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Biological and Medical Applications of Materials and Interfaces

Facile Fabrication of Nanoscale Porphyrinic Covalent Organic Polymers for Combined Photodynamic and Photothermal Cancer Therapy Yanshu Shi, Sainan Liu, Ying Liu, Chunqiang Sun, Mengyu Chang, Xueyan Zhao, Chunling Hu, and Maolin Pang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b00361 • Publication Date (Web): 11 Mar 2019 Downloaded from http://pubs.acs.org on March 12, 2019

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ACS Applied Materials & Interfaces

Facile Fabrication of Nanoscale Porphyrinic Covalent Organic Polymers for Combined Photodynamic and Photothermal Cancer Therapy Yanshu Shi,†⊥ Sainan Liu,†,‡⊥ Ying Liu,†,§ Chunqiang Sun,† Mengyu Chang,†,‡ Xueyan Zhao,†,§ Chunling Hu,†,‡ and Maolin Pang*,†,‡ †State

Key Laboratory of Rare Earth Resource Utilization, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, P. R. China ‡University of Science and Technology of China, Hefei 230026, P. R. China §Changchun University of Science and Technology, Changchun 130022, P. R. China ABSTRACT: Photodynamic therapy (PDT) of cancers is usually inefficient due to the relatively low level of oxygen in cancer cells, therefore, it needs to combine with other treatment strategies such as chemotherapy or photothermal therapy (PTT) to achieve the best anticancer efficacy. Although porphyrin-containing materials have been widely studied for PDT, the photothermal effect is rarely reported. Herein, nanoscale porphyrin-containing covalent organic polymers (PCOP) were produced via a room temperature solution-based aging method. The resulting nanoparticles possess high photothermal conversion efficiency (21.7%) and excellent photodynamic effect. For the first time, the in vitro and in vivo test indicated an enhanced antitumor efficacy for PCOP with combined PDT and PTT. This study provides an efficient approach to fabricate nano COP, and also demonstrates the great potential of porphyrin-containing COP for biomedical applications.

KEYWORDS: covalent organic polymer; porphyrin; morphology control; photothermal therapy; photodynamic therapy.

1. INTRODUCTION Among the cancer treatment methods, the light-induced and non-invasive phototherapy has received considerable interest due to the simplicity, preciseness and less side effect.1-6 Photothermal therapy (PTT) employs photothermal agents to convert light energy into heat and then kill cancer cells via the hyperthermia effect. Photodynamic therapy (PDT) utilizes the generated toxic reactive oxygen species (ROS) to cause cancer cells apoptosis and necrosis upon laser irradiation.3,5,6 However, due to the extra-active cancer cells, the oxygen level in the tumor site is usually very low, which is also called tumor hypoxia.6,7 Such a low-oxygen condition will severely affect the PDT therapeutic effect. Therefore, single photodynamic therapy sometimes is inefficient and it needs to combine with other treatment strategies such as chemotherapy or PTT to achieve the best anticancer efficacy.4,8-11 For example, Zheng et al. fabricated the porphysome nanoparticles to cope with the low-oxygen condition in hypoxic tumors and found an nanostructure-driven conversion mechanism from PDT to PTT.6 Covalent organic frameworks (COF), covalent organic polymers (COP) or porous organic polymers (POP) are newly emerging porous and functional materials, which are built from versatile organic monomers and linked by covalent bonds.12-15 Owing to the good stability and high surface area, these materials exhibit great potentials in gas storage and separation, catalysis, optoelectronic devices, and energyrelated applications.12-15 Among them, attributed to the inherited merits from the porphyrin functional groups, porphyrin-containing covalent organic frameworks (PCOF) or

polymers (PCOP) attract broad attention.16-23 For example, Yaghi and coworkers prepared porphyrin based COF-366 and COF-367, and systematically investigated their catalytic properties for reduction of CO2.16,20 Jiang et al. fabricated and studied the photo- and proton conductivities for a series of porphyrin-containing COF.19,21,22 Banerjee et al. also reported preparation and application of several porphyrin based COF with outstanding chemical stability and crystallinity.17,23 Until now, PCOF or PCOP were mainly used for catalysis and optoelectronic applications. Therefore, fabrication of novel PCOF or PCOP, and exploration of new applications are of great importance. Porphyrin-containing materials could generate cytotoxic singlet oxygen (1O2) efficiently, which will oxidize biomacromolecules and subsequently lead to the cancer cell apoptosis and necrosis.3,6 Although porphyrin-containing materials have been widely studied for PDT, the photothermal Scheme 1. Preparation and Application of PCOP for PDT and PTT

