength of the lanthanide-centered luminescence greatly depends on its electronic structure, but remains unchanged in various ligand environment. The variation of the latter, in turn, provides a tool for enhancement of the luminescence. Red and near infra-red (NIR) luminescence of Eu(III) and Yb(III) compounds is of particular impact on their applicability in bioimaging and biosensing [6,7]. Transition of lanthanide compounds into nanoparticulate form can be regarded as most convenient route for bioanalytical application of lanthanide-centered luminescence [7–10]. Nanoparticles based on lanthanide oxides are excellent candidates for cellular contrast agents and photothermal therapy where powerful lasers are used as excitation light sources [11]. However, the efficacy of lanthanide oxide-based nanoparticles luminescence in aqueous dispersions is low, restricting their applicability in biosensing. Ligand-tometal energy transfer is well-known tool to sensitize metal-centered luminescence of lanthanide complexes in solutions and solids [8,12,13]. Variation of the structure of antenna ligand shifts the excitation

⁎ Corresponding author at: Arbuzov Institute of Organic and Physical Chemistry, FRC Kazan Scientific Center, Russian Academy of Sciences, Arbuzov str., 8, 420088 Kazan, Russian Federation. E-mail address: [email protected] (R.R. Zairov).

https://doi.org/10.1016/j.msec.2019.110057 Received 1 June 2019; Received in revised form 22 July 2019; Accepted 3 August 2019 Available online 05 August 2019 0928-4931/ © 2019 Elsevier B.V. All rights reserved.

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

water non-soluble Ln(III) complexes with corresponding ligands under intensive stirring (2200 rpm) from DMF to PSS-containing water solution. 0.5 mL of DMF solution of Ln(TTA)3PhO (C = 4.5 mM) was poured to 2.5 ml of PSS-containing water solution (1 g/L in 0.5 М solution of NaCl, рН 6.0). The ternary complex Ln(TTA)3PhO was obtained by preliminary mixing of Ln(TTA)3 and PhO in the DMF solutions at the 1:1 molar ratio. For the synthesis of heterolanthanide nanoparticles, EueYb ratio was controlled by molar ratios of [Eu(TTA)3PhO] and [Yb (TTA)3PhO] in DMF solution. The resulted colloidal solution has been sonicated for 30 min (sonication bath temperature was controlled to be 20 ± 2°С). Excess amounts of PSS were separated from colloids via centrifugation (10,000 rpm, 15 min) and supernatant drain. One layered PSS-coated aqueous colloids were obtained via redispersion (using sonication) in bidistilled water (equal to supernatant volume). Dynamic light scattering (DLS) measurements were performed using Malvern Mastersize 2000 particle analyzer operating with a HeeNe laser (633 nm) and emitting vertically polarized light as a light source. Transmission electron microscopy (TEM) images have been obtained with 120 (Carl Zeiss), Japan. Samples have been sonicated in water for 30 min and then dispersed on 200 mesh copper grids with continuous formvar support films. The images have been acquired at an accelerating voltage of 100 kV. EDS experiments were carried out on transmission electron microscope with energy-dispersive X-ray detector from Thermo Scientific. Luminescence spectra and lifetime measurements in visible range have been recorded using Hitachi F-7100 luminescent spectrometer. NIR photoluminescence spectra were recorded by an Edinburgh Instruments FLS980 Photoluminescence Spectrometer. A continuous-wave xenon lamp was used as excitation source for steady-state measurements, coupled to a double-grating monochromator for wavelength selection. Time-resolved PL emission was obtained in Multi Channel Scaling (MCS) mode, exciting the sample by a microsecond xenon flashlamp with pulse duration 1–2 μs and repetition frequency 10 Hz. The light emitted from the sample was collected by a double-grating monochromator and recorded by a photon counting R5509-73 photomultiplier tube cooled at −80 °C. Powder X-ray diffraction (PXRD) measurements were performed on a Bruker D8 Advance diffractometer equipped with Vario attachment and Vantec linear PSD, using Cu radiation (40 kV, 40 mA) monochromated by the curved Johansson monochromator (λ Cu Kα1 1.5406 Å). Roomtemperature data were collected in the reflection mode with a flat-plate sample. The samples were loaded on a standard zero diffraction silicon plate, which was kept spinning (15 rpm) throughout the data collection. Patterns were recorded in the 2Θ range between 3° and 90°, in 0.008° steps, with a step time of 0.1–4.0 s. Several diffraction patterns in various experimental modes were collected and summed for the sample. Processing of the obtained data performed using EVA software packages.

wavelength to lower energy range, restricting the absorption by living tissues and making indirect excitation effective. In this regard, lanthanide complexes are more promising building blocks for the synthesis of highly luminescent nanoparticles compared to inorganic lanthanide salts and oxides. Encapsulation of lanthanide complexes into nanoparticles can be performed by different techniques. The stimuli-mediated precipitation of the complexes with further hydrophilic coating of the nanoprecipitates provides convenient synthetic approach for the encapsulation. Solvent-mediated precipitation has been previously introduced as facile synthetic procedure for conversion of lanthanide complexes from molecular to nanoparticulate form with bright and stable in time lanthanide-centered luminescence [14]. Easy manipulations with the colloids including surface charge control through sequential phase separation and re-dispersion as well as high stability in biological background make them promising for biosensing and bioimaging applications [15–17]. Along with ligand-to-metal, metal-to-metal energy transfer occurs when the metal atoms are in close proximity within the nanoparticle [18]. Because the energy of the Eu3+ 5D2-7F0 transition is approximately twice as large as that of the Yb3+ 2F5/2-2F7/2 transition, energy transfer may be possible between Eu3+ and Yb3+ [19]. Furthermore, few reports regarding the down-conversion luminescence properties and energy-transfer mechanism for the Eu3+-Yb3+ system have been published thus far [20–22]. The present report introduces Eu(III), Yb(III) and Lu(III) ternary complexes with thenoyltriflouro1,3-diketonate (TTA−) and phosphine oxide derivative (PhO) as building blocks for development of monoand hetero-metallic polystyrenesulfonate-coated nanoparticles exhibiting Eu(III)- or Yb(III)-centered luminescence and dual Eu(III)-Yb (III)-centered luminescence in the aqueous colloids. Main factors affecting the luminescence of the building blocks in the colloids are discussed. The applicability of the heterometallic polystyrenesulfonate-coated nanoparticles in sensing is exemplified by the sensing of lomefloxacin as the representative of fluoroquinolone antibiotics through the dual redNIR luminescence response. It is worth noting that the energy transfer is revealed as the factor enhancing the sensing ability of the nanoparticles. The represented herein cytotoxicity and cellular uptake behavior of the heterolanthanide nanoparticles highlights the nanoparticles as promising basis for both cellular imaging and sensing. 2. Experimental section 2.1. Materials Eu(TTA)3·2H2O and Yb(TTA)3·2H2O were synthesized in accordance with the literature procedure [23]. Synthesis of Z-2-(2-hydroxy-4-methyl-5-chlorphenyl)-2-phenylethenyl-bis(3,4-dimethoxyphenyl) phosphine oxide (PhO) was previously reported [24]. Poly(sodium 4-styrenesulfonate) (PSS) (MWaverage = 70,000) (Acros Organics) and sodium chloride (Sigma-Aldrich) were used as received without further purification. N,N-dimethylformamide (DMF) (Acros Organics) was twice distilled over P2O5. DAPI and propidium iodide were purchased from Sigma. The M-HeLa clone 11 human, epithelioid cervical carcinoma, strain of HeLa, clone of M–HeLa; WI-38 VA-13 cell culture, subline 2RA (human embryonic lung) from the Type Culture Collection of the Institute of Cytology (Russian Academy of Sciences) and Chang liver cell line (Human liver cells) from N. F. Gamaleya Research Center of Epidemiology and Microbiology were used in the experiments.

