Potassium Ferrate-loaded Porphyrin-based (VI) Metal-organic Frameworks for Combined Photodymanic and Chemodynamic Tumor Therapy

doi:10.15541/jim20210157

Abstract

Abstract:

Metal-organic frameworks (MOFs) are widely used in biomedicine due to their porous structure, high specific surface area, abundant functional groups with metal active sites, good biocompatibility, and suitable degradability. In this study, a multifunctional composite nanoparticle (Fe(VI)@PCN@BSA) was prepared for combined photodynamic and chemodynamic therapy of tumors, which was constructed by loading potassium ferrate (K₂FeO₄, Fe(VI)) in porphyrin-based MOFs (PCN-224) and following a surface coating with biocompatible bovine serum albumin (BSA). The results showed that the particle sizes of PCN-224 and Fe(VI)@PCN@BSA nanoparticles were about 90 nm and 100 nm, respectively. Interestingly, Fe(VI)@PCN@BSA nanoparticles could catalyze H₂O₂to produce •OH under a simulating tumor environmental condition. Meanwhile, they catalyzed to decompose H₂O₂ to produce O₂, and thereby increased the production of singlet oxygen (¹O₂) under 660 nm laser irradiation, which enhanced the photodynamic effect. More importantly, in vitro evaluation indicated that Fe(VI)@PCN@BSA nanoparticles were biocompatible, and exhibited enhanced photodynamic and chemodynamic combined therapeutic efficacy against tumor cells. Hence, Fe(VI)@PCN@BSA nanoparticles have a great potential application in tumor therapy.

Key words: metal-organic framework, potassium ferrate, tumor microenvironment, combination therapy

CLC Number:

TQ174

WANG Yuwei, CHEN Jiajie, TIAN Zhengfang, ZHU Min, ZHU Yufang. Potassium Ferrate-loaded Porphyrin-based (VI) Metal-organic Frameworks for Combined Photodymanic and Chemodynamic Tumor Therapy[J]. Journal of Inorganic Materials, 2021, 36(12): 1305-1315.

Figures/Tables 11

Fig. 1 TEM images of (a) PCN-224, (b) Fe(VI)@PCN-224 and (c) Fe(VI)@PCN@BSA nanoparticles, and (d) elemental mapping of Fe(VI)@PCN@BSA nanoparticles

Fig. 2 XRD patterns of K2FeO4, PCN-224, Fe(VI)@PCN-224, and Fe(VI)@PCN@BSA nanoparticles

Fig. 3 DLS size distributions of (a) PCN-224, (b) Fe(VI)@PCN-224 and (c) Fe(VI)@PCN@BSA nanoparticles, and (d) Zeta potentials of BSA, PCN-224, Fe(VI)@PCN, and Fe(VI)@PCN@BSA nanoparticles

Fig. 4 Changes of (a) size and (b) Zeta potential of Fe(VI)@PCN@BSA nanoparticles in H2O, PBS and DEME

Fig. 5 (a) UV-Vis absorption spectra of PCN-224, Fe(VI)@PCN-224, and Fe(VI)@PCN@BSA suspensions (inset is pictures of the suspensions), and (b) Fourier transform infrared spectra of BSA, PCN-224, Fe(VI)@PCN-224, and Fe(VI)@PCN@BSA nanoparticles

Fig. 6 Chemodynamic properties of Fe(VI)@PCN@BSA nanoparticles (a) UV-Vis absorption spectra of TMB solutions under different conditions with inset showing photographs of TMB solutions after reaction for 10 min under different conditions; (b) Absorbance changes of TMB solutions with time after adding Fe(VI)@PCN@BSA nanoparticles (50 µg/mL) into TMB solutions under pH 6.0 with H2O2 (10 mmol/L); (c) Absorbance changes of TMB solutions with time after adding Fe(VI)@PCN@BSA nanoparticles (50 µg/mL) into TMB solutions with pH 6.0; (d) Absorbance changes of TMB solutions with time under pH 6.0 with H2O2 (10 mmol/L); (e) Curves of absorbance at 652 nm versus time for TMB solutions with Fe(VI)@PCN@BSA nanoparticles under acidic (pH 6.0) or neutral (pH 7.4) conditions with or without H2O2; (f) Absorbance changes at 652 nm versus time for TMB solutions under pH 6.0 with different concentrations of H2O2 after adding the same amount of Fe(VI)@PCN@BSA nanoparticles