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effect is rarely reported.7,24,25 It should be mentioned that different from traditional porphyrin-containing materials, porphyrin based conjugated polymers (PCOF and PCOP) are expected to exhibit good stability and photothermal effect owing to the extended conjugated structures and strong π-π stacking interactions.2,26-30 Actually, two dimensional conjugated polymers have been widely studied for PTT.2,26-31 We also prepared metalated COP (MCOP) and Fe-doped poly(p-phenylenediamine) (PPD), and the in vitro as well as in vivo tests proved their feasibility for PTT.26,27 So far, there are no reports about utilization of porphyrincontaining two dimensional conjugated polymers for combined PDT and PTT. Therefore, in this study, nanoscale PCOP constructed from 5,10,15,20-Tetrakis(4aminophenyl)porphine (Tph) and 2,5-Dihydroxy-1,4benzenedicarboxaldehyde (Dha) was synthesized by a room temperature solution-based aging method, and then for the first time, the antitumor efficacy via synergetic PDT and PTT were evaluated in vitro and in vivo (Scheme 1). 2. EXPERIMENTAL SECTION Dha (1 mg, 0.009517 mmol) and Tph (2 mg, 0.01849 mmol) were mixed in 1.5 mL of CH2Cl2 and 0.5 mL of CHCl3, and then aging in the dark for 24 h at room temperature. The products were washed with CH2Cl2 twice. The detailed experimental procedures are shown in SI. 3. RESULT AND DISCUSSION Suitable particle size and water-dispersity are prerequisites for biomedical applications, which will permit long circulation time and better therapeutic efficiency.1-5 Nonetheless, miniaturization of PCOP or PCOF into nanoscale is quite difficult due to the fast speed of Schiff base condensation reaction, and it restricts the biomedical applications of these materials to some extent. Therefore, facile and effective strategies to synthesize nano PCOP or PCOF are greatly needed. Herein, a solution-based room temperature aging method was used to prepare nanosized PCOP. In our previous studies, we have found that solvents indeed affect the morphology of nanomaterials, especially for MOF, COF or COP.32-36 Therefore, we tried different solvents to prepare PCOP, however, only aggregated or non-uniform particles were obtained in most cases (Figure S1). Finally, we chose CH2Cl2

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and CHCl3 as the co-solvent to prepare PCOP in this study, because the monomers of Tph and Dha could be dissolved easily in CH2Cl2 and CHCl3, and a homogeneous solution was formed thereafter, which is quite important for the fabrication of monodispersed PCOP nanoparticles in the following aging process.37-39 Figure 1 shows the scanning electron microscopy (SEM) images, powder X-ray diffraction (PXRD) pattern and Fourier transform infrared spectra (FT-IR) for the as-synthesized products. Spherical monodispersed nanoparticles (about 150 nm) were obtained by such an aging method (Figure 1a,b and S2). The dynamic hydraulic diameter of PCOP was about 200 nm and the zeta potential was tested to be around 30.8 mV (Figure S3). Since the cell membranes is negative, the positive charge permits PCOP nanoparticles to be easily internalized by the cell due to the high affinity.40,41 To further downsizing the PCOP into nanoscale, different acids were introduced to control the morphology of PCOP.26,27,42 Among them, trifluoroacetic acid (TFA) indeed can be used to control the size of PCOP. As shown in Figure S4, spheres with sizes around hundreds of nanometers were obtained in the presence of 0.05 or 0.08 mL of TFA, and the size of PCOP could be reduced to 50-100 nm efficiently by adding 0.1 or 0.2 mL of TFA. However, the nanoparticles are aggregated seriously. The PXRD pattern confirmed the formation of amorphous PCOP (Figure 1c). Absorptions in the range of 3100-3400 cm1 could be found in the FT-IR spectra for Tph and Dha, which were assigned to the N-H (Tph) and O-H (Dha) stretching bands. A strong absorption band ascribed to C=O (Dha) at 1667 cm-1 was also observed. Whereas, for the product, the absorption bands of N-H (Tph), O-H (Dha) and C=O (Dha) were disappeared, while a new absorption band centered at around 1620 cm-1 (C=N) appeared, indicating the occurrence of the Schiff base reaction between Tph and Dha (Figure 1d).16,20,23,26,27,43,44 According to the N2 sorption isotherms (Figure S5), the Brunauer-Emmett Teller (BET) surface area is about 110 m2 g-1. The thermogravimetric analysis (TGA)

Figure 2. Photographs for (a) PCOP (150 μg mL-1, in DMEM) and (b) the whole body of mice after injection with PCOP (0.1 mL, 500 μg mL-1) under laser irradiation (808 nm, 0.8 W cm-2). (c) Temperature change curves of PCOP irradiated with 808 nm laser (1.2 W cm-2). (d) Photostability test for PCOP (150 μg mL-1, 0.4 mL DMEM). Figure 1. (a) and (b) SEM images, (c) PXRD pattern, and (d) FTIR spectra of PCOP.