2.3. Cytotoxicity assays Cytotoxic effects of the test compounds on human line cells were estimated by means of the multifunctional Cytell Cell Imaging system (GE Health Care Life Science, Sweden) using the Cell Viability Bio App which precisely counts the number of cells and evaluates their viability from fluorescence intensity data. Two fluorescent dyes that selectively penetrate the cell membranes and fluoresce at different wavelengths were used in the experiments. A low-molecular-weight 4′,6-diamidin-2phenylindol dye (DAPI) is able to penetrate intact membranes of living cells and color nuclei in blue, while high-molecular propidium iodide dye penetrates only damaged membranes of dead cells staining them in yellow. As a result, living cells are painted in blue and dead cells are painted in yellow. The cells were cultured in a standard Eagle's nutrient medium manufactured at the Chumakov Institute of Poliomyelitis and Virus Encephalitis (PanEco company) and supplemented with 10% fetal calf serum and 1% nonessential amino acids. The cells were plated into

2.2. Synthesis of the PSS-stabilized colloids Polyelectrolyte nanoparticles have been synthesized as a result of polyelectrolyte molecules adsorption on the surface of nanosized templates. Hard nanosized templates were obtained via precipitation of 2

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

a 96-well plate (Eppendorf) at a concentration of 1 × 105 cells/mL, 150 μL of medium per well, and cultured in a CO2 incubator at 37 °C. One day later, the 150 μL of the colloids at various dilutions were added to the wells seeded by the cells. The colloids were diluted by nutrient media immediately before their addition. The experiments were repeated three times. Intact cells cultured in parallel with experimental cells were used as a control. Flow cytometry measurements were performed for M-Hela cells after the incubation for 2,4 and 6 h by the colloids (0.09 and 0.18 mM) with the use of Guava easyCyte 8HT, USA, the untreated cells were applied as negative control. Fluorescent microscopy images of the M-HeLa cells both incubated by the EueYb nanoparticles for 24 h and stained with Hoechst 33342 (blue) was carried out using a Nikon Eclipse Ci-S fluorescence microscope (Nikon, Japan) at a magnification of 1000×. The cell nuclei are stained with Hoechst 33342. Three independent experiments and three replicates for each experiment were performed. The statistical analysis of the data was done by Mann-Whitney tests with the statistical significance at p < 0.05.

solutions. Previous reports on PSS-stabilized colloids based on different lanthanide complexes reveal specific core-shell morphology where nanosized precipitated complex species are coated by the polyelectrolyte [14]. The PSS molecules were found to be the best choice for colloid stabilization of the positively charged nanoprecipitates of Ln(III) chelates formed in the specific synthetic conditions. The previously estimated high stability of the PSS-coated colloids indicates that the polyanionic nature of PSS molecules is enough to provide efficient adsorption onto positively charged nanoprecipitates. Moreover, the poor complexation of the sulfonate groups with lanthanide ions restricts their stripping by the polyelectrolyte, thus, providing the stability of the nanoprecipitates. TEM images of dried colloids reveal the size of the nanoprecipitated complexes within 50–100 nm (Fig. 2). DLS measurements of the PSScoated colloids based on different lanthanide complexes indicate the similarity in their average size, which is within 150–200 nm (Fig. 4). This value is greater than the size revealed for the dried colloids (Fig. 2). The size discrepancy derives from the exterior hydrated layer of the PSS-coated colloids, where the coating by PSS molecules is greatly facilitated by both the counter-ions and the positively charged nanoprecipitates. The inequality of the lanthanide complexes packed into nanosized colloid species derives from high extent of the molecular blocks located at the surface of nanoparticles. This, in turn, results in specific activity of interfacial molecular blocks versus those located in the core zones of the nanoparticles. In particular, the τ1 of the complexes within the nanoparticles is greater than the same value of the molecular complexes in the solutions (Table 1). The tendency points to protecting effect of the exterior layer of the PSS-coated nanoparticles from the quenching effects of both oxygenated conditions and solvation or hydration of the complexes in solutions. This was previously reported for another lanthanide complexes converted from molecular to nanoparticulate forms [18,24]. Previously reported positive charge of the “naked” nanoprecipitates [27] points to the enhanced hydration of the interfacial lanthanide ions due to the ligand exchange processes provoked by both water molecules and –SO3− groups of the PSS-based layer. The time resolved measurements of PSS-[Yb(TTA)3PhO] colloids (Fig. S1) also revealed the two-exponential decay with τ1 = 8.6 and τ2 = 20 μs (Table S1). This fact confirms that the tendency revealed for PSS-[Eu(TTA)3PhO] is the same for the other both homo- and heterolanthanide counterparts. The Fig. 3 illustrates the uneven composition of the complexes in the PSS-coated colloids, highlighting the influence of the core and the shell on the luminescence properties. XRD is a powerful tool for the comparative analysis of [Ln (TTA)3PhO] with previously reported [Ln(TTA)3L] complexes [28–31] (discussed in detail within ESI (Figs. S2–S5)) and dried PSS-[Ln (TTA)3PhO] nanoparticles. PXRD analysis of dried PSS-[Ln(TTA)3PhO] nanoparticles indicates the presence of several broadened amorphouslike peaks in their diffractograms (Fig. 3b). The revealed XRD patterns show no signature of coherent scattering from large crystal domains in the samples. This, in turn, can be explained by either ultra-small level of the particle size, of the order of a few nanometers or amorphous nature of the nanoprecipitates. Taking into account rather wide size distribution presented in Fig. 2 both the nanostructuring and amorphous-like packing should be noted for explanation of the observed patterns. Thus, the applied synthetic conditions do not facilitate the formation of large single crystals, leading to precipitation of amorphous-like nano-sized particles. The [Eu(TTA)3PhO] and [Yb(TTA)3PhO] samples (Fig. 3) exhibit very similar PXRD pattern, which reflects the similarity in the parameters of their crystallographic cell, as reported for some isostructural Eu(TTA)3- and Yb(TTA)3-based ternary complexes [28–31]. This experimental evidence points to similarity in the packing modes of Eu- and Yb-complexes in the nanoprecipitates. This, in turn, derives from the isostructural ligand environment in complexes [Ln (TTA)3PhO], where Ln = Eu and Yb.

