Protein-assisted synthesis of nanoscale covalent organic frameworks for phototherapy of cancer

Tingting Sun, Rui Xia, Junli Zhou, Xiaohua Zheng, Shi Liu* and Zhigang Xie*
State Key Laboratory of Polymer Physics and Chemistry, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, 5625 Renmin Street, Changchun 130022, China. E-mail: liushi@ciac.ac.cn; xiez@ciac.ac.cn

Received 29th April 2020 , Accepted 23rd June 2020

First published on 23rd June 2020


Covalent organic frameworks (COFs) represent a promising class of crystalline porous materials in various fields, but their applications as biomaterials are usually limited by the large sizes and low colloid stability in aqueous solution. Inspired by the biomimetic mineralization strategies for preparing nanoparticles, herein a homogeneous and stable porphyrin-based COF material (COF-B) has been developed with the assistance of bovine serum albumin (BSA), which exhibits both photothermal and photodynamic activity under the excitation of a laser at a single wavelength. COF-B possesses not only good water dispersibility, but also robust photostability and biocompatibility. Moreover, COF-B shows excellent phototherapy efficiency with effective inhibition or even complete elimination of tumors upon irradiation. This protein-assisted synthesis of COF materials propels the preparation of stable nanoscale COFs and the application of COFs as highly efficient biomedical materials.


Introduction

Covalent organic frameworks (COFs), as an emerging class of crystalline porous materials which are covalently linked two-dimensional (2D) or three-dimensional (3D) polymeric networks, have attracted increasing interest.1–7 Besides the applications in catalysis,8–11 sensing,12,13 gas storage and separation,14–16 efforts have been made to apply COF materials in biological fields.17–22 However, most of the reported COFs exhibit large sizes and low dispersibility in aqueous solution, which severely limit their further biomedical applications. Biomineralization is a biologically induced self-assembly process for living organisms to fabricate specifical molecular architectures to provide structural protection for soft tissues.23–25 This natural biological process has inspired biomimetic mineralization strategies for developing a general method to encapsulate bioactive molecules within protective exteriors.26 Such strategies can increase the tolerance to organic solvents, and enhance the thermal stability, or extend the shelf-lifetime of functional biomacromolecules.27–30 For instance, a variety of biomacromolecules including proteins, deoxyribonucleic acid (DNA), enzymes and antibodies have been reported to induce the formation of metal organic frameworks (MOFs), and control the morphologies of the porous materials via a biomimetic mineralization process.30–34 Accordingly, considering the good biocompatibility and water solubility of proteins, we hypothesized that the presence of proteins would facilitate the preparation of nanoscale COFs and increase their dispersibility in aqueous media.

Porphyrin and its derivatives have been widely used to construct various MOFs and COFs,35–41 because of their versatility in many fields, such as catalysis,42,43 sensing,44,45 optoelectronics46,47 and biomedical applications.48–50 Due to their outstanding characteristics, some porphyrin derivatives have been approved for clinical use.51,52 Phototherapy including photodynamic therapy (PDT),53–58 phtotothermal therapy (PTT)59–61 and combination of both therapies62,63 is a major application of porphyrins in biomedical fields. Phototherapy has attracted intense attention owing to the low invasiveness, high specificity and minimal side effects in comparison to traditional cancer therapies.64–84 Our group has been committed to the application of porphyrins in phototherapy. For example, photoactive MOF@porous organic polymers (MOF@POP) nanocomposite was designed via a self-template approach for PDT of cancer,85 and in another work, nanocomposite integrating MOF with chlorin-based POP was synthesized for interface enhanced phototherapy.86 Although good phototherapy effect was realized in both works, the high contents of MOF templates in photoactive agents might increase burdens on the organisms.