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ACS Applied Materials & Interfaces curve demonstrated the good thermal stability of the resulting PCOP (Figure S6). All of these results suggested the formation of PCOP by such a solution-based room temperature aging method. The photothermal effect of PCOP was evaluated first. As shown in Figure 2a-2c, the temperature increased with increasing the irradiation times (1-10 min) and concentrations of PCOP (16-200 μg mL-1). The photostability of PCOP under laser irradiation was also tested. After six consecutive on-off cycles, the photothermal effect showed no obvious changes, indicating the excellent photostability of PCOP (Figure 2d).26,27,43,44 The photothermal conversion efficiency of PCOP was about 21.7% (Figure S7).26,27,43-45 Moreover, the photothermal effects of the monomers were also investigated. As shown in Figure S8, Dha didn’t show any photothermal effect under 808 nm laser irradiation (0.9 W cm-2), whereas Tph exhibited weak photothermal effect. However, after the formation of PCOP, a significant temperature increment was observed, indicating the excellent photothermal effect of PCOP. The highly extended conjugated two dimensional structure with strong π-π stacking interactions were probably accounted for the excellent photothermal effect, which is quite similar to the other two-dimensional materials, such as graphene etc.6,11,26-31 After absorbing the light energy, the unique highly ordered periodic honeycomb-like structure facilitated the heat conduction and transportation process, making PCOP an excellent photothermal agent.6,11,26-31 Subsequently, the photodynamic effect of PCOP was investigated. Indocyanine green (ICG) was selected as an indicator to check the generated singlet oxygen.46-48 As shown in Figure 3a, there were several broad bands at 470, 600 and 680 nm, which probably belonged to the π-π* absorptions and porphyrin group of PCOP, respectively.16-23 The absorption of pure ICG at 778 nm decreased a little under laser irradiation

Figure 3. UV-vis spectra of (a) PCOP dispersed in DI water, and (b) ICG solution in the presence of PCOP under 650 nm laser irradiation (180 s, 100 mW cm-2). (c) Fluorescent photographs of HeLa cells incubated with PCOP of different concentrations under 650 nm laser irradiation (10 min, 100 mW cm-2). Cell nuclei were stained by DAPI.

due to the instability of ICG (Figure S9). However, the absorption intensity decreased rapidly under 650 nm laser irradiation after the introduction of PCOP (180 s, 100 mW cm2), implying the excellent photodynamic effect of PCOP (Figure 3b). The generated ROS was also checked by 2,7dichlorodihydrofluorescein diacetate (DCFH-DA).44 The control group was almost colorless. However, in the presence of different concentrations of PCOP, green emission was observed under laser irradiation (Figure 3c). Finally, Vitamin C (ascorbic acid) was introduced as a ROS scavenger to prove the generation of 1O2. In the presence of PCOP and Vitamin C, the absorption of ICG at 778 nm only decreased a little (Figure S9b), which further confirmed the generation of 1O2 under laser irradiation, and also indicated that PCOP could be internalized by the cells efficiently. The possible mechanism and reason for producing ROS is that PCOP contains a large amount of porphyrin functional groups, upon laser irradiation, PCOP was excited to its triplet state, and then highly reactive 1O 2 was generated via various approaches when PCOP returned to its ground state.3,24,49-51 Moreover, we also investigated the photodynamic and photothermal effect of PCOP irradiated by lasers with different wavelengths. Due to the stronger absorption intensity of PCOP at 650 nm than that at 808 nm, PCOP exhibited better photodynamic effect under 650 nm laser irradiation, which is quite similar to the other porphyrin-containing COPs.24,47 However, the photothermal effect of PCOP is negligible under 650 nm laser irradiation (Figure S10). While upon 808 nm laser irradiation, besides the outstanding photothermal effect, PCOP also showed weak photodynamic effect (Figure S11). Therefore, in this study, in order to achieve the best antitumor efficacy, the optimum wavelengths of the laser for PDT and PTT were 650 and 808 nm, respectively. The biocompatibility and cytotoxicity of PCOP was studied by the standard 3-(4,5-dimethythiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT).26,27,43,44 As shown in Figure S12, there were still around 90% of cells alive after 24 h cultivation even at 120 µg mL-1, indicating low cytotoxicity of PCOP. However, with the 650 and/or 808 nm laser irradiation, the cell

