Polystyrene (PS)-diphenyloxazole (PPO) nanoparticles with attached cross-linked poly-N-isopropylacrylamide (PNIPAM) chains were obtained resulting in PS-PPO-PNIPAM hybrid nanosystems (NS). Fluorescence spectra of chlorin e added to PS-PPO-PNIPAM hybrid NS revealed electronic excitation energy transfer (EEET) from PS matrix and encapsulated PPO to chlorin e . EEET efficiency increased strongly during 1 h after chlorin e 6 6 addition, indicating that uptake of chlorin e by PNIPAM part of hybrid NS still proceeds during this time. Heating of PS-PPO-PNIPAM-chlorin e NS from 21 to 39 °C results in an enhancement of EEET efficiency; this is consistent with PNIPAM conformation transition that reduces the distance between PS-PPO donors and chlorin e acceptors. Meanwhile, a relatively small part of chlorin e present in the solution is bound 6 6 by PNIPAM; thus, further studies in this direction are necessary. Keywords: Styrene nanoparticles, Stimuli-responsive materials, PNIPAM, Diphenyloxazole, Conformation transition, Chlorin e , Electronic excitation energy transfer, Radiodynamic therapy Background optimal for EEET; chemical conjugation [2, 3], electro- The main disadvantage of the photodynamic therapy of static attraction [8, 12], surfactant , or polymer shell cancer is the low depth of the excitation beam penetra-  could be mentioned. Earlier, in the frames of design- tion into the tissue . Thus, radiodynamic therapy ap- ing nanosystems (NS) for X-ray excited sensitizing of proach to cancer treatment (where sensitizer could be singlet oxygen, we studied EEET in polystyrene (PS)-di- efficiently excited with the X-rays able to penetrate deep phenyloxazole (PPO)-chlorin e NS, where photosensi- into the body) was proposed  and is intensively stud- tizer chlorin e was bound to PS-PPO nanoparticle ied in the last years [3–5]; one of the research scopes is (which can be used as scintillator [13, 14]) via surfactant the development of sensitizers that generate singlet oxy- (sodium dodecylsulphate) shell . gen upon X-ray excitation [5–8]. The key process in Poly(N-isopropylacrylamide) (PNIPAM) belongs to such X-ray sensitizer is the electronic excitation energy stimuli-responsive materials that change their properties transfer (EEET) between its scintillating and sensitizing in response to internal or external stimulus . Linear components [2, 6, 9–11]. Another important component PNIPAM is known to undergo conformational transition of the mentioned X-ray sensitizer is the way of keeping upon heating, i.e., the polymer shrinks (due to becoming scintillating and sensitizing parts together at the distance hydrophobic and thus expelling water molecules) at the temperatures over the lower critical solution * Correspondence: email@example.com temperature (LCST) that equals 32 °C for linear Faculty of Physics, Taras Shevchenko National University of Kyiv, PNIPAM . Considerable decrease in the PNIPAM Volodymyrs’ka Str., 64/13, Kyiv 01601, Ukraine shell width upon temperature transition over LCST was Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Losytskyy et al. Nanoscale Research Letters (2018) 13:166 Page 2 of 7 shown for PS-PNIPAM nanoparticles in . At the the State University of New York at Buffalo). Fifty milli- same time, for the PNIPAM chains conjugated to dex- molars of TRIS-HCl buffer (pH 7.2) was used as solvent. tran, the temperature of conformation transition was shown to be 2–4 °C higher as compared to linear PNI- Synthesis and Characterization of Nanosystems PAM of similar molecular weight and polydispersity due Polystyrene-poly(N-isopropylacrylamide) hybrid nano- to the steric interaction between PNIPAM chains hin- systems, doped with PPO (PS-PPO-PNIPAM hybrid dering the conformation transition . NS), were synthesized as follows. First, PS-co-PNIPAM In this work, PS-PPO nanoparticles covered by core nanoparticles doped with PPO were prepared by cross-linked PNIPAM shell (Figs. 1 and 2) were obtained microemulsion polymerization [13, 14, 19, 20]. Briefly, resulting in PS-PPO-PNIPAM hybrid NS. The possibility 0.2 g of NIPAM, 0.2 g of sodium dodecylsulphate, and of using cross-linked PNIPAM for attaching chlorin e 0.01 g of NaH PO ×H O were dissolved in 90 g of 6 2 4 2 sensitizer to PS-PPO NP scintillator was studied. This H O. Then, 0.09 g of PPO was dissolved in 1.8 g of styr- polymer has the conformational