Two-dimensional nanosheets with high curcumin loading content for multimodal imaging-guided combined chemo-photothermal therapy

Biomaterials 223 (2019) 119470

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Two-dimensional nanosheets with high curcumin loading content for multimodal imaging-guided combined chemo-photothermal therapy

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Feng Liua,b,c, Lin Lina,c, Ying Zhanga,b,c, Shu Shenga,b,c, Yanbing Wanga,c,d, Caina Xua,c,∗∗, Huayu Tiana,b,c,d,∗, Xuesi Chena,b,c,d a

Key Laboratory of Polymer Ecomaterials, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun, 130022, China University of Chinese Academy of Sciences, Beijing, 100049, China c Jilin Biomedical Polymers Engineering Laboratory, Changchun, 130022, China d University of Science and Technology of China, Hefei, 230026, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Two-dimensional nanosheets Curcumin Polydopamine Combined therapy

Nowadays, two-dimensional (2D) nanomaterials with many fascinating physicochemical properties have drawn extensive attention as drug delivery platforms for cancer theranostics. Nevertheless, current existing 2D nanomaterial-based drug delivery systems normally undergo the bottlenecks of hash preparation process, low drug loading content and unsatisfactory therapeutic outcome. Herein, we developed a novel nanoparticles-induced assemble strategy to construct 2D nanosheets with ultra-high curcumin loading content of 59.6 % and excellent stability in water. Furthermore, a distinct photothermal effect and multimodal imaging property after polydopamine coating could be obtained, thereby leading to precise and efficient ablation of tumor in combination of curcumin-induced chemotherapy. More importantly, the design principle of our work offers novel facile strategy to assemble metal-binding drugs into 2D nanomedicine with high drug content and well-defined shapes.

1. Introduction Recently, some families of 2D nanomaterials with extraordinary physicochemical properties have attracted more and more attentions in biomedical applications [1–3]. To date, graphene, carbon-based 2D materials, Bi2Se3 and transition metal dichalcogenides are extensively explored as drug delivery systems (DDS) due to their unique physicochemical properties and high surface-to-volume ratios, showing the outstanding performance in cancer therapy [4–7]. Nevertheless, despite these great advances and potentials, most of current existing 2D nanomaterials were prepared via a “bottom-up” method [8–11], which might encounter various handicaps such as the harsh synthesis environment and inevitable deteriorations of quality and yield. Besides, the previously reported 2D nanomaterials-based DDS normally suffered from a low drug loading content and encapsulation efficiency. Therefore, developing a facile and robust approach for constructing a new drug formulation on the basis of 2D nanomaterial, so as to achieve largely enhanced drug content capability, would be particularly desirable for boosting their potential for cancer theranostics.

Zeolitic imidazolate framework-8 (ZIF-8), constructed by the coordination interaction between zinc ions and 2-methylimidazole, is an ideal nanocarrier for metal-binding drugs delivery. Although employing ZIF-8 as drug carrier for tumor therapy has been widely investigated [12–14], the interactions between ZIF-8 and metal-binding drugs are rarely reported. Herein, we developed a novel facile nanoparticles (NPs)-induced assemble strategy to construct curcumin-involved 2D nanosheets (CM NSs), that was, utilizing ZIF-8 NPs to induce and assist the self-assemble of curcumin. As-constructed CM NSs held advantages of ultra-high curcumin loading content (CLC %) of 59.6 %, which was higher than most of curcumin-involved drug delivery systems (Table S1). After further polymerization of dopamine on the surface of CM NSs, photothermal effect and multi-modal imaging including photoacoustic imaging (PAI), photothermal imaging and fluorescence imaging could be achieved, enabling a noninvasive visualization of distribution profiles at tumor region and accomplishing multimodal imaging guided combined chemotherapy and photothermal therapy (PTT) (Scheme 1). The morphology, components, photothermal effect and PAI property of the rational designed system were investigated

∗ Corresponding author. Key Laboratory of Polymer Ecomaterials, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun, 130022, China. ∗∗ Corresponding author. Key Laboratory of Polymer Ecomaterials, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun, 130022, China. E-mail addresses: [email protected] (C. Xu), [email protected] (H. Tian).

https://doi.org/10.1016/j.biomaterials.2019.119470 Received 2 June 2019; Received in revised form 22 August 2019; Accepted 1 September 2019 Available online 05 September 2019 0142-9612/ © 2019 Elsevier Ltd. All rights reserved.

