Abstract
Photodynamic therapy (PDT) is a widely-used technology for cancer therapy, but conventional photosensitizers still face some drawbacks, such as hydrophobicity, inadequate pharmacokinetics, low cell/tissue specificity, and uncontrollable photodynamic performance during the therapeutic process. Herein, we present a controllable photodynamic performance based on two-dimensional metal-organic frameworks (2D Zn-TCPP MOF) that displayed a week PDT effect under a neutral environment upon exposure to a 660 nm laser due to the degeneracy of Q bands of TCPP. However, the 2D Zn-TCPP MOF showed a significantly enhanced PDT effect in an acidic environment under irradiation with a 660 nm laser due to the released TCPP from decomposed MOF structure. From the in vitro outcomes, the 2D Zn-TCPP MOF showed controllable photodynamic performance from neutral to acidic environments. Due to the acidic tumor microenvironment, the 2D Zn-TCPP MOF presented the strongest antitumor effect in vivo under irradiation with a 660 nm laser. This work offers a promising strategy to develop a next-generation photosensitizer.
Similar content being viewed by others
References
Wu, X. Q.; Jiang, X. F.; Fan, T. J.; Zheng, Z. W.; Liu, Z. Y.; Chen, Y. B.; Cao, L. Q.; Xie, Z. J.; Zhang, D. W. et al. Recent advances in photodynamic therapy based on emerging two-dimensional layered nanomaterials. Nano Res. 2020, 13, 1485–1508.
Dougherty, T. J.; Gomer, C. J.; Henderson, B. W.; Jori, G.; Kessel, D.; Korbelik, M.; Moan, J.; Peng, Q. Photodynamic therapy. JNCI J. Natl. Cancer Inst. 1998, 90, 889–905.
Chen, Q.; Chen, J. W.; Yang, Z. J.; Zhang, L.; Dong Z. L.; Liu, Z. NIR-II light activated photodynamic therapy with protein-capped gold nanoclusters. Nano Res. 2018, 11, 5657–5669.
Lo, P. C.; Rodríguez-Morgade, M. S.; Pandey, R. K.; Ng, D. K. P.; Torres, T.; Dumoulin, F. The unique features and promises of phthalocyanines as advanced photosensitisers for photodynamic therapy of cancer. Chem. Soc. Rev. 2020, 49, 1041–1056.
Wang, Y. Z.; Wang, H. W.; Zhou, L.; Lu, J.; Jiang, B. L.; Liu, C. X.; Guo, J. C. Photodynamic therapy of pancreatic cancer: Where have we come from and where are we going? Photodiagn. Photodyn. Ther. 2020, 31, 101876.
Lucky, S. S.; Soo, K. C.; Zhang, Y. Nanoparticles in photodynamic therapy. Chem. Rev. 2015, 115, 1990–2042.
Dolmans, D. E. J. G. J.; Fukumura, D.; Jain, R. K. Photodynamic therapy for cancer. Nat. Rev. Cancer 2003, 3, 380–387.
Hong, E. J.; Choi, D. G.; Shim, M. S. Targeted and effective photodynamic therapy for cancer using functionalized nanomaterials. Acta Pharm. Sin. B 2016, 6, 297–307.
Zhu, W. J.; Yang, Y.; Jin, Q. T.; Chao, Y.; Tian, L. L.; Liu, J. J.; Dong Z. L.; Liu, Z. Two-dimensional metal-organic-framework as a unique theranostic nano-platform for nuclear imaging and chemophotodynamic cancer therapy. Nano Res. 2019, 12, 1307–1312.
Chouikrat, R.; Seve, A.; Vanderesse, R.; Benachour, H.; Barberi-Heyob, M.; Richeter, S.; Raehm, L.; Durand, J. O.; Verelst, M.; Frochot, C. Non polymeric nanoparticles for photodynamic therapy applications: Recent developments. Curr. Med. Chem. 2012, 19, 781–792.
