Taming Reactive Oxygen Species: Mitochondria-Targeting Aggregation-Induced Emission Luminogen for Neuron Protection via Photosensitization-Triggered Autophagy

Name: Taming Reactive Oxygen Species: Mitochondria-Targeting Aggregation-Induced Emission Luminogen for Neuron Protection via Photosensitization-Triggered Autophagy
Uploaded: 2021-09-03

Chao Chen; Ruoyao Zhang; Jianyu Zhang; Yufan Zhang; Haoke Zhang; Zaiyu Wang; Xiaolin Huang; Sijie Chen; Ryan T. K. Kwok; Jacky W. Y. Lam; Dan Ding; Ben Zhong Tang

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ID: W3197845456
Title: Taming Reactive Oxygen Species: Mitochondria-Targeting Aggregation-Induced Emission Luminogen for Neuron Protection via Photosensitization-Triggered Autophagy
Abstract: Open AccessCCS ChemistryCOMMUNICATION14 Jul 2022Taming Reactive Oxygen Species: Mitochondria-Targeting Aggregation-Induced Emission Luminogen for Neuron Protection via Photosensitization-Triggered Autophagy Chao Chen†, Ruoyao Zhang†, Jianyu Zhang†, Yufan Zhang, Haoke Zhang, Zaiyu Wang, Xiaolin Huang, Sijie Chen, Ryan T. K. Kwok, Jacky W. Y. Lam, Dan Ding and Ben Zhong Tang Chao Chen† Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 †C. Chen, R. Zhang, and J. Zhang contributed equally to this work.Google Scholar More articles by this author , Ruoyao Zhang† Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 †C. Chen, R. Zhang, and J. Zhang contributed equally to this work.Google Scholar More articles by this author , Jianyu Zhang† Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 †C. Chen, R. Zhang, and J. Zhang contributed equally to this work.Google Scholar More articles by this author , Yufan Zhang State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Sciences, Nankai University, Tianjin 300071 Google Scholar More articles by this author , Haoke Zhang Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 Google Scholar More articles by this author , Zaiyu Wang Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 Google Scholar More articles by this author , Xiaolin Huang Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 Google Scholar More articles by this author , Sijie Chen Ming Wai Lau Centre for Reparative Medicine, Karolinska Institutet, Hong Kong 999077 Google Scholar More articles by this author , Ryan T. K. Kwok Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 Google Scholar More articles by this author , Jacky W. Y. Lam Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 Google Scholar More articles by this author , Dan Ding *Corresponding authors: E-mail Address: [email protected] E-mail Address: [email protected] State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Sciences, Nankai University, Tianjin 300071 Google Scholar More articles by this author and Ben Zhong Tang *Corresponding authors: E-mail Address: [email protected] E-mail Address: [email protected] Department of Chemistry, Hong Kong Branch of Chinese National Engineering Research Center for Tissue Restoration and Reconstruction, Institute for Advanced Study, State Key Laboratory of Molecular Nanoscience, Division of Life Science, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong 999077 Center for Aggregation-Induced Emission, SCUT-HKUST Joint Research Institute, State Key Laboratory of Luminescent Materials and Devices, South China University of Technology, Guangzhou 510640 Shenzhen Institute of Aggregate Science and Technology, School of Science and Engineering, The Chinese University of Hong Kong, Shenzhen 518172 AIE Institute, Guangzhou Development District, Huangpu, Guangzhou 510530 Google Scholar More articles by this author https://doi.org/10.31635/ccschem.021.202101217 SectionsSupplemental MaterialAboutAbstractPDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareFacebookTwitterLinked InEmail Oxidative damage to cells leads to accumulated harmful wastes, which in turn aggravate the imbalance of reactive oxygen species (ROS) and related diseases. Therefore, provoking the cellular defense system against severe oxidation and maintaining ROS homeostasis are desired. Herein, we designed and synthesized a powerful mitochondria-targeting aggregation-induced emission photosensitizer (named DTCSPY) by maximal restriction of heat dissipation. It is demonstrated that taming ROS generation within mitochondria through photosensitization-triggered autophagy via DTCSPY achieved a better neuroprotective effect against oxidative damages than N-acety-l-cysteine and vitamin C. This work not only provides a new way to design high-performance photosensitizers by regulating the photophysical property, but also verifies the concept that taming ROS can be used for cell protection against destructive oxidation, thereby displaying broad prospects for alleviating oxidation-related diseases and promoting cell-based therapy. Download figure Download PowerPoint Introduction Life is a contradictory process full of dynamic balance, such as immune homeostasis, energy equilibrium, reactive oxygen species (ROS) balance, and so on.1–3 The balance of these dynamic systems is finely tuned within a normal range to maintain fitness. Among various dynamic systems, ROS balance has drawn great attention due to its critical role and extensive participation in life and disease processes.3–5 For example, ROS within normal levels are closely involved in cell differentiation and development, whereas too much ROS leads to superfluous oxidized substances, which exacerbate the ROS imbalance and elicit many severe diseases (e.g., cancer, inflammation, neurodegenerative diseases, and ischemia-reperfusion injury).4–6 Therefore, developing agents or methods to maintain the ROS homeostasis and eradicate the harmful oxidized wastes are highly desired. At present, antioxidants (such as N-acetyl-l-cysteine [NAC], vitamin C, vitamin E, etc.) are commonly used to maintain the ROS balance.7 Although antioxidants can quickly scavenge redundant ROS, they can neither remove the accumulated harmful wastes nor generate durable protection due to their quick redox mechanism in living cells. In contrast, autophagy inducers (e.g., rapamycin, resveratrol, and many natural compounds) increase the level of autophagy, which enables cells to digest harmful substances via their own defense system to achieve a long-term protection.8 However, most autophagy inducers belong to chemotherapy agents, and the lack of specific and controllable delivery and visual tracking contribute to some common drawbacks, such as multiple targets, organ toxicity, and elusive mechanism,9–11 thereby limiting their further application. Compared with chemotherapy, phototherapy has the inherent advantages of high selectivity and super spatiotemporal resolution, exhibiting a promising prospect for specific delivery and accurate treatment.12–20 Photodynamic therapy (PDT) is a successful demonstration of phototherapy in the precise treatment of diseases and easily achieves localized delivery of massive ROS via engineered control of light.21–25 Inspired by this, we wondered whether phototherapy can trigger a cell’s own protective system to remove harmful oxidized components and maintain the ROS balance with the help of a functional photosensitizer (PS). According to literature reports, moderate ROS derived from mitochondria is crucial for stimulating the cell’s defense system, especially for inducing active autophagy to remove harmful wastes.26,27 Thereby, we proposed provoking a cell’s defensive autophagy for enduring protection against oxidation damages via photocontrolled ROS generation within mitochondria. Traditional PSs usually possess conjugated planar structures, and they easily form aggregates in the physiological environment. After excitation, these PS will predominantly consume energy through heat production due to strong intermolecular π–π interactions in the aggregate state, leading to reduced ROS generation as well as fluorescence emission. Therefore, it is hard to accurately and effectively control ROS generation with traditional PSs.28 Contrary to traditional PSs, PSs with aggregation-induced emission (AIE-PSs) can effectively produce ROS and fluorescence in aggregates thanks to the twisted structures, which strongly inhibit the thermal decay, exhibiting great potential in biomedical application.29–33 Thus, we can conveniently control the required amount and exact location of ROS using AIE-PS-based phototherapy. As we know, the major pathway of energy consumption by heat generation is composed of intermolecular interactions (e.g., π–π interaction) and intramolecular motions.34,35 Although the twisted skeleton of AIE-PS can effectively inhibit the intermolecular interactions in the aggregate state, limiting the heat decay from intramolecular motion requires further optimization, such as flexible alkene groups of twisted AIE-PSs can still consume energy through heat dissipation. Based on these considerations, two mitochondria-targeted AIE-PSs (DTCSPY and DTCSPE) with twisted skeletons were designed. The structure of DTCSPY contains a comparatively rigid alkyne group, which is capable of further hindering the thermal dissipation due to less intramolecular motion. For comparison, a more flexible alkene-based π-bridge was introduced into the structure of DTCSPE. As expected, the ROS generation efficiency of DTCSPY is much better than that of DTCSPE both in phosphate-buffered saline (PBS) solutions and live cells due to maximal inhibition of thermal decay (both intermolecular interactions and intramolecular motions). Furthermore, we propose and demonstrate a new concept of taming ROS for cell protection using HT22 neuron cells and adipose-derived stem cells (ADSCs) suffering from oxidative damages, bringing new insight into the biomedical application of PSs. Additionally, the experimental results also show that taming ROS by AIE-PSs exhibits a better protective effect than the widely used antioxidants (NAC and vitamin C). The biological mechanism behind the protective effect is also illustrated. Results and Discussion DTCSPY and DTCSPE were synthesized through Knoevenagel condensation and methylation as shown in Figure 1a and Supporting Information Scheme S1. The chemical structures of the two molecules were fully characterized by 1H NMR, 13C NMR, and high-resolution mass spectrometry (HRMS). DTCSPY and DTCSPE share the same electron donating and accepting skeleton but different π-bridges. Pyridinium was introduced as the mitochondria-targeting moiety. Then photophysical properties of DTCSPY and DTCSPE were investigated. As shown in Figure 1b and Supporting Information Figure S1, the absorption maxima of DTCSPY and DTCSPE were 490 nm, and the emission spectra were centered at 700 and 710 nm, respectively, in dimethyl sulfoxide (DMSO)/water mixtures. Figures 1c and 1d show that the AIE-PSs exhibited typical AIE activity and remarkable ROS generation capability much greater than Rose Bengal (RB, a high-performance PS) under the same condition. To further specify the type of ROS generated from DTCSPE and DTCSPY, singlet oxygen sensor green (SOSG, for singlet oxygen detection) and hydroxyphenyl fluorescein (HPF, for hydroxyl radical detection) were utilized as relevantly specific ROS indicators. As shown in Supporting Information Figure S2, DTCSPY showed obviously stronger ROS generation ability than that of DTCSPE in terms of producing both singlet oxygen and hydroxyl radicals. These results indicated that a rigid alkyne in a twisted AIE-PS could further improve ROS generation ability by hindering thermal dissipation. Accordingly, DTCSPY decorated with a rigid alkyne-based π-bridge displayed better performance in both AIE activity and ROS production capability than that of DTCSPE featuring a flexible alkene-based π-bridge (Figures 1c and 1d and Supporting Information Figures S2 and S3). Figure 1 | (a) Chemical structures of DTCSPY and DTCSPE. (b) Normalized UV-vis/photoluminescence (PL) spectra of DTCSPY and DTCSPE in DMSO/water (1:99) mixture. (c) Plots of relative emission intensity (I/I0) of DTCSPY and DTCSPE in mixtures of DMSO/toluene with different toluene fractions (vol %). (d) Plots of fluorescence intensity of DCF at 520 nm in PBS involving different PSs (5 μM): DTCSPY, DTCSPE, and RB versus different irradiation times, respectively. Download figure Download PowerPoint Density functional theory (DFT) at the level of CAM-B3LYP/6-31G(d,p) was conducted to further understand the relationship between chemical structures and different ROS generation performance.36 Optimized geometries and electron cloud distribution separately depicted a comparable large dihedral angle of the stilbene segment (>21°) and relatively distant highest occupied molecular orbital (HOMO)–lowest unoccupied molecular orbital (LUMO) separation in both AIE-PSs (Figure 