Degradable Hybrid CuS Nanoparticles for Imaging-Guided Synergistic Cancer Therapy via Low-Power NIR-II Light Excitation

Abstract

Open AccessCCS ChemistryRESEARCH ARTICLE1 May 2021Degradable Hybrid CuS Nanoparticles for Imaging-Guided Synergistic Cancer Therapy via Low-Power NIR-II Light Excitation Yidan Sun, Hua Shi, Xiaoyang Cheng, Luyan Wu, Yuqi Wang, Zhengyang Zhou, Jian He, Hong-Yuan Chen and Deju Ye Yidan Sun State Key Laboratory of Analytical Chemistry for Life Science, Chemistry and Biomedicine Innovation Center (ChemBIC), School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023 , Hua Shi Department of Radiology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210008. , Xiaoyang Cheng State Key Laboratory of Analytical Chemistry for Life Science, Chemistry and Biomedicine Innovation Center (ChemBIC), School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023 , Luyan Wu State Key Laboratory of Analytical Chemistry for Life Science, Chemistry and Biomedicine Innovation Center (ChemBIC), School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023 , Yuqi Wang State Key Laboratory of Analytical Chemistry for Life Science, Chemistry and Biomedicine Innovation Center (ChemBIC), School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023 , Zhengyang Zhou Department of Radiology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210008. , Jian He Department of Radiology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210008. , Hong-Yuan Chen State Key Laboratory of Analytical Chemistry for Life Science, Chemistry and Biomedicine Innovation Center (ChemBIC), School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023 and Deju Ye *Corresponding author: E-mail Address: [email protected] State Key Laboratory of Analytical Chemistry for Life Science, Chemistry and Biomedicine Innovation Center (ChemBIC), School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210023 https://doi.org/10.31635/ccschem.020.202000266 SectionsSupplemental MaterialAboutAbstractPDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareFacebookTwitterLinked InEmail Near-infrared (NIR)-II light-excitable photonic agents capable of generating tumor hyperthermia and cytotoxic free radicals are promising for synergistic phototherapy of tumors. However, the lack of NIR-II excitable agents makes it challenging to achieve combinational tumor phototherapy. Here, the authors have reported on a tumor-targeting and degradable hybrid copper sulfide (CuS) nanoparticle ([email protected]) via loading a hydrophilic Azo initiator (AIBA) into an amphiphilic lipid-encapsulating CuS nanoparticle. [email protected] shows high photothermal conversion efficiency (PCE ≈ 47.5%) at 1064 nm, enabling heat production to trigger tumor hyperthermia and thermal decomposition of AIBA into cytotoxic free alkyl radicals upon irradiation with a 1064-nm laser under low-power density (0.5 W/cm2). Moreover, alkyl radicals can drive degradation of [email protected] and embedded CuS nanodisks, releasing Cu2+ ions that can catalyze a Fenton-like reaction for hydroxyl radical (•OH) production to promote tumor therapy. Findings demonstrate promise for combinational photothermal therapy (PTT), oxygen-independent alkyl radical therapy, and chemodynamic therapy (CDT) of tumors. Download figure Download PowerPoint Introduction Phototherapy that uses light to control tumor cell death has shown promise in cancer treatment due to its non-invasiveness, high spatiotemporal controllability, and reduced side effects.1 Many phototherapy strategies, including photothermal therapy (PTT) and photodynamic therapy (PDT), have been developed to promote cancer treatment. PTT involves the use of photothermal agents that absorb light and generate heat to kill tumor cells upon near-infrared (NIR) light irradiation, permitting localized tumor therapy.2 In recent years, many prominent optically active materials (e.g., organic dyes,3 semiconducting polymers,4 carbon nanotubes,5 two-dimensional [2-D] nanomaterials,6 gold nanomaterials,7 and semiconductor transition metal oxide/sulfide nanomaterials8) have been developed as photothermal agents for tumor PTT. Despite encouraging results, tumor recurrence and metastasis during PTT remain challenging; insufficient heat within tumors, the