NIR-II photothermal therapy for effective tumor eradication enhanced by heterogeneous nanorods with dual catalytic activities
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Ya Ding1(
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Rational design and exploitation of nanomaterials with superior treatment properties for suitable indications is a way out to relieve cost constraint of therapy and solve the unsatisfactory efficacy for cancer patients. In this work, we propose a greatly facile approach to produce heterogeneous Pd-Au nanorods (Pd-Au NRs) that solve the current bottleneck problems of photothermal thermal therapy (PTT) as well as completely eliminate tumors in animal models without toxic side effects. Depositing Pd clusters on both tips of Au NRs offers Pd-Au NRs three novel functions, i.e., the extension of the absorption into NIR-II region, the activation of prodrug of 5-fluorouracil (5-Fu) via the bioorthogonal reaction, and the peroxidase-mimic activity to produce ·OH. The heterogeneous nanorods showed a high and stable photothermal conversion efficiency (52.07%) in a safer NIR-II irradiation region (1,064 nm), which not only eliminate most of tumor cells at only one dose of the irradiation for 5 min but also improve the in situ conversion of 5-fluoro-1-propargyluracil and H2O2 into active 5-Fu and ·OH to eradicate residual tumors for inhibiting tumor metastasis. This dual catalytic activity-synergistic mechanism of PTT demonstrates the importance of material design in solving current bottleneck problem of tumor therapy.
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NIR-II photothermal therapy for effective tumor eradication enhanced by heterogeneous nanorods with dual catalytic activities
), Ya Ding1(
)
Abstract
Rational design and exploitation of nanomaterials with superior treatment properties for suitable indications is a way out to relieve cost constraint of therapy and solve the unsatisfactory efficacy for cancer patients. In this work, we propose a greatly facile approach to produce heterogeneous Pd-Au nanorods (Pd-Au NRs) that solve the current bottleneck problems of photothermal thermal therapy (PTT) as well as completely eliminate tumors in animal models without toxic side effects. Depositing Pd clusters on both tips of Au NRs offers Pd-Au NRs three novel functions, i.e., the extension of the absorption into NIR-II region, the activation of prodrug of 5-fluorouracil (5-Fu) via the bioorthogonal reaction, and the peroxidase-mimic activity to produce ·OH. The heterogeneous nanorods showed a high and stable photothermal conversion efficiency (52.07%) in a safer NIR-II irradiation region (1,064 nm), which not only eliminate most of tumor cells at only one dose of the irradiation for 5 min but also improve the in situ conversion of 5-fluoro-1-propargyluracil and H2O2 into active 5-Fu and ·OH to eradicate residual tumors for inhibiting tumor metastasis. This dual catalytic activity-synergistic mechanism of PTT demonstrates the importance of material design in solving current bottleneck problem of tumor therapy.
References(47)
Lu, Y.; Aimetti, A. A.; Langer, R.; Gu, Z. Bioresponsive materials. Nat. Rev. Mater. 2017, 2, 16075.
Wang, J.; Li, Y. Y.; Nie, G. J. Multifunctional biomolecule nanostructures for cancer therapy. Nat. Rev. Mater. 2021, 6, 766–783.
Sung, H.; Ferlay, J.; Siegel, R. L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: Cancer J. Clin. 2021, 71, 209–249.
Fan, W. P.; Yung, B.; Huang, P.; Chen, X. Y. Nanotechnology for multimodal synergistic cancer therapy. Chem. Rev. 2017, 117, 13566–13638.
Wei, H.; Wang, E. K. Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes. Chem. Soc. Rev. 2013, 42, 6060–6093.
Liu, Y. J.; Bhattarai, P.; Dai, Z. F.; Chen, X. Y. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 2019, 48, 2053–2108.
Sun, H. T.; Zhang, Q.; Li, J. C.; Peng, S. J.; Wang, X. L.; Cai, R. Near-infrared photoactivated nanomedicines for photothermal synergistic cancer therapy. Nano Today 2021, 37, 101073.
Huang, X. J.; Zhang, W. L.; Guan, G. Q.; Song, G. S.; Zou, R. J.; Hu, J. Q. Design and functionalization of the NIR-responsive photothermal semiconductor nanomaterials for cancer theranostics. Acc. Chem. Res. 2017, 50, 2529–2538.
Abbas, M.; Zou, Q. L.; Li, S. K.; Yan, X. H. Self-assembled peptide- and protein-based nanomaterials for antitumor photodynamic and photothermal therapy. Adv. Mater. 2017, 29, 1605021.
Liu, S.; Pan, X. T.; Liu, H. Y. Two-dimensional nanomaterials for photothermal therapy. Angew. Chem., Int. Ed. 2020, 59, 5890–5900.