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Scheme 1. Schematic illustration of (A) Preparation procedure of CMPD NSs and (B) CMPD NSs for multimodal imaging-guided chemo-PTT combined tumor therapy.

SEM images (Fig. S3), ZIF-8 NPs were observed in the products synthesized at mass ratio of 0.5/1 and 1/1. In view of this, we speculated that at the low mass ratio of curcumin to ZIF-8, the amount of curcumin is not high enough to dissociate all the ZIF-8 NPs, resulting the existence of mixture of CM NSs and ZIF-8 NPs, causing the low CLC % of the product. However, with the increasing amount of curcumin, the dissociation of ZIF-8 increased as well, leading to the elevation of the ratio of CM NSs. When the amount of curcumin is high enough to disintegrate the all the ZIF-8 NPs, the CLC % would keep at a relative steady state, meanwhile the CLE % would decrease with increasing amount of curcumin further. In light of these results, CM NSs with high CLC % of 59.6 % and CLE % of 96.7 % were selected for subsequent investigation (Fig. 1A) [20]. Unlike spherical-like morphology of ZIF-8 NPs (Fig. 1B), CM NSs displayed sheet-like morphology with an average diameter of 210 nm (Fig. 1C and D). As shown in Fig. 1E, the zeta potential of CM NSs revealed a significant negatively charged surface (−16.4 mV) compared with that of ZIF-8 (20.7 mV), ascribed to the existence of abundant negatively charged curcumin molecules on the surface of CM NSs [21,22]. As demonstrated in Fig. 1F, The significantly decreased Brunauer-Emmett-Teller (BET) specific surface area of CM NSs (471.0 m2/g) compared with ZIF-8 (921.5 m2/g) implied apparent alteration of structure between CM NSs and ZIF-8 NPs, which was further confirmed by the transformation of crystalline pattern (Fig. S1). SEM-EDS disclosed the presence of zinc element in CM NSs (Fig. S4), whose amount was measured to be 12.2 wt% by inductively coupled plasma mass spectroscopy (ICP-MS) (Table S2). The characteristic peak at 752 cm−1 assigned to bending vibration of imidazole ring as observed in FTIR spectra, which indicated that 2-methylimidazole still existed in the CM NSs (Fig. 1G) [23]. In addition, the existence of 2-methylimidazole was confirmed by the 1H NMR of CM NSs digested in trifluoroacetic acid-d (Fig. 1H).

through a series of characterizations. Cell uptake, cytotoxicity and apoptosis in vitro were well-characterized. In vivo experiments disclosed multimodal imaging guided combined chemo-PTT of polydopamine (PDA)-coated CM NSs (CMPD NSs) enabled effective elimination of tumors with minimal nonspecific damages to normal tissues, demonstrating the great potential of CMPD NSs for cancer theranostics. 2. Results and discussion 2.1. Construction and characterization of CM NSs The construction of CM NSs was depicted in Scheme 1. First, ZIF-8 NPs were synthesized according to the previously reported procedure with modification [15]. The successful synthesis of ZIF-8 NPs was validated by characteristic X-ray diffraction (XRD) result (Fig. S1) [16,17]. It was demonstrated that Zn2+ binding strategy could improve the dispersibility and therapeutic outcome of curcumin [18,19]. Motivated by the building blocks of Zn2+ and 2-methylimidazole in ZIF-8 NPs, we then embarked on investigating the interaction between ZIF-8 NPs and curcumin by incubating them in methanol. Intriguingly, the novel 2D CM NSs were formed after 24 h of incubation. The obvious absorption peak of curcumin at 405 nm appeared in UV–vis spectrum of CM NSs (Fig. S2), demonstrating the existence of curcumin in CM NSs. As evaluated by UV–vis spectra, CLC % of CM NSs increased from 32.8 to 64.7 % with the increasing mass ratio of curcumin to ZIF-8 (curcumin/ ZIF-8) from 0.5/1 to 2/1. Meanwhile, the curcumin loading efficiency (CLE %) reached peak value of 96.7 % at mass ratio of 1.5/1, and then decreased. To explore the reason that CLC % increased with increasing curcumin amount, we then characterized the morphology of products synthesized at different mass ratio of curcumin to ZIF-8. As shown in 2