3. Results and discussion 3.1. Homometallic PSS-[Ln(TTA)3PhO] colloids Mixed ligand europium(III) complex, namely [Eu(TTA)3PhO], was proven to give better luminescence performance compared to [Eu (TTA)3·2H2O], where PhO ligand in the coordination sphere of europium(III) sensitizes Eu(III)-centered luminescence through both ligandto-metal energy transfer and expelling of water molecules from the inner sphere of lanthanide [25]. The synthesis of the PSS-[Eu (TTA)3PhO] colloids was previously described [14], although the present synthetic procedure was modified for better uniformity in size of homometallic PSS-coated colloids (for more details see the Experimental Section). In particular, water non-soluble brightly luminescent in red spectral region [Eu(TTA)3PhO] was quantitatively converted from DMF solutions to water dispersible colloidal form keeping the emission intensity. Intensive NIR luminescence peculiar for Yb(III)centered luminescence [12,13] was also registered in DMF solution for [Yb(TTA)3PhO]. Similar to [Eu(TTA)3PhO], [Yb(TTA)3PhO] was converted to aqueous PSS-[Yb(TTA)3PhO] colloids (for more details see the Experimental Section). Comparison of the luminescence spectra of [Ln (TTA)3PhO] (Ln = Eu or Yb) (Fig. 1a) in DMF and PSS-[Ln(TTA)3PhO] in aqueous solutions indicates resemblance in the spectral patterns for the both complexes (Fig. 1b, c). Excited state lifetime values of [Eu(TTA)3PhO] in both molecular (in DMF) and nanoparticulate (PSS-[Eu(TTA)3PhO] in water) forms are presented in Table 1. The mono-exponential decay for [Eu(TTA)3PhO] in the DMF solutions becomes two-exponential in PSS-[Eu(TTA)3PhO]. Typically, a two-exponential decay can be ascribed to the presence of different environments around the Eu-complexes, which may depend on its position inside or at the surface of the nanoparticles, where the presence of local defects and interface states may provide non-radiative recombination paths. Furthermore, the difference in the refraction index values inside and at the surface of the nanoparticles also plays a role on the radiative lifetime (τrad), according to Eq. (1), where n indicates the refractive index, I(5D0-7FJ)/I(5D0-7F1) is the ratio between the total integrated emission from the Eu 5D0 level to the 7FJ manifold (J = 0–6) and the integrated intensity of the transition 5D0-7F1 [26]: 5 7 ⎛ 1 ⎞ = 14.65 n3 I ( D0 ⟶ FJ ) 5 7 I ( D0 ⟶ F1) ⎝ τrad ⎠Eu ⎜

⎟

(1)

The calculated τrad-values (τ1 and τ2) providing the best fitting to the experimental decay data point to two forms of [Eu(TTA)3PhO] complexes in the nanoparticulate form. One of them (τ1) is much greater, while τ2 is somewhat smaller than the τ-value in the DMF 3

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

Fig. 1. Structure of Ln(TTA)3PhO (a). Normalized luminescence spectra of Ln(TTA)3PhO in DMF (1) and PSS-[Ln(TTA)3PhO] in H2O (2); Ln = Eu (b) and Ln = Yb (c). λex = 370 nm, C = 0.75 mM. (d, e) Schematic illustration of the synthesis of PSS-[Ln(TTA)3PhO] colloids from DMF solution of [Ln(TTA)3PhO] according to Mode I (d) Mode II (e).

3.2. Heterometallic colloids

Table 1 Excited state lifetimes of Eu(III) within [Eu(TTA)3PhO] and PSS-[Eu (TTA)3PhO]. τ1, ms [Eu(TTA)3PhO] in DMF Lu,Yb = 0 PSS-[Eu(TTA)3PhO] in water Lu,Yb = 0

0.44 0.57

A1 4498.10 1644.24

τ2, ms

0.34

Two different techniques have been applied in synthesis of the heterometallic colloids. The first technique is based on the mixing of both Yb(III) and Eu(III) complexes in DMF solutions with varied Eu:Yb atomic ratios with further pouring of mixed solutions to aqueous solutions of PSS (Fig. 1d). This technique opens the opportunity for the formation of heterometallic PSS-[(Eu/Yb)(TTA)3PhO] nanoparticles built from both Yb(III) and Eu(III) complexes. The second technique is based on separate addition of the DMF solutions of Yb(III) and Eu(III)

A2

1486.29

Fig. 2. TEM images of dried samples of PSS-[Yb(TTA)3PhO] (a, b), PSS-[Eu/Yb(TTA)3PhO] (d, e) colloids, and corresponding size distribution diagrams (c, f). 4

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

Fig. 3. Schematic representation of the structure of nanoparticles core and difference between surface and bulk [Eu(TTA)3PhO] (a). XRD measurements of: powder Eu(TTA)3 (1), PSS-[Eu(TTA)3 PhO] (2), PSS-[(Eu/Yb)(TTA)3 PhO] (3), PSS-[Yb(TTA)3 PhO] (4), powder Yb(TTA)3 (5) (b).