Yang, J.; Yao, M. H.; Jin, R. M.; Zhao, D. H.; Zhao, Y. D.; Liu, B. Polypeptide-engineered hydrogel coated gold nanorods for targeted drug delivery and chemo-photothermal therapy. ACS Biomater. Sci. Eng. 2017, 3, 2391–2398.
Zhang, Z. J.; Wang, L. M.; Wang, J.; Jiang, X. M.; Li, X. H.; Hu, Z. J.; Ji, Y. L.; Wu, X. C.; Chen, C. Y. Mesoporous silica-coated gold nanorods as a light-mediated multifunctional theranostic platform for cancer treatment. Adv. Mater. 2012, 24, 1418–1423.
Shen, S.; Tang, H. Y.; Zhang, X. T.; Ren, J. F.; Pang, Z. Q.; Wang, D. G.; Gao, H. L.; Qian, Y.; Jiang, X. G.; Yang, W. L. Targeting mesoporous silica-encapsulated gold nanorods for chemo-photothermal therapy with near-infrared radiation. Biomaterials 2013, 34, 3150–3158.
Ye, X. C.; Zheng, C.; Chen, J.; Gao, Y. Z.; Murray, C. B. Using binary surfactant mixtures to simultaneously improve the dimensional tunability and monodispersity in the seeded growth of gold nanorods. Nano Lett. 2013, 13, 765–771.
Chen, Y. S.; Zhao, Y.; Yoon, S. J.; Gambhir, S. S.; Emelianov, S. Miniature gold nanorods for photoacoustic molecular imaging in the second near-infrared optical window. Nat. Nanotechnol. 2019, 14, 465–472.
Sugiura, T.; Matsuki, D.; Okajima, J.; Komiya, A.; Mori, S.; Maruyama, S.; Kodama, T. Photothermal therapy of tumors in lymph nodes using gold nanorods and near-infrared laser light with controlled surface cooling. Nano Res. 2015, 8, 3842–3852.
Terentyuk, G.; Panfilova, E.; Khanadeev, V.; Chumakov, D.; Genina, E.; Bashkatov, A.; Tuchin, V.; Bucharskaya, A.; Maslyakova. G.; Khlebtsov, N. et al. Gold nanorods with a hematoporphyrin-loaded silica shell for dual-modality photodynamic and photothermal treatment of tumors in vivo. Nano Res. 2014, 7, 325–337.
Zeng, J. Y.; Zhang, M. K.; Peng, M. Y.; Gong, D.; Zhang, X. Z. Porphyrinic metal–organic frameworks coated gold nanorods as a versatile nanoplatform for combined photodynamic/photothermal/chemotherapy of tumor. Adv. Funct. Mater. 2018, 28, 1705451.
Nam, J.; Son, S.; Ochyl, L. J.; Kuai, R.; Schwendeman, A.; Moon, J. J. Chemo-photothermal therapy combination elicits anti-tumor immunity against advanced metastatic cancer. Nat. Commun. 2018, 9, 1074.
Deng, X. R.; Liang, S.; Cai, X. C.; Huang, S. S.; Cheng, Z. Y.; Shi, Y. S.; Pang, M. L.; Ma, P. A.; Lin, J. Yolk–shell structured Au nanostar@metal–organic framework for synergistic chemo-photothermal therapy in the second near-infrared window. Nano Lett. 2019, 19, 6772–6780.
Rautio, J.; Meanwell, N. A.; Di, L.; Hageman, M. J. The expanding role of prodrugs in contemporary drug design and development. Nat. Rev. Drug. Discov. 2018, 17, 559–587.
Dong, S. M.; Dong, Y. S.; Jia, T.; Liu, S. K.; Liu, J.; Yang, D.; He, F.; Gai, S. L.; Yang, P. P.; Lin, J. GSH-depleted nanozymes with hyperthermia-enhanced dual enzyme-mimic activities for tumor nanocatalytic therapy. Adv. Mater. 2020, 32, 2002439.
Dong, Y. S.; Tu, Y. L.; Wang, K. W.; Xu, C. F.; Yuan, Y. Y.; Wang, J. A general strategy for macrotheranostic prodrug activation: Synergy between the acidic tumor microenvironment and bioorthogonal chemistry. Angew. Chem., Int. Ed. 2020, 59, 7168–7172.
Wang, W. J.; Zhang, X. Z.; Huang, R.; Hirschbiegel, C. M.; Wang, H. S.; Ding, Y.; Rotello, V. M. In situ activation of therapeutics through bioorthogonal catalysis. Adv. Drug Deliv. Rev. 2021, 176, 113893.
Yao, Q. X.; Lin, F.; Fan, X. Y.; Wang, Y. P.; Liu, Y.; Liu, Z. F.; Jiang, X. Y.; Chen, P. R.; Gao, Y. Synergistic enzymatic and bioorthogonal reactions for selective prodrug activation in living systems. Nat. Commun. 2018, 9, 5032.