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Fig. 1. Characterization of ZIF-8 NPs and CM NSs. (A) CLC % and efficiency CLE % of CM NSs constructed from mixing curcumin and ZIF-8 NPs at different weight ratio. SEM images of (B) ZIF-8 NPs and (C) CM NSs. (D) Size, (E) Zeta potential, (F) Nitrogen absorption curves and (G) FTIR spectra of ZIF-8 NPs and CM NSs (In Figure D, inset is the photograph of ZIF-8 NPs and CM NSs solutions). (H) 1H NMR of ZIF-8 NPs and CM NSs digested in trifluoroacetic acid-d. (I) Simulated coordination mode of the 2-methylimidazole/curcumin/Zn2+ complex.

methanol could compete with 2-methylimidazole to coordinate Zn2+ of ZIF-8, causing the dissociation of ZIF-8 and subsequently assemble of Zn2+, curcumin and 2-methylimidazole. Moreover, on account of the rigid plane molecule structure of curcumin, the assemblies tend to be 2D nanostructure.

To further determine the structure of CM NSs, we then quantitatively analyzed components and their interaction modes in CM NSs. As shown in Fig. S5, an obvious absorption peak at 406 nm (assigned to ππ* transition of curcumin) and a shoulder peak at 501 nm (charge transfer between Zn2+ and curcumin) were observed in UV–vis spectra of CM NSs, indicating that the curcumin was binding to Zn2+ in CM NSs. Besides, the coordination interaction between curcumin and Zn2+ was further verified by the FTIR (Fig. S6) [24]. Similarly, the characteristic peak at 419 cm−1 (stretching vibration of Zn–N) in FTIR spectra disclosed that 2-methylimidazole coordinated to Zn2+ as well in CM NSs (Fig. 1G) [25]. Furthermore, the molar ratio of curcumin, 2methylimidazole and Zn2+ calculated from ICP-MS and UV–vis spectra was nearly 1:2:1 (Table S2, Figs. 1A and S7). This result suggested that two 2-methylimidazole molecules and one curcumin molecule were involved in the coordination of one Zn2+ ion, in which one nitrogen atom of 2-methylimidazole was connected to Zn2+, and another could connect to another Zn2+ to form the continuous network (Fig. 1I). Previous studies showed that the 1,3-diketone part of curcumin can transform automatically into a keto-enol tautomeric form, the keto-enol form is more stable and can strongly chelate the metal ions, such as Zn2+ and Cu2+ [18,26]. Since ZIF-8 NPs are constructed by the coordination interaction between Zn2+ and 2-methylimidazole, we speculated the there is strong interaction between ZIF-8 NPs and high amount of curcumin, that is, curcumin with high amount in the