2a), which contributes to the twisted structures, AIE activity, and efficient ROS generation in aggregates. To further explain the different ROS performance of DTCSPY and DTCSPE, the energy gap (ΔE) and spin-orbital coupling (SOC) between singlet and triplet states were analyzed.37 Although the results showed almost the same level of SOC efficiency of these two PSs, the small energy difference between S1 and T2 (ΔES1-T2) indicates the efficient channel of intersystem crossing (ISC). Moreover, ΔES1-T2 of DTCSPY is much smaller than that of DTCSPE, which is mainly responsible for its higher ROS generation efficiency (Figure 2b). Figure 2 | (a) Optimized geometries and electron cloud distributions of HOMO and LUMO of DTCSPE and DTCSPY. (b) Diagram of energy level of singlet and triplet states of DTCSPE and DTCSPY based on optimized singlet geometries. ΔE and SOC constants are also indicated. Download figure Download PowerPoint As many serious neuron diseases are closely associated with ROS imbalance, oxidative damages, and overloaded oxidized wastes,38,39 we used HT22 murine hippocampal neuronal cells to validate that taming ROS generation can trigger cellular defense against severe oxidative damages. First, the mitochondria-targeting ability of DTCSPY and DTCSPE was evaluated in HT22 neuron cells through costaining with commercial mitochondrial probe Mito-Tracker Deep Red FM (MTDR). As depicted in Figures 3a–3c and Supporting Information Figure S4, both DTCSPY and DTCSPE can illuminate the mitochondria with a high signal to background ratio because of excellent mitochondria-targeted ability and AIE activity. Pearson’s correlation coefficient between DTCSPY/DTCSPE and MTDR both reached ∼0.86, suggesting outstanding mitochondria-targeted capability. Subsequently, ROS generation efficiency of DTCSPY and DTCSPE in HT22 neuron cells were investigated using 2′,7′-dichlorodihydrofluorescein diacetate (DCF-DA). HT22 cells cannot oxidize the DCF-DA to highly green-emissive DCF themselves (Figure 3d), and the cells without light irradiation (Figure 3e) or AIE-PS (Figure 3f) hardly displayed DCF fluorescence. In contrast, after treatment with AIE-PS (DTCSPY and DTCSPE) and light irradiation, significant signals were observed, indicating that efficient ROS was generated in HT22 neuron cells (Figures 3g and 3h). Figure 3i shows that NAC (a ROS scavenger) could suppress the strong signal, further demonstrating that it was indeed the ROS generated by AIE-PS that oxidized DCF-DA to DCF. The quantitative analysis of Figures 3d–3i is depicted in Supporting Information Figure S5. Additionally, compared with the DTCSPE-treated group, DTCSPY-treated cells exhibited much stronger fluorescence, displaying more efficient ROS generation, which was consistent with the results of the theoretical calculation and in vitro tests in PBS solutions. Figure 3 | (a–c) CLSM images of colocalization between 5 μM DTCSPY (a) and 1 μM MTDR (b) in HT22 neuronal cells; (c) overlap between (a) and (b); Scale bar: 10 μm. (d–i) CLSM images indicate ROS production in HT22 neuronal cells treated with pure DCF-DA (d), “DTCSPY + DCF-DA” (e), “light + DCF-DA” (f), “DTCSPE + DCF-DA + light” (g), DTCSPY + DCF-DA + light” (h), and “DTCSPY + DCF-DA + light + NAC” (i). Green fluorescence: DCF. DTCSPE/DTCSPY: 5 μM; DCF-DA: 25 μM; Scale bar: 25 μm. Download figure Download PowerPoint After verifying the mitochondria-targeted and ROS generation capabilities of AIE-PSs in HT22 neuron cells, we examined whether controllable ROS generation within mitochondria can trigger a defensive autophagy against oxidative damage. First, we confirmed that both DTCSPY and DTCSPE had good biocompatibility in darkness by the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay (Figure 4a). Then, we optimized experimental conditions to control the ROS level by treating the cells with AIE-PS in different concentrations under light irradiation. As displayed in Figure 4b, when incubated concentrations of DTCSPY and DTCSPE are ≤0.5 and 2.5 μM, respectively, the cell viability of HT22 neuron cells was >85%, indicating the amount of ROS generated within these ranges (0–0.5 μM for DTCSPY and 0–2.5 μM for DTCSPE) was tolerable in neuron cells. Next, for comparison, the concentration of 0.5 μM was selected for DTCSPY and DTCSPE to explore the protective effect by adjusting the irradiation time. Briefly, HT22 neuron cells were incubated with 0.5 μM DTCSPY and DTCSPE for 90 min, then treated with light irradiation for different time (0, 1, 3, and 5 min). After another 6 h incubation, the cells were subsequently exposed to 100 μM of hydrogen peroxide (H2O2) for 1 h and finally measured at 48 h. As shown in Figure 4c, the protective effect of neuron cells increased with prolonged irradiation time, suggesting that the amount of ROS generated by AIE-PS needs to reach a certain level to trigger the cell’s defense system. Compared with DTCSPE-treated cells, DTCSPY-treated cells exhibited a much stronger protective effect because the ROS threshold was easier to reach to provoke the defense system due to the more efficient ROS generation upon light irradiation. Moreover, using bright-field and confocal laser scanning microscopy (CLSM) images, the state and quantity of live or dead cells between the DTCSPY-treated and control group were monitored and found ( Supporting Information Figure S6)to be consistent with the protective effect in Figure 4c. Finally, both NAC and vitamin C, the widely used agents for resisting oxidative damages, were selected for comparison. As shown in Figure 4d, DTCSPY can trigger a more effective protection against H2O2 than NAC and vitamin C, demonstrating the importance of long-term defense triggered by DTCSPY. In addition, in a chloroquine (CQ, an autophagy inhibitor)-added group, the protective effect of DTCSPY treatment was lost, suggesting this protection was mediated by autophagy. To further explore whether this method can be applied to other cell types, ADSCs isolated from BALB/c mice were subjected to the same protection protocol.40 As displayed in Supporting Information Figure S7, the cell viability was elevated significantly in the “DTCSPY + Light” group compared with other groups, which were unable to generate the required ROS to trigger cell protection. Furthermore, the protective effect on ADSCs against H2O2 vanished in the “DTCSPY + Light + CQ” group, suggesting the protective effect provoked by ROS generated from DTCSPY was regulated by autophagy. Figure 4 | (a) Viability of HT22 neuronal cells treated with different concentrations of DTCSPY and DTCSPE in darkness for 24 h. (b) Viability of HT22 neuronal cells incubated with different concentrations of DTCSPY and DTCSPE, under light irradiation (50 mW/cm2) for 5 min and measured at 24 h. (c) Evaluation of the protective effect against H2O2 (100 μM) in HT22 neuronal cells treated with 0.5 μM DTCSPY and DTCSPE at 48 h, respectively. (d) Determination of protective effect against H2O2 in HT22 cells treated with different agents at 48 h. Light irradiation: 50 mW/cm2; DTCSPY/DTCSPE: 0.5 μM; vitamin C: 100 μM; NAC: 10 mM; CQ: 50 μM. H2O2-treated group served as control group. All cell viability values were divided by the group without any treatment for comparison convenience. Statistical comparisons of “DTCSPY + Light” group versus other groups in (d) were analyzed by one-way ANOVA with a Tukey post-hoc test. Unpaired Student’s t-test (two-tailed) was used in (b) and (c). **P < 0.01; ***P < 0.001. n = 4 for each group. ANOVA, analysis of variance. Download figure Download PowerPoint Further experiments were conducted to confirm that the protective effect was from DTCSPY-triggered autophagy under this optimized condition. As the punctate distribution of LC3B is one of the best hallmarks of autophagy induction, immunofluorescence staining of LC3B was analyzed using CLSM.41 As shown in Figure 5a, “Control” group without any treatment and “DTCSPY” group without light irradiation mainly exhibited diffuse distribution of LC3B, while massive LC3B puncta were observed in “DTCSPY + Light” group at 6 h after light irradiation, which indicated that effective autophagy was induced by DTCSPY-generated ROS. Quantified results also revealed a 6.4-fold and a 5.0-fold increase of LC3B puncta in “DTCSPY + Light” group compared with that of “Control” and “DTCSPY” groups. Next, the LC3B conversion from full-length LC3B-I to LC3B-II was detected at 6 h by western blots, another important hallmark of autophagy. As depicted in Figure 5b and Supporting Information Figure S8, the ratio of LC3B-II/LC3B-I in “DTCSPY + Light” group was 1.8-fold higher than that of “Control” and “DTCSPY” groups, suggesting activated autophagy in the experimental group. Moreover, two other necessary proteins (ATG5 and Beclin 1) involved in autophagy were also elevated in “DTCSPY + Light” group compared with the other two groups.42 These results together verified that controlling the ROS generation within mitochondria using DTCSPY can effectively trigger autophagy, which contributed to the cell protection from severe oxidative damage. Figure 5 | (a) Representative CLSM images and quantitative analysis of LC3B dots in different groups. LC3B (red signals) indicates autophagosome. Scale bar: 10 μm. ***P < 0.001, in comparison with “DTCSPY + Light” group. n = 4 (sights). Statistical comparisons were analyzed by one-way ANOVA with a Tukey post-hoc test. (b) Mechanism analysis of cytoprotective autophagy with different treatments using western blots. ANOVA, analysis of variance. Download figure Download PowerPoint Conclusion A powerful mitochondria-targeting AIE-PS (DTCSPY) was designed and synthesized to inhibition thermal dissipation from both intermolecular interactions and intramolecular motions. Because of the twisted structure, both DTCSPY and DTCSPE can effectively generate ROS in the aggregated state (much better than RB) due to inhibition of the intermolecular interactions, such as π–π interaction. However, DTCSPY, constructed with an alkyne-containing π-bridge, exhibited the best performance compared with DTCSPE (featured with alkane-containing π-bridge) and RB in ROS generation efficiency due to further restriction of intramolecular motions in the relatively rigid skeleton, providing a new way to design high-performance PSs by regulating photophysical property. HT22 neuron cells were selected as a model to demonstrate the new concept that taming ROS generation can trigger cell protection against severe oxidative damages. To the best of our knowledge, this demonstration is the first attempt to trigger neuron protection by control of ROS via phototherapy. Furthermore, we have applied this method to protect stem cells (ADSCs) from serious oxidation-induced damage. It not only provides a promising strategy against oxidative damages, which can be induced by acute inflammation, neurodegenerative diseases, ischemia-reperfusion injury, and radiotherapy or chemotherapy, but also exhibits great potential to improve the survival of therapeutic cells in hostile disease environment during stem-cell transplantation and chimeric antigen receptor T (CAR T)-cell-based therapy.43,44 Supporting Information Supporting Information is available and includes the experimental section, synthetic procedures, structural characterization, and supporting figures. Conflict of Interest There is no conflict of interest to report. Funding Information This work was financially supported by the National Science Foundation of China (nos. 21788102, 51873092, and 51961160730), the Research Grants Council of Hong Kong (nos. 16305518, 16305618, N-HKUST609/19, A-HKUST605/16, and C6009-17G), the Innovation and Technology Commission (nos. ITC-CNERC14SC01 and ITCPD/17-9), Ming Wai Lau Centre for Reparative Medicine Associate Member Program (no. MWLC19SC02), and the National Key Research and Development Program of China (no. 2017YFE0132200). Preprint Acknowledgment Research presented in this article was posted on a preprint server prior to publication in CCS Chemistry. The corresponding preprint article can be found here: DOI: 10.26434/chemrxiv.13134695.v1 References 1. Honda K.; Littman D. R.The Microbiota in Adaptive Immune Homeostasis and Disease.Nature2016, 535, 75–84. Google Scholar 2. López M.; Varela L.; Vázquez M. J.; Rodríguez-Cuenca S.; González C. 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Investig.2007, 117, 1466–1476. Google Scholar Previous articleNext article FiguresReferencesRelatedDetails Issue AssignmentVolume 4Issue 7Page: 2249-2257Supporting Information Copyright & Permissions© 2021 Chinese Chemical SocietyKeywordsneuron protectionphotosensitizeraggregation-induced emissionreactive oxygen speciesmitochondrial targeting Downloaded 1,155 times PDF DownloadLoading ...