In this work, nanoscale COFs have been prepared in the presence of protein, which is in favor of forming homogeneous and stable COFs for potential cancer treatments. 5,10,15,20-Tetrakis(4-aminophenyl)-21H,23H-porphyrin (TAPP) and 1,3,5-triformylphloroglucinol (TFP) were used as the building blocks, and bovine serum albumin (BSA), a biocompatible and water soluble medical adjuvant, was selected as a model protein (Scheme 1a). The synthesized COF at the presence of BSA (COF-B) shows uniform morphology and good colloid stability, and TAPP as the building block endows COF-B with both PTT and PDT activity under the excitation of a single laser (685 nm). Furthermore, the combined phototherapy activity of COF-B was well validated by in vitro and in vivo experiments (Scheme 1b). This work not only presents a new approach for preparing stable COFs, but also highlights the potential application of COFs in biomedical fields.


image file: d0qm00274g-s1.tif
Scheme 1 Schematic illustration of (a) the preparation of COF-B and (b) the application of COF-B in combined phototherapy.

Results and discussion

Synthesis and characterizations of COF-B

Firstly, TAPP (Scheme S1, ESI)85,87 and TFP (Scheme S2, ESI)88 were synthesized according to previous methods. Then, COF materials with (COF-B) or without (COF-0) the existence of BSA were synthesized in mixed solvent of methanol and acetone at 40 °C for 24 h by employing TAPP and TFP as building blocks. By altering the feed ratios of BSA, the size and homogeneity of the materials could be adjusted. As shown in transmission electron microscopy (TEM) images (Fig. S1, ESI), the COF possesses optimal morphology and dispersibility when the mass ratio of BSA is 34% in the feed, namely COF-B, so it is selected for subsequent studies. This method of the protein-assisted synthesis of COFs is also applicable to other systems, such as COFs obtained by replacing BSA with ovalbumin (OVA, Fig. S2a, ESI) or TFP with terephthalaldehyde (Fig. S2b, ESI).

The chemical structure of COF-B was confirmed by Fourier transform infrared (FTIR) spectra (Fig. S3, ESI) and 13C cross-polarization magic angle spinning (CP-MAS) solid-state NMR spectrum (Fig. S4, ESI). The newly appeared stretching vibration band of C–N at 1284 cm−1 and the strongly attenuated stretching vibration bands of N–H in the FTIR spectrum of COF-B (Fig. S3, ESI) indicate the successful reaction of the starting materials. And there are also stretching bands of C[double bond, length as m-dash]O and C[double bond, length as m-dash]C appear at 1618 cm−1 and 1574 cm−1 respectively. In 13C CP-MAS solid-state NMR spectrum of COF-B (Fig. S4, ESI), resonances attributed to carbons of ketone and enamine could be observed at 176 and 148 ppm respectively, further confirming the condensation of the reactants.

High-resolution TEM (HR-TEM, Fig. 1a) and scanning TEM (STEM, Fig. 1b) images confirm the uniform spherical morphology of COF-B with sizes of about 200 nm. Compared with COF-0, COF-B showed better stability in water as indicated by the obvious precipitates in COF-0 solution after storage for 4 days (Fig. S5a, ESI). The presence of protein in COF-B could provide the hydrophilic segments, which is beneficial to the enhanced stability. The contacts between BSA and COF materials might include covalent and noncovalent interactions, resulting in the controlled size and good stability. Moreover, COF-B could well maintain the sizes and morphology for up to 4 months (Fig. S5b, ESI). The chemical composition of COF-B displayed in energy dispersive X-ray spectroscopy (EDS) mapping images gives a homogeneous distribution of carbon, nitrogen, oxygen and sulfur elements (Fig. 1b), demonstrating the existence of BSA. Besides, the more negative zeta potential of COF-B than that of COF-0 (Fig. S6, ESI) provides a secondary proof for this. The content of BSA within COF-B was further quantified by thermogravimetric analysis (TGA), and the weight loss of COF-B compared to that of COF-0 gave 4.1 wt% content of BSA (Fig. 1c). The powder X-ray diffraction (PXRD) data confirm the crystallizability of the as-synthesized COF-B (Fig. 1d). In the absorption spectra in Fig. 1e, different from the typical Soret band and three Q bands with lower intensity, COF-B exhibits several broad bands with peaks of similar intensity. The high absorbance at 685 nm of COF-B is beneficial for its phototherapy activity under 685 nm laser illumination. The porosity of COF-B has also been investigated via nitrogen adsorption isotherm. A BET surface area of 406 m2 g−1 for COF-B is observed, and the pore size determined by HK method is 4.7 Å (Fig. 1f). The large surface area of COF-B and its porous structure might be favorable for the adsorption of oxygen and light harvesting, thus in favor of phototherapy of tumors.62