transition at physio- ene and the obtained mixture was added dropwise dur- logical temperatures (for cross-linked PNIPAM, LCST ing 30 min, too. The mixture was stirred at 700 rpm, should be higher than 32 °C). Thus, shrinking of and Ar was bubbled into the mixture for 30 min. After cross-linked PNIPAM network following heating under the temperature increased to 70 °C, 0.01 g of K S O 2 2 8 excitation could result in decrease of the distance be- dissolved in 1 ml of H O was injected to initiate the tween PS-PPO donor and chlorin e acceptor that would polymerization. Secondly, PNIPAM shell layer was fabri- increase the efficiency of EEET and thus the efficiency of cated after 4 h heating at 70 °C. For this purpose, aque- tumor destruction. ous solution of monomer NIPAM (0.69 g) and cross-linker N,N′-methylenebisacrylamide (BIS) (0.06 g) were added into the reactor using a syringe. The reac- Experimental tion was allowed to continue for 3 h at 70 °C and add- Materials itional 1 h at 90 °C. The mixture was cooled to room Styrene (ST, Ukraine) of p.a. quality was purified via temperature and dialyzed during 48 h using cellulose standard method directly before polymerization. membrane with MWCO 3500 Da. N-Isopropylacrylamide (NIPAM, Sigma-Aldrich Inc.), Transition electron microscopy (TEM) images of the N,N′-methylenebisacrylamide (BIS, Sigma-Aldrich Inc.), obtained nanosystems are presented in Fig. 2. For the potassium persulfate K S O (KPS, Ukraine), sodium sample preparation, 400 mesh Cu grids with plain car- 2 2 8 phosphate monobasic dehydrate NaH PO ×2H O bon film were rendered hydrophilic by a glow discharge 2 4 2 (Ukraine), and anionic surfactant sodium dodecyl sulfate treatment (Elmo, Cordouan Technologies Bordeaux (SDS, Sigma-Aldrich Inc.) were of reagent grade and France). A 5-μl drop was deposited and let adsorbed for used without further purification. Chlorin e (Frontier 1 min, then the excess of solution was removed with a Scientific Inc.) was kindly provided by T.Y. Ohulchans- piece of filter paper. The observations of the kyy (Institute for Lasers, Photonics and Biophotonics at PS-PPO-PNIPAM nanosystems were carried on two TEMs, Tecnai G2 or CM12 (FEI, Eindhoven, Netherlands), and the images were acquired with a ssCCD Eagle camera on the Tecnai and a Megaview SIS Camera on the CM12. It is seen from Fig. 2 that the ob- tained hybrid nanosystems consist of several bound spherical PS-PPO NP; we believe that they are bound by cross-linked PNIPAM polymer net. Thus, PS-PPO-PNIPAM hybrid nanosystems were obtained. Spectral Measurements and Sample Preparation Absorption spectra were measured using a Specord M40 spectrophotometer (Carl Zeiss, Germany). Fluorescence excitation and emission spectra were registered with the help of a Cary Eclipse fluorescent spectrophotometer (Varian, Australia). Absorption and fluorescence mea- surements were performed in 1 × 1 cm quartz cell at room temperature. Fifty millimolars of TRIS-HCl buffer, Fig. 1 Structures of the components of the PS-PPO-PNIPAM hybrid pH 7.2, was used as a solvent. For spectral measure- nanosystem and chlorin e ments, the obtained solution of PS-PPO-PNIPAM Losytskyy et al. Nanoscale Research Letters (2018) 13:166 Page 3 of 7 Fig. 2 TEM images of the obtained PS-PPO-PNIPAM hybrid nanosystems with lower (left) and higher (right) magnification hybrid NS was dissolved 100 times in buffer. Stock solu- hybrid nanosystems in 50 mM Tris-HCl buffer (pH 7.2) tion of chlorin e at the concentration 10 mM was pre- are presented in Fig. 3. Absorption spectrum contains pared in DMF and further diluted in buffer to 1 mM the bands corresponding to styrene (maximum near concentration. Small aliquot of this 1 mM solution of 260 nm) and PPO (maximum near 307 nm). At the chlorin e was then added to 100 times dissolved buffer same time, fluorescence emission spectrum upon excita- solution of NS; the final concentration of chlorin e was tion at 250 nm (the range of styrene absorption) resulted 2 μM, and DMF admixture was thus 0.02%. Fluorescence in the spectrum that belongs exclusively to PPO (with excitation and emission spectra of PS-PPO-PNIPAM hy- maximum at 367 nm), while the emission of styrene brid NS solution with chlorin e was measured in 0, 5, (due at 307 nm ) was not observed. Thus, EEET 10, 20, 40, 60, 80, and 100 min after the addition of from styrene to incorporated PPO is near to complete. chlorin e to the solution of PS-PPO-PNIPAM hybrid EEET is also supported by the excitation spectrum of NS. In nearly 80 min, the saturation was reached. PPO emission (380 nm) where styrene band near For temperature-dependent measurements, solution 260 nm is clearly observed (Fig. 3). It should be added of PS-PPO-PNIPAM hybrid NS in the presence of that clear vibronic structure could be observed in PPO chlorin e was placed into the thermostatted cell emission spectrum (which is not observed for the PPO holder (T = 23 °C). In 88 min after the preparation of the sample, after the uptake of chlorin e by PS-PPO-PNIPAM hybrid NS reached saturation, water flow from the water bath was switched on heating the sample to 39 °C (this temperature should exceed LCST for the cross-linked PNIPAM). Fluorescence ex- citation spectra of chlorin e (emission at 680 nm) were then measured in different time intervals after the heating was started. Experimental results state that the conformation transition starts in about 3 min after the heating was started. It should be mentioned that in about 18 min after the heating was started, coagulation of the NS occurred giving macroscopic clots (which however disappear after the solution was cooled down, thus coagulation is reversible). Temperature experiment was performed three times, and similar tendencies were obtained. Fig. 3 Absorption (black solid line), fluorescence excitation (emission at 380 nm, normalized; black short-dashed line), and emission (excitation at 250 nm, normalized; red solid line) spectra of the Results and Discussion obtained PS-PPO-PNIPAM hybrid nanosystems in 50 mM Tris-HCl Absorption, fluorescence excitation, and fluorescence buffer (pH 7.2) emission spectra of the obtained PS-PPO-PNIPAM Losytskyy et al. Nanoscale Research Letters (2018) 13:166 Page 4 of 7 water solution ) that additionally points to the PPO incorporation into the PS matrix. Further, to the solution of the obtained PS-PPO-PNIPAM hybrid nanosystems in 50 mM Tris-HCl buffer (pH 7.2), the photosensitizer chlorin e was added. Absorption spectrum of chlorin e shows almost no change in the presence of hybrid nanosystems as compared to buffer solution, except small decrease of the optical density in the max- ima (Fig. 4). At the same time, effect of the addition of chlorin e to PS-PPO-PNIPAM hybrid NS on fluorescence spectra is much more noticeable as compared to absorption ones. First of all, the presence of chlorin e leads to the quenching of PPO fluorescent emission of PS-PPO-PNIPAM hybrid NS, and this quenching does Fig. 5 Fluorescence spectra of PS-PPO-PNIPAM hybrid NS free enhance during about an hour (Fig. 5). Generally, such (black solid line) and upon addition of chlorin e measured in quenching could be due to either EEET (that would lead 0 min (black short-dashed line) and in 80 min (black dash-dotted line). to the quenching of donor emission at all emission The excitation wavelength is 250 nm. Fifty millimolars of Tris-HCl buffer, wavelengths) or reabsorption (that would lead to the pH 7.2, is used as solvent. Differences of the spectra (solid, short-dashed and dash-dotted red lines) indicate the contribution of reabsorption and quenching of donor emission at the wavelengths of the electronic excitation energy transfer (EEET) to emission quenching acceptor absorption). Differences of PPO emission spec- tra (Fig. 5) show that immediately after chlorin e addition, the contribution of reabsorption to PPO emis- At the same time, emission of chlorin e upon excitation sion quenching is significant (but EEET also takes place). to its own absorption (at 400 nm) is only slightly chan- At the same time, the contribution of reabsorption fur- ged in the presence of PS-PPO-PNIPAM NS. Together ther decreases with time and this of EEET grows. with the small change in chlorin e absorption (Fig. 4), Another effect of addition of chlorin e to this means that only small part of chlorin e molecules 6 6 PS-PPO-PNIPAM hybrid NS is the appearing of chlorin is bound to PS-PPO-PNIPAM NS. e emission (upon excitation of PS at 250 nm) that is Finally, the PS-PPO band appears in excitation shifted to the long-wavelength region as compared to spectrum of chlorin e added to PS-PPO-PNIPAM hy- the one of free chlorin e ; both intensity and shift do in- brid NS (emission at 680 