Bharathiraja, S.; Moorthy, M. S.; Manivasagan, P.; Seo, H.; Lee, K. D.; Oh, J. Chlorin e6 conjugated silica nanoparticles for targeted and effective photodynamic therapy. Photodiagn. Photodyn. Ther. 2017, 19, 212–220.
Li, Y. J.; Hu, J.; Liu, X.; Liu, Y.; Lv, S. X.; Dang, J. J.; Ji, Y.; He, J. L.; Yin, L. C. Photodynamic therapy-triggered on-demand drug release from ROS-responsive core-cross-linked micelles toward synergistic anti-cancer treatment. Nano Res. 2019, 12, 999–1008.
Sun, J. Y.; Kormakov, S.; Liu, Y.; Huang, Y.; Wu, D. M.; Yang, Z. G. Recent progress in metal-based nanoparticles mediated photodynamic therapy. Molecules 2018, 23, 1704.
Huang, C. L.; Zhang, Z. M.; Guo, Q.; Zhang, L.; Fan, F.; Qin, Y.; Wang, H.; Zhou, S.; Ou-Yang, W. B.; Sun, H. F. et al. A dual-model imaging theragnostic system based on mesoporous silica nanoparticles for enhanced cancer phototherapy. Adv. Health. Mater. 2019, 8, 1900840.
Li, X. S.; Fan, H. H.; Guo, T.; Bai, H. R.; Kwon, N.; Kim, K. H.; Yu, S.; Cho, Y.; Kim, H.; Nam, K. T. et al. Sequential protein-responsive nanophotosensitizer complex for enhancing tumor-specific therapy. ACS Nano 2019, 13, 6702–6710.
Zeng, X. M.; Yan, S. Q.; Chen, P.; Du, W.; Liu, B. F. Modulation of tumor microenvironment by metal-organic-framework-derived nanoenzyme for enhancing nucleus-targeted photodynamic therapy. Nano Res. 2020, 13, 1527–1535.
Lin, A. L.; Li, S. Z.; Xu, C. H.; Li, X. S.; Zheng, B. Y.; Gu, J. J.; Ke, M. R.; Huang, J. D. A pH-responsive stellate mesoporous silica based nanophotosensitizer for in vivo cancer diagnosis and targeted photodynamic therapy. Biomater. Sci. 2019, 7, 211–219.
Gai, S. L.; Yang, G. X.; He, P. P.; He, F.; Lin, J.; Jin, D. Y.; Xing, B. G. Recent advances in functional nanomaterials for light-triggered cancer therapy. Nano Today 2018, 19, 146–187.
Huang, K.; Li, Z. J.; Lin, J.; Han, G.; Huang, P. Two-dimensional transition metal carbides and nitrides (MXenes) for biomedical applications. Chem. Soc. Rev. 2018, 47, 5109–5124.
Saleem, J.; Wang, L. M.; Chen, C. Y. Carbon-based nanomaterials for cancer therapy via targeting tumor microenvironment. Adv. Health. Mater. 2018, 7, 1800525.
Kuo, W. S.; Shao, Y. T.; Huang, K. S.; Chou, T. M.; Yang, C. H. Antimicrobial amino-functionalized nitrogen-doped graphene quantum dots for eliminating multidrug-resistant species in dual-Modality photodynamic therapy and bioimaging under two-photon excitation. ACS Appl. Mater. Interfaces 2018, 10, 14438–14446.
Xiao, L.; Gu, L.; Howell, S. B.; Sailor, M. J. Porous silicon nanoparticle photosensitizers for singlet oxygen and their phototoxicity against cancer cells. ACS Nano 2011, 5, 3651–3659.
Chan, M. H.; Pan, Y. T.; Lee, I. J.; Chen, C. W.; Chan, Y. C.; Hsiao, M.; Wang, F.; Sun, L. D.; Chen, X. Y.; Liu, R. S. Minimizing the heat effect of photodynamic therapy based on inorganic nanocomposites mediated by 808 nm near-infrared light. Small 2017, 13, 1700038.
Liu, J. N.; Bu, W. B.; Shi, J. L. Chemical design and synthesis of functionalized probes for imaging and treating tumor hypoxia. Chem. Rev. 2017, 117, 6160–6224.
Liu, J.; Jiang, X. T.; Zhang, R. Y.; Zhang, Y.; Wu, L. M.; Lu, W.; Li, J. Q.; Li, Y. C.; Zhang, H. MXene — enabled electrochemical microfluidic biosensor: Applications toward multicomponent continuous monitoring in whole blood. Adv. Funct. Mater. 2019, 29, 1807326.
Master, A.; Livingston, M.; Gupta, A. S. Photodynamic nanomedicine in the treatment of solid tumors: Perspectives and challenges. J. Control. Release 2013, 168, 88–102.
He, C. B.; Liu, D. M.; Lin, W. B. Nanomedicine applications of hybrid nanomaterials built from metal-ligand coordination bonds: Nanoscale metal-organic frameworks and nanoscale coordination polymers. Chem. Rev. 2015, 115, 11079–11108.
Wang, W. Q.; Wang, L.; Li, Z. S.; Xie, Z. G. BODIPY-containing nanoscale metal-organic frameworks for photodynamic therapy. Chem. Commun. 2016, 52, 5402–5405.
Liu, W.; Wang, Y. M.; Li, Y. H.; Cai, S. J.; Yin, X. B.; He, X. W.; Zhang, Y. K. Fluorescent imaging-guided chemotherapy-and-photodynamic dual therapy with nanoscale porphyrin metal-organic framework. Small 2017, 13, 1603459.
Lan, G. X.; Ni, K. Y.; Xu, Z. W.; Veroneau, S. S.; Song, Y.; Lin, W. B. Nanoscale metal-organic framework overcomes hypoxia for photodynamic therapy primed cancer immunotherapy. J. Am. Chem. Soc. 2018, 140, 5670–5673.
Lu, K. D.; Aung, T.; Guo, N. N.; Weichselbaum, R.; Lin, W. B. Nanoscale metal-organic frameworks for therapeutic, imaging, and sensing applications. Adv. Mater. 2018, 30, 1707634.
Lan, G. X.; Ni, K. Y.; Veroneau, S. S.; Feng, X. Y.; Nash, G. T.; Luo, T. K.; Xu, Z. W.; Lin, W. B. Titanium-based nanoscale metal-organic framework for type I photodynamic therapy. J. Am. Chem. Soc. 2019, 141, 4204–4208.
Lu, K. D.; He, C. B.; Lin, W. B. Nanoscale metal-organic framework for highly effective photodynamic therapy of resistant head and neck cancer. J. Am. Chem. Soc. 2014, 136, 16712–16715.
Lu, K. D.; He, C. B.; Lin, W. B. A chlorin-based nanoscale metal-organic framework for photodynamic therapy of colon cancers. J. Am. Chem. Soc. 2015, 137, 7600–7603.
Feng, D. W.; Chung, W. C.; Wei, Z. W.; Gu, Z. Y.; Jiang, H. L.; Chen, Y. P.; Darensbourg, D. J.; Zhou, H. C. Construction of ultrastable porphyrin Zr metal-organic frameworks through linker elimination. J. Am. Chem. Soc. 2013, 135, 17105–17110.
Feng, D. W.; Gu, Z. Y.; Chen, Y. P.; Park, J.; Wei, Z. W.; Sun, Y. J.; Bosch, M.; Yuan, S.; Zhou, H. C. A highly stable porphyrinic zirconium metal-organic framework with shp-a topology. J. Am. Chem. Soc. 2014, 136, 17714–17717.
Park, J.; Jiang, Q.; Feng, D. W.; Mao, L. Q.; Zhou, H. C. Size-controlled synthesis of porphyrinic metal-organic framework and functionalization for targeted photodynamic therapy. J. Am. Chem. Soc. 2016, 138, 3518–3525
Wu, M. X.; Yang, Y. W. Metal-organic framework (MOF)-based drug/cargo delivery and cancer therapy. Adv. Mater. 2017, 29, 1606134.