environment as the prerequisite for formation of solid solutions [36,37]. The formation of heterometallic solid solution resulting in the co-precipitation of Eu- and Yb-complexes is visible in PXRD spectra (Fig. 3b). In particular, the angular maxima of the diffuse peaks for PSS[Eu(TTA)3PhO] and PSS-[Yb(TTA)3PhO] are within 7–9° and 19–21° of 2θ angles correspondingly, while the diffusion peak of the EueYb colloids occupies an intermediate position between the similar peaks of PSS-[Eu(TTA)3PhO] and PSS-[Yb(TTA)3PhO]. This shift of the diffuse peak maximum acquires a completely definite meaning in the case of EueYb colloids indicating the formation of the nanostructured system which is the solid solution of Eu(TTA)3 and Yb(TTA)3. Moreover, the heterometallic nature of the dried EueYb colloids is manifested by the peaks corresponding to Yb(III) and Eu(III) component in the EDS spectra (Figs. S19–S21). The effect of such co-precipitation on photophysical properties of the heterometallic colloids is worth discussing in detail. The 1:1 molar ratio of the complexes in the heterometallic colloids is the content providing most enhanced effect of the Yb- or Lu-component on τ-values of Eu(III)-centered luminescence (Table 2). In particular, the increase in τ1 and τ2 values in the EueLu colloids from 0.57 to 0.62 ms and 0.35 to 0.38 ms, correspondingly, is explained by the above mentioned dilution effect of the non-luminescent component ([Lu(TTA)3PhO]) on the Eu(III) luminescence. Moreover, the similar tendency is observed under the decrease in Eu-content in the EueYb colloids synthesized by the Mode II. These results indicate that the selfquenching in the homolanthanide colloids tends to decrease at the smaller concentrations. The Yb-component should provide similar effect on the Eu-centered luminescence in the EueYb colloids. However, the corresponding τ-values are 0.55 and 0.31 ms, which is much lower than the above mentioned values in the EueLu colloids. This result points to the quenching of Eu(III)-centered luminescence in the EueYb colloids through Eu → Yb energy transfer. The spectra presented in Fig. 5 confirm the quenching of Eu-luminescence in the EueYb colloids. It is worth anticipating an enhancement of the Yb-centered luminescence by Eu → Yb energy transfer. Indeed, the Yb-centered luminescence is only slightly stronger for the EueYb colloids versus those synthesized by separate addition of Eu- and Yb-components (Fig. 5). This result points to another factors beyond the energy transfer affecting Yb-centered luminescence in the EueYb colloids. It is worth noting that “exterior” [Ln(TTA)3PhO] complexes exhibit greater dechelation (Fig. 3a) versus the “inner” complexes. Thus, the predominant exterior location of the Yb-blocks in the EueYb colloids can be assumed as the factor affecting the Yb-centered luminescence, while the reasons for this are not clear from the presented data. It is worth noting that similar with other lanthanide-containing nanoparticles [6–9] the Eu(III)-centered luminescence of the colloids reveals rather small degradation from photobleaching which is evident from the insignificant intensity decrease under the irradiation of the samples for 1 h (Fig. S6). The poor photobleaching of the colloids is the prerequisite for their application in sensing and bioimaging.

complexes into the aqueous solution of PSS. This, in turn, favors formation of separate monolanthanide nanoparticles, e.g. PSS-[Eu (TTA)3PhO], PSS-[Yb(TTA)3PhO], and PSS-[Lu(TTA)3PhO] (Fig. 1e) in molar concentrations according to Fig. 4. Diffusing in water apart from each other, monolanthanide nanoparticles have low probability (if any) for interacting energetically. EueLu colloids with varied Eu:Lu atomic ratios were also synthesized, and their steady state and time-resolved luminescence spectra were recorded in order to reveal the effect of the concentration-induced quenching [32–35] on Eu(III)-centered luminescence of both homometallic and heterometallic colloids. The size, electrokinetic potential (ζ) and polydispersity index (PDI) values evaluated from the DLS measurements and TEM images of the synthesized colloids in water are collected in Fig. 4 and presented as size distribution diagrams in Fig. 2 for dry samples. It is worth noting that the presented data (Fig. 4) reveal no significant difference between EueLu, EueYb, YbeLu colloids and their homometallic counterparts. Moreover, the colloids are enough hydrophilic to remain without any detectable precipitation for three days at least (Fig. S6). This fact significantly facilitates any manipulations with the colloids which is of great impact on their further practical applicability. The time-resolved luminescence measurements recorded for EueYb colloids (Figs. S7–S18) similar with the Eu-colloids reveal the two-exponential decay which is ascribed by the two lifetime values. The latter are presented in Table 2 along with the fitting parameters A1(2). Comparison of the τ1(2)-values (Table 2) in PSS-[(EueLu)(TTA)3PhO] with those measured in PSS-[Eu(TTA)3PhO] reveals detectable increase on going from the homo- to heterometallic colloids when [Eu(TTA)3PhO] is mixed with [Lu(TTA)3PhO] in one DMF solution (Mode I). The socalled concentration-induced quenching common for the lanthanide complexes tightly packed into nanosized colloids [18] explains the greater quenching of the Eu(III)-centered luminescence in the homolanthanide versus heterolanthanide (EueLu) colloids. The τ1(2)-values of Eu(III)-centered luminescence in EueYb heterometallic colloids synthesized by the procedure designated as Mode I reveal the tendency to decrease compared to the values measured in both PSS-[(EueLu) (TTA)3PhO] and PSS-[Eu(TTA)3PhO] (Table 1). It is worth noting that the quenching effect of Eu-to-Yb energy transfer is partly masked by the opposite effect arisen from the dilution of the Eu(III) complexes by the Yb(III) ones. Smaller effect of the Yb-component on the τ1(2)-values of Eu(III)-centered luminescence is observed for the colloids synthesized by means of the separate addition of the components (Mode II in Table 2) versus the EueYb colloids synthesized by Mode I. It is worth noting that the synthetic procedure designated as Mode I facilitates joining of both Eu- and Yb-components in each nanoparticle versus the Mode II restricting the formation of heterometallic nanoparticles. This difference indicates that formation of EueYb nanoprecipitates in Mode I is more favorable than formation of the homometallic nanoparticles. This tendency is supported by well-known regularities, which claim the similarity in electronic structure of metal ions and isostructural ligand 5

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

Fig. 4. Hydrodynamic diameters, polydispersity indices and electrokinetic potentials measured by DLS in homometallic colloids (PSS-[Ln(TTA)3PhO], where Ln = Eu, Lu, Yb) and their heterometallic EueLu, EueYb, YbeLu counterparts under the varied Eu:Lu, Eu:Yb, Yb:Lu ratios at CLn = 0.75 mM.