nm, where the contribution of crease with time and reach saturation in about an hour (Fig. 6). This shift points to the influence of the PNI- PAM surrounding on the bound molecules of chlorin e . Fig. 6 Fluorescence spectra of chlorin e free and added to PS- PPO-PNIPAM hybrid NS (measured in 0, 5, 10, 20, 40, and 80 min after addition). Excitation wavelengths are 250 and 400 nm; 50 mM Tris-HCl buffer, pH 7.2, was used as solvent. Short-dashed Fig. 4 Absorption spectra of chlorin e (2 μM) free (black line) and arrows indicate spectra excited at 250 and 400 nm. Solid arrow in the presence of PS-PPO-PNIPAM hybrid nanosystems (red line) in indicates the increasing time (t) after the addition of chlorin e 50 mM Tris-HCl buffer, pH 7.2 for the spectra excited at 250 nm Losytskyy et al. Nanoscale Research Letters (2018) 13:166 Page 5 of 7 Thus, chlorin e binds to PS-PPO-PNIPAM hybrid NS that causes EEET from PS matrix and encapsulated PPO to chlorin e . EEET efficiency enhances with time (dur- ing about an hour after chlorin e addition), indicating that uptake of chlorin e by PNIPAM network of PS-PPO-PNIPAM hybrid NS still proceeds during this time. At the same time, a relatively small part of chlorin e present in the solution is bound by PNIPAM. It should be also mentioned that PS-PPO NP were shown to emit the fluorescence of PPO  or attached porphyrin  when excited with X-rays. Thus, EEET from PS to chlorin e observed in PS-PPO-PNIPAM hy- brid NS under the UV excitation of PS means that the energy of X-rays could be also transferred to chlorin e in the studied NS. At the same time, rather high concen- tration of PS-PPO NP is required for the direct observa- tion of X-ray stimulated emission of such NP [13, 14]. Fig. 7 Fluorescence excitation spectra of chlorin e free and added to PS-PPO-PNIPAM hybrid NS (measured in 0, 10, 80, and 100 min after One of the ways to increase the sensitivity of such NS to addition), and PS-PPO-PNIPAM hybrid NS itself. Emission wavelengths X-rays could be the addition of components containing for chlorin e are 660 nm (normalized intensity) and 680 nm. Emission heavy atoms. wavelength for PS-PPO-PNIPAM NS is 380 nm (normalized intensity). PNIPAM is known to experience the conformation Fifty millimolars of Tris-HCl buffer, pH 7.2, is used as solvent transition at LCST equal to 32 °C. For the cross-linked polymer, the LCST value should be still higher. If our the PNIPAM-bound chlorin e to the total emission of PS-PPO-PNIPAM hybrid NS consists of cross-linked chlorin e is close to maximum). This band is weak at PNIPAM network surrounding PS-PPO NPs, and first, but further, its intensity strongly increases with chlorin e is bound to PNIPAM network, we could ex- time (Fig. 7). At the same time, this PS-PPO band is very pect the decrease of PPO-chlorin e distance and thus weak in the excitation spectrum of chlorin e upon the increase of EEET efficiency upon heating the whole emission at 660 nm (i.e., at maximum of the free chlorin hybrid NS. e spectrum) even after 100 min after the addition of To verify this idea, the effect of heating of chlorin e . PS-PPO-PNIPAM hybrid NS in the presence of Fig. 9 The dependence on the time after the heating to 39 °C Fig. 8 Fluorescence excitation spectra (normalized at 404 nm) of was switched on of the ratio of the emission intensity of chlorin chlorin e added to PS-PPO-PNIPAM hybrid NS at 23 °C (black line) e added to PS-PPO-PNIPAM hybrid NS at 680 nm upon excitation at 6 6 and at 39 °C (in 14 min after heating was switched on; red line). 320 nm (absorption by PPO with further EEET to chlorin e )to that Emission wavelength 680 nm; 50 mM Tris-HCl buffer, pH 7.2, was upon excitation at 404 nm (direct excitation of chlorin e ). Error bars used as solvent account for the noise of the registered excitation spectra Losytskyy et al. Nanoscale Research Letters (2018) 13:166 Page 6 of 7 Fig. 10 Proposed scheme of the processes in the solution of PS-PPO-PNIPAM hybrid NS in the presence of chlorin e upon addition of chlorin e 6 6 (process 1), passing of about 1 h (process 2) and further heating from 23 to 39 °C (process 3) chlorin e on fluorescence excitation spectra of the conformation transition of the PNIPAM network chlorin e was studied. Heating experiment was per- that leads to the decrease of the distance between formed three times; similar tendencies were