image file: d0qm00274g-f1.tif
Fig. 1 Basic characterizations of COF-B. (a) HR-TEM, (b) STEM and EDS mapping images of COF-B. (c) TGA analysis of COF-0 and COF-B under air atmosphere. (d) PXRD pattern of COF-B. (e) Normalized absorption spectra of COF-B in water and TAPP in acetone. (f) Nitrogen adsorption and desorption isotherms of COF-B measured at 77 K. Inset: Pore size distribution from HK method.

Photothermal performance of COF-B

To verify the phototherapy ability of COF-B, their photothermal performance upon 685 nm laser irradiation was first evaluated. At a fixed laser power density, the increase of temperature exhibited an evident concentration-dependent pattern, whereas only insignificant changes in temperature were observed for pure water without COF-B (Fig. 2a). Furthermore, the temperature elevation of COF-B also possesses a laser power-dependent tendency (Fig. 2b). An infrared (IR) thermal imager was also used to monitor the efficient photothermal conversion performance of COF-B (100 μg mL−1) during laser irradiation, as shown in Fig. 2c. As an important parameter for photothermal agent, the photothermal conversion efficiency (η) determined according to previous method89 is 25.6% (Fig. 2d and Fig. S7, ESI), which is comparable to or a little higher than some reported porphyrin-based COFs,62,90,91 although it is lower than some porphyrin-containing molecules.61,92,93 Then, the photothermal stability of COF-B was investigated via multiple cycles of heating/cooling, and the temperature elevation kept almost unchanged after five cycles (Fig. 2e). The favorable photothermal conversion behavior and stability of COF-B are indispensable for their potential application in PTT of tumors.
image file: d0qm00274g-f2.tif
Fig. 2 Photothermal performance of COF-B. (a) Photothermal conversion behavior of COF-B at different concentrations from 0 to 150 μg mL−1 under 685 nm laser irradiation (0.8 W cm−2). (b) Photothermal conversion behavior of COF-B under 685 nm laser irradiation with power densities from 0.4 to 1.0 W cm−2. (c) IR images of COF-B upon 685 nm laser irradiation (0.8 W cm−2). (d) Photothermal response of COF-B under 685 nm laser irradiation (0.8 W cm−2) and the laser was turned off 10 min later. (e) Temperature variations of COF-B under 685 nm laser irradiation over five cycles of heating/cooling.

Photodynamic activity of COF-B

Considering the widespread application of porphyrin on both PTT and PDT, the ROS generation ability of COF-B induced by 685 nm laser illumination was further studied with indocyanine green (ICG) as a ROS indicator.94–96 Under laser irradiation, the ICG solution with the presence of COF-B showed dramatically decreased absorbance at 778 nm (Fig. 3a) within 60 s, validating the generation of singlet oxygen (1O2). On the contrary, only negligible changes in absorbance were detected in the ICG solution without COF-B (Fig. 3b). More obviously, the quantitative data of the absorption changes (Fig. 3c) further confirmed the photodynamic activity of COF-B upon laser irradiation. Afterwards, the intracellular ROS generation of COF-B in human cervical carcinoma (HeLa) cells under laser irradiation was further investigated by using confocal laser scanning microscopy (CLSM) with DCFH-DA as the indicator. DCFH-DA is nonfluorescent, but it could be oxidized into green fluorescent 2′,7′-dichloroflorescein (DCF) by ROS. As shown in Fig. 3d, obvious green fluorescence is observed in HeLa cells treated with both COF-B and 685 nm laser irradiation (COF-B + Laser) due to the generation of ROS. However, there is negligible green fluorescence in the cells without treatment (Control) and with treatment of COF-B or 685 nm laser irradiation only (COF-B or Laser). These results indicate that COF-B could be applied in PDT of tumors.
image file: d0qm00274g-f3.tif
Fig. 3 Photodynamic activity of COF-B. Time-dependent absorption spectra of ICG solution (a) with or (b) without the presence of COF-B in water after irradiation with 685 nm laser (80 mW cm−2) for different time (0–60 s). (c) Comparison of the decay rate of ICG solution with (red) and without (blue) the presence of COF-B upon irradiation. A0 is the initial absorbance and A is the absorbance at every point in time at 778 nm in (a) (ICG + COF-B) and (b) (ICG). (d) CLSM analysis of ROS generation in HeLa cells after different treatments with DCFH-DA as the probe.