6

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

3.3. Sensing properties of the EueYb colloids

Table 2 Excited state lifetimes (τ1(2)) of Eu(III)-centered luminescence in heterolanthanide EueLu and EueYb colloids at various Eu:Lu and Eu:Yb ratios synthesized by Mode I and Mode II procedures. A1(2) defines contribution of each exponent in biexponential deconvolution.

Mode 1

Eu-Yb

Eu-Lu

Mode 2

Eu-Yb

χEu

τ1, msa

A1

τ2, msa

A2

0 0.25 0.5 0.75 1 0 0.25 0.5 0.75 1 0 0.25 0.5 0.75 1

– 0.56 0.55 0.57 0.57 – 0.59 0.62 0.56 0.57 – 0.62 0.61 0.57 0.57

– 456.39 804.84 1475.10 1665.02 – 947.18 943.36 1828.35 1644.24 – 682.16 1503.00 1840.09 1563.66

– 0.31 0.31 0.33 0.36 – 0.34 0.38 0.34 0.34 – 0.37 0.36 0.34 0.35

– 394.58 582.67 1201.64 2280.52 – 842.42 1662.64 1679.88 1486.28 – 953.72 1568.77 1491.62 1894.17

Previous studies on luminescence response of PSS-[Eu(TTA)3PhO] on fluoroquinolones in aqueous solutions [17] suggest a way for practical applicability of PSS-[Eu/Yb(TTA)3PhO] colloids. Moreover, the presence of [Yb(TTA)3PhO] complex provides additional opportunity for sensing fluoroquinolones via NIR channel. Fig. 6 shows the response of Eu- and Yb-centered luminescence of the EueYb colloids on various concentrations of lomefloxacin, which is the representative of fluoroquinolone antibiotics (FQ) well-known for high antibacterial activity. The luminescence response is presented as I/I0, where I0 and I are the intensities of the main bands of Yb- and Eu-centered luminescence at 980 nm and 612 nm, correspondingly, measured before and after the addition of the FQ. The I/I0 plotted versus the FQ concentration are presented for both heterometallic and homometallic colloids in order to compare the FQ-induced luminescence response of both Eu- (Fig. 6a) and Yb-centered (Fig. 6b) luminescence. Before discussing the FQ-induced changes in the luminescence of the EueYb colloids it is worth noting both similarity and difference in the luminescence response of Eu- and Yb-components of PSS-[Eu (TTA)3PhO] and PSS-[Yb(TTA)3PhO] colloids. Both Eu(III)- and Yb(III)centered luminescence exhibit the concentration-induced quenching in the solutions of the FQ. This, in turn, points to substitution of the antenna-ligands (TTA- and PhO) or even stripping the Eu(III) or Yb(III) ions through their complex formation with the FQ molecules as the predominant processes. However, the decrease in I/I0 values is less pronounced for the Eu-centered luminescence versus the Yb-centered one (Fig. 5). The difference can be explained by the greater contribution of ternary complex formation, when the FQ molecule is coordinated by substituting the water molecule from the coordination sphere of [Eu (TTA)3PhO]. The ternary complex formation at smaller FQ concentrations was revealed for PSS-[Eu(TTA)3PhO] colloids [18]. However, at higher FQ concentrations both substitution of the antenna-ligands (TTA− and PhO) and stripping the Eu(III) ions through their complex formation with the FQ molecules become the predominant processes [18]. The greater decrease in I/I0 values of Yb-luminescence for PSS[Yb(TTA)3PhO] colloids (Fig. 5) points to insignificant contribution of the ternary complex formation and predominant quenching of the luminescence arisen from the above mentioned ligand and ion exchange processes. It is worth noting that monitoring of the Yb-centered luminescence for PSS-[Yb(TTA)3PhO] colloids provides 3 times lower detection value versus the monitoring of the Eu-luminescence for the Eu-counterparts. The lower detection limit (LOD) of lomefloxacin under the monitoring of the NIR luminescence of EueYb colloids was calculated from the additional luminescence measurements (Fig. S22 and calculation

a

The standard deviations are < 1%. For all fittings adj-R2 values are 0.99995 or higher.

Fig. 5. Luminescence spectra of the EueYb colloids at 1:1 Eu:Yb ratio (1) and the colloids those synthesized by separate addition of Eu- and Yb-components at the 1:1 ratio 1 (2). λex. = 391 nm, CLn = 0.75 mM.

Fig. 6. I/I0 monitored at 612 nm (λex. = 370 nm) (a) for PSS-[Eu(TTA)3PhO] (1) and EueYb colloids at the 1:1 ratio (2); I/I0 monitored at 978 nm (λex. = 390 nm) (b) for PSS-[Yb(TTA)3PhO] (1) and EueYb colloids at the 1:1 ratio (2) at various FQ concentrations, CLn = 0.025 mM. 7

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

incubation by EueYb colloids for 24 h. The corresponding IC50–values for M-HeLa and Chang liver are very similar with the previously reported values for PSS-coated Tb(III)-colloids [16], although the greater cytotoxic effect is revealed for WI-38 (Table 3, Fig. S23). The reason for the specific cytotoxic effect on the cells of WI-38 line is unclear at the moment, and further studies required for its recognition lye out of the present work scope. The flow cytometry measurements were performed with the use of M-HeLa line in order to reveal the time duration required for the cell internalization of EueYb nanoparticles. The measurements (Fig. S24) reveal 6 h for the greatest fluorescence of the incubated M-HeLa cells, although concentration of the nanoparticles also affects their cell internalization kinetics. The fluorescence microscopy images of the M-HeLa cells incubated by the EueYb nanoparticles were performed to confirm their cell internalization (Fig. 7) and reveal their ability to mark the cells by the red Eu(III)-centered luminescence. Dynamics of cell uptake can be seen at 2, 4, and 6 h (Fig. S25). The cell nuclei were stained by Hoechst 33342 intercalating dye DNA (blue spot) in order to evaluate the nanoparticles localization within the cell organelles. The images presented in Fig. 7 highlight the EueYb nanoparticles as rather efficient cellular contrast agents with the ability to stain the cells by red fluorescence. The images point to predominant localization of the nanoparticles within the cell cytoplasm without internalization into the cell nuclei, although, an accurate determination of localization of the nanoparticles within cell organelles requires more detailed studies lying out of the present work scope. Nevertheless, the efficient staining of the cell cytoplasm resulted from the cell internalization of the nanoparticles is a prerequisite for sensing of fluoroquinolone antibiotics through the Eu(III)-centered luminescence of the nanoparticles.

