Visual dual chemodynamic/photothermal therapeutic nanoplatform based on superoxide dismutase plus Prussian blue

Shan Lei; Jinxing Chen; Kun Zeng; Mozhen Wang; Xuewu Ge

doi:10.1007/s12274-019-2348-1

Nano Research 2019, 12(5): 1071-1082 https://doi.org/10.1007/s12274-019-2348-1

Research Article | Issue | Published: 06 March 2019

Visual dual chemodynamic/photothermal therapeutic nanoplatform based on superoxide dismutase plus Prussian blue

Show Author's Information Hide Author's Information Shan Lei, Jinxing Chen, Kun Zeng, Mozhen Wang(

), Xuewu Ge(

)

CAS Key Laboratory of Soft Matter Chemistry,Department of Polymer Science and Engineering, University of Science and Technology of China,Hefei,230026,China;

Keywords:

fluorescence, Prussian blue, copper-zinc superoxide dismutase, Fenton reagent, near-infrared (NIR) photothermal therapy

Topics:

Biocompatibility Chemotherapy Copper compounds Enzymes Fluorescence Fluorophores Infrared devices Medical nanotechnology Nanoparticles Oxidation Silica SiO2 nanoparticles Sulfur compounds Synthesis (chemical)Tumors Zinc compounds

Cite this article:

Lei S, Chen J, Zeng K, et al. Visual dual chemodynamic/photothermal therapeutic nanoplatform based on superoxide dismutase plus Prussian blue. Nano Research, 2019, 12(5): 1071-1082. https://doi.org/10.1007/s12274-019-2348-1

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Abstract Full text Electronic supplementary material About this article

Abstract

Enzyme-based anticancer therapy is more attractive for the less side effect than conventional chemotherapy. However, the poor stability and low membrane permeability of enzymes during the intracellular delivery are constraints for its practical applications. In this work, we synthesized novel near-infrared (NIR)-responsive core–shell-structured Prussian blue@fibrous SiO₂ (PBFS) nanoparticles as the carrier of superoxide dismutase (SOD) and a glutathione (GSH)-activated Fenton reagent (DiFe). The PBFS nanoparticles are further modified with a GSH-responsive cationic polymer (poly(2-(acryloyloxy)-N, N-dimethyl-N-(4-(((2-((2-(((4-methyl-2-oxo-2H-chromen-7-yl)carbamoyl)oxy)ethyl)disulfaneyl)ethoxy)carbonyl)amino)benzyl)ethan-1-aminium, PSS) containing disulfide bonds and fluorophores. After SOD and DiFe are loaded on the PBFS-PSS nanoparticles, dual chemodynamic/photothermal therapeutic nanoparticulate systems (PBFS-PSS/DiFe/SOD) are obtained. In vitro experiments show that PBFS-PSS/DiFe/SOD nanoparticles have good biocompatibility and can be tracked under fluorescence microscope during the intracellular delivery process in MCF-7 tumor cells due to the GSH-activated release of fluorophores. They also exhibit high efficiency in NIR photothermal conversion and GSH-activated Fenton reaction in tumor cells, thus achieving high-efficient killing effect of tumor cells based on the combination of photothermal and chemodynamic therapeutic performance (PTT and CDT). This work offers a novel pathway to construct a visual multifunctional nanomedicine platform for future cancer therapy.

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About this article

Visual dual chemodynamic/photothermal therapeutic nanoplatform based on superoxide dismutase plus Prussian blue

Show Author's information Hide Author's Information Shan Lei, Jinxing Chen, Kun Zeng, Mozhen Wang(

), Xuewu Ge(

)

CAS Key Laboratory of Soft Matter Chemistry,Department of Polymer Science and Engineering, University of Science and Technology of China,Hefei,230026,China;

Abstract

Keywords: fluorescence, Prussian blue, copper-zinc superoxide dismutase, Fenton reagent, near-infrared (NIR) photothermal therapy

References(52)

Yan, M.; Du, J. J.; Gu, Z.; Liang, M.; Hu, Y. F.; Zhang, W. J.; Priceman, S.; Wu, L.; Zhou, Z. H.; Liu, Z. et al. A novel intracellular protein delivery platform based on single-protein nanocapsules. Nat. Nanotech. 2010, 5, 48-53.

DOI Google Scholar

Trachootham, D.; Alexandre, J.; Huang, P. Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach? Nat. Rev. Drug Discov. 2009, 8, 579-591.