Fig. 7 Changes of dissolved O2 in NaAc solutions under (a) pH 6.0 and (b) pH 7.4 with different H2O2 concentrations after the addition of Fe(VI)@PCN@BSA nanoparticles (50 μg/mL)

Fig. 8 (a-c) UV-Vis absorbance spectra of the DPBF solutions with Fe(VI)@PCN@BSA nanoparticles (50 μg/mL) and (d) absorbance changes of DPBF solutions at 439 nm for different groups (a) Without 660 nm laser irradiation; (b) With 660 nm laser irradiation; (c) With H2O2 (10 mmol/L) and 660 nm laser irradiation

Fig. 9 Cell viabilities of MDA-MB-231 cells and human dermal fibroblasts after 24 h incubation with Fe(VI)@PCN@BSA nanoparticles at different concentrations

Fig. 10 Fluorescence images of MDA-MB-231 cells after different treatments for observing intracellular ROS Control: cells were cultured in normal medium; NPs: cells were cultured in normal medium with Fe(VI)@PCN@BSA nanoparticles; H2O2 (pH 6.0): cells were cultured in the medium at pH 6.0 with H2O2 (100 µmol/L); NPs+H2O2 (pH 6.0): cells were cultured in the medium at pH 6.0 with H2O2 (100 µmol/L) and Fe(VI)@PCN@BSA nanoparticles; Laser: 660 nm laser irradiation after cells culture in normal medium; NPs+Laser: 660 nm laser irradiation after cell culture in normal medium with Fe(VI)@PCN@BSA nanoparticles; NPs+H2O2 (pH 6.0)+Laser: 660 nm laser irradiation after cell culture in the medium at pH 6.0 with H2O2 (100 µmol/L) and Fe(VI)@PCN@BSA nanoparticles

Fig. 11 Synergistic therapeutic effect of Fe(VI)@PCN@BSA nanoparticles on MDA-MB-231 cells (*P < 0.05, **P < 0.01, ***P < 0.001)