Table 3 IC50 (mM) of EueYb colloids on human cell lines. Test compounds

IC50 (mM) Human cell lines

Eu-Yb colloids

M-HeLa

Chang liver

WI-38

0.09

0.09

0.04

The experiments were repeated three times.

details are in SI) performed within 0–10−5 M of lomefloxacin. The LOD at the level of 1.9 μM is not the smallest among the known values [38]. Nevertheless, the improvement of the lower detection limit will be done in future as it has been previously reported for another PSS-coated Eucolloids [17]. Comparison of the luminescence response of the heterometallic and homometallic colloids reveals the difference between them. The I/I0 versus FQ concentration profile of Yb-centered luminescence is characterized by more sharp decrease when measured for the EueYb than for PSS-[Yb(TTA)3PhO] colloids. The opposite tendency is evident under the comparison of Eu-centered luminescence for the heterometallic and homometallic colloids. In particular, the increase in I/I0 values is more pronounced for the EueYb versus PSS-[Eu(TTA)3PhO] colloids. The revealed tendencies can be explained by the neighborhood of the Eu- and Yb-blocks in the EueYb colloids. In particular, the FQinduced degradation of Yb-blocks should enhance the Eu-centered luminescence due to decreasing quenching through Eu → Yb energy transfer. Thus, the mutual interference between the Eu- and Yb-blocks is the reason for detectable changing in the sensing properties of the heterolanthanide colloids versus their homometallic counterparts.

4. Conclusions 3.4. Cytotoxicity, cellular uptake and cellular contrasting ability of EueYb colloids

The present work introduces facile synthetic approach to make hydrophilic heterometallic nanoparticles with both Eu(III)- or Yb(III)centered luminescence and the dual Eu(III)-Yb(III)-centered luminescence with the use of the isostructural 1,3-diketonate complexes of Ln (III) (Ln = Eu, Yb, Lu) as the lanthanide-based building blocks of the nanoparticles. The difference in photophysical properties of homometallic and heterometallic colloids reveals restricted or enhanced energy transfer between the lanthanide-blocks self-assembled within heterometallic nanoparticles as the reason for tuning their photophysical properties. In particular, the concentration induced quenching common for the homometallic nanoparticles with Eu(III)-centered luminescence can be significantly decreased by the non-luminescent isostructural Lu(III) complex self-assembled with the luminescent Eu (III) counterparts in the Eu-Lu-based colloids. The quenching of Eu(III)centered luminescence in the EueYb nanoparticles due to Eu → Yb energy transfer is accompanied by increase in the NIR luminescence of Yb(III) complexes. The comparative analysis of the substrate

Nanoparticulate lanthanide complexes are well-known basis for cellular imaging and subcellular sensing [6–12]. Our previous reports [16,19] are worth noting for revealing the potential of the PSS-coated Tb(III) complexes for cellular imaging resulted from their low cytotoxicity and efficient cell internalization. A similarity in the core-shell architecture of the developed and previously reported colloids is a reason for anticipating low cytotoxicity of EueYb colloids. Poor leaching of Eu(III) ions from the colloids in aCSF (artificial cerebrospinal fluid. Contains sodium, calcium, magnesium, and potassium cations together with phosphate, hydrocarbonate, and chloride anions) was previously demonstrated for the PSS-coated Eu-colloids [39] as an example of stability of the EueYb colloids in biological background. The cell viability of the three well-known cell lines which are M-HeLa clone 11 human, WI-38 VA-13 cell culture, subline 2RA (human embryonic lung) and Chang liver cell line was determined after their

Fig. 7. Fluorescence microscopy images of the M-HeLa cells incubated by the EueYb nanoparticles for 6 h (C = 0.18 mM). 8

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

(lomefloxacin)-induced response of Eu- and Yb-centered luminescence monitored in Eu-, Yb- and Eu-Yb-based nanoparticles reveals greater sensitivity of heterometallic nanoparticles versus the homometallic ones. The results highlight the impact of Eu → Yb energy transfer on both photophisical and sensing properties of EueYb colloids. Cell viability measurements of both normal (Chang liver, WI-38) and cancer cells (M-HeLa) incubated by EueYb nanoparticles indicate rather low cytotoxic effect on WI-38 and M-HeLa, while the greater effect on Chang liver cells. The flow cytometry measurements reveal the time duration (6 h) required for efficient internalization of EueYb nanoparticles into the M-HeLa cells. Fluorescent microscopy images of the M-HeLa cells incubated by EueYb nanoparticles highlight them as promising candidates for cellular imaging. These results along with the sensing ability of EueYb nanoparticles on lomefloxacin additives via both red and NIR channels make them promising basis for sensing.

[11] A. Zatsepin, Y. Kuznetsova, No title, Appl. Mater. Today 12 (2018) 34–42. [12] S.V. Eliseeva, J.C.G. Bünzli, Lanthanide luminescence for functional materials and bio-sciences, Chem. Soc. Rev. 39 (2010) 189–227, https://doi.org/10.1039/ b905604c. [13] S.J. Butler, D. Parker, Anion binding in water at lanthanide centres: from structure and selectivity to signalling and sensing, Chem. Soc. Rev. 42 (2013) 1652–1666, https://doi.org/10.1039/c2cs35144g. [14] A. Mustafina, R. Zairov, M. Gruner, A. Ibragimova, D. Tatarinov, I. Nizameyev, N. Nastapova, V. Yanilkin, M. Kadirov, V. Mironov, A. Konovalov, Synthesis and photophysical properties of colloids fabricated by the layer-by-layer polyelectrolyte assembly onto Eu(III) complex as a core, Colloids Surf. B: Biointerfaces 88 (2011) 490–496, https://doi.org/10.1016/j.colsurfb.2011.07.039. [15] R. Zairov, A. Solovieva, N. Shamsutdinova, S. Podyachev, M. Shestopalov, T. Pozmogova, S. Miroshnichenko, A. Mustafina, A. Karasik, Polyelectrolyte-coated ultra-small nanoparticles with Tb(III)-centered luminescence as cell labels with unusual charge effect on their cell internalization, Mater. Sci. Eng. C 95 (2019) 166–173, https://doi.org/10.1016/j.msec.2018.10.084. [16] R.R. Zairov, R.N. Nagimov, S.N. Sudakova, D.V. Lapaev, V.V. Syakaev, G.S. Gimazetdinova, A.D. Voloshina, M. Shykula, I.R. Nizameev, A.I. Samigullina, A.T. Gubaidullin, S.N. Podyachev, A.R. Mustafina, Polystyrenesulfonate-coated nanoparticles with low cytotoxicity for determination of copper(II) via the luminescence of Tb(III) complexes with new calix[4]arene derivatives, Microchim. Acta 185 (2018) 4–13, https://doi.org/10.1007/s00604-018-2923-2. [17] N. Davydov, R. Zairov, A. Mustafina, V. Syakayev, A. Konovalov, M. Mustafin, Determination of fluoroquinolone antibiotics through the fluorescent response of Eu (III) based nanoparticles fabricated by layer-by-layer technique, Anal. Chim. Acta 784 (2013) 65–71, https://doi.org/10.1016/j.aca.2013.04.054. [18] R. Zairov, A. Mustafina, N. Shamsutdinova, I. Nizameev, B. Moreira, S. Sudakova, S. Podyachev, A. Fattakhova, G. Safina, I. Lundstrom, A. Gubaidullin, A. Vomiero, High performance magneto-fluorescent nanoparticles assembled from terbium and gadolinium 1,3-diketones, Sci. Rep. 7 (2017), https://doi.org/10.1038/srep40486. [19] J. Liao, D. Zhou, S. Liu, H.R. Wen, X. Qiu, J. Chen, Efficient near-infrared emission in Eu3+-Yb3+-Y 3+ tri-doped cubic ZrO2 via down-conversion for silicon solar cells, Phys. B Condens. Matter 436 (2014) 59–63, https://doi.org/10.1016/j.physb. 2013.10.043. [20] X. Wei, J. Zhao, W. Zhang, Y. Li, M. Yin, Cooperative energy transfer in Eu3+, Yb3+ codoped Y2O3 phosphor, J. Rare Earths 28 (2010) 166–170, https://doi.org/ 10.1016/S1002-0721(09)60073-9. [21] M.K. Lau, J.H. Hao, Near-infrared quantum cutting in Eu3+-Yb3+ co-doped YAG through downconversion for silicon solar cell, Energy Procedia 15 (2012) 129–134, https://doi.org/10.1016/j.egypro.2012.02.015. [22] Q. Luo, X. Qiao, X. Fan, H. Fu, J. Huang, Y. Zhang, B. Fan, X. Zhang, Sensitized Yb3+luminescence of Eu3+/Yb3+-codoped fluorosilicate glass ceramics, J. Am. Ceram. Soc. 95 (2012) 1042–1047, https://doi.org/10.1111/j.1551-2916.2011. 04932.x. [23] L.R. Melby, N.J. Rose, E. Abramson, J.C. Caris, Synthesis and fluorescence of some trivalent lanthanide complexes, J. Am. Chem. Soc. 86 (1964) 5117–5125, https:// doi.org/10.1021/ja01077a015. [24] R.R. Zairov, D.A. Tatarinov, N.A. Shamsutdinova, A.R. Mustafina, I.K. Rizvanov, V.V. Syakaev, V.F. Mironov, A.I. Konovalov, Polymethoxyphenyl-substituted [2-(5chloro-2-hydroxy-4-methylphenyl)-2-phenylvinyl]phosphine oxides: synthesis and complexation with Eu(TTA)3, Russ. J. Org. Chem. 50 (2014) 547–551, https://doi. org/10.1134/S1070428014040186. [25] H. Iwanaga, Investigation of strong photoluminescence and highly soluble Eu(III) complexes with phosphine oxides and β-diketonates, J. Lumin. 200 (2018) 233–239, https://doi.org/10.1016/j.jlumin.2018.03.070. [26] C. Malba, U.P. Sudhakaran, S. Borsacchi, M. Geppi, F. Enrichi, M.M. Natile, L. Armelao, T. Finotto, R. Marin, P. Riello, A. Benedetti, Structural and photophysical properties of rare-earth complexes encapsulated into surface modified mesoporous silica nanoparticles, Dalton Trans. 43 (2014) 16183–16196, https:// doi.org/10.1039/c4dt00760c. [27] R. Zairov, G. Khakimullina, S. Podyachev, I. Nizameev, G. Safiullin, R. Amirov, A. Vomiero, A. Mustafina, Hydration number: crucial role in nuclear magnetic relaxivity of Gd(III) chelate-based nanoparticles, Sci. Rep. 7 (2017), https://doi.org/ 10.1038/s41598-017-14409-6. [28] R.R. Zairov, A.V. Yagodin, M. Khrizanforov, A.G. Martynov, I.R. Nizameev, V.V. Syakaev, A.T. Gubaidullin, T. Kornev, O. Kaman, Y.H. Budnikova, Y.G. Gorbunova, A.R. Mustafina, Unusual magnetic relaxation behavior of hydrophilic colloids based on gadolinium(III) octabutoxyphthalocyaninate, J. Nanopart. Res. 21 (2019), https://doi.org/10.1007/s11051-018-4455-4. [29] V. Vallet, A. Fischer, Z. Szabó, I. Grenthe, The structure and bonding of Y, Eu, U, Am and Cm complexes as studied by quantum chemical methods and X-ray crystallography, Dalton Trans. 39 (2010) 7666–7672, https://doi.org/10.1039/b926508b. [30] S.K. Cary, M. Livshits, J.N. Cross, M.G. Ferrier, V. Mocko, B.W. Stein, S.A. Kozimor, B.L. Scott, J.J. Rack, Advancing understanding of the +4 metal extractant thenoyltrifluoroacetonate (TTA-); synthesis and structure of MIVTTA4(MIV = Zr, Hf, Ce, Th, U, Np, Pu) and MIII(TTA)4-(MIII = Ce, Nd, Sm, Yb), Inorg. Chem. 57 (2018) 3782–3797, https://doi.org/10.1021/acs.inorgchem.7b03089. [31] M. Atanassova, V. Lachkova, N. Vassilev, B. Shivachev, S. Varbanov, I. Dukov, Effect of p-tert-butylcalix[4]arene fitted with phosphinoyl pendant arms as synergistic agent in the solvent extraction of trivalent lanthanoids with 4,4,4-trifluoro-1-(2-thienyl)-1,3-butanedione and structural study of solid complexes by IR, NMR and X-ra, Polyhedron 27 (2008) 3306–3312, https://doi.org/10.1016/j.poly. 2008.07.015. [32] J. Li, J.G. Li, J. Li, S. Liu, X. Li, X. Sun, Y. Sakka, Development of Eu3+activated monoclinic, perovskite, and garnet compounds in the Gd2O3-Al2O3phase diagram