Publication Year: 2021
Publication Date: 2021-09-03
Language: en
Type: article
Indexed In: ['crossref']

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4550, 4557, 4559, 4790, 4890], 'contributed': [109, 182, 255, 3430], 'equally': [110, 183, 256], 'to': [111, 184, 257, 806, 814, 817, 904, 983, 997, 1028, 1055, 1084, 1109, 1136, 1145, 1155, 1170, 1255, 1274, 1295, 1347, 1357, 1370, 1381, 1398, 1529, 1572, 2004, 2055, 2220, 2281, 2330, 2410, 2608, 2689, 2738, 2780, 2785, 2809, 2811, 2817, 2949, 2960, 2991, 2996, 3216, 3335, 3431, 3520, 3553, 3588, 3603, 3619, 3648, 3664, 3703, 3752, 3834, 4530, 4570, 4779, 5023], 'this': [112, 118, 185, 191, 258, 264, 297, 359, 421, 483, 505, 569, 633, 676, 800, 2934, 2944, 3227, 3642, 3662, 3825], 'work.Google': [113, 186, 259], 'Scholar': [114, 187, 260, 293, 355, 417, 479, 501, 565, 629, 672, 796, 3866, 3935, 3959, 3980, 3998, 4014, 4035, 4054, 4082, 4113, 4170, 4190, 4221, 4243, 4276, 4309, 4360, 4386, 4405, 4424, 4464, 4495, 4542, 4582, 4602, 4619, 4662, 4683, 4721, 4742, 4786, 4814, 4839, 4878, 4935, 4959, 4979, 5007, 5029, 5079, 5101, 5146, 5164, 5182], 'More': [115, 188, 261, 294, 356, 418, 480, 502, 566, 630, 673, 797], 'articles': [116, 189, 262, 295, 357, 419, 481, 503, 567, 631, 674, 798], 'by': [117, 190, 263, 296, 358, 420, 482, 504, 568, 632, 675, 799, 863, 908, 1242, 1439, 1629, 1688, 1876, 2405, 2595, 2613, 2694, 2777, 2913, 2938, 3022, 3029, 3151, 3174, 3299, 3342, 3482, 3607, 3652, 3687, 3761, 4703, 4922], 'author': [119, 192, 265, 298, 360, 422, 484, 506, 570, 634, 677, 801], ',': [120, 193, 266, 299, 361, 423, 485, 507, 571, 635], 'Zhang†': [122, 195], 'Medicinal': [273, 652], 'Biology,': [275, 654], 'Bioactive': [279, 658], 'Materials,': [280, 659], 'Ministry': [281, 660], 'Education,': [283, 662], 'College': [284, 663], 'Sciences,': [287, 666], 'Nankai': [288, 667], 'University,': [289, 668], 'Tianjin': [290, 669], '300071': [291, 670], 'Google': [292, 354, 416, 478, 500, 564, 628, 671, 795, 3865, 3934, 3958, 3979, 3997, 4013, 4034, 4053, 4081, 4112, 4169, 4189, 4220, 4242, 4275, 4308, 4359, 4385, 4404, 4423, 4463, 4494, 4541, 4581, 4601, 4618, 4661, 4682, 4720, 4741, 4785, 4813, 4838, 4877, 4934, 4958, 4978, 5006, 5028, 5078, 5100, 5145, 5163, 5181], 'Wang': [363, 4124, 4333, 4432, 4478, 4800, 4886, 5037, 5107, 5117], 'Huang': [425, 4196, 4508], 'Chen': [487, 4670, 4685, 4798, 4816, 4841, 4882, 5109, 5125], 'Ming': [488, 3796], 'Wai': [489, 3797], 'Lau': [490, 3798], 'Centre': [491, 3799], 'Reparative': [493, 3801], 'Medicine,': [494], 'Karolinska': [495], 'Institutet,': [496], 'Kwok': [511, 4751, 4898], 'Lam': [575, 4755, 4902], '*Corresponding': [638, 682], 'authors:': [639, 683], 'E-mail': [640, 644, 684, 688], 'Address:': [641, 645, 685, 689], '[email': [642, 646, 686, 690], 'protected]': [643, 647, 687, 691], 'Emission,': [747], 'SCUT-HKUST': [748], 'Joint': [749], 'Institute,': [751, 788], 'Luminescent': [756], 'Materials': [757, 4230, 4592], 'Devices,': [759], 'South': [760], 'China': [761, 3767, 3817], 'Guangzhou': [765, 789, 793], '510640': [766], 'Shenzhen': [767, 785], 'Aggregate': [770], 'School': [774], 'Kong,': [784], '518172': [786], 'AIE': [787, 1775, 1893, 2059, 2290, 4710, 4806, 4856], 'Development': [790, 3814], 'District,': [791], 'Huangpu,': [792], '510530': [794], 'https://doi.org/10.31635/ccschem.021.202101217': [802], 'SectionsSupplemental': [803], 'MaterialAboutAbstractPDF': [804], 'ToolsAdd': [805], 'favoritesDownload': [807], 'CitationsTrack': [808], 'Citations': [809], 'ShareFacebookTwitterLinked': [810], 'InEmail': [811], 'Oxidative': [812, 3992, 4023, 4706], 'damage': [813], 'cells': [815, 1135, 1570, 1601, 1605, 2219, 2247, 2317, 2325, 2339, 2378, 2432, 2500, 2616, 2649, 2702, 2734, 2764, 2796, 2844, 3039, 3058, 3093, 3114, 3613, 3667, 3709], 'leads': [816, 1027], 'accumulated': [818, 1101], 'harmful': [819, 1063, 1102, 1138, 1257, 1297], 'wastes,': [820], 'which': [821, 1032, 1133, 1402, 1519, 2053, 2136, 2442, 2988, 3292, 3429, 3683], 'in': [822, 1004, 1018, 1114, 1222, 1331, 1352, 1395, 1411, 1465, 1563, 1670, 1730, 1760, 1833, 1849, 1866, 1891, 1938, 1953, 1973, 2048, 2065, 2244, 2261, 2314, 2375, 2420, 2453, 2456, 2477, 2497, 2562, 2593, 2619, 2627, 2672, 2756, 2866, 2889, 2917, 2967, 2978, 3009, 3048, 3090, 3112, 3170, 3188, 3255, 3281, 3315, 3352, 3364, 3382, 3396, 3401, 3452, 3467, 3544, 3583, 3594, 3710, 3824, 3836, 3857, 3949, 3988, 4046, 4072, 4162, 4259, 4299, 4351, 4485, 4534, 4591, 4808, 5018, 5091, 5133, 5139, 5174], 'turn': [823], 'aggravate': [824], 'the': [825, 837, 910, 916, 1034, 1057, 1062, 1086, 1100, 1129, 1159, 1193, 1223, 1262, 1266, 1286, 1332, 1353, 1399, 1405, 1419, 1433, 1454, 1462, 1466, 1470, 1525, 1543, 1549, 1615, 1621, 1637, 1649, 1682, 1702, 1716, 1738, 1749, 1771, 1792, 1798, 1998, 2007, 2031, 2056, 2070, 2078, 2094, 2098, 2108, 2118, 2235, 2275, 2328, 2338, 2393, 2402, 2428, 2446, 2449, 2554, 2596, 2610, 2615, 2643, 2653, 2678, 2691, 2696, 2733, 2759, 2772, 2787, 2804, 2813, 2818, 2836, 2846, 2863, 2875, 2907, 2925, 2961, 2972, 2979, 2993, 3001, 3010, 3018, 3083, 3152, 3219, 3231, 3239, 3329, 3360, 3383, 3408, 3418, 3432, 3533, 3545, 3556, 3571, 3595, 3621, 3637, 3645, 3705, 3733, 3762, 3773, 3787, 3809, 3965, 3973, 4155, 4486, 4563, 4610, 4774, 4824, 4950, 4996, 4999, 5019, 5140, 5155, 5175], 'imbalance': [826, 1036], 'reactive': [828, 962], 'oxygen': [829, 963, 1808, 1814, 1855, 5202], 'species': [830, 964], '(ROS)': [831, 965], 'related': [833], 'diseases.': [834], 'Therefore,': [835, 1050, 1366], 'provoking': [836, 1302], 'cellular': [838, 2228], 'defense': [839, 1143, 1288, 2229, 2789, 2814, 2911], 'system': [840, 1144, 1254, 2815], 'against': [841, 888, 927, 1310, 2230, 2579, 2899, 3006, 3086, 3110, 3632, 3680, 4455, 4656], 'severe': [842, 1040, 2231, 3436, 3633], 'oxidation': [843, 1311], 'maintaining': [845], 'ROS': [846, 874, 920, 990, 1011, 1026, 1035, 1058, 1087, 1235, 1263, 1278, 1315, 1359, 1375, 1392, 1426, 1550, 1594, 1628, 1779, 1801, 1829, 1842, 1873, 1896, 2014, 2063, 2072, 2143, 2205, 2224, 2307, 2372, 2389, 2403, 2440, 2495, 2557, 2570, 2611, 2656, 2775, 2805, 2821, 2995, 3023, 3419, 3543, 3584, 3626, 3655, 3950, 3969, 4648, 5017], 'homeostasis': [847, 1059], 'are': [848, 1015, 1066, 1081, 2189, 2201, 2637], 'desired.': [849, 1068], 'Herein,': [850], 'we': [851, 1244, 1300, 1415, 1431, 1585, 2213, 2566, 2583, 2604, 3659], 'designed': [852, 3517], 'synthesized': [854, 1662, 3519], 'a': [855, 884, 901, 949, 980, 1147, 1204, 1217, 1250, 1269, 1303, 1514, 1535, 1589, 1632, 1788, 1863, 1867, 1884, 1904, 2025, 2278, 2576, 2782, 2798, 2895, 2918, 3178, 3306, 3309, 3486, 3600, 3617, 3677, 3830, 4264, 4653, 4713], 'powerful': [856, 3512], 'mitochondria-targeting': [857, 1717, 2236, 3513], 'aggregation-induced': [858, 1386], 'emission': [859, 1387, 1750, 1946], 'photosensitizer': [860, 1271], '(named': [861], 'DTCSPY)': [862], 'maximal': [864, 1573], 'restriction': [865, 3590], 'heat': [867, 1344, 1440, 1471, 1492], 'dissipation.': [868, 1493, 1879], 'It': [869, 3673], 'is': [870, 948, 976, 1216, 1282, 1368, 1442, 1520, 1555, 1652, 2129, 2137, 2418, 3236, 3644, 3729, 3747], 'demonstrated': [871], 'that': [872, 918, 1559, 1626, 1770, 1846, 1862, 1900, 2133, 2222, 2370, 2386, 2398, 2407, 2585, 2771, 3218, 3294, 3322, 3373, 3416, 3624, 3946], 'taming': [873, 919, 1593, 1627, 2223, 3625], 'generation': [875, 1316, 1360, 1376, 1441, 1551, 1780, 1843, 1874, 2015, 2064, 2144, 2225, 2308, 2558, 2571, 2822, 3420, 3585, 3627], 'within': [876, 979, 1012, 1317, 2572, 2658, 3421, 4929], 'mitochondria': [877, 1281, 2276, 2573, 3422], 'through': [878, 1343, 1491, 1663, 2248], 'photosensitization-triggered': [879], 'autophagy': [880, 1119, 1152, 1294, 1306, 2578, 2922, 3225, 3243, 3296, 3381, 3397, 3495], 'DTCSPY': [882, 1512, 1554, 1658, 1698, 1723, 1742, 1838, 1881, 1926, 1935, 1950, 2075, 2128, 2179, 2239, 2270, 2311, 2470, 2520, 2587, 2634, 2664, 2686, 2708, 2892, 2929, 3026, 3045, 3064, 3098, 3424, 3537], 'achieved': [883], 'better': [885, 1557, 1633, 1889, 3549], 'neuroprotective': [886], 'effect': [887, 1635, 1651, 2693, 2761, 2802, 2865, 2927, 3003, 3020, 3085, 3109, 3221], 'oxidative': [889, 1609, 