References 40

[1]	LIU CHUANG, XING JIE, AKAKURU OZIOMA UDOCHUKWU, et al. Nanozymes-engineered metal-organic frameworks for catalytic cascades-enhanced synergistic cancer therapy. Nano Letters, 2019, 19(8): 5674-5682. DOI URL
[2]	TANG ZHONGMIN, LIU YTANTAN, HE MINGYUAN, et al. Chemodynamic therapy: tumor microenvironment-mediated fenton and fenton-like reaction. Angewandte Chemie International Edition, 2019, 58(4): 946-956. DOI URL
[3]	MIN HUAN, WANG JING, QI YINGQIU, et al. Biomimetic metal-organic framework nanoparticles for cooperative combination of antiangiogenesis and photodynamic therapy for enhanced efficacy. Advanced Materials, 2019, 31(15): 1808200. DOI URL
[4]	DAI XINXIN, DU TING, HAN KAI. Engineering nanoparticles for optimized photodynamic therapy. ACS Biomaterials Science & Engineering, 2019, 5(12): 6342-6354.
[5]	CHANG MENGYU, WANG MAN, WANG MEIFANG, et al. A multifunctional cascade bioreactor based on hollow structured Cu₂MoS₄ for synergetic cancer chemo-dynamic therapy/starvation therapy/phototherapy/immunotherapy with remarkably enhanced efficacy. Advanced Materials, 2019, 31(51): 1905271. DOI URL
[6]	SCHUBERT JONAS, RADEKE CARMEN, FERY ANDREAS, et al. The role of pH, metal ions and their hydroxides in charge reversal of protein-coated nanoparticles. Physical Chemistry Chemical Physics, 2019, 21(21): 11011-11018. DOI URL
[7]	ZENG JINYUE, ZHANG MINGKANG, PENG MENGYUN, et al. Porphyrinic metal-organic frameworks coated gold nanorods as a versatile nanoplatform for combined photodynamic/photothermal/ chemotherapy of tumor. Advanced Functional Materials, 2018, 28(8): 1705451. DOI URL
[8]	CHEN JIAJIE, LIU JIAXING, HU YAPING, et al. Metal-organic framework-coated magnetite nanoparticles for synergistic magnetic hyperthermia and chemotherapy with pH-triggered drug release. Science and Technology of Advanced Materials, 2019, 20(1): 1043-1054. DOI URL
[9]	CHEN JIAJIE, ZHU YUFANG, WU CHENGTIE, et al. Nanoplatform-based cascade engineering for cancer therapy. Chemical Society Reviews, 2020, 49(24): 9057-9094. DOI URL
[10]	WANG ZHENG, ZHANG FAN, SHAO DAN, et al. Janus nanobullets combine photodynamic therapy and magnetic hyperthermia to potentiate synergetic anti-metastatic immunotherapy. Advanced Science, 2019, 6(22): 1901690. DOI URL
[11]	ZHANG YA-RU, LIN RUN, LI HONG-JUN, et al. Strategies to improve tumor penetration of nano-medicines through nanoparticle design. Wiley Interdisciplinary Reviews-Nanomedicine and Nanobiotechnology, 2019, 11(1): e1519.
[12]	PRASAD MINAKSHI, LAMBE UPENDRA P, BRAR BASANTI, et al. Nanotherapeutics: an insight into healthcare and multi- dimensional applications in medical sector of the modern world. Biomedicine & Pharmacotherapy, 2018, 97: 1521-1537. DOI URL
[13]	LU KUANGDA, AUNG THEIET, GUO NINING, et al. Nanoscale metal-organic frameworks for therapeutic, imaging, and sensing applications. Advanced Materials, 2018, 30(37): 1707634. DOI URL
[14]	MAO FANGXIN, WEN LING, SUN CAIXIA, et al. Ultrasmall biocompatible Bi₂Se₃ nanodots for multimodal imaging-guided synergistic radiophotothermal therapy against cancer. ACS Nano, 2016, 10(12): 11145-11155. DOI URL
[15]	WU CHUANDE, ZHAO MIN. Incorporation of molecular catalysts in metal-organic frameworks for highly efficient heterogeneous catalysis. Advanced Materials, 2017, 29(14): 1605446. DOI URL
[16]	CHEN JIAJIE, LIN SHIYANG, ZHAO DOUDOU, et al. Palladium nanocrystals-engineered metalorganic frameworks for enhanced tumor inhibition by synergistic hydrogen/photodynamic therapy. Advanced Functional Materials, 2020, 31(4): 2006853. DOI URL
[17]	WANG SHUNZHI, MCGUIRK C MICHAEL, D’AQUINO ANDREA, et al. Metal-organic framework nanoparticles. Advanced Materials, 2018, 30(37): 1800202. DOI URL
[18]	CHEN HUANG, ZHANG LINGYU, LIU SONG, et al. Double enhanced energy storage density via polarization gradient design in ferroelectric poly(vinylidene fluoride)-based nanocomposites. Chemical Engineering Journal, 2021, 411(18): 128585. DOI URL
[19]	ZHANG YAN, WANG FAMING, LIU CHAOQUN, et al. Nanozymes decorated metal-organic frameworks for enhanced photodynamic therapy. ACS Nano, 2018, 12(1): 651-661. DOI URL
[20]	FU JINGKE, LI TAO, ZHU YINGCHUN, et al. Ultrasound- activated oxygen and ROS generation nanosystem systematically modulates tumor microenvironment and sensitizes sonodynamic therapy for hypoxic solid tumors. Advanced Functional Materials, 2019, 29(51): 1906195. DOI URL
[21]	NOVIKOV ALEXANDER S, KUZNETSOV MAXIM L, POMBEIRO ARMANDO J L, et al. Generation of HO• radical from hydrogen peroxide catalyzed by aqua complexes of the group III metals [M(H₂O)_n]³⁺ (M=Ga, In, Sc, Y, or La): a theoretical study. ACS Catalysis, 2013, 3(6): 1195-1208. DOI URL
[22]	LIN WENXIN, GONG JIANQIU, FANG LIQUAN, et al. A photodynamic system based on endogenous bioluminescence for in vitro anticancer studies. Zeitschrift fur Anorganische und Allgemeine Chemie, 2019, 645(18/19): 1161-1164. DOI URL
[23]	PARK JIHYE, JIANG QIN, FENG DAWEI, et al. Size-controlled synthesis of porphyrinic metal-organic framework and functionalization for targeted photodynamic therapy. Journal American Chemical Society, 2016, 138(10): 3518-3525. DOI URL
[24]	ZHAO WEI, ZHAO YONGMEI, WANG QINGFU, et al. Remote light-responsive nanocarriers for controlled drug delivery: advances and perspectives. Small, 2019, 15(45): 1903060. DOI URL
[25]	ElSHAMI FAWZYA I, RAMADAN ABD EL-MOTALEB M, IBRAHIM MOHAMED M, et al. Metformin containing nickel (II) complexes: synthesis, structural characterization, binding and kinetic interactions with BSA, antibacterial and in-vitro cytotoxicity studies. Applied Organometallic Chemistry, 2020, 34(3): e5437.
[26]	NIU JIN, LIANG JINGJING, GAO ANG, et al. Micropore-confined amorphous SnO₂ subnanoclusters as robust anode materials for Na-ion capacitors. Journal of Materials Chemistry A, 7(38): 21711-21721. DOI URL
[27]	ZHOU BENQING, SONG JUN, WANG MENG, et al. BSA- bioinspired gold nanorods loaded with immunoadjuvant for the treatment of melanoma by combined photothermal therapy and immunotherapy. Nanoscale, 2018, 10(46): 21640-21647. DOI URL
[28]	LIU WEI, WANG YONGMEI, LI YUHAO, et al. Fluorescent imaging-guided chemotherapy-and photodynamic dual therapy with nanoscale porphyrin metal-organic framework. Small, 2017, 13(17): 1603459. DOI URL
[29]	SHOME ARPITA, RATHER ADIL MAJEED, MANNA UTTAM. Chemically reactive protein nanoparticles for synthesis of a durable and deformable superhydrophobic material. Nanoscale Advances, 2019, 1(5): 1746-1753. DOI URL
[30]	ZHANG YUAN, XING YANG, XIAN MING, et al. Folate- targeting and bovine serum albumin-gated mesoporous silica nanoparticles as a redox-responsive carrier for epirubicin release. New Journal of Chemistry, 2019, 43(6): 2694-2701. DOI URL
[31]	GUO MINGZHEN, HE JIANAG, MA SHUANG, et al. Determination of Hg²⁺based on the selective enhancement of peroxidase mimetic activity of hollow porous gold nanoparticles. Nano Brief Reports and Reviews, 2017, 12(4): 1750050.
[32]	FENG WEI, HAN XIUGUO, WANG RONGYAN, et al. Nanocatalysts-augmented and photothermal-enhanced tumor-specific sequential nanocatalytic therapy in both NIR-I and NIR-II biowindows. Advance Material, 2019, 31(5): 1805919.
[33]	ZHANG YONGHE, WANG BEILEI, ZHAO RUIBO, et al. Multifunctional nanoparticles as photosensitizer delivery carriers for enhanced photodynamic cancer therapy. Materials Science & Engineering C-Materials for Biological Application, 2020, 115: 111099.
[34]	HANDE GUNDYZ, SAFACAN KONLEMEN, EENGIN U AKKAYA. Singlet oxygen probes: diversity in signal generation mechanisms yields a larger color palette. Coordination Chemistry Reviews, 2021, 429: 213641. DOI URL
[35]	YIN SHENGYAN, SONG GUOSHENG, YANG YUE, et al. Persistent regulation of tumor microenvironment via circulating catalysis of MnFe₂O₄@metal-organic frameworks for enhanced photodynamic therapy. Advanced Functional Materials, 2019, 29(25): 2006853.
[36]	BAJAJ AVINASH, SAMANTA BAPPADITYA, YAN HAOHENG, et al. Stability, toxicity and differential cellular uptake of protein passivated-Fe₃O₄ nanoparticles. Journal of Materials Chenistry, 2009, 19(35): 6328-6331.
[37]	LIN LISEN, SONG JIBIN, SONG LIANG, et al. Simultaneous fenton-like ion delivery and glutathione depletion by MnO₂-based nanoagent to enhance chemodynamic therapy. Angewandte Chemie- International Edition, 2018, 57(18): 4902-4906. DOI URL
[38]	TARPEY MARGARRT M, FRIDOVICH IRWIN. Methods of detection of vascular reactive species nitric oxide, superoxide, hydrogen peroxide, and peroxynitrite. Circulation Research, 2001, 89(3): 224. DOI URL
[39]	ETHIRAJAN MANIVANNAN, CHEN YIHUI, JOSHI PENNY, et al. The role of porphyrin chemistry in tumor imaging and photodynamic therapy. Chemical Society Reviews, 2011, 40(1): 340-362. DOI URL
[40]	CHEN JIAJIE, ZHU YUFANG, KASKEL STEFAN. Porphyrin- based metal-organic frameworks for biomedical applications. Angewandte Chemie-International Edition, 2020, 60(10): 5010-5035. DOI URL