Cellular uptake and cytotoxicity of COF-B toward cancer cells

Effective cellular uptake is imperative for exerting the therapeutic effects of nanoparticles, so the internalization of COF-B by HeLa cells was investigated via CLSM. Cells were incubated with COF-B for 0.5 and 2 h, and then cell nuclei were stained with Hoechst 33258. As shown in Fig. S8 (ESI), all HeLa cells exhibit bright red fluorescence with increasing intensity from 0.5 to 2 h, indicating a time-dependent cellular uptake. To investigate the in vitro phototherapy effect of COF-B, HeLa and murine colon cancer (CT26) cells were selected, and their viabilities after different treatments were studied via 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assays. The cells were first incubated with various concentrations (0–150 μg mL−1) of COF-B, and then irradiated with 0.8 W cm−2 of 685 nm laser for 10 min (Laser) or not (Dark). As shown in Fig. 4a and b, there was no obvious cytotoxicity observed for cells in Dark groups. But for the cells in Laser groups, the viabilities significantly decreased with increasing concentrations of COF-B. Nevertheless, single PDT or PTT showed lower cytotoxicity toward HeLa cells (Fig. S9, ESI). Furthermore, to visualize the phototherapy effect of COF-B, calcein-acetoxymethyl (Calcein-AM) and propidium iodide (PI) staining was employed to differentiate dead (red) and live (green) HeLa cells (Fig. 4c). The cells without any treatment (Control) and those treated with only 685 nm laser irradiation (Laser) or COF-B (COF-B) lived well and showed bright green fluorescence. Nevertheless, nearly all the cells treated with COF-B followed by laser irradiation (COF-B + Laser) exhibited red fluorescence. These results intuitively certified the outstanding therapeutic effect of COF-B upon irradiation.
image file: d0qm00274g-f4.tif
Fig. 4 In vitro phototherapy effect of COF-B. Cell viabilities of (a) HeLa and (b) CT26 cells treated with COF-B without or with 685 nm laser irradiation. Error bars were based on the standard error of mean (n = 4). (c) Fluorescence images of Calcein AM (live cells, green) and PI (dead cells, red) costained HeLa cells after different treatments.

In vivo phototherapy efficacy of COF-B

Inspired by the in vitro therapeutic effect, the in vivo phototherapy efficacy of COF-B on mouse cervical carcinoma (U14) tumor-bearing.

Kunming (KM) mice upon 685 nm laser irradiation was studied. When the average volume of tumors reached ∼100 mm3, the mice were randomly divided into four groups as above, namely, control, COF-B, Laser and COF-B + Laser. After intravenous injection of COF-B (20 mg kg−1) for 6 h, the mice in Laser and COF-B + Laser groups were irradiated with 685 nm laser for 10 min, and the temperature changes of tumors during irradiation were recorded with an IR thermal imager every two minutes. As displayed in Fig. 5a, the tumors in COF-B + Laser group showed a much higher temperature increase than those in Laser group under irradiation, confirming the good photothermal effect of COF-B in vivo. Then, tumor volumes and body weights of mice were monitored every two days until the 12th day. In Fig. 5b, a gradual uptrend in tumor volumes was observed for the mice in Control, COF-B and Laser groups during treatment, and there was no significant inhibitory effect for mice treated with only COF-B or laser. On the contrary, the mice in COF-B + Laser group exhibited obvious repression of tumor progression, indicating that COF-B with laser irradiation could effectively inhibit the tumor growth. After 12 days, all the mice were sacrificed followed by dissection of the tumors. As shown in the photo of excised tumors in Fig. 5c, there were large tumors with similar sizes in Control, COF-B and Laser groups, while in COF-B + Laser group, only two small tumors remained, and the other two tumors even completely disappeared. Hematoxylin and eosin (H&E) staining of tumors further proved the significant tumor inhibition effect of mice in COF-B + Laser group (Fig. 5d). To evaluate the biosafety of COF-B and laser irradiation, the body weights of the mice were recorded and plotted with time. As shown in Fig. S10 (ESI), the gradual increased body weights of the mice suggest that the above treatments have no evident toxic effects on mice. The H&E staining of excised heart, liver, spleen, lung and kidney in Control and COF-B + Laser groups manifests that 685 nm laser irradiation on tumors after intravenous injection of COF-B has no obvious damage to main organs of the mice (Fig. S11, ESI). These results certify that treatments with COF-B and laser irradiation simultaneously possess excellent phototherapy effect and insignificant systemic toxicity, showing great potential for cancer treatment.