2207, 2232, 2580, 2881, 3437, 3634, 3681], 'damages': [890, 1312], 'than': [891, 1558, 1636, 1784, 1845, 1899, 2132, 2901, 3372, 3550], 'N-acety-l-cysteine': [892], 'vitamin': [894, 1076, 1078, 1643, 2873, 2904, 3129], 'C.': [895, 3878, 4001, 4551, 4745, 5167], 'This': [896, 3756], 'work': [897, 3757], 'not': [898, 3674], 'only': [899, 3675], 'provides': [900, 3676], 'new': [902, 1590, 1612, 3601, 3622], 'way': [903, 3602], 'design': [905, 3604], 'high-performance': [906, 1789, 3605], 'photosensitizers': [907], 'regulating': [909, 3608], 'photophysical': [911, 1720, 3609], 'property,': [912], 'but': [913, 1709, 3698], 'also': [914, 1624, 1653, 2190, 3304, 3399, 3699], 'verifies': [915], 'concept': [917, 1591, 3623], 'can': [921, 1091, 1097, 1248, 1389, 1416, 1459, 1487, 2226, 2273, 2574, 2893, 2946, 3425, 3540, 3628, 3684, 3843], 'be': [922, 2860, 2947, 3685, 3844], 'used': [923, 1083, 1639, 2214, 2877, 3187], 'cell': [925, 1019, 1596, 2644, 2951, 2973, 2998, 3146, 3433, 3630], 'protection': [926, 1107, 1309, 1597, 2898, 2935, 2963, 3434, 3631, 3651], 'destructive': [928], 'oxidation,': [929], 'thereby': [930, 1183], 'displaying': [931, 2437], 'broad': [932], 'prospects': [933], 'alleviating': [935], 'oxidation-related': [936], 'diseases': [937, 1041, 1227, 2200], 'promoting': [939], 'cell-based': [940], 'therapy.': [941], 'Download': [942, 944, 1989, 1991, 2192, 2194, 2548, 2550, 3208, 3210, 3506, 3508], 'figure': [943, 1990, 2193, 2549, 3209, 3507], 'PowerPoint': [945, 1992, 2195, 2551, 3211, 3509], 'Introduction': [946], 'contradictory': [950], 'process': [951], 'full': [952], 'dynamic': [954, 974, 988], 'balance,': [955, 966], 'such': [956, 1174, 1479, 3559], 'as': [957, 1073, 1175, 1361, 1363, 1480, 1668, 1715, 1826, 3142, 3560, 3616, 3942, 4263, 4413, 4652], 'immune': [958], 'homeostasis,': [959], 'energy': [960, 1342, 1437, 1490, 2079, 2110, 2169], 'equilibrium,': [961], 'so': [968], 'on.1–3': [969], 'balance': [971, 991, 1264], 'these': [973, 1337, 1496, 2105, 2659], 'systems': [975], 'finely': [977], 'tuned': [978], 'normal': [981, 1013], 'range': [982], 'maintain': [984, 1056, 1085, 1261], 'fitness.': [985], 'Among': [986], 'various': [987], 'systems,': [989], 'has': [992, 1192], 'drawn': [993], 'great': [994, 1409, 3701], 'attention': [995], 'due': [996, 1108, 1346, 1528, 1571, 2816, 3552, 3587], 'its': [998, 2141], 'critical': [999], 'role': [1000], 'extensive': [1002], 'participation': [1003], 'life': [1005], 'disease': [1007, 3712], 'processes.3–5': [1008], 'For': [1009, 1533], 'example,': [1010], 'levels': [1014], 'closely': [1016, 2202], 'involved': [1017, 3395], 'differentiation': [1020], 'development,': [1022], 'whereas': [1023], 'too': [1024], 'much': [1025, 1556, 1782, 2130, 2434, 2799], 'superfluous': [1029], 'oxidized': [1030, 1064, 1258, 2211, 2408], 'substances,': [1031], 'exacerbate': [1033], 'elicit': [1038], 'many': [1039, 1125, 2197], '(e.g.,': [1042, 1121, 1447], 'cancer,': [1043], 'inflammation,': [1044, 3689], 'neurodegenerative': [1045, 3690], 'diseases,': [1046, 3691], 'ischemia-reperfusion': [1048, 3692], 'injury).4–6': [1049], 'developing': [1051], 'agents': [1052, 2878, 3118], 'or': [1053, 2345, 2842, 3696], 'methods': [1054], 'eradicate': [1061], 'wastes': [1065, 1103], 'highly': [1067, 2331], 'At': [1069], 'present,': [1070], 'antioxidants': [1071, 1090, 1640], '(such': [1072], 'N-acetyl-l-cysteine': [1074], '[NAC],': [1075], 'C,': [1077, 2874, 2905], 'E,': [1079], 'etc.)': [1080], 'commonly': [1082], 'balance.7': [1088], 'Although': [1089, 1453, 2093], 'quickly': [1092], 'scavenge': [1093], 'redundant': [1094], 'ROS,': [1095], 'they': [1096, 1327], 'neither': [1098], 'remove': [1099, 1256, 1296], 'nor': [1104], 'generate': [1105, 2992, 3542], 'durable': [1106], 'their': [1110, 1141, 1185], 'quick': [1111], 'redox': [1112], 'mechanism': [1113, 1647], 'living': [1115], 'cells.': [1116, 2674], 'In': [1117, 2353, 2915], 'contrast,': [1118, 2354], 'inducers': [1120, 1153], 'rapamycin,': [1122], 'resveratrol,': [1123], 'natural': [1126], 'compounds)': [1127], 'increase': [1128, 3311], 'level': [1130, 1999, 2100, 2170, 2612, 2784], 'autophagy,': [1132, 3428], 'enables': [1134], 'digest': [1137], 'substances': [1139], 'own': [1142, 1252], 'achieve': [1146], 'long-term': [1148, 2910], 'protection.8': [1149], 'However,': [1150, 3563], 'most': [1151], 'belong': [1154], 'chemotherapy': [1156], 'agents,': [1157], 'lack': [1160], 'specific': [1162, 1208, 1828], 'controllable': [1164, 2569], 'delivery': [1165, 1209, 1232], 'visual': [1167], 'tracking': [1168], 'contribute': [1169], 'some': [1171], 'common': [1172], 'drawbacks,': [1173], 'multiple': [1176], 'targets,': [1177], 'organ': [1178], 'toxicity,': [1179], 'elusive': [1181], 'mechanism,9–11': [1182], 'limiting': [1184, 1469], 'further': [1186, 1477, 1523, 1796, 1871, 2005, 2068, 2396, 2941, 3589], 'application.': [1187], 'Compared': [1188, 2791], 'with': [1189, 1265, 1377, 1385, 1504, 1883, 1957, 2204, 2250, 2277, 2357, 2427, 2445, 2502, 2617, 2705, 2716, 2766, 2792, 2862, 2985, 3041, 3060, 3095, 3116, 3177, 3321, 3407, 3469, 3485, 3496, 3566, 3575, 3578, 4074, 4573, 4712, 4768, 4858, 4969], 'chemotherapy,': [1190, 3697], 'phototherapy': [1191, 1221, 1247], 'inherent': [1194], 'advantages': [1195], 'high': [1197, 2279], 'selectivity': [1198], 'super': [1200], 'spatiotemporal': [1201], 'resolution,': [1202], 'exhibiting': [1203, 1408], 'promising': [1205, 3678], 'prospect': [1206], 'accurate': [1211], 'treatment.12–20': [1212], 'Photodynamic': [1213, 4377, 4453, 4489, 4528], 'therapy': [1214], '(PDT)': [1215], 'successful': [1218], 'demonstration': [1219, 3643], 'precise': [1224], 'treatment': [1225, 2356, 2930, 3156, 3262], 'easily': [1229, 1328], 'achieves': [1230], 'localized': [1231], 'massive': [1234, 3276], 'engineered': [1237], 'control': [1238, 1374, 1418, 2609, 2849, 3143, 3653], 'light.21–25': [1240], 'Inspired': [1241], 'this,': [1243], 'wondered': [1245], 'whether': [1246, 2568, 2943], 'trigger': [1249, 2227, 2575, 2786, 2894, 2997, 3427, 3629, 3649], 'cell’s': [1251, 1287, 1304, 2788], 'protective': [1253, 1634, 1650, 2692, 2760, 2801, 2864, 2926, 3002, 3019, 3084, 3108, 3220], 'components': [1259], 'help': [1267], 'functional': [1270, 1994], '(PS).': [1272], 'According': [1273], 'literature': [1275], 'reports,': [1276], 'moderate': [1277], 'derived': [1279], 'from': [1280, 1473, 1608, 1803, 2955, 3025, 3223, 3332, 3435, 3524, 3669], 'crucial': [1283], 'stimulating': [1285], 'system,': [1289], 'especially': [1290], 'inducing': [1292], 'active': [1293], 'wastes.26,27': [1298], 'Thereby,': [1299], 'proposed': [1301], 'defensive': [1305, 2577], 'enduring': [1308], 'photocontrolled': [1314], 'mitochondria.': [1318], 'Traditional': [1319], 'PSs': [1320, 1384, 1977, 3606], 'usually': [1321], 'possess': [1322], 'conjugated': [1323], 'planar': [1324], 'structures,': [1325, 1401, 2058], 'form': [1329], 'aggregates': [1330, 1396], 'physiological': [1333], 'environment.': [1334], 'After': [1335, 2552, 2728], 'excitation,': [1336], 'PS': [1338], 'will': [1339], 'predominantly': [1340], 'consume': [1341, 1489], 'production': [1345, 1897, 2496], 'strong': [1348, 2394], 'intermolecular': [1349, 1445, 1463, 1579, 3526, 3557], 'π–π': [1350, 1448, 3561], 'interactions': [1351, 1446, 1464, 1580, 3527], 'aggregate': [1354, 1467], 'state,': [1355, 1468], 'leading': [1356], 'reduced': [1358], 'well': [1362], 'fluorescence': [1364, 1394, 1966], 'emission.': [1365], 'it': [1367, 2399], 'hard': [1369], 'accurately': [1371], 'effectively': [1373, 1390, 1460, 3426, 3541], 'traditional': [1378, 1382], 'PSs.28': [1379], 'Contrary': [1380], 'PSs,': [1383, 2107], '(AIE-PSs)': [1388], 'produce': [1391], 'thanks': [1397], 'twisted': [1400, 1455, 1485, 1505, 1868, 2057, 3534], 'strongly': [1403], 'inhibit': [1404, 1461], 'thermal': [1406, 1526, 1576, 1878, 3522], 'decay,': [1407], 'potential': [1410, 3702], 'biomedical': [1412, 1616], 'application.29–33': [1413], 'Thus,': [1414], 'conveniently': [1417], 'required': [1420, 2994], 'amount': [1421, 2654, 2773], 'exact': [1423], 'location': [1424], 'using': [1427, 1598, 2320, 2827, 3251, 3423, 3499], 'AIE-PS-based': [1428], 