upregulation of heat shock proteins in tumor cells, and inflammatory responses can lead to incomplete tumor cell death and promote resistance and metastasis.9–13 In addition, in vivo PTT of tumors is usually achieved by raising the tumor temperature >50 °C, which may damage the skin and surrounding normal tissues.14,15 PDT that relies on tumor-localizing photosensitizers to generate singlet oxygen (1O2) and other reactive oxygen species to kill tumor cells upon light excitation represents a supplementary phototherapy to PTT.16 Phototherapy combining PTT with PDT can reportedly lower photothermal temperature and reduce hyperthermia-induced inflammation, thereby substantially improving antitumor efficacy.17,18 However, as PDT is reliant on tumor oxygen (O2) levels,19 the phototherapeutic efficacy of combined PTT/PDT can be compromised by a hypoxic tumor microenvironment. Alternately, O2-independent generation of cytotoxic free alkyl radicals via photothermal decomposition of Azo initiators upon excitation of photothermal agents can reportedly induce tumor cell death.20,21 Such an O2-irrelevant PDT-like therapy can overcome tumor hypoxia and greatly improve therapeutic efficacy against tumors. However, most studies have used photothermal agents with excitation in the NIR-I region (650–950 nm),20–25 which may have low maximum permissible exposure (MPE; e.g., 0.33 W cm−2 at 808 nm) and insufficient tissue penetration depth.26 Considering that NIR-II light (1000–1700 nm) has less tissue scattering, greater penetration depth, and higher MPE (e.g., 1 W/cm2 at 1064 nm) than NIR-I light,27,28 combined therapy that allows for excitation by NIR-II light to produce heat and tumor O2-independent free radicals may be preferable in treating deep-seated hypoxic tumors.29 Yet a lack of efficient NIR-II excitable photothermal agents and free radical generators poses challenges to combinational tumor phototherapy under NIR-II light excitation. Semiconductor copper sulfide (CuS) nanoparticles are prominent photonic materials for molecular imaging and tumor phototherapy.30,31 Given their strong absorption in NIR-I and NIR-II windows, high photothermal conversion efficiency (PCE), and low toxicity, they have been widely used in photothermal tumor ablation.32,33 Recently, some CuS nanoparticles (CuS NPs) have been shown to catalyze a Fenton-like reaction enabling persistent conversion of hydrogen peroxide (H2O2) to highly cytotoxic hydroxyl radicals (•OH) to elicit chemodynamic therapy (CDT) of tumors.34,35 Although CuS NPs present multifunctional benefits for tumor therapy, NIR-II light-excitable CuS NPs capable of combining phototherapy with CDT to eradicate hypoxic tumors have not yet been explored. In this study, we describe the design and synthesis of a tumor-targeting and degradable hybrid CuS NP (denoted as [email protected]) for fluorescence (FL) imaging-guided synergistic phototherapy of cancer under low-power NIR-II light irradiation. We demonstrate that [email protected] can accumulate in tumor cells via folate receptor (FR)-mediated active delivery and endocytosis, producing a strong photothermal effect causing hyperthermia and triggering generation of cytotoxic alkyl radicals and •OH under excitation with a 1064-nm laser. Thus, [email protected] allows for combined PTT, O2-independent PDT-like therapy, and CDT for efficient tumor cell death under normoxic and hypoxic conditions. This study reveals the potential of integrating NIR-II excitable PTT and complementary modalities to enhance tumor therapy. Experimental Method Synthesis of [email protected] CuS nanodisks (CuS NDs; 0.7 mg Cu), 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC; 4 mg), 1,2-distearoyl-sn-glycero-3-phosphoethanolamine-N-[methoxy (polyethylene glycol)-2000] (DSPE-PEG2000-OMe; 3.2 mg), 1,2-distearoyl-sn-glycero-3-phosphoethanolamine-N-[folate (polyethylene glycol)-2000] (DSPE-PEG2000-FA; 0.04 mg), and 1,2-distearoyl-sn-glycero-3-phosphoethanolamine-N-[amino (polyethylene glycol)-2000] (DSPE-PEG2000-NH2; 0.8 mg) were dissolved in a mixed organic solvent consisting of CH3OH (1 mL), CH2Cl2 (5 mL), and hexane (8 mL). The solution was sonicated at room temperature (r.t.) for 5 min before being added to 15 mL aqueous solution containing AIBA (10 mg). The mixture