2.2. Construction and characterization of CMPD NSs Recently, PDA materials are drawing increasing attention due to great biocompatibility, biodegradability and capability of adhering onto the surface of diverse types of materials [27–30]. Moreover, the strong absorption in NIR region of PDA makes it a promising candidate to function as an ideal theranostic platform [31–33]. Considering the advantages of PDA as well as bottlenecks of chemotherapy, we then coated PDA on the surface of CM NSs to construct a multifunctional theranostic CMPD NSs for multimodal imaging guided combined tumor chemo-PTT. As-constructed CMPD NSs showed sheet-like morphology with rough surface (Fig. 2A), hydrodynamic size of 350 nm (Fig. 2B) and zeta potential of −25.4 mV (Fig. S8). The rougher surface, increased hydrodynamic size and decreased zeta potential relative to CM NSs suggested the successful coating of PDA, which was further evidenced by color change and a broad absorption band ranging from UV to NIR region (Fig. 2C). SEM-EDS revealed the presence of zinc in CMPD NSs as well (Fig. 2D), which was detected to be 8.1 wt% by ICP3

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Fig. 2. Characterization of CMPD NSs. (A) SEM image, (B) Size, (C) UV–vis absorption spectrum and (D) SEM-EDS of CMPD NSs. In Figure C, inset is the photograph of solution of CMPD NSs. (E) ΔT curves of CMPD NSs solutions with different concentrations irradiated with 808 nm laser (1.0 W/cm2) for 10 min. (F) ΔT curves of CMPD NSs solutions (100 μg/mL) irradiated with 808 nm laser with different power density for 10 min. (G) ΔT curves of CMPD NSs solutions after four cycles of heating and cooling. (H) PAI signal intensity and PAI images of CMPD NSs with different concentration. (I) Stability of CMPD NSs in FBS, cell culture medium and PBS.

PTT. We then investigated the stability of CMPD NSs in cell culture medium, fetal calf serum (FBS) and phosphate buffered saline (PBS). As shown in Fig. 2I, CMPD NSs retained their colloidal stability in cell culture medium, FBS and PBS after 2 days, demonstrating that aggregation or dissociation hardly occurred during incubation duration. The curcumin release behavior of CMPD NSs in PBS with different pH values was evaluated. As revealed in Fig. S10, compared with relatively low curcumin release content of 69.1% in neutral PBS (pH 7.4), the cumulative release of curcumin reached to 92.3% after 48 h in acidic PBS (pH 6.5), demonstrating the pH-responsive release feature of CMPD NSs.

MS (Table S2). The decreased percentage of zinc in CMPD NSs compared with CM NSs could be attributed to the coating of PDA, confirming the existence of PDA. In view of strong and broad absorption in NIR region, the photothermal property of CMPD NSs was studied upon 808 nm NIR laser irradiation. As illustrated in Fig. 2E, the relative temperature change (ΔT) of pure water was only 4 °C under the laser irradiation (808 nm, 1.0 W/ cm2, 10 min). In sharp contrast, the ΔT of CMPD NSs increased from 12.9 to 51.8 °C with the elevated concentration from 50 to 500 μg/mL under the same conditions. In addition, the ΔT curves of CMPD NSs also exhibited laser power dependent manner (Fig. 2F). The reversible heating and cooling process result showed that maximum temperature of CMPD NSs solution negligibly changed during four heating and cooling cycles (Fig. 2G), indicating excellent photothermal stability of CMPD NSs. The photothermal conversion efficiency of CMPD NSs was calculated to be 20.2 % according to previous reported work (Fig. S9) [34], which was comparable with some reported materials used for PTT [35–40]. The excellent heating reproducibility as well as high photothermal conversion efficiency suggested that CMPD NSs held great potential for cancer PTT. The PAI property of CMPD NSs was then evaluated. As shown in Fig. 2H, the PAI signal intensity increased with elevated concentration of CMPD NSs. These results suggested that CMPD NSs might function as theranostic agent for PAI guided chemo-