'phototherapy.': [1429, 3657], 'As': [1430, 1547, 1728, 1831, 2196, 2259, 2625, 2754, 2887, 2965, 3230, 3253, 3350], 'know,': [1432], 'major': [1434], 'pathway': [1435], 'consumption': [1438], 'composed': [1443], 'interaction)': [1449], 'intramolecular': [1451, 1474, 1531, 1582, 3529, 3592], 'motions.34,35': [1452], 'skeleton': [1456, 1708], 'AIE-PS': [1458, 1869, 2346, 2358, 2406, 2618, 2778, 3514], 'decay': [1472, 1577], 'motion': [1475], 'requires': [1476], 'optimization,': [1478], 'flexible': [1481, 1537, 1905], 'alkene': [1482], 'groups': [1483, 3169], 'AIE-PSs': [1486, 1500, 1630, 1772, 2050, 2561], 'still': [1488], 'Based': [1494], 'on': [1495, 2181, 3004, 3829], 'considerations,': [1497], 'two': [1498, 1683, 2106, 3387, 3410], 'mitochondria-targeted': [1499, 2287, 2304, 2555], '(DTCSPY': [1501, 2359], 'DTCSPE)': [1503, 2361, 2669], 'skeletons': [1506], 'were': [1507, 1661, 1685, 1726, 1745, 1752, 1824, 2091, 2318, 2367, 2703, 2735, 2851, 2883, 2958, 2989, 3149, 3172, 3214, 3279, 3398, 3480, 3614], 'designed.': [1508], 'structure': [1510, 1544], 'contains': [1513], 'comparatively': [1515], 'rigid': [1516, 1864, 1885, 3597], 'alkyne': [1517, 1865], 'group,': [1518, 2430, 2924, 3016], 'capable': [1521], 'hindering': [1524, 1877], 'dissipation': [1527, 3523], 'less': [1530], 'motion.': [1532], 'comparison,': [1534, 2677], 'more': [1536, 2438, 2819, 2896], 'alkene-based': [1538, 1906], 'π-bridge': [1539, 1887, 1907], 'was': [1540, 1713, 2002, 2242, 2373, 2400, 2443, 2650, 2670, 2683, 2807, 2931, 2936, 2975, 3027, 3186, 3222, 3249, 3297, 3337, 3369, 3516, 3758, 3827], 'introduced': [1541, 1714], 'into': [1542, 1614], 'DTCSPE.': [1546, 1928], 'expected,': [1548], 'efficiency': [1552, 2103, 2145, 2309, 3586], 'DTCSPE': [1561, 1660, 1700, 1725, 1744, 1804, 1848, 1902, 1937, 1952, 2163, 2177, 2241, 2272, 2313, 2589, 2636, 2688, 2710, 3047, 3100, 3539, 3576], 'both': [1562, 1853, 1892, 2049, 2269, 2299, 2586, 2870, 3525, 3536], 'phosphate-buffered': [1564], 'saline': [1565], '(PBS)': [1566], 'solutions': [1567], 'live': [1569, 2841], 'inhibition': [1574, 3521, 3554], '(both': [1578], 'motions).': [1583], 'Furthermore,': [1584, 3000, 3658], 'propose': [1586], 'demonstrate': [1588, 3620], 'HT22': [1599, 2215, 2245, 2315, 2324, 2376, 2478, 2498, 2563, 2647, 2700, 3037, 3056, 3091, 3113, 3611], 'neuron': [1600, 2199, 2246, 2316, 2377, 2564, 2648, 2673, 2701, 2763, 3612, 3650], 'adipose-derived': [1603], 'stem': [1604, 3666], '(ADSCs)': [1606, 3668], 'suffering': [1607], 'damages,': [1610, 2208, 2882, 3682], 'bringing': [1611], 'insight': [1613], 'application': [1617], 'PSs.': [1619], 'Additionally,': [1620, 2425], 'experimental': [1622, 2606, 3384, 3734], 'results': [1623, 1860, 2095, 2447, 3303, 3413], 'show': [1625, 1769], 'exhibits': [1631, 3700], 'widely': [1638, 2876], '(NAC': [1641], 'C).': [1644], 'biological': [1646], 'behind': [1648], 'illustrated.': [1654], 'Results': [1655], 'Discussion': [1657], 'Knoevenagel': [1664], 'condensation': [1665], 'methylation': [1667], 'shown': [1669, 1729, 1832, 2755, 2888, 3254], 'Figure': [1671, 1731, 1736, 1836, 1919, 2148, 2267, 2383, 2423, 2459, 2628, 2757, 2858, 2867, 2890, 2970, 3031, 3256, 3353, 3358, 3439], '1a': [1672], 'Supporting': [1674, 1734, 1834, 1913, 2265, 2421, 2856, 2968, 3356, 3725, 3727], 'Information': [1675, 1735, 1835, 1914, 2266, 2422, 2857, 2969, 3357, 3726, 3728, 3755, 5192], 'Scheme': [1676], 'S1.': [1677], 'chemical': [1679, 2010], 'structures': [1680, 1924, 2011], 'molecules': [1684], 'fully': [1686], 'characterized': [1687], '1H': [1689], 'NMR,': [1690, 1692], '13C': [1691], 'high-resolution': [1694], 'mass': [1695], 'spectrometry': [1696], '(HRMS).': [1697], 'share': [1701], 'same': [1703, 1793, 2099, 2962], 'electron': [1704, 2020, 2155], 'donating': [1705], 'accepting': [1707], 'different': [1710, 1958, 1976, 1985, 2013, 2071, 2620, 2720, 3042, 3061, 3117, 3453, 3497], 'π-bridges.': [1711], 'Pyridinium': [1712], 'moiety.': [1718], 'Then': [1719], 'properties': [1721], 'investigated.': [1727], '1b': [1732], 'S1,': [1737], 'absorption': [1739], 'maxima': [1740], '490': [1746], 'nm,': [1747, 1758], 'spectra': [1751, 1933], 'centered': [1753], 'at': [1754, 1970, 1997, 2751, 3077, 3101, 3119, 3286, 3339], '700': [1755], '710': [1757], 'respectively,': [1759, 2642], 'dimethyl': [1761], 'sulfoxide': [1762], '(DMSO)/water': [1763], 'mixtures.': [1764], 'Figures': [1765, 1915, 2262, 2416], '1c': [1766, 1909], '1d': [1768, 1911], 'exhibited': [1773, 2433, 2797, 3270, 3570], 'typical': [1774], 'activity': [1776, 1894], 'remarkable': [1778], 'capability': [1781, 1898], 'greater': [1783], 'Rose': [1785], 'Bengal': [1786], '(RB,': [1787], 'PS)': [1790], 'under': [1791, 2622, 3067, 3226], 'condition.': [1794, 3229], 'To': [1795, 2067, 2940, 3636], 'specify': [1797], 'type': [1799], 'generated': [1802, 2374, 2404, 2657, 2776, 3024], 'DTCSPY,': [1806, 1980, 3564], 'singlet': [1807, 1813, 1854, 2087, 2172, 2183], 'sensor': [1809], 'green': [1810], '(SOSG,': [1811], 'detection)': [1815, 1823], 'hydroxyphenyl': [1817], 'fluorescein': [1818], '(HPF,': [1819], 'hydroxyl': [1821, 1857], 'radical': [1822], 'utilized': [1825], 'relevantly': [1827], 'indicators.': [1830], 'S2,': [1837], 'showed': [1839, 2096], 'obviously': [1840], 'stronger': [1841, 2435, 2800], 'ability': [1844, 1875, 2237, 2288], 'terms': [1850], 'producing': [1852], 'radicals.': [1858], 'These': [1859, 3412], 'indicated': [1861, 3293], 'could': [1870, 2391], 'improve': [1872, 3704], 'Accordingly,': [1880], 'decorated': [1882], 'alkyne-based': [1886], 'displayed': [1888, 2350, 2626, 2966], 'performance': [1890, 2073, 3573], 'featuring': [1903], '(Figures': [1908, 2379], 'S2': [1916], 'S3).': [1918], '1': [1920, 2473, 2746], '|': [1921, 2150, 2461, 3033, 3441], '(a)': [1922, 2151, 2471, 2484, 3034, 3442], '(b)': [1929, 2166, 2476, 3053, 3189, 3490], 'Normalized': [1930], 'UV-vis/photoluminescence': [1931], '(PL)': [1932], 'DMSO/water': [1939], '(1:99)': [1940], 'mixture.': [1941], '(c)': [1942, 2481, 3080], 'Plots': [1943, 1964], 'relative': [1945], 'intensity': [1947, 1967], '(I/I0)': [1948], 'mixtures': [1954], 'DMSO/toluene': [1956], 'toluene': [1959], 'fractions': [1960], '(vol': [1961], '%).': [1962], '(d)': [1963, 3105, 3171], 'DCF': [1969, 2333, 2351], '520': [1971], 'nm': [1972], 'PBS': [1974, 2457], 'involving': [1975], '(5': [1978], 'μM):': [1979], 'DTCSPE,': [1981, 2077, 2135, 3066], 'RB': [1983, 3582], 'versus': [1984, 3167], 'irradiation': [1986, 2342, 2697, 2718, 2768, 3069, 3268], 'times,': [1987], 'respectively.': [1988, 3104], 'Density': [1993, 4971], 'theory': [1995], '(DFT)': [1996], 'CAM-B3LYP/6-31G(d,p)': [2001], 'conducted': [2003, 3215], 'understand': [2006], 'relationship': [2008], 'between': [2009, 2086, 2112, 2295, 2467, 2483, 2845], 'performance.36': [2016], 'Optimized': [2017, 2152], 'geometries': [2018, 2153], 'cloud': [2021, 2156], 'distribution': [2022, 3233, 3272], 'separately': [2023], 'depicted': [2024, 2260, 2419, 3351], 'comparable': [2026], 'large': [2027], 'dihedral': [2028], 'angle': [2029], 'stilbene': [2032], 'segment': [2033], '(>21°)': [2034], 'relatively': [2036, 3596], 'distant': [2037], 'highest': [2038], 'occupied': [2039], 'molecular': [2040, 2044], 'orbital': [2041, 2045], '(HOMO)–lowest': [2042], 'unoccupied': [2043], '(LUMO)': [2046], 'separation': [2047], '(Figure': [2051, 2146, 2335, 2343, 2347, 2601], '2a),': [2052], 'contributes': [2054], 'activity,': [2060], 'efficient': [2062, 2119, 2371, 2439, 2820], 'aggregates.': [2066], 'explain': [2069], 'gap': [2080], '(ΔE)': [2081], 'spin-orbital': [2083], 'coupling': [2084], '(SOC)': [2085], 'triplet': [2089, 2174], 'states': [2090, 2175], 'analyzed.37': [2092], 'almost': [2097], 'SOC': [2102, 2187], 'small': [2109], 'difference': [2111], 'S1': [2113], 'T2': [2115], '(ΔES1-T2)': [2116], 'indicates': [2117, 3458], 'channel': [2120], 'intersystem': [2122], 'crossing': [2123], '(ISC).': [2124], 'Moreover,': [2125, 2826, 3386], 'ΔES1-T2': [2126], 'smaller': [2131], 'mainly': [2138, 3269], 'responsible': [2139], 'higher': [2142, 3371], '2b).': [2147], '2': [2149], 'distributions': [2157], 'HOMO': [2159], 'LUMO': [2161], 