was sonicated with an ultrasonic probe (25% amplitude) for 10 min. Next, the organic solvent was removed under vacuum, and the resultant aqueous solution was sonicated for another 5 min to obtain a transparent solution and then passed through 0.22-μm filters three times. Excess DSPE-PEG and DPPC in solution were removed via ultracentrifugation (30 kDa filter, 4000 rpm, 10 min) with deionized water three times. The stock solution was obtained and kept in the dark at 4 °C. The concentration was determined based on inductively coupled plasma mass spectrometry (ICP-MS). Evaluation of cytotoxicity Cytotoxicity was measured via methyl thiazolyltetrazolium (MTT) assay. Human carcinoma KB cells were seeded on 96-well cell culture plates at a density of 1 × 104 cells per well and grew overnight. Cells were then incubated with either [email protected], [email protected], or CuS-FA at different concentrations (0, 1, 10, 25, 50, 100, 150, and 200 μg/mL) for 4 h. Then, the medium was removed, and the cells were washed three times with phosphate-buffered saline (PBS). Fresh medium (100 μL) was added to each well, and cells were then irradiated with or without a laser (1064 or 808 nm, 0.5 W/cm2) for 5 min. The cells were kept in culture for another 24 h after irradiation. 3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide in PBS buffer (50 μL, 1 mg/mL) was added into each well, and the cells were incubated at 37 °C for 4 h. Then, the culture medium was carefully removed, and dimethyl sulfoxide (DMSO; 100 μL) was added into each well. The absorbance at 490 nm in each well was determined using a microplate reader (Tecan Austria GmbH, Austria). Each experiment was repeated five times. Animals and tumor models BALB/c female nude mice at 5–6 weeks old were purchased from the Model Animal Research Center at Nanjing University (Nanjing, China). Animal care and euthanasia were carried out with the approval of the Institutional Animal Care and Use Committee at Nanjing University. The sentence can be corrected to "To establish subcutaneous (s.c.) tumor models, KB cells (2.0 × 106 cells) were suspended in 50 μL of 50% v/v mixture of matrigel and RPMI-1640 medium (10% fetal bovine serum, 100 U/mL penicillin, and 100 µg/mL streptomycin), and then injected s.c. into nude mice. The length (L) and width (W) of each tumor were measured with a caliper, and tumor volume was calculated using the formula of V = (L × W2)/2. Tumors with a single aspect of ∼5–7 mm were formed after 10–15 days before being used for FL imaging and synergistic therapy. FL imaging of KB tumors in vivo KB tumor-bearing mice were intravenously (i.v.) injected with [email protected] or [email protected] (20 μM Cy 5.5 in 75 μL saline, n = 3). Whole-body FL images were acquired before injection and at 4-, 8-, 12-, 24-, 48-, and 72-h postinjection (excitation: 660 nm; emission: 710 nm). Tumor FL intensities were quantified by region-of-interest measurement using Living Image software (PerkinElmer, Waltham, MA). NIR-II light-excited synergistic therapy of tumors in vivo Mice bearing KB tumors were randomly divided into seven groups (n = 5 per group) according to treatment with (1) PBS, (2) CuS-FA, (3) [email protected], (4) PBS + 1064 nm, (5) CuS-FA + 1064 nm, (6) [email protected] + 808 nm, or (7) [email protected] + 1064 nm. Mice were i.v. injected with either 200 μL PBS, CuS-FA, or [email protected] (250 μg/mL). After 24 h, tumors were irradiated with either an 808- or 1064-nm laser (0.5 W/cm2) for 10 min. An infrared (IR) thermal camera was used to monitor the temperature in mice during irradiation. The tumor volume and body weight of each mouse were measured every 2 days and monitored for up to 16 days. Relative tumor volumes were calculated as V/V0 (V0 denotes tumor volume upon initiation of treatment). All mice were sacrificed on day 16, at which point their tumors were excised and photographed. Results and Discussion Design of tumor-targeting and NIR-II light-excitable [email protected] Figure 1a shows the design of [email protected] via encapsulation of a water-soluble Aza initiator, 2,2′-azobis[2-methylpropionamidine] dihydrochloride (AIBA), within the cavity of hybrid nanoparticles consisting of hydrophobic CuS NDs, amphiphilic phospholipids (DPPC), and polymers (DSPE-PEG2000). Due to strong NIR-II absorption and high PCE, CuS NDs can act as effective NIR-II-excited photothermal agents. We chose AIBA as the free alkyl radical generator due to its high stability at a physiologically relevant temperature (37 °C) and propensity to generate alkyl radicals via heat-induced decomposition. Moreover, its small size and hydrophilicity allow it to easily diffuse out from the lipid layers of hybrid CuS NPs upon degradation. To enhance delivery and uptake into tumor cells, folic acid ligands targeting FRs overexpressed on tumor cells were introduced on the surface of hybrid nanoparticles. A NIR fluorophore (Cy 5.5 with FL emission at 695 nm) was adopted for noninvasive FL imaging-guided therapy. Figure 1b illustrates the general process of NIR-II light-excited synergistic tumor therapy in vivo using [email protected] Upon systemic administration, [email protected] could accumulate in tumor sites via FR-mediated active delivery, producing strong NIR FL to pinpoint tumor tissues. Guided by FL imaging, precise irradiation of [email protected] with a 1064-nm NIR-II laser-generated localized heat in tumor sites. The elevated temperature triggered a strong photothermal effect to evoke hyperthermia in tumors. It also induced thermal decomposition of AIBA into highly reactive free alkyl radicals and N2 within [email protected], which produced high interior pressure to drive [email protected] degradation. Consequently, AIBA alkyl radicals were released into the cell cytoplasm, eliciting PDT-like cytotoxicity against tumor cells. These alkyl radicals also reacted with embedded CuS NDs, triggering their degradation to release Cu2+ into cytoplasm. Cu2+ subsequently reacted with endogenous H2O2 to produce •OH through a Fenton-like reaction, causing additional CDT toward tumor cells. Therefore, [email protected] represents a synergistic therapy combining PTT, O2-independent generation of alkyl radicals for PDT-like therapy, and CDT under low-power NIR-II light excitation to achieve promising antitumor effects. Figure 1 | (a) General design and preparation of [email protected] (b) Proposed mechanism of [email protected] for synergistic PTT, PDT-like therapy, and CDT of tumors under 1064-nm laser irradiation. After systemic administration, [email protected] accumulated in tumors via FR-mediated active delivery, emitting strong Cy 5.5 FL. Upon irradiation with the 1064-nm laser, local heat was generated to enable PTT of tumors. Moreover, the elevated temperature could also trigger thermal decomposition of AIBA into AIBA free alkyl radicals and N2, which further induced [email protected] degradation and CuS NDs decomposition. The cytotoxic AIBA alkyl radicals were burst into cytoplasm to elicit O2-independent PDT-like therapy; meanwhile, the release of Cu2+ could catalyze a Fenton-like reaction that allowed conversion of endogenous H2O2 to •OH for tumor CDT. Download figure Download PowerPoint Preparation of [email protected] To prepare [email protected], oleylamine (OA)-decorated CuS NDs were first synthesized through a modified high-temperature chemical reaction.36 Transmission electron microscopy (TEM) analysis showed that the CuS NDs displayed a uniform structure, with a mean diameter of ∼13 nm and a thickness of ∼3 nm ( Supporting Information Figure S1a). Dynamic light scattering (DLS) analysis confirmed good monodispersity of CuS NDs ( Supporting Information Figure S1b). Elemental mapping revealed the presence of Cu and S in the CuS NDs ( Supporting Information Figure S1c), which was further confirmed via X-ray photoelectron spectroscopy (XPS) ( Supporting Information Figures S2a–S2d). Powder X-ray diffraction (PXRD) pattern analysis indicated that CuS NDs mainly consisted of hexagonal CuS (covellite, JCPDS 06-0464; Supporting Information Figure S2e). Notably, CuS NDs exhibited strong absorption >1000 nm with peak absorbance in the NIR-II window ( Supporting Information Figure S2f). We then prepared hybrid CuS NPs using an emulsion approach,37 which involved amphiphilic lipid-assisted coassembly of hydrophobic CuS NDs, DPPC, and DSPE-PEG2000 in aqueous solutions (Figure 1a). Composites to prepare CuS NPs were optimized first; the optimum weight ratio of DPPC, DSPE-PEG2000, and CuS NDs (based on Cu's mass) was ∼2∶2∶0.35 in CuS NPs, which showed a narrow size distribution, high stability, and low dark cytotoxicity ( Supporting Information Table S1). To minimize premature decomposition under a physiological temperature (37 °C) while maximizing the generation and release of alkyl radicals under NIR-II light stimulation, two Aza initiators with different decomposition temperatures and molecular sizes, AIBA and 2,2′-Azobis[2-(2-imidazolin-2-yl)propane] dihydrochloride (AIBI), were screened ( Supporting Information Figures S3a and S3b). AIBA was deemed superior to AIBI because (1) its longer, 10-h half-life decomposition temperature (Tt1/2,10 h = 56 °C) compared with AIBI (Tt1/2,10 h = 44 °C) made it more stable at 37 °C and (2) its smaller size facilitated the diffusion and release of more alkyl radicals from hybrid CuS NPs upon irradiation under a 1064-nm laser ( Supporting Information Figures S3c and S3d). Therefore, AIBA was chosen as the optimum alkyl radical initiator and readily loaded into the hybrid CuS NPs via emulsion. To further introduce FA ligands and Cy 5.5 fluorophores, a mixture of DSPE-PEG2000-OMe, DSPE-PEG2000-FA, and DSPE-PEG2000-NH2 (79:1:20 by mass) was used as an amphiphilic polymer to prepare [email protected]2, which subsequently coupled with Cy 5.5-NHS ester to generate the desired [email protected] For comparison, AIBA-free CuS NPs (CuS-FA), FA-free untargeted CuS NPs ([email protected]), and CuS NDs-free nanoparticles ([email protected]) were also synthesized. TEM analysis indicated that [email protected] appeared as spherical nanoparticles, with an average size of ∼125 nm. Enlarged TEM images revealed multiple layers of CuS NDs, closely packed on the edge of [email protected] (Figure 2a). Scanning electron microscopy (SEM) images showed a hollow interior of [email protected], which displayed occasionally concave membranes upon enlargement (Figure 2b). DLS analysis indicated that [email protected] had a narrow size distribution in aqueous solution ( Supporting Information Figure S4). Due to the presence of negative Cy 5.5 fluorophores on the surface, the zeta potential of [email protected] was much more negative (−33.23 mV) than that of [email protected]2 (−9.01 mV) ( Supporting Information Figure S3d). As with CuS NDs, [email protected] showed strong absorption in the NIR-II region ( Supporting Information Figure S5), which exhibited a dark green color in aqueous solution (Figure 2c). The molar extinction coefficients at 808 and 1064 nm were ∼1.18 × 103 and ∼2.49 × 103/M cm, respectively, confirming stronger absorption in the NIR-II region than in the NIR-I window. Moreover, [email protected] displayed a characteristic absorption peak of Cy 5.5 at 685 nm and a strong NIR FL emission at 695 nm ( Supporting Information Figure S6). Thermogravimetric analysis (TGA) indicated that the loading capacity and efficiency of AIBA in [email protected] were ∼13.3% and ∼11.8%, respectively ( Supporting Information Figure S7 and Note S1). Based on TGA and UV–Vis absorption, the ratio of mass concentration among AIBA, CuS NDs (based on Cu2+), Cy 5.5, and FA in [email protected] was ∼1.7∶1.0∶0.036∶0.0078 ( Supporting Information Note S1). [email protected] exhibited negligible changes in hydrodynamic size distribution, NIR-I FL at 695 nm, and NIR-II absorbance at 1064 nm in the PBS buffer or RPMI-1640 culture medium for 4 high stability under physiological ( Supporting Information Figure Figure 2 | (a) TEM and an nanoparticle of [email protected] (b) of [email protected] and an nanoparticle shows of [email protected] in of [email protected] at indicated concentration (0, and μg/mL) irradiation with the 1064-nm laser (0.5 W/cm2) for 5.5 min. thermal images of [email protected] solutions after 5.5 min irradiation. of [email (30 μg/mL) irradiation with a 1064-nm laser and 0.5 W/cm2) for 5.5 min. of in [email protected], CuS-FA, or AIBA solution under 1064-nm laser irradiation (0.5 5 FL of in [email protected] solution under 1064-nm laser irradiation (0.5 W/cm2) for 1, and 5 min. thermal images of [email protected] solution irradiation for 1, and 5 min. FL of at nm in PBS, PBS containing [email protected], or [email protected] 1064-nm laser irradiation (0.5 5 min) for of FL of at nm upon in different solutions irradiation (1) PBS, (2) [email protected], (3) CuS-FA, (4) [email protected] + (5) [email protected] + and (6) [email protected] with are mean (n = 3). Download figure Download PowerPoint generation of AIBA alkyl radicals via NIR-II light excitation Next, the photothermal of [email protected] under NIR-II laser irradiation (1064 nm) were The temperature of the [email protected] solution with concentration and density and a concentration of the temperature from to °C after irradiation with the 1064-nm laser at a density of 0.5 which was of its MPE W/cm2). to a temperature under laser irradiation, we the density to 0.8 its MPE W/cm2) ( Supporting Information Figure The temperature of the [email protected] solution (30 μg/mL) under irradiation at 1064 nm was higher than at 808 nm with of thickness ( Supporting Information Figure due to higher tissue at 1064 nm compared with 808 nm. These that irradiation of [email protected] with the 1064-nm laser was superior to that with the laser. The of [email protected] at 1064 nm was ( Supporting Information Figure and Note with that of most other reported NIR-II excitable photothermal agents ( Supporting Information Table The high of [email protected] could be to high absorbance at 1064 nm. The closely packed CuS NDs within [email protected] to the high as After confirming the high of [email protected] at 1064 nm, the thermal decomposition of AIBA into free radicals in [email protected] was via three we used = = as a to free analysis showed after [email protected] with the 1064-nm laser, radical indicated the generation of alkyl radicals (Figure alkyl radical were in the solution containing AIBA or AIBA-free CuS-FA upon that AIBA and CuS NPs a combined in generating free we used as a to monitor free radical The [email protected] solution showed FL after being with the 1064-nm laser, to that upon at °C for 5 min ( Supporting Information Figure As the irradiation was the temperatures and FL of solutions as in the solution containing CuS-FA and free AIBA irradiation (Figure and Supporting Information Figure FL in solutions containing [email protected] or AIBA as the water temperature FL in solutions at 37 °C, negligible generation of free the temperature °C, strong FL free radical generation was ( Supporting Information Figure These that free radical generation in the [email protected] solution was to heat from the strong photothermal effect under 1064-nm irradiation. Notably, [email protected] could the generation of substantially higher FL compared with CuS free [email protected] after irradiation a capacity to produce free radicals (Figure we used as another to the of free radical As shown in Figure and Supporting Information Figure FL in the [email protected] solution irradiation, which well with the FL in Figure and confirmed the generation of free radicals in the acid was added to the the reduced FL was greatly or N2 was added to the reduced FL was These demonstrate that the generation of free radicals from [email protected] of different from of [email protected] and embedded CuS NDs upon NIR-II light excitation We the of [email protected] after irradiation with the 1064-nm laser for 5 min. TEM analysis indicated that some [email protected] and into small nanoparticles and which was confirmed by DLS analysis and with the absorption of [email protected] (Figure which was also in the solution containing CuS NDs and free irradiation ( Supporting Information Figure to the degradation of [email protected], the maximum temperature of the solution repeated irradiation with the 1064-nm laser ( Supporting Information Figure AIBA-free CuS-FA exhibited changes in hydrodynamic and absorption irradiation ( Supporting Information Figure We further the potential release of Cu2+ in the of [email protected] solution after irradiation different Figure shows Cu2+ of CuS in the after 5 which to of CuS after irradiation for 10 min. comparison, a negligible of Cu2+ was in the of CuS-FA solution irradiation for 5 and 10 min. These that NIR-II thermal decomposition of AIBA into free radicals and N2 can drive [email protected] degradation and induce CuS NDs decomposition into Cu2+ Figure | (a) TEM of [email protected] and an nanoparticle after 1064-nm laser

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