Figure 4. (a) Cell viability test against HeLa cells for PCOP, PCOP + 650 nm (PDT), PCOP + 808 nm (PTT) and PCOP + 650 nm + 808 nm (PDT + PTT). (b) Photographs of dissected tumors of different groups. (c) The relative tumor volume and (d) body weight of mice treated with different methods.



over different times were investigated after tail vein injection. As shown in Figure 6a, most PCOP nanoparticles were in liver with few in tumor tissue due to the absence of targeting effect.52 The concentration of PCOP reached the maximum value at 12 h and then gradually decreased in all tested organs, indicating the efficient clearance of PCOP out of the body.43 The amount of PCOP excreted from mice was also tested and high levels of Fe were detected in feces (Figure 6b), further confirming the excretion of PCOP nanoparticles from mice.43

Figure 5. Hematoxylin and eosin (H&E) stained images of major organs of all groups.

viability decreased rapidly, especially for PCOP + 650 nm + 808 nm group (Figure 4a). These results demonstrated the excellent cytotoxicity and photothermal as well as photodynamic effect of PCOP on killing cancer cells under laser irradiation.26,27 In an effort to observe the cellular uptake process for the PCOP nanoparticles, rhodamine B (RhB)-loaded PCOP was prepared, and then incubated with HeLa cells.43,44 The fluorescence intensity gradually increased, indicating more PCOP nanoparticles were uptaken by cells (Figure S13). The internalized PCOP nanoparticles were mainly in the cytoplasm. Furthermore, the in vivo antitumor efficacy of PCOP was studied.26,27,43,44 As shown in Figure 4b,c and S14, the mean tumor volume of the PCOP + PDT + PTT group was the smallest in all groups. The PCOP + PDT and PCOP + PTT groups also exhibit certain antitumor efficacy and the tumor suppression efficacy for PCOP + PTT group is much better than that of PCOP + PDT group. However, for the left three control groups, there are almost no suppressions on the tumor growth. Moreover, the average weight for all mice increased slightly (Figure 4d). Additionally, the pathomorphological analysis results indicated that there were no obvious lesions (Figure 5), which further implied the low in vivo toxicity of PCOP.26,27,43,44 In order to investigate the biodistribution and metabolism process of PCOP, PCOP was post-metalated with Fe, and the exact amount of Fe was determined by ICP/MS. The biodistribution of PCOP in major organs and tumor tissues

4. CONCLUSION Nanoscale porphyrin-containing covalent organic polymer (PCOP) based on 5,10,15,20-Tetrakis(4aminophenyl)porphine (Tph) and 2,5-Dihydroxy-1,4benzenedicarboxaldehyde (Dha) was prepared by a facile solution based aging method at room temperature. The synthesized PCOP exhibited excellent photodynamic and photothermal effect. Both in vitro and in vivo test indicated an enhanced antitumor efficacy and it demonstrated the synergetic PDT and PTT application of porphyrin-containing covalent organic polymer for the first time, which illustrated the great potential of PCOP in the applications of treatment of tumors and also expanded the application of PCOP, especially in the biomedical field. Hopefully, more functional COPs or COFs nanoparticles could be produced via such a room temperature solution-based aging method, and their applications could be broadened in versatile research fields.

ASSOCIATED CONTENT The Supporting Information is available free of charge on the ACS Publications website at http://pubs.acs.org. Experimental details, SEM images, TGA patterns, DLS and zeta potential results, UV-vis spectra, N2 sorption isotherms, cell viability test, photos for cell and mice.

AUTHOR INFORMATION *E-mail: [email protected].

AUTHOR CONTRIBUTIONS ⊥These

authors contributed equally.

Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT This project was financially supported by the National Natural Science Foundation of China (NSFC 21471145), the Science and Technology Development Planning Project of Jilin Province (20170101179JC), and the “Hundred Talents Program” of Chinese Academy of Science (Y620021001).

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Figure 6. (a) The in vivo biodistribution of Fe after intravenous injection of Fe-PCOP. (b) Excretion percentages of PCOP nanoparticles in feces of mice.

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