DOI Google Scholar

Nelson, S. K.; Bose, S. K.; Grunwald, G. K.; Myhill, P.; McCord, J. M. The induction of human superoxide dismutase and catalase in vivo: A fundamentally new approach to antioxidant therapy. Free Radical Biol. Med. 2006, 40, 341-347.

DOI Google Scholar

Tsang, C. K.; Liu, Y.; Thomas, J.; Zhang, Y. J.; Zheng, X. F. S. Superoxide dismutase 1 acts as a nuclear transcription factor to regulate oxidative stress resistance. Nat. Commun. 2014, 5, 3446.

DOI Google Scholar

Cerutti, P. A. Prooxidant states and tumor promotion. Science 1985, 227, 375-381.

DOI Google Scholar

Ma, P. A.; Xiao, H. H.; Yu, C.; Liu, J. H.; Cheng, Z. Y.; Song, H. Q.; Zhang, X. Y.; Li, C. X.; Wang, J. Q.; Gu, Z. et al. Enhanced cisplatin chemotherapy by iron oxide nanocarrier-mediated generation of highly toxic reactive oxygen species. Nano Lett. 2017, 17, 928-937.

DOI Google Scholar

Dai, Y. L.; Yang, Z.; Cheng, S. Y.; Wang, Z. L.; Zhang, R. L.; Zhu, G. Z.; Wang, Z. T.; Yung, B. C.; Tian, R.; Jacobson, O. et al. Toxic reactive oxygen species enhanced synergistic combination therapy by self-assembled metal-phenolic network nanoparticles. Adv. Mater. 2018, 30, 1704877.

DOI Google Scholar

Yang, Z.; Dai, Y. L.; Yin, C.; Fan, Q. L.; Zhang, W. S.; Song, J.; Yu, G. C.; Tang, W.; Fan, W. P.; Yung, B. C. et al. Activatable semiconducting theranostics: Simultaneous generation and ratiometric photoacoustic imaging of reactive oxygen species in vivo. Adv. Mater. 2018, 30, 1707509.

DOI Google Scholar

Imlay, J.; Chin, S. M.; Linn, S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 1988, 240, 640-642.

DOI Google Scholar

Kwon, B.; Han, E.; Yang, W.; Cho, W.; Yoo, W.; Hwang, J.; Kwon, B. M.; Lee, D. Nano-fenton reactors as a new class of oxidative stress amplifying anticancer therapeutic agents. ACS Appl. Mater. Interfaces 2016, 8, 5887-5897.

DOI Google Scholar

Zhang, C.; Bu, W. B.; Ni, D. L.; Zhang, S. J.; Li, Q.; Yao, Z. W.; Zhang, J. W.; Yao, H. L.; Wang, Z.; Shi, J. L. Synthesis of iron nanometallic glasses and their application in cancer therapy by a localized Fenton reaction. Angew. Chem., Int. Ed. 2016, 55, 2101-2106.

DOI Google Scholar

Kartha, S.; Yan, L. S.; Weisshaar, C. L.; Ita, M. E.; Shuvaev, V. V.; Muzykantov, V. R.; Tsourkas, A.; Winkelstein, B. A.; Cheng, Z. L. Superoxide dismutase-loaded porous polymersomes as highly efficient antioxidants for treating neuropathic pain. Adv. Healthcare Mater. 2017, 6, 1700500.

DOI Google Scholar

Chen, Y. P.; Chen, C. T.; Hung, Y.; Chou, C. M.; Liu, T. P.; Liang, M. R.; Chen, C. T.; Mou, C. Y. A new strategy for intracellular delivery of enzyme using mesoporous silica nanoparticles: Superoxide dismutase. J. Am. Chem. Soc. 2013, 135, 1516-1523.

DOI Google Scholar

Wang, X.; Niu, D. C.; Li, P.; Wu, Q.; Bo, X. W.; Liu, B. J.; Bao, S.; Su, T.; Xu, H. X.; Wang, Q. G. Dual-enzyme-loaded multifunctional hybrid nanogel system for pathological responsive ultrasound imaging and T₂-weighted magnetic resonance imaging. ACS Nano 2015, 9, 5646-5656.

DOI Google Scholar

Liu, W. L.; Liu, T.; Zou, M. Z.; Yu, W. Y.; Li, C. X.; He, Z. Y.; Zhang, M. K.; Liu, M. D.; Li, Z. H.; Feng, J. et al. Aggressive man-made red blood cells for hypoxia-resistant photodynamic therapy. Adv. Mater. 2018, 30, 1802006.

DOI Google Scholar

Nukolova, N. V.; Aleksashkin, A. D.; Abakumova, T. O.; Morozova, A. Y.; Gubskiy, I. L.; Kirzhanova, E. A.; Abakumov, M. A.; Chekhonin, V. P.; Klyachko, N. L.; Kabanov, A. V. Multilayer polyion complex nanoformulations of superoxide dismutase 1 for acute spinal cord injury. J. Control. Release 2018, 270, 226-236.

DOI Google Scholar

Huang, L.; Ao, L. J.; Hu, D. H.; Wang, W.; Sheng, Z. H.; Su, W. Magneto-plasmonic nanocapsules for multimodal-imaging and magnetically guided combination cancer therapy. Chem. Mater. 2016, 28, 5896-5904.

DOI Google Scholar

Li, Z. L.; Hu, Y.; Miao, Z.; Xu, H.; Li, C.; Zhao, Y.; Li, Z.; Chang, M.; Ma, Z.; Sun, Y. et al. Dual-stimuli responsive bismuth nanoraspberries for multimodal imaging and combined cancer therapy. Nano Lett. 2018, 18, 6778-6788.

DOI Google Scholar

Wang, Y. Z.; Song, Y. J.; Zhu, G. X.; Zhang, D. C.; Liu, X. W. Highly biocompatible BSA-MnO₂ nanoparticles as an efficient near-infrared photothermal agent for cancer therapy. Chin. Chem. Lett. 2018, 29, 1685-1688.

DOI Google Scholar

Wang, Z. R.; He, Q.; Zhao, W. G.; Luo, J. W.; Gao, W. P. Tumor-homing, pH-and ultrasound-responsive polypeptide-doxorubicin nanoconjugates overcome doxorubicin resistance in cancer therapy. J. Control. Release 2017, 264, 66-75.

DOI Google Scholar

Cho, H. Y.; Lee, T.; Yoon, J.; Han, Z. L.; Rabie, H.; Lee, K. B.; Su, W. W.; Choi, J. W. Magnetic oleosome as a functional lipophilic drug carrier for cancer therapy. ACS Appl. Mater. Interfaces 2018, 10, 9301-9309.

DOI Google Scholar

Lai, J. P.; Shah, B. P.; Garfunkel, E.; Lee, K. B. Versatile fluorescence resonance energy transfer-based mesoporous silica nanoparticles for real-time monitoring of drug release. ACS Nano 2013, 7, 2741-2750.

DOI Google Scholar

Xu, Z. G.; Liu, S. Y.; Kang, Y. J.; Wang, M. F. Glutathione-and pH-responsive nonporous silica prodrug nanoparticles for controlled release and cancer therapy. Nanoscale 2015, 7, 5859-5868.

DOI Google Scholar

Xie, Y. Y.; Wang, J.; Wang, M. Z.; Ge, X. W. Fabrication of fibrous amidoxime-functionalized mesoporous silica microsphere and its selectively adsorption property for Pb²⁺ in aqueous solution. J. Hazard. Mater. 2015, 297, 66-73.

DOI Google Scholar

Chen, J. X.; Lei, S.; Xie, Y. Y.; Wang, M. Z.; Yang, J.; Ge, X. W. Fabrication of high-performance magnetic lysozyme-imprinted microsphere and its NIR-responsive controlled release property. ACS Appl. Mater. Interfaces 2015, 7, 28606-28615.

DOI Google Scholar

Chen, J. X; Lei, S.; Zeng, K.; Wang, M. Z.; Asif, A.; Ge, X. W. Catalase-imprinted Fe₃O₄/Fe@fibrous SiO₂/polydopamine nanoparticles: An integrated nanoplatform of magnetic targeting, magnetic resonance imaging, and dual-mode cancer therapy. Nano Res. 2017, 10, 2351-2363.

DOI Google Scholar

Marzenell, P.; Hagen, H.; Sellner, L.; Zenz, T.; Grinyte, R.; Pavlov, V.; Daum, S.; Mokhir, A. Aminoferrocene-based prodrugs and their effects on human normal and cancer cells as well as bacterial cells. J. Med. Chem. 2013, 56, 6935-6944.

DOI Google Scholar

Hagen, H.; Marzenell, P.; Jentzsch, E.; Wenz, F.; Veldwijk, M. R.; Mokhir, A. Aminoferrocene-based prodrugs activated by reactive oxygen species. J. Med. Chem. 2012, 55, 924-934.

DOI Google Scholar

Wu, Q.; He, Z. G.; Wang, X.; Zhang, Q.; Wei, Q. C.; Ma, S. Q.; Ma, C.; Li, J. Y.; Wang, Q. G. Cascade enzymes within self-assembled hybrid nanogel mimicked neutrophil lysosomes for singlet oxygen elevated cancer therapy. Nat. Commun 2019, 10, 240.

DOI Google Scholar

Li, W. P.; Su, C. H.; Tsao, L. C.; Chang, C. T.; Hsu, Y. P.; Yeh, C. S. Controllable CO release following near-infrared light-induced cleavage of iron carbonyl derivatized prussian blue nanoparticles for CO-assisted synergistic treatment. ACS Nano 2016, 10, 11027-11036.

DOI Google Scholar

Chen, W. S.; Zeng, K.; Liu, H.; Ouyang, J.; Wang, L. Q.; Liu, Y.; Wang, H.; Deng, L.; Liu, Y. N. Cell membrane camouflaged hollow Prussian blue nanoparticles for synergistic photothermal-/chemotherapy of cancer. Adv. Funct. Mater. 2017, 27, 1605795.

DOI Google Scholar

Zhou, B.; Jiang, B. P.; Sun, W. Y.; Wei, F. M.; He, Y.; Liang, H.; Shen, X. C. Water-dispersible Prussian blue hyaluronic acid nanocubes with near-infrared photoinduced singlet oxygen production and photothermal activities for cancer theranostics. ACS Appl. Mater. Interfaces 2018, 10, 18036-18049.

DOI Google Scholar

Sing, K. S. W. Reporting physisorption data for gas/solid systems with special reference to the determination of surface area and porosity (Recommendations 1984). Pure Appl. Chem. 1985, 57, 603-619.

DOI Google Scholar

Brunauer, S.; Deming, L. S.; Deming, W. E.; Teller, E. On a theory of the van der Waals adsorption of gases. J. Am. Chem. Soc. 1940, 62, 1723-1732.

DOI Google Scholar

Mandel, R.; Ryser, H. J. P.; Niaki, B.; Ghani, F.; Shen, W. C. Isolation of variants of Chinese hamster ovary cells with abnormally low levels of GSH: Decreased ability to cleave endocytosed disulfide bonds. J. Cell. Physiol. 1991, 149, 60-65.

DOI Google Scholar

Gandra, N.; Wang, D. D.; Zhu, Y.; Mao, C. B. Virus-mimetic cytoplasm-cleavable magnetic/silica nanoclusters for enhanced gene delivery to mesenchymal stem cells. Angew. Chem., Int. Ed. 2013, 52, 11278-11281.

DOI Google Scholar

Staben, L. R.; Koenig, S. G.; Lehar, S. M.; Vandlen, R.; Zhang, D. L.; Chuh, J.; Yu, S. F.; Ng, C.; Guo, J.; Liu, Y. Z. et al. Targeted drug delivery through the traceless release of tertiary and heteroaryl amines from antibody-drug conjugates. Nat. Chem. 2016, 8, 1112-1119.

DOI Google Scholar

Liu, X.; Xiang, J. J.; Zhu, D. C.; Jiang, L. M.; Zhou, Z. X.; Tang, J. B.; Liu, X. R.; Huang, Y. Z.; Shen, Y. Q. Fusogenic reactive oxygen species triggered charge-reversal vector for effective gene delivery. Adv. Mater. 2016, 28, 1743-1752.

DOI Google Scholar

Truong, N. P.; Jia, Z. F.; Burges, M.; McMillan, N. A. J.; Monteiro, M. J. Self-catalyzed degradation of linear cationic poly(2-dimethylaminoethyl acrylate) in water. Biomacromolecules 2011, 12, 1876-1882.

DOI Google Scholar

Truong, N. P.; Gu, W. Y.; Prasadam, I.; Jia, Z. F.; Crawford, R.; Xiao, Y.; Monteiro, M. J. An influenza virus-inspired polymer system for the timed release of siRNA. Nat. Commun. 2013, 4, 1902.