image file: d0qm00274g-f5.tif
Fig. 5 In vivo phototherapy effect of COF-B after intravenous injection. (a) IR images of mice in Laser and COF-B + Laser groups upon 685 nm laser irradiation. (b) Changes of relative tumor volumes of mice measured every 2 days. Error bars were based on the standard error of mean (n = 4). (c) Photo of excised tumors after various treatments for 12 days. The red circles indicate the disappeared tumors. (d) H&E staining of tumors in corresponding groups.

Conclusions

In summary, a kind of homogeneous and stable porphyrin-based COF material (COF-B) was developed with the assistance of BSA, which exhibits uniform dimensions and higher colloid stability in water than its counterpart without BSA. Small size and robust stability are in favor of the cellular uptake and cancer treatment upon irradiation. Under irradiation with laser at a single wavelength, COF-B possesses photothermal and photodynamic activity simultaneously with excellent photostability. More importantly, both in vitro and in vivo experiments have certified the potent phototherapy effect and excellent biocompatibility of COF-B. The method proposed here as a new approach for preparing stable COF materials promotes the potential application of COFs in biomedical fields.

Experimental

Synthesis of TAPP, TFP and COFs

The synthesis of TAPP and TFP refers to previous methods.85,87,88 The COFs with different BSA contents were synthesized by varying the feed ratios of BSA. For the synthesis of COF-B, TAPP (13.5 mg, 0.02 mmol), TFP (5.6 mg, 0.027 mmol), BSA (20 mg, 34 wt% feed ratio), acetic acid (6 M, 100 μL), as well as mixed solvent of methanol (20 mL) and acetone (20 mL) were added to a flask (100 mL). The mixture was stirred at 40 °C for 24 h under nitrogen. Then, the target product was obtained after washing with N,N-dimethylformamide, acetone and water for several times via centrifugation (10[thin space (1/6-em)]000 rpm × 10 min). The final product was obtained with a yield of 75%. COFs with BSA feeding ratios of 0, 21 wt% and 51 wt% were also synthesized under the same conditions. Homogeneous COFs were also obtained by replacing BSA with OVA (20 mg) or TFP with terephthalaldehyde (0.027 mmol).

Photothermal performance of COF-B

COF-B at different concentrations (0–150 μg mL−1) was irradiated with 685 nm laser (0.8 W cm−2) for 10 min. The temperature increase of COF-B at a constant concentration (100 μg mL−1) upon 685 nm laser irradiation (0.4–1.0 W cm−2) was also monitored. To measure the photothermal conversion efficiency of COF-B, previous method89 was used. Moreover, the photostability of COF-B upon 685 nm laser irradiation was investigated via recording the temperature variations of COF-B in aqueous solution over five cycles of heating/cooling.

Photodynamic activity of COF-B

In vitro ROS detection of COF-B was performed via a modified method by using ICG as the probe. 3 mL of COF-B (75 μg mL−1) in water containing ICG was illuminated by 685 nm laser (80 mW cm−2) for 60 s. The absorption spectra of the mixture were measured every 10 s. The generation rate of ROS was determined by the relative reduction in absorbance (A/A0) over time, where A0 is the initial absorbance and A is the absorbance at every point in time at 778 nm. For the control experiment, the absorption spectra of ICG solution without COF-B were also recorded under the same conditions.

Intracellular ROS detection

The ROS generated intracellularly was detected by DCFH-DA. First, HeLa cells in COF-B and COF-B + Laser groups were incubated with COF-B (150 μg mL−1) for 4 h, and then they were washed three times followed by addition of DMEM containing DCFH-DA and further incubation for 20 min. The cells in Control and Laser groups were also washed and incubated with DMEM containing DCFH-DA for 20 min. For cells in Laser and COF-B + Laser groups, laser irradiation was applied subsequently (80 mW cm−2, 10 min). Finally, the green fluorescence in cells was detected as soon as possible.

Cellular uptake

HeLa cells were seeded in six-well culture plates (1 × 105 cells well−1) with clean coverslips and cultured for 24 h. Then, the cells were incubated with COF-B (150 μg mL−1) for 0.5 or 2 h, followed by being washed with PBS and fixed with 4% paraformaldehyde. Finally, Hoechst 33258 were used to stain the cellular nuclei.

In vitro phototherapy efficacy

The in vitro cytotoxicity of COF-B was evaluated via MTT assays. HeLa and CT26 cells were seeded in 96-well plates (8 × 103 cells well−1) and cultured for 24 h. Afterwards, cells were incubated with culture medium or COF-B (0–150 μg mL−1) for 4 h. Then, the cells in Laser groups were illuminated with 685 nm laser (0.8 W cm−2, 10 min). Thereafter, cells in both Laser and Dark groups were incubated for another 20 h, and then MTT solution (5 mg mL−1, 20 μL) was added, followed by further incubation for 4 h. Then, the culture medium was removed, and dimethyl sulfoxide (150 μL) was added. At last, the absorbance of the formed formazan product (490 nm) was recorded via a microplate reader. For single PDT group, ice-bath was used to control the temperature of cells.97 For single PTT group, vitamin C (1 mM) was used as the ROS scavenger to inhibit the PDT efficacy of COF-B.98

Live-dead cell staining

First, HeLa cells in COF-B and COF-B + Laser groups were incubated with COF-B (150 μg mL−1) for 4 h. 685 nm laser irradiation (0.8 W cm−2, 10 min) was performed on Laser and COF-B + Laser groups. Then, the cells in four groups were cultured for another 20 h, and Calcein-AM and PI were added to stain the cells for 30 min. Finally, images of the treated cells were obtained from a fluorescence microscope.

In vivo phototherapy efficacy

Animal care and handling procedures were performed according to the guidelines of the Regional Ethics Committee for Animal Experiments. Female KM mice were obtained and raised under required conditions. To evaluate the antitumor effects, U14 xenograft tumors were used. The mice were randomly divided into four groups, namely, Control, COF-B, Laser and COF-B + Laser. After the mice in COF-B and COF-B + Laser groups were intravenously injected with COF-B (20 mg kg−1) for 6 h, the mice in Laser and COF-B + Laser groups were irradiated with 685 nm laser for 10 min. The temperature changes of tumors during irradiation were recorded with an IR thermal imager every two minutes. The tumor dimensions (length and width) and body weights of mice were measured every two days. And the tumor volumes were calculated with the formula: width2 × length/2 (mm3). 12 days later, the mice in four groups were all sacrificed followed by dissection of tumors and main organs.

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

We greatly acknowledge the financial support from the National Natural Science Foundation of China (Project No. 51973214).

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Footnote

Electronic supplementary information (ESI) available: Additional details on materials and characterization; supplemental schemes related to synthetic routes of TAPP and TFP; supplemental figures about TEM images, FTIR spectra, 13C CP-MAS solid-state NMR spectrum, stability of COF-0 and COF-B, zeta potential of COF-0 and COF-B, linear plot of the cooling time versus −ln[thin space (1/6-em)]θ, CLSM images, changes in body weight of mice, and H&E staining of main organs. See DOI: 10.1039/d0qm00274g

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