Acknowledgement The authors gratefully acknowledge the Assigned SpectralAnalytical Center of FRC Kazan Scientific Center of RAS. R.Z. and A.V. acknowledge the Swedish Institute for partial support (NIR luminescence measurements) through the VISBY program. A.V. acknowledges the ÅFORSK Foundation for financial support for equipment. A.V. acknowledges the Kempe and Knut & Alice Wallenberg Foundation for partial funding. Sensing properties of the EueYb colloids were studied in KFU. Declaration of competing interest There are no conflicts of interest to declare. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.msec.2019.110057. References [1] X. Chen, G. Zhou, X. Peng, J. Yoon, Biosensors and chemosensors based on the optical responses of polydiacetylenes, Chem. Soc. Rev. 41 (2012) 4610–4630, https://doi.org/10.1039/c2cs35055f. [2] L. Mao, Y. Liu, S. Yang, Y. Li, X. Zhang, Y. Wei, Recent advances and progress of fluorescent bio-/chemosensors based on aggregation-induced emission molecules, Dyes Pigments 162 (2019) 611–623, https://doi.org/10.1016/j.dyepig.2018.10. 045. [3] X. Zhang, K. Wang, M. Liu, X. Zhang, L. Tao, Y. Chen, Y. Wei, Polymeric AIE-based nanoprobes for biomedical applications: recent advances and perspectives, Nanoscale 7 (2015) 11486–11508, https://doi.org/10.1039/c5nr01444a. [4] X. Zhang, X. Zhang, B. Yang, Y. Zhang, Y. Wei, A new class of red fluorescent organic nanoparticles: noncovalent fabrication and cell imaging applications, ACS Appl. Mater. Interfaces 6 (2014) 3600–3606, https://doi.org/10.1021/am4058309. [5] X. Zhang, X. Zhang, B. Yang, J. Hui, M. Liu, Z. Chi, S. Liu, J. Xu, Y. Wei, Novel biocompatible cross-linked fluorescent polymeric nanoparticles based on an AIE monomer, J. Mater. Chem. C 2 (2014) 816–820, https://doi.org/10.1039/ c3tc31852d. [6] Q. Liu, X. Zou, Y. Shi, B. Shen, C. Cao, S. Cheng, W. Feng, F. Li, An efficient dyesensitized NIR emissive lanthanide nanomaterial and its application in fluorescence-guided peritumoral lymph node dissection, Nanoscale 10 (2018) 12573–12581, https://doi.org/10.1039/C8NR02656D. [7] J.C.G. Bünzli, Lanthanide light for biology and medical diagnosis, J. Lumin. 170 (2016) 866–878, https://doi.org/10.1016/j.jlumin.2015.07.033. [8] S. Comby, E.M. Surender, O. Kotova, L.K. Truman, J.K. Molloy, T. Gunnlaugsson, Lanthanide-functionalized nanoparticles as MRI and luminescent probes for sensing and/or imaging applications, Inorg. Chem. 53 (2014) 1867–1879, https://doi.org/ 10.1021/ic4023568. [9] A. Mukhametshina, A. Petrov, S. Fedorenko, K. Petrov, I. Nizameev, A. Mustafina, O. Sinyashin, Luminescent nanoparticles for rapid monitoring of endogenous acetylcholine release in mice atria, Luminescence (2018) 1–6, https://doi.org/10. 1002/bio.3450. [10] A.R. Mukhametshina, S.V. Fedorenko, A.M. Petrov, G.F. Zakyrjanova, K.A. Petrov, L.F. Nurullin, I.R. Nizameev, A.R. Mustafina, O.G. Sinyashin, Targeted nanoparticles for selective marking of neuromuscular junctions and ex vivo monitoring of endogenous acetylcholine hydrolysis, ACS Appl. Mater. Interfaces (2018), https://doi.org/10.1021/acsami.8b04471.

9

Materials Science & Engineering C 105 (2019) 110057

R.R. Zairov, et al.

[33]

[34]

[35] [36]

Svoistva Elementov Periodicheskoi Systemy (Metal Chemistry Properties of the Elements of the Periodic System), Moscow: Nauka, 1966. [37] W.B. Pearson, A Handbook of Lattice Spacing and Structures of Metals and Alloys, Pergamon Press, London, New York, 1958. [38] W. Kong, X. Yang, M. Yang, H. Zhou, Z. Ouyang, M. Zhao, Photoluminescent nanosensors capped with quantum dots for high-throughput determination of trace contaminants: strategies for enhancing analytical performance, TrAC Trends Anal. Chem. 78 (2016) 36–47, https://doi.org/10.1016/j.trac.2015.07.013. [39] R.R. Zairov, N. Shamsutdinova, А. Fattakhova, А. Pyataev, А. Abdullin, А. Gerasimov, А. Gubaidullin, А. Mustafina, Nanoparticles based on gadolinium(iii) and europium(iii) complexes for biovisualization, Russ. Chem. Bull. 65 (2016) 1325–1331, https://doi.org/10.1007/s11172-016-1456-2.

as efficient red-emitting phosphors, J. Solid State Chem. 206 (2013) 104–112, https://doi.org/10.1016/j.jssc.2013.08.003. D.F. Parra, A. Mucciolo, H.F. Brito, Green luminescence system containing a Tb3+β-diketonate complex doped in the epoxy resin as sensitizer, J. Appl. Polym. Sci. 94 (2004) 865–870, https://doi.org/10.1002/app.20771. Z. Wang, J.G. Li, Q. Zhu, X. Li, X. Sun, Sacrificial conversion of layered rare-earth hydroxide (LRH) nanosheets into (Y1-xEux)PO4nanophosphors and investigation of photoluminescence, Dalton Trans. 45 (2016) 5290–5299, https://doi.org/10.1039/ c5dt01983d. H.-W. Song, Recent developments on rare earth doped oxide nanocrystals, Chinese J. Lumin. 28 (2008) 921–936. R.S. Kornilov, I.I., Matveeva, N.M., Pryakhina, L.I., Polyakova, Metallokhimicheskie

10