Park, J.; Jiang, Q.; Feng, D. W.; Zhou, H. C. Innentitelbild: Controlled generation of singlet oxygen in living cells with tunable ratios of the photochromic switch in metal-organic frameworks (Angew. Chem. 25/2016). Angew. Chem. 2016, 128, 7124–7124.
Zhao, M. T.; Wang, Y. X.; Ma, Q. L.; Huang, Y.; Zhang, X.; Ping, J. F.; Zhang, Z. C.; Lu, Q. P.; Yu, Y. F.; Xu, H. et al. Ultrathin 2D metal-organic framework nanosheets. Adv. Mater. 2015, 27, 7372–7378.
He, Y. P.; Tan, Y. X.; Zhang, J. Stable Mg-Metal-Organic Framework (MOF) and unstable Zn-MOF based on nanosized Tris((4-carboxyl)phenylduryl)amine ligand. Cryst. Growth Des. 2013, 13, 6–9.
Zhao, Y. W.; Jiang, L.; Shangguan, L.; Mi, L.; Liu, A. R.; Liu, S. Q. Synthesis of porphyrin-based two-dimensional metal-organic framework nanodisk with small size and few layers. J. Mater. Chem. A 2018, 6, 2828–2833.
Jiang, Y. Y.; Sun, L. B.; Du, J. F.; Liu, Y. C.; Shi, H. Z.; Liang, Z. Q.; Li, J. Y. Multifunctional zinc metal-organic framework based on designed H4TCPP ligand with aggregation-induced emission effect: CO2 adsorption, luminescence, and sensing property. Cryst. Growth Des. 2017, 17, 2090–2096.
Zhao, Y. W.; Kuang, Y.; Liu, M.; Wang, J. N.; Pei, R. J. Synthesis of metal-organic framework nanosheets with high relaxation rate and singlet oxygen yield. Chem. Mater. 2018, 30, 7511–7520.
Wang, Y. X.; Zhao, M. T.; Ping, J. F.; Chen, B.; Cao, X. H.; Huang, Y.; Tan, C. L.; Ma, Q. L.; Wu, S. X.; Yu, Y. F. et al. Bioinspired design of ultrathin 2D bimetallic metal-organic-framework nanosheets used as biomimetic enzymes. Adv. Mater. 2016, 28, 4149–4155.
Fu, H. G.; Chen, Y.; Yu, Q. L.; Liu, Y. A tumor-targeting Ru/polysaccharide/protein supramolecular assembly with high photodynamic therapy ability. Chem. Commun. 2019, 55, 3148–3151.
Fang, C. H.; Jia, H. L.; Chang, S.; Ruan, Q. F.; Wang, P. Chen, T.; Wang, J. F. (Gold core)/(titania shell) nanostructures for plasmonenhanced photon harvesting and generation of reactive oxygen species. Energy Environ. Sci. 2014, 7, 3431–3438.
Hang, L. F.; Li, H. L.; Zhang, T.; Men, D. D.; Zhang, C.; Gao, P.; Zhang, Q. L. Au@Prussian blue hybrid nanomaterial synergy with a chemotherapeutic drug for tumor diagnosis and chemodynamic therapy. ACSAppl. Mater. Interfaces 2019, 11, 39493–39502.
Acknowledgements
This work is supported by the National Natural Science Foundation of China (NSFC) (Nos. 51903162 and U1903120) and Science foundation of Guangdong Second Provincial General Hospital (No. YN2018-001).
Author information
Authors and Affiliations
Corresponding authors
Electronic Supplementary Material
12274_2020_3093_MOESM1_ESM.pdf
Controllable photodynamic performance via an acidic microenvironment based on two-dimensional metal-organic frameworks for photodynamic therapy
Rights and permissions
About this article
Cite this article
Hang, L., Zhang, T., Wen, H. et al. Controllable photodynamic performance via an acidic microenvironment based on two-dimensional metal-organic frameworks for photodynamic therapy. Nano Res. 14, 660–666 (2021). https://doi.org/10.1007/s12274-020-3093-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12274-020-3093-1