'DTCSPY.': [2165, 2914], 'Diagram': [2167], 'based': [2180], 'optimized': [2182, 2605, 3228], 'geometries.': [2184], 'ΔE': [2185], 'constants': [2188], 'indicated.': [2191], 'serious': [2198, 3670], 'associated': [2203], 'imbalance,': [2206], 'overloaded': [2210], 'wastes,38,39': [2212], 'murine': [2216], 'hippocampal': [2217], 'neuronal': [2218, 2479, 2499, 3038, 3057, 3092], 'validate': [2221], 'damages.': [2233, 3635], 'First,': [2234, 2582], 'evaluated': [2243], 'costaining': [2249], 'commercial': [2251], 'mitochondrial': [2252], 'probe': [2253], 'Mito-Tracker': [2254], 'Deep': [2255], 'Red': [2256], 'FM': [2257], '(MTDR).': [2258], '3a–3c': [2263], 'S4,': [2268], 'illuminate': [2274], 'signal': [2280], 'background': [2282], 'ratio': [2283, 3361], 'because': [2284, 2803], 'excellent': [2286], 'activity.': [2291], 'Pearson’s': [2292], 'correlation': [2293], 'coefficient': [2294], 'DTCSPY/DTCSPE': [2296], 'MTDR': [2298, 2475], 'reached': [2300], '∼0.86,': [2301], 'suggesting': [2302, 2770, 2933, 3017, 3379], 'outstanding': [2303], 'capability.': [2305], 'Subsequently,': [2306], 'investigated': [2319], '2′,7′-dichlorodihydrofluorescein': [2321], 'diacetate': [2322], '(DCF-DA).': [2323], 'cannot': [2326], 'oxidize': [2327], 'DCF-DA': [2329, 2409, 2504, 2516, 2522, 2529], 'green-emissive': [2332], 'themselves': [2334], '3d),': [2336], 'without': [2340, 3154, 3260, 3266], 'light': [2341, 2363, 2531, 2623, 2717, 2824, 3068, 3267, 3290], '3e)': [2344], '3f)': [2348], 'hardly': [2349], 'fluorescence.': [2352], 'after': [2355, 3289], 'irradiation,': [2364, 3291], 'significant': [2365], 'signals': [2366], 'observed,': [2368], 'indicating': [2369, 2652], '3g': [2380], '3h).': [2382], '3i': [2384], 'shows': [2385], 'NAC': [2387, 2871, 2902], '(a': [2388], 'scavenger)': [2390], 'suppress': [2392], 'signal,': [2395], 'demonstrating': [2397, 2906], 'indeed': [2401], 'DCF.': [2411, 2537], 'quantitative': [2413, 3447], 'analysis': [2414, 3205, 3448, 3492, 3503], '3d–3i': [2417], 'S5.': [2424], 'compared': [2426, 2984, 3320, 3406, 3574], 'DTCSPE-treated': [2429, 2793], 'DTCSPY-treated': [2431, 2795, 2847], 'fluorescence,': [2436], 'generation,': [2441], 'consistent': [2444, 2861], 'theoretical': [2450], 'calculation': [2451], 'vitro': [2454], 'tests': [2455], 'solutions.': [2458], '3': [2460], '(a–c)': [2462], 'CLSM': [2463, 2492, 3444], 'images': [2464, 2493, 3445], 'colocalization': [2466], '5': [2468, 2539, 2726, 3073, 3440], 'μM': [2469, 2474, 2662, 2667, 2682, 2707, 2740, 3097], 'cells;': [2480], 'overlap': [2482], '(b);': [2486], 'Scale': [2487, 2544, 3460], 'bar:': [2488, 2545, 3461], '10': [2489, 3134, 3462], 'μm.': [2490, 2547, 3463], '(d–i)': [2491], 'indicate': [2494], 'treated': [2501, 2715, 3040, 3094, 3115], 'pure': [2503], '(d),': [2505], '“DTCSPY': [2506, 2527, 2980, 3011, 3163, 3282, 3316, 3365, 3402, 3470], '+': [2507, 2511, 2515, 2517, 2521, 2523, 2528, 2530, 2532, 2981, 3012, 3014, 3164, 3283, 3317, 3366, 3403, 3471], 'DCF-DA”': [2508, 2512], '(e),': [2509], '“light': [2510], '(f),': [2513], '“DTCSPE': [2514], 'light”': [2518, 2524], '(g),': [2519], '(h),': [2525], 'NAC”': [2533], '(i).': [2534], 'Green': [2535], 'fluorescence:': [2536], 'DTCSPE/DTCSPY:': [2538], 'μM;': [2540, 2543, 3128, 3132], 'DCF-DA:': [2541], '25': [2542, 2546], 'verifying': [2553], 'capabilities': [2559], 'cells,': [2565, 2794], 'examined': [2567], 'damage.': [2581, 3438, 3672], 'confirmed': [2584], 'had': [2590], 'good': [2591], 'biocompatibility': [2592], 'darkness': [2594, 3049], '3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium': [2597], 'bromide': [2598], '(MTT)': [2599], 'assay': [2600], '4a).': [2602], 'Then,': [2603], 'conditions': [2607], 'treating': [2614], 'concentrations': [2621, 2632, 3043, 3062], 'irradiation.': [2624, 2825], '4b,': [2629], 'when': [2630], 'incubated': [2631, 2704, 3059], '≤0.5': [2638], '2.5': [2640], 'μM,': [2641], 'viability': [2645, 2974, 3147], '>85%,': [2651], 'ranges': [2660], '(0–0.5': [2661], '0–2.5': [2666], 'tolerable': [2671], 'Next,': [2675, 3328], 'concentration': [2679], '0.5': [2681, 2706, 3096, 3127], 'selected': [2684, 2884, 3615], 'explore': [2690, 2942], 'adjusting': [2695], 'time.': [2698], 'Briefly,': [2699], '90': [2712], 'min,': [2713], 'then': [2714], 'time': [2721], '(0,': [2722], '1,': [2723, 4811], '3,': [2724], 'min).': [2727], 'another': [2729, 3345], '6': [2730, 3287, 3340], 'h': [2731, 2747, 3288, 3341], 'incubation,': [2732], 'subsequently': [2736], 'exposed': [2737], '100': [2739, 3131], 'hydrogen': [2742], 'peroxide': [2743], '(H2O2)': [2744], 'finally': [2749], 'measured': [2750, 3076], '48': [2752, 3102, 3120], 'h.': [2753, 3052, 3079, 3121], '4c,': [2758], 'increased': [2765], 'prolonged': [2767], 'time,': [2769], 'needs': [2779], 'reach': [2781, 2810], 'certain': [2783], 'system.': [2790], 'threshold': [2806], 'easier': [2808], 'provoke': [2812], 'upon': [2823], 'bright-field': [2828], 'confocal': [2830], 'laser': [2831], 'scanning': [2832], 'microscopy': [2833], '(CLSM)': [2834], 'images,': [2835], 'state': [2837, 3547], 'quantity': [2839], 'dead': [2843], 'group': [2850, 2983, 3140, 3153, 3166, 3259, 3265, 3285, 3319, 3368, 3405], 'monitored': [2852], 'found': [2854, 3845], '(': [2855], 'S6)to': [2859], '4c.': [2868], 'Finally,': [2869], 'resisting': [2880], 'comparison.': [2886], '4d,': [2891], 'effective': [2897, 3295], 'H2O2': [2900, 3007, 3087, 3111], 'importance': [2908], 'triggered': [2912], 'addition,': [2916], 'chloroquine': [2919], '(CQ,': [2920], 'an': [2921, 3567, 4709], 'inhibitor)-added': [2923], 'lost,': [2932], 'mediated': [2937], 'autophagy.': [2939, 3030, 3349], 'method': [2945, 3663], 'applied': [2948, 3661], 'other': [2950, 2986, 3168, 3388, 3409], 'types,': [2952], 'ADSCs': [2953, 3005], 'isolated': [2954], 'BALB/c': [2956], 'mice': [2957], 'subjected': [2959], 'protocol.40': [2964], 'S7,': [2971], 'elevated': [2976, 3400], 'significantly': [2977], 'Light”': [2982, 3165, 3284, 3318, 3367, 3404, 3472], 'groups,': [2987, 3378], 'unable': [2990], 'protection.': [2999], 'vanished': [3008], 'Light': [3013, 3122], 'CQ”': [3015], 'provoked': [3021], 'regulated': [3028], '4': [3032, 3200, 3476], 'Viability': [3035, 3054], '24': [3051, 3078], '(50': [3070], 'mW/cm2)': [3071], 'min': [3074], 'Evaluation': [3081], '(100': [3088], 'μM)': [3089], 'h,': [3103], 'Determination': [3106], 'irradiation:': [3123], '50': [3124, 3137], 'mW/cm2;': [3125], 'DTCSPY/DTCSPE:': [3126], 'C:': [3130], 'NAC:': [3133], 'mM;': [3135], 'CQ:': [3136], 'μM.': [3138], 'H2O2-treated': [3139], 'served': [3141], 'group.': [3144, 3203, 3385, 3473], 'All': [3145], 'values': [3148], 'divided': [3150], 'any': [3155, 3261], 'comparison': [3158, 3468], 'convenience.': [3159], 'Statistical': [3160, 3478], 'comparisons': [3161, 3479], 'analyzed': [3173, 3250, 3481], 'one-way': [3175, 3483], 'ANOVA': [3176, 3484], 'Tukey': [3179, 3487], 'post-hoc': [3180, 3488], 'test.': [3181, 3489], 'Unpaired': [3182], 'Student’s': [3183], 't-test': [3184], '(two-tailed)': [3185], '(c).': [3191], '**P': [3192], '<': [3193, 3196, 3465], '0.01;': [3194], '***P': [3195, 3464], '0.001.': [3197], 'n': [3198, 3474], '=': [3199, 3475], 'each': [3202], 'ANOVA,': [3204, 3502], 'variance.': [3207, 3505], 'Further': [3212], 'experiments': [3213], 'confirm': [3217], 'DTCSPY-triggered': [3224], 'punctate': [3232], 'LC3B': [3235, 3248, 3277, 3313, 3330, 3450, 3455], 'one': [3237], 'best': [3240, 3572, 3638], 'hallmarks': [3241], 'induction,': [3244], 'immunofluorescence': [3245], 'staining': [3246], 'CLSM.41': [3252], '5a,': [3257], '“Control”': [3258, 3324, 3375], '“DTCSPY”': [3264, 3326, 3377], 'diffuse': [3271], 'LC3B,': [3274], 'while': [3275], 'puncta': [3278, 3314], 'observed': [3280], 'induced': [3298, 3686], 'DTCSPY-generated': [3300], 'ROS.': [3301], 'Quantified': [3302], 'revealed': [3305], '6.4-fold': [3307], '5.0-fold': [3310], 'groups.': [3327, 3454], 'conversion': [3331], 'full-length': [3333], 'LC3B-I': [3334], 'LC3B-II': [3336], 'detected': [3338], 'western': [3343, 3500], 'blots,': [3344], 'important': [3346], 'hallmark': [3347], '5b': [3354], 'S8,': [3359], 'LC3B-II/LC3B-I': [3363], '1.8-fold': [3370], 'activated': [3380], 'necessary': [3389], 'proteins': [3390], '(ATG5': [3391], 'Beclin': [3393, 5128], '1)': [3394], 'groups.42': [3411], 'together': [3414], 'verified': [3415], 'controlling': [3417], 'Representative': [3443], 'dots': [3451], '(red': [3456], 'signals)': [3457], 'autophagosome.': [3459], '0.001,': [3466], '(sights).': [3477], 'Mechanism': [3491, 4655], 'cytoprotective': [3494], 'treatments': [3498], 'blots.': [3501], 'Conclusion': [3510], 'A': [3511, 4029, 4567], '(DTCSPY)': [3515], 'motions.': [3530], 'Because': [3531], 'structure,': [3535], 'aggregated': [3546], '(much': [3548], 'RB)': [3551], 'interactions,': [3558], 'interaction.': [3562], 'constructed': [3565], 'alkyne-containing': [3568], 'π-bridge,': [3569], '(featured': [3577], 'alkane-containing': [3579], 'π-bridge)': [3580], 'motions': [3593], 'skeleton,': [3598], 'providing': [3599], 'property.': [3610], 'model': [3618], 'our': [3640], 'knowledge,': [3641], 'first': [3646], 'attempt': [3647], 'have': [3660], 'protect': [3665], 'oxidation-induced': [3671], 'strategy': [3679], 'acute': [3688], 'injury,': [3693], 'radiotherapy': [3695], 'survival': [3706], 'therapeutic': [3708], 'hostile': [3711], 'environment': [3713], 'during': [3714], 'stem-cell': [3715], 'transplantation': [3716], 'chimeric': [3718], 'antigen': [3719], 'receptor': [3720], 'T': [3721, 5169], '(CAR': [3722], 'T)-cell-based': [3723], 'therapy.43,44': [3724], 'available': [3730], 'includes': [3732], 'section,': [3735], 'synthetic': [3736], 'procedures,': [3737], 'structural': [3738], 'characterization,': [3739], 'supporting': [3741], 'figures.': [3742], 'Conflict': [3743], 'Interest': [3745], 'There': [3746], 'no': [3748], 'conflict': [3749], 'interest': [3751], 'report.': [3753], 'Funding': [3754], 'financially': [3759], 'supported': [3760], 'Foundation': [3765], '(nos.': [3768, 3780, 3792], '21788102,': [3769], '51873092,': [3770], '51961160730),': [3772], 'Grants': [3775], 'Council': [3776], '16305518,': [3781], '16305618,': [3782], 'N-HKUST609/19,': [3783], 'A-HKUST605/16,': [3784], 'C6009-17G),': [3786], 'Innovation': [3788], 'Technology': [3790], 'Commission': [3791], 'ITC-CNERC14SC01': [3793], 'ITCPD/17-9),': [3795], 'Medicine': [3802], 'Associate': [3803], 'Member': [3804], 'Program': [3805, 3815], '(no.': [3806, 3818], 'MWLC19SC02),': [3807], '2017YFE0132200).': [3819], 'Preprint': [3820], 'Acknowledgment': [3821], 'presented': [3823], 'article': [3826, 3842, 5185], 'posted': [3828], 'preprint': [3831, 3841], 'server': [3832], 'prior': [3833], 'publication': [3835], 'CCS': [3837], 'Chemistry.': [3838], 'corresponding': [3840], 'here:': [3846], 'DOI:': [3847], '10.26434/chemrxiv.13134695.v1': [3848], 'References': [3849], '1.': [3850], 'Honda': [3851], 'K.;': [3852, 3889, 3910, 3913, 3915, 4318, 4517, 4754, 4901, 5036], 'Littman': [3853], 'D.': [3854, 3884, 4179, 4851, 4911, 4940, 5044], 'R.The': [3855], 'Microbiota': [3856], 'Adaptive': [3858], 'Immune': [3859], 'Homeostasis': [3860], 'Disease.Nature2016,': [3862], '535,': [3863], '75–84.': [3864], '2.': [3867], 'López': [3868], 'M.;': [3869, 3896, 3908, 3983, 4040, 4125, 4280, 4427, 4498, 4789, 4795, 5110], 'Varela': [3870], 'L.;': [3871, 4142, 4889, 4912, 5104, 5122], 'Vázquez': [3872], 'M.': [3873, 3940], 'J.;': [3874, 4061, 4135, 4174, 4177, 4193, 4197, 4224, 4322, 4326, 4330, 4334, 4336, 4367, 4408, 4429, 4433, 4435, 4437, 4475, 4479, 4519, 4552, 4556, 4671, 4724], 'Rodríguez-Cuenca': [3875], 'S.;': [3876, 3898, 4116, 4199, 4252, 4328, 4439, 4525, 4545, 4690, 4750, 4761, 4852, 4984, 4986, 5045], 'González': [3877], 'R.;': [3879, 3882, 3891, 3900, 3906, 4002, 4431, 4605, 4821, 5011, 5042], 'Velagapudi': [3880], 'V.': [3881], 'Morgan': [3883], 'A.;': [3885, 4982], 'Schoenmakers': [3886], 'E.;': [3887, 4019, 4988], 'Agassandian': [3888], 'Lage': [3890], 'De': [3892], 'Morentin': [3893], 'P.': [3894, 5010], 'B.': [3895, 4765, 4803, 4916, 5051], 'Tovar': [3897], 'Nogueiras': [3899], 'Carling': [3901], 'D.;': [3902, 4093, 4195, 4246, 4256, 4324, 4369, 4560, 4696, 4763, 4801, 4914, 5032, 5034, 5054, 5108], 'Lelliott': [3903], 'C.;': [3904, 3917, 4087, 4365, 4391, 4686, 4817, 4842, 4883, 4962], 'Gallego': [3905], 'Orešič': [3907], 'Chatterjee': [3909], 'Saha': [3911], 'A.': [3912, 4057, 5013], 'Rahmouni': [3914], 'Diéguez': [3916], 'Vidal-Puig': [3918], 'A.Hypothalamic': [3919], 'AMPK': [3920], 'Fatty': [3922], 'Acid': [3923], 'Metabolism': [3924], 'Mediate': [3925], 'Thyroid': [3926], 'Regulation': [3927, 4611], 'Energy': [3929, 4565, 4924], 'Balance.Nat.': [3930, 3975], 'Med.2010,': [3931], '16,': [3932], '1001–1008.': [3933], '3.': [3936], 'D’Autréaux': [3937], 'B.;': [3938, 4038, 4123, 4284], 'Toledano': [3939], 'B.ROS': [3941], 'Signalling': [3943], 'Molecules:': [3944], 'Mechanisms': [3945], 'Generate': [3947], 'Specificity': [3948], 'Homeostasis.Nat.': [3951], 'Rev.': [3952], 'Mol.': [3953], 'Cell': [3954, 4009, 4614, 4701, 5170], 'Biol.2007,': [3955, 4615], '8,': [3956, 4659, 5076], '813–824.': [3957], '4.': [3960], 'Kawagishi': [3961], 'H.;': [3962, 4058, 4121, 4312, 4469, 4473, 4503, 4509, 4623, 4641, 4726, 4748, 4819, 5120], 'Finkel': [3963], 'T.Unraveling': [3964], 'Truth': [3966], 'about': [3967], 'Antioxidants:': [3968], 'Disease:': [3971], 'Finding': [3972], 'Right': [3974], 'Med.2014,': [3976], '20,': [3977], '711–713.': [3978], '5.': [3981], 'Schieber': [3982], 'Chandel': [3984, 4003], 'N.': [3985, 4004, 4943], 'S.ROS': [3986], 'Function': [3987], 'Redox': [3989], 'Signaling': [3990], 'Stress.Curr.': [3993], 'Biol.2014,': [3994], '24,': [3995], 'R453–R462.': [3996], '6.': [3999], 'Reczek': [4000], 'S.ROS-Dependent': [4005], 'Signal': [4006], 'Transduction.Curr.': [4007], 'Opin.': [4008], 'Biol.2015,': [4010], '33,': [4011, 4383], '8–13.': [4012], '7.': [4015], 'Blokhina': [4016], 'O.;': [4017], 'Virolainen': [4018], 'Fagerstedt': [4020], 'V.Antioxidants,': [4022], 'Damage': [4024], 'Deprivation': [4027], 'Stress:': [4028], 'Review.Ann.': [4030], 'Bot.2003,': [4031], '91,': [4032], '179–194.': [4033], '8.': [4036], 'Levine': [4037], 'Packer': [4039], 'Codogno': [4041], 'P.Development': [4042], 'Inducers': [4045], 'Clinical': [4047], 'Medicine.J.': [4048], 'Clin.': [4049, 5177], 'Investig.2015,': [4050], '125,': [4051], '14–24.': [4052], '9.': [4055], 'Partridge': [4056], 'Burstein': [4059], 'H.': [4060, 4173, 4637, 4640, 4846, 5082], 'Winer': [4062], 'E.': [4063], 'P.Side': [4064], 'Effects': [4065], 'Chemotherapy': [4067, 4101, 4153], 'Combined': [4069], 'Chemohormonal': [4070], 'Therapy': [4071, 4151, 4454, 5153, 5171], 'Women': [4073], 'Early-Stage': [4075], 'Breast': [4076], 'Cancer.JNCI': [4077], 'Monographs2001,': [4078], '2001,': [4079], '135–142.': [4080], '10.': [4083], 'Ma': [4084], 'Y.;': [4085, 4095, 4118, 4140, 4144, 4146, 4203, 4205, 4320, 4332, 4371, 4389, 4500, 4513, 4547, 4626, 4692, 4746, 4893, 4897, 4905, 5106], 'Yan': [4086], 'Guo': [4088, 4850], 'Z.;': [4089, 4133, 4201, 4282, 4363, 4505, 4791, 4881, 5049, 5052], 'Tan': [4090, 4285], 'G.;': [4091, 4131, 4250, 4515, 4558, 4629, 5116], 'Niu': [4092], 'Li': [4094, 4115, 4122, 4192, 4223, 4311, 4331, 4366, 4407, 4426, 4468, 4497, 4514, 4758, 4794, 5035], 'Zhu': [4096, 5105], 'H.Spatio-Temporally': [4098], 'Reporting': [4099], 'Dose-Dependent': [4100], 'Uniting': [4103], 'Dual-Modal': [4104], 'MRI/NIR': [4105], 'Imaging.Angew.': [4106], 'Chem.': [4107, 4215, 4304, 4355, 4419, 4459, 4537, 4596, 4872], 'Int.': [4108, 4216, 4597, 4873], 'Ed.2020,': [4109, 4598, 4874], '59,': [4110, 4875], '21143–21150.': [4111], '11.': [4114], 'Ho': [4119], 'S.': [4120, 4622, 4628, 4631, 4646], 'Deng': [4126], 'X.;': [4127, 4393, 4441, 4507, 4549, 4585, 4688, 4694, 4759, 4799, 4844, 4891, 4895, 4907, 5038, 5118], 'Yang': [4128, 4200, 4392, 5048], 'N.;': [4129, 4632, 4793, 5047, 5124], 'Liu': [4130, 4257, 4561, 4586, 4667, 4727, 4820, 4848, 5041, 5055], 'Lu': [4132, 4319], 'Xu': [4134, 4390, 4466, 4544, 4747, 5121], 'Shi': [4136], 'Q.;': [4137, 4314, 4471, 4728, 4849], 'Han': [4138], 'Wu': [4143, 4253, 4281, 4693, 4884], 'Zhao': [4145, 4506, 4880, 5103], 'Nie': [4147], 'G.Combination': [4148], 'Tumour-Infarction': [4150], 'Co-Delivery': [4156], 'Doxorubicin': [4158], 