2.3. Cellular uptake and combined chemo-PTT in vitro Confocal laser scanning microscopy (CLSM) and flow cytometry analysis were conducted to investigate the cellular uptake of CMPD NSs and intracellular curcumin release. As illustrated in Fig. 3A and S11A, CMPD NSs treated HeLa and MCF-7 cells exhibited bright green fluorescence compared with free curcumin, demonstrating that nanomedicine formulation could promote the cell internalization of curcumin. It was worthwhile noting that there was strong fluorescence in both the nucleus region and cytoplasm, suggesting that CMPD NSs could be 4

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Fig. 3. Cellular uptake and combined Chemo-PTT in vitro. (A) CLSM images and (B) Flow cytometry of HeLa cells treated with curcumin and CMPD NSs. (C) Cell viability, (D) Live/dead staining images and (E) Cell apoptosis results of HeLa cells treated with different formulations (n = 3). In Figure A and D, the scale bar are 20 and 100 μm, respectively. In Figure C, D and E, cells in CMPD/L group were irradiated with 808 nm NIR laser (1.0 W/cm2) for 10 min. In Figure D and E, from left to right: Control, Curcumin, CMPD and CMPD/L. *p < 0.05; **p < 0.01; ***p < 0.001.

2.4. Multimodal imaging potential of CMPD NSs in vivo

endocytosed into the cells and curcumin had been released from CMPD NSs. Furthermore, the quantitative flow cytometry analysis results gave similar outcomes (Fig. 3B and S11B). To evaluate the antitumor potential of CMPD NSs, methyl thiazolyl tetrazolium (MTT) assay was conducted to evaluate their in vitro cytotoxicity. HeLa and MCF-7 cells treated with CMPD NSs showed a dosage-dependent cell death, which was much higher than that of free curcumin at the same curcumin doses, the enhanced cytotoxicity could be ascribed to efficient endocytosis of CMPD NSs. In comparison, the CMPD/L group exhibited obviously highest cytotoxicity among all the groups, nearly 90 % HeLa cells and 75 % MCF-7 cells were eradicated at the concentration of 100 μg/mL, revealing the high efficiency of combined chemo-PTT treatment (Figs. 3C and S12). Moreover, the cell cytotoxicity of different treatments was further visualized by live/dead staining and apoptosis analysis, demonstrating that CMPD/L treatment exhibited the most potent tumor cells killing efficacy through the apoptosis pathway (Fig. 3D and E and S13).

We then evaluated the potential of CMPD NSs as a theranostic nanoplatform for in vivo application (Fig. 4A). For PAI, 4T1 tumor-bearing mice were intravenously injected with CMPD NSs and the PAI signal intensity was recorded on the PAI instrument at different time intervals. As observed in Fig. 4B, The PAI signal of tumor site reached the highest level at 12 h post-injection and then decreased with the extension of time, which was consistent with PAI images (Fig. 4C). The thermal images of tumor irradiated with 808 nm NIR laser were visualized by a thermal camera. As shown in Fig. 4D, PBS treated group showed negligible elevation of temperature at tumor site and only reached 36.8 °C. Notably, the tumor temperature reached at 58.4 °C after the 10 min of irradiation (1.0 W/cm2), which was high enough to induce instantaneous and irreversible cell death in the tumors. All these results indicated that CMPD NSs could function as an ideal PAI and photothermal agent for imaging-guided cancer therapy. To investigate biodistribution and tumor accumulation behavior of CMPD NSs, ex vivo fluorescence imaging of 4T1 tumor-bearing mice was further carried out using rhodamine B labeled CMPD NSs (CMPD@ 5

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Fig. 4. Multimodal imaging potential of CMPD NSs in vivo. (A) Schematic illustration of in vivo multimodal imaging potential of CMPD NSs. (B) Quantification of PAI intensity and (C) Representative PAI images of HeLa tumor-bearing living mice at different time points after intravenous injection of CMPD NSs. (D) Photothermal images of HeLa tumor-bearing living mice injected with PBS and CMPD NSs under the 808 nm laser irradiation (1.0 W/cm2, 10 min). (E) Ex vivo fluorescence image of excised major organs and tumor form mice after injected with CMPD NSs solution for 12 h.

RB NSs). As observed in Fig. 4E, there was strong red fluorescence signal at the tumor region, validating efficient tumor accumulation of CMPD@RB NSs. Besides, liver and kidney also displayed visible dim fluorescence, which could be owning to the absorption of the mononuclear phagocyte system and possible renal excretion, respectively. Previously published paper of Chen's group demonstrated that 2D Au nanoring achieved the lowest MPS uptake and highest tumor accumulation compared with Au nanospheres and Au nanoplates of similar size [41]. In view of this, we speculated that the ultra-high tumor target ability of CMPD NSs maybe not only caused by EPR effect, but also contributed by the shape effect due to the enhanced intracellular uptake of materials with irregular shapes.

tumors in this group completely disappeared after treatment as shown in Fig. 5D, proving the admirable potentials of combined chemo-PTT therapy. Moreover, the H&E staining of tumor slides revealed highest ratio of necrosis/latestage apoptosis as observed in CMPD/L group, confirming the excellent therapeutic effect of combined therapy (Fig. 5E). No noticeable side effects such as abnormal weight loss (Fig. S14), major organ damage or inflammation were noted in all groups (Fig. S15), indicating the low systemic toxicity during the treatment. 3. Conclusion In conclusion, we constructed curcumin-involved 2D nanosheets with excellent stability and ultra-high drug loading content through a novel nanoparticles-induced self-assembly strategy. After further polymerization of dopamine on the surface of CM NSs, CMPD NSs possessed capabilities of multimodal imaging and PTT, enabling precise and efficient ablation of tumor. In vivo experimental results demonstrated that CMPD NSs could accomplish multimodal imaging-guided potent combined tumor chemo-PTT with negligible side effect on normal tissues. Moreover, our novel strategy would open new perspectives in the design drug-involved nanomedicine with high drug content and well-defined shape for cancer theranostics.

2.5. Combined chemo-PTT in vivo Efficient combined therapeutic efficiency in vitro as well as excellent photothermal effect would signify the ability of CMPD NSs for chemoPTT cancer therapy in vivo. The therapeutic performance was investigated on HeLa tumor-bearing nude mice. When the tumor volume reached nearly 60 mm3, tumor-bearing mice were randomly divided into PBS, curcumin, CMPD and CMPD/L groups. The intravenously injected dose of curcumin and CMPD were 3.3 and 10 mg/kg in all corresponding groups, respectively. CMPD/L group was irradiated with the 808 nm NIR laser for 10 min at power density of 1.0 W/cm2 (Fig. 5A). As demonstrated in Fig. 5B and C, curcumin, CMPD and CMPD/L groups all showed obvious tumor growth suppression compared with PBS group. As expected, CMPD group exhibited more preferable therapeutic effect than curcumin group due to the improved stability in blood circulation and excellent tumor accumulation of nanosheets formulation. Notably, CMPD/L group exhibited the superior inhibition effect of tumor growth among all groups, two out of four

Acknowledgements The authors are thankful to National Natural Science Foundation of China (51873208, 51520105004, 51833010), National Science and Technology Major Projects for Major New Drugs Innovation and Development (2018ZX09711003-012), National program for support of Top-notch young professionals, Jilin Scientific and Technological Development Program (20180414027GH) for financial support to this 6

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Fig. 5. Combined chemo-PTT in vivo. (A) Treatment schedule of HeLa tumor-bearing mice treated with different formulations. (B) The tumor volume of HeLa tumorbearing mice treated with different formulations as a function of time (n = 4). (C) The average tumor mass of excised tumors on 14th day (n = 4). (D) The photo of excised tumors on 14th day. (E) H&E staining images of tumors on 14th day (scale bar is 100 μm). ***p < 0.001, **p < 0.01.

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