demon- PS-PPO and chlorin e molecules, and thus to still strated. Results of one of these experiments are higher increase of PS-PPO-to-chlorin e EEET efficiency presented in Figs. 8 and 9. Thus, the solution of (Fig. 10, process 3). PS-PPO-PNIPAM hybrid NS in the presence of chlorin e was heated to the temperature of 39 °C Conclusions (this temperature should exceed LCST for the The fluorescent study revealed the uptake of chlorin e cross-linked PNIPAM); the heating started after the by PS-PPO-PNIPAM hybrid NS as well as electronic ex- uptake of chlorin e by PS-PPO-PNIPAM hybrid NS citation energy transfer from the PS matrix via encapsu- reached saturation. During the heating, the ratio of lated PPO to chlorin e ; uptake reached saturation in chlorin e fluorescence intensities (emission at about an hour. 680 nm) upon excitation at 320 nm (I ;thatis ex320 Heating of PS-PPO-PNIPAM-chlorin e NS from 21 chlorin e emission due to PPO-to-chlorin e EEET) 6 6 to 39 °C results in enhancement of EEET efficiency; this and 404 nm (I ; that is chlorin e emission upon ex404 6 is consistent with PNIPAM conformation transition that excitation to its own Soret band) was studied (Figs. 8 reduces the distance between PS-PPO donors and and 9); we believe this ratio to reflect the efficiency chlorin e acceptors. of PPO-to-chlorin e EEET. Thus, the first 3 min Meanwhile, a relatively small part of chlorin e present after heating started, I /I decreased from 0.9 ex320 ex404 in the solution is bound to PNIPAM; thus, further stud- to 0.85, perhaps due to the decrease of the chlorin ies in this direction are necessary. e -to-PNIPAM binding affinity upon temperature in- crease. Further, the value of I /I ratio in- Abbreviations ex320 ex404 EEET: Electronic excitation energy transfer; LCST: Lower critical solution creased up to 1.02, which was accompanied by the temperature; NS: Nanosystem; PNIPAM: Poly-N-isopropylacrylamide; increased light scattering (Fig. 8; scattering is mani- PPO: Diphenyloxazole; PS: Polystyrene; TEM: Transmission electron fested as the intensity increase near 660 nm). This microscopy could be explained by conformation transition in Funding PNIPAM that leads to reducing of cross-linked PNI- This work was supported by the Ministry of Education and Science of PAM network volume. This causes the decrease of Ukraine (program “Science in Universities”, project no. 16БФ051-03 “The the distance between PS-PPO donor and chlorin e study of electronic-vibrational processes in composites and nanosystems promising for solar energetics, low-power-consuming light sources and acceptor molecules bound to PNIPAM network and medicine”). thus to increasing of EEET efficiency. In summary, processes in the solution of Availability of Data and Materials PS-PPO-PNIPAM hybrid NS in the presence of chlorin The data supporting the conclusions of this article are included within the article. e addition could be described as follows. First, addition of chlorin e to the solution of PS-PPO-PNIPAM hybrid Authors’ Contributions NS in buffer (Fig. 10, process 1) leads to the penetration ML carried out spectral measurements and wrote the article. LV and ON of the small part of chlorin e into the PNIPAM network 6 performed the synthesis of nanosystems. NK performed TEM characterization of nanosystems and participated in the discussion. VY participated in the of the hybrid NS; this resulted in EEET from PS and design of the study and discussion of the results and coordination. All PPO to chlorin e . Such penetration proceeds during authors read and approved the final manuscript. about an hour accompanied with the increase in EEET efficiency (Fig. 10, process 2). Further heating of the Competing Interests sample to the temperature exceeding LCST results in The authors declare that they have no competing interests. Losytskyy et al. Nanoscale Research Letters (2018) 13:166 Page 7 of 7 Publisher’sNote 19. Zhang F, Wang C-C (2008) Preparation of thermoresponsive core-shell Springer Nature remains neutral with regard to jurisdictional claims in polymeric microspheres and hollow PNIPAM microgels. Colloid Polym Sci published maps and institutional affiliations. 286:889–895 20. 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Nanoscale Research Letters – Springer Journals
Published: May 31, 2018
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