'Thrombin': [4160], 'Encapsulated': [4161], 'Tumour-Targeted': [4163], 'Nanoparticles.Nat.': [4164, 4930], 'Biomed.': [4165], 'Eng.2020,': [4166], '4,': [4167], '732–742.': [4168], '12.': [4171], 'Vreman': [4172], 'Wong': [4175], 'Stevenson': [4178], 'K.Phototherapy:': [4180], 'Current': [4181], 'Methods': [4182], 'Future': [4184], 'Directions.Semin.': [4185], 'Perinatol.2004,': [4186], '28,': [4187], '326–333.': [4188], '13.': [4191], 'Cui': [4194, 4368], 'He': [4198, 4894], 'Luo': [4204], 'Pu': [4206, 4225, 4372, 4394, 4409, 4504], 'K.Organic': [4207], 'Semiconducting': [4208, 4229], 'Pro-Nanostimulants': [4209], 'Near-Infrared': [4211, 4414], 'Photoactivatable': [4212, 4415], 'Cancer': [4213, 4346, 4379, 4777, 4833, 4870, 5173], 'Immunotherapy.Angew.': [4214], 'Ed.2019,': [4217], '58,': [4218], '12680–12687.': [4219], '14.': [4222], 'K.Development': [4226], 'Organic': [4228, 4734, 5073], 'Deep-Tissue': [4232], 'Optical': [4233, 4829], 'Imaging,': [4234], 'Phototherapy': [4235], 'Photoactivation.Chem.': [4237], 'Soc.': [4238, 4974], 'Rev.2019,': [4239], '48,': [4240], '38–71.': [4241], '15.': [4244], 'Mao': [4245, 5033], 'Hu': [4247, 4553], 'F.;': [4248, 4467, 4554, 4666, 4887], 'Qi': [4249, 4723], 'Ji': [4251, 4749], 'W.;': [4254, 4286, 4316, 4444, 4477, 4522, 4635, 4638, 4644, 4669, 4847, 4885, 5040, 5114], 'B.One-Step': [4258], 'Vivo': [4260], 'Metabolic': [4261], 'Labeling': [4262], 'Theranostic': [4265], 'Approach': [4266, 4569], 'Overcoming': [4268], 'Drug-Resistant': [4269], 'Bacterial': [4270], 'Infections.Mater.': [4271], 'Horiz.2020,': [4272], '7,': [4273], '1138–1143.': [4274], '16.': [4277], 'Ying': [4278], 'Z.': [4279], 'Tu': [4283], 'Jiang': [4287, 4370], 'H.Genetically': [4289], 'Encoded': [4290], 'Fluorescent': [4291, 4341], 'RNA': [4292], 'Sensor': [4293], 'Ratiometric': [4295], 'Imaging': [4296, 4676, 5095], 'MicroRNA': [4298], 'Living': [4300], 'Tumor': [4301], 'Cells.J.': [4302], 'Am.': [4303, 4354, 4458, 4536], 'Soc.2017,': [4305], '139,': [4306], '9779–9782.': [4307], '17.': [4310], 'Yao': [4313, 4470], 'Sun': [4315, 4476, 4796, 4908], 'Shao': [4317, 4499, 4516], 'Chung': [4321], 'Kim': [4323, 4501, 4523, 4621, 4624, 4633, 4642], 'Fan': [4325, 4434, 4474, 4518], 'Long': [4327, 4438], 'Du': [4329, 4436, 4888], 'Yoon': [4335], 'Peng': [4337, 4445, 4480, 4526], 'X.Aminopeptidase': [4338], 'N': [4339], 'Activatable': [4340], 'Probe': [4342], 'Tracking': [4344, 5059], 'Metastatic': [4345], 'Image-Guided': [4348, 4869], 'Surgery': [4349], 'Situ': [4352], 'Spraying.J.': [4353], 'Soc.2020,': [4356, 4538], '142,': [4357, 4539], '6381–6389.': [4358], '18.': [4361], 'Zeng': [4362], 'K.Activatable': [4373], 'Polymer': [4374, 4411], 'Nanoenzymes': [4375], 'Immunometabolic': [4378], 'Therapy.Adv.': [4380], 'Mater.,': [4381, 4400], '2021,': [4382], '2007247.': [4384], '19.': [4387], 'K.Photoactivatable': [4395], 'Protherapeutic': [4396], 'Nanomedicine': [4397], 'Cancer.Adv.': [4399], '2020,': [4401], '32,': [4402, 4836], '2002661.': [4403], '20.': [4406], 'K.Semiconducting': [4410], 'Nanomaterials': [4412], 'Protherapeutics': [4416], 'Cancer.Acc.': [4418], 'Res.2020,': [4420], '53,': [4421], '752.': [4422], '21.': [4425], 'Xia': [4428], 'Tian': [4430, 4845], 'Song': [4440, 4792], 'Foley': [4442, 4520], 'X.Near-Infrared': [4446], 'Light-Initiated': [4447], 'Superoxide': [4449], 'Radical': [4450], 'Generator:': [4451], 'Rejuvenating': [4452], 'Hypoxic': [4456], 'Tumors.J.': [4457], 'Soc.2018,': [4460], '140,': [4461], '14851–14859.': [4462], '22.': [4465], 'Ge': [4472], 'X.Hypoxia-Activated': [4481], 'NIR': [4482], 'Photosensitizer': [4483, 4767], 'Anchoring': [4484], 'Mitochondria': [4487, 4608], 'Therapy.Chem.': [4490, 4678], 'Sci.2019,': [4491], '10,': [4492, 4932], '10586–10594.': [4493], '23.': [4496], 'Xiong': [4510, 4892], 'T.;': [4511, 4938], 'Kang': [4512, 4788], 'X.Unimolecular': [4527], 'O2-Economizer': [4529], 'Overcome': [4531], 'Hypoxia': [4532], 'Resistance': [4533], 'Phototherapeutics.J.': [4535], '5380–5388.': [4540], '24.': [4543], 'Yuan': [4546], 'Cai': [4548, 4584, 4896], 'Liang': [4555, 4691], 'B.Tuning': [4562], 'Singlet-Triplet': [4564], 'Gap:': [4566], 'Unique': [4568], 'Efficient': [4571, 4918], 'Photosensitizers': [4572, 4674], '(AIE)': [4576], 'Characteristics.Chem.': [4577], 'Sci.2015,': [4578], '6,': [4579, 5143], '5824–5830.': [4580], '25.': [4583], 'B.Aggregation-Induced': [4587], 'Emission:': [4588], 'Recent': [4589], 'Advances': [4590], 'Biomedical': [4594, 4809], 'Applications.Angew.': [4595], '132,': [4599], '9952–9970.': [4600], '26.': [4603], 'Scherz-Shouval': [4604], 'Elazar': [4606], 'Z.ROS,': [4607], 'Autophagy.Trends': [4613], '17,': [4616], '422–427.': [4617], '27.': [4620], 'Park': [4627], 'Yu': [4630, 4744], 'Nam': [4636], 'An': [4639], 'Ahn': [4645], 'C.Mitochondrial': [4647], 'Activates': [4649], 'ERK/Autophagy': [4650], 'Pathway': [4651], 'Protected': [4654], 'Deoxypodophyllotoxin-Induced': [4657], 'Apoptosis.Oncotarget2017,': [4658], '111581.': [4660], '28.': [4663], 'Lovell': [4664], 'Zheng': [4672], 'G.Activatable': [4673], 'Rev.2010,': [4679], '110,': [4680], '2839–2857.': [4681], '29.': [4684], 'Ni': [4687, 4843], 'Jia': [4689], 'D.Massively': [4698], 'Evoking': [4699], 'Immunogenic': [4700], 'Death': [4702], 'Focused': [4704], 'Mitochondrial': [4705, 5016], 'Stress': [4707], 'Using': [4708, 4949, 5093], 'Twisted': [4714], 'Structure.Adv.': [4716], 'Mater.2019,': [4717], '31,': [4718], '1904914.': [4719], '30.': [4722], 'Ou': [4725, 4818], 'D.Gathering': [4730], 'Brings': [4731], 'Strength:': [4732], 'How': [4733], 'Aggregates': [4735], 'Boost': [4736], 'Disease': [4737], 'Phototheranostics.Aggregate2021,': [4738], '2,': [4739], '95–113.': [4740], '31.': [4743], 'W.Y.;': [4757], 'Krishnan': [4760], 'Z.Mitochondrion-Anchoring': [4766], 'Characteristics': [4771], 'Synergistically': [4772], 'Boosts': [4773], 'Radiosensitivity': [4775], 'Cells': [4778, 5063, 5092, 5137], 'Ionizing': [4780], 'Radiation.Adv.': [4781], 'Mater.2017,': [4782], '29,': [4783], '1606167.': [4784], '32.': [4787], 'P.;': [4797, 4909, 4941, 5112], 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[4942], 'C.A': [4944], 'New': [4945], 'Hybrid': [4946], 'Exchange–Correlation': [4947], 'Functional': [4948, 4972], 'Coulomb-Attenuating': [4951], 'Method': [4952], '(CAM-B3LYP).Chem.': [4953], 'Phys.': [4954], 'Lett.2004,': [4955], '393,': [4956], '51–57.': [4957], '37.': [4960], 'Adamo': [4961], 'Jacquemin': [4963], 'D.The': [4964], 'Calculations': [4965], 'Properties': [4968], 'Time-Dependent': [4970], 'Theory.Chem.': [4973], 'Rev.2013,': [4975], '42,': [4976], '845–856.': [4977], '38.': [4980], 'Popa-Wagner': [4981], 'Mitran': [4983], 'Sivanesan': [4985], 'Chang': [4987], 'Buga': [4989], 'A.-M.ROS': [4990], 'Brain': [4992], 'Diseases:': [4993], 'Good,': [4995], 'Bad,': [4997], 'Ugly.Oxid.': [5000], 'Med.': [5001], 'Cell.': [5002], 'Longev.2013,': [5003], '2013,': [5004], '963520.': [5005], '39.': [5008], 'Angelova': [5009], 'Abramov': [5012], 'Y.Role': [5014], 'Brain:': [5020], 'From': [5021], 'Physiology': [5022], 'Neurodegeneration.FEBS': [5024], 'Lett.2018,': [5025], '592,': [5026], '692–702.': [5027], '40.': [5030], 'Qin': [5039], 'Chiam': [5043], 'Tomczak': [5046], 'B.Precise': [5056], 'Long-Term': [5058], 'Adipose-Derived': [5061], 'Stem': [5062], 'Their': [5065], 'Regenerative': [5066], 'Capacity': [5067], 'Superb': [5069], 'Bright': [5070], 'Stable': [5072], 'Nanodots.ACS': [5074], 'Nano2014,': [5075], '12620–12631.': [5077], '41.': [5080], 'Pugsley': [5081], 'R.Quantifying': [5083], 'Autophagy:': [5084], 'Measuring': [5085], 'LC3': [5086], 'Puncta': [5087], 'Autolysosome': [5089], 'Formation': [5090], 'Multispectral': [5094], 'Flow': [5096], 'Cytometry.Methods2017,': [5097], '112,': [5098], '147–156.': [5099], '42.': [5102], 'Xiao': [5113], 'Rao': [5115], 'Jin': [5119], 'Sui': [5123], 'Q.Morphine': [5126], 'Induces': [5127], '1-': [5129], 'ATG5-Dependent': [5131], 'Human': [5134, 5156], 'Neuroblastoma': [5135], 'SH-SY5Y': [5136], 'Rat': [5141], 'Hippocampus.Autophagy2010,': [5142], '386–394.': [5144], '43.': [5147], 'Goldman': [5148], 'S.Stem': 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