DOI Google Scholar

Kaneti, Y. V.; Chen, C. Y.; Liu, M. S.; Wang, X. C.; Yang, J. L.; Taylor, R. A.; Jiang, X. C.; Yu, A. B. Carbon-coated gold nanorods: A facile route to biocompatible materials for photothermal applications. ACS Appl. Mater. Interfaces 2015, 7, 25658-25668.

DOI Google Scholar

Zhang, R. L.; Zhao, J.; Han, G. M.; Liu, Z. J.; Liu, C.; Zhang, C.; Liu, B. H.; Jiang, C. L.; Liu, R. Y.; Zhao, T. T. et al. Real-time discrimination and versatile profiling of spontaneous reactive oxygen species in living organisms with a single fluorescent probe. J. Am. Chem. Soc. 2016, 138, 3769-3778.

DOI Google Scholar

Wang, Q.; Tian, S. L.; Ning, P. Degradation mechanism of methylene blue in a heterogeneous Fenton-like reaction catalyzed by ferrocene. Ind. Eng. Chem. Res. 2014, 53, 643-649.

DOI Google Scholar

Lin, F. X.; Zeng, K.; Yang, W. X.; Wang, M. Z.; Rong, J. L.; Xie, J.; Zhao, Y.; Ge, X. W. γ-Ray-radiation-scissioned chitosan as a gene carrier and its improved in vitro gene transfection performance. Chin. J. Chem. Phys. 2017, 30, 231-238.

DOI Google Scholar

Lin, M. T.; Beal, M. F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443, 787-795.

DOI Google Scholar

Wang, S. H.; Shang, L.; Li, L. L.; Yu, Y. J.; Chi, C. W.; Wang, K.; Zhang, J.; Shi, R.; Shen, H. Y.; Waterhouse, G. I. N. et al. Metal-organic-framework-derived mesoporous carbon nanospheres containing porphyrin-like metal centers for conformal phototherapy. Adv. Mater. 2016, 28, 8379-8387.

DOI Google Scholar

Qu, X. W.; Qiu, P. H.; Zhu, Y.; Yang, M. Y.; Mao, C. B. Guiding nanomaterials to tumors for breast cancer precision medicine: From tumor-targeting small-molecule discovery to targeted nanodrug delivery. NPG Asia Mater. 2017, 9, e452.

DOI Google Scholar

Simón-Gracia, L.; Hunt, H.; Teesalu, T. Peritoneal carcinomatosis targeting with tumor homing peptides. Molecules 2018, 23, 1190.

DOI Google Scholar

Hu, M.; Furukawa, S.; Ohtani, R.; Sukegawa, H.; Nemoto, Y.; Reboul, J.; Kitagawa, S.; Yamauchi, Y. Synthesis of Prussian blue nanoparticles with a hollow interior by controlled chemical etching. Angew. Chem., Int. Ed. 2012, 124, 1008-1012.

DOI Google Scholar

Zhang, Y. Y.; Ang, C. Y.; Li, M. H.; Tan, S. Y.; Qu, Q. Y.; Zhao, Y. L. Polymeric prodrug grafted hollow mesoporous silica nanoparticles encapsulating near-infrared absorbing dye for potent combined photothermal-chemotherapy. ACS Appl. Mater. Interfaces 2016, 8, 6869-6879.

DOI Google Scholar

Wang, C.; Wang, J. Q.; Zhang, X. D.; Yu, S. J.; Wen, D.; Hu, Q. Y.; Ye, Y. Q.; Bomba, H.; Hu, X. L.; Liu, Z. et al. In situ formed reactive oxygen species-responsive scaffold with gemcitabine and checkpoint inhibitor for combination therapy. Sci. Transl. Med. 2018, 10, eaan3682.

DOI Google Scholar

Li, Y. M.; Liu, G. H.; Wang, X. R.; Hu, J. M.; Liu, S. Y. Enzyme-responsive polymeric vesicles for bacterial-strain-selective delivery of antimicrobial agents. Angew. Chem., Int. Ed. 2016, 55, 1760-1764.

DOI Google Scholar

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Acknowledgements

Publication history

Received: 29 November 2018

Revised: 02 February 2019

Accepted: 18 February 2019

Published: 06 March 2019

Issue date: May 2019

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Acknowledgements

We thank Prof. Z. S. Ge and Prof. L. H. Yang in the Department of Polymer Science and Engineering of USTC for their kind help in providing the 808 nm semiconductor laser device and infrared imaging devices, respectively. This work was supported by the National Natural Science Foundation of China (Nos. 51473152 and 51573174).