Du, Z.; Liu, C.; Song, H. L.; Scott, P.; Liu, Z. Q.; Ren, J. S.; Qu, X. G. Neutrophil-membrane-directed bioorthogonal synthesis of inflammation-targeting chiral drugs. Chem. 2020, 6, 2060–2072.
Chang, M. Y.; Hou, Z. Y.; Wang, M.; Yang, C. Z.; Wang, R. F.; Li, F.; Liu, D. L.; Peng, T. L.; Li, C. X.; Lin, J. Single-atom Pd nanozyme for ferroptosis-boosted mild-temperature photothermal therapy. Angew Chem., Int. Ed. 2021, 60, 12971–12979.
Hu, Y. H.; Lv, T.; Ma, Y.; Xu, J. J.; Zhang, Y. H.; Hou, Y. L.; Huang, Z. J.; Ding, Y. Nanoscale coordination polymers for synergistic NO and chemodynamic therapy of liver cancer. Nano Lett. 2019, 19, 2731–2738.
Xiang, S. J.; Fan, Z. X.; Ye, Z. C.; Zhu, T. B.; Shi, D.; Ye, S. F.; Hou, Z. Q.; Chen, X. L. Endogenous Fe2+-activated ROS nanoamplifier for esterase-responsive and photoacoustic imaging-monitored therapeutic improvement. Nano Res. 2022, 15, 907–918.
Sancho-Albero, M.; Rubio-Ruiz, B.; Pérez-López, A. M.; Sebastián, V.; Martín-Duque, P.; Arruebo, M.; Santamaría, J.; Unciti-Broceta, A. Cancer-derived exosomes loaded with ultrathin palladium nanosheets for targeted bioorthogonal catalysis. Nat. Catal. 2019, 2, 864–872.
Su, G. X.; Jiang, H. Q.; Zhu, H. Y.; Lv, J. J.; Yang, G. H.; Yan, B.; Zhu, J. J. Controlled deposition of palladium nanodendrites on the tips of gold nanorods and their enhanced catalytic activity. Nanoscale 2017, 9, 12494–12502.
Petreni, A.; Bonardi, A.; Lomelino, C.; Osman, S. M.; ALOthman, Z. A.; Eldehna, W. M.; El-Haggar, R.; McKenna, R.; Nocentini, A.; Supuran, C. T. Inclusion of a 5-fluorouracil moiety in nitrogenous bases derivatives as human carbonic anhydrase IX and XII inhibitors produced a targeted action against MDA-MB-231 and T47D breast cancer cells. Eur. J. Med. Chem. 2020, 190, 112112.
Wang, X.; Ma, Y. C.; Sheng, X.; Wang, Y. C.; Xu, H. X. Ultrathin polypyrrole nanosheets via space-confined synthesis for efficient photothermal therapy in the second near-infrared window. Nano Lett. 2018, 18, 2217–2225.
Mugaka, B. P.; Zhang, S.; Li, R. Q.; Ma, Y.; Wang, B.; Hong, J.; Hu, Y. H.; Ding, Y.; Xia, X. H. One-pot preparation of peptide-doped metal–amino acid framework for general encapsulation and targeted delivery. ACS Appl. Mater. Interfaces 2021, 13, 11195–11204.
Liu, A. Y.; Wang, H. S.; Hou, X. S.; Ma, Y.; Yang, G. J.; Hou, Y. L.; Ding, Y. Combinatory antitumor therapy by cascade targeting of a single drug. Acta Pharm. Sin. B. 2020, 10, 667–679.
Cui, T.; Ma, Y.; Yang, J. Y.; Liu, S.; Wang, Z. Z.; Zhang, F. F.; Wang, J.; Cai, T.; Dong, L.; Hong, J. et al. Protein corona-guided tumor targeting therapy via the surface modulation of low molecular weight PEG. Nanoscale 2021, 13, 5883–5891.
Ge, C. C.; Fang, G.; Shen, X. M.; Chong, Y.; Wamer, W. G.; Gao, X. F.; Chai, Z. F.; Chen, C. Y.; Yin, J. J. Facet energy versus enzyme-like activities: The unexpected protection of palladium nanocrystals against oxidative damage. ACS Nano 2016, 10, 10436–10445.
Nikoobakht, B.; El-Sayed, M. A. Preparation and growth mechanism of gold nanorods (NRs) using seed-mediated growth method. Chem. Mater. 2003, 15, 1957–1962.
Liu, M. Z.; Guyot-Sionnest, P. Mechanism of silver(I)-assisted growth of gold nanorods and bipyramids. J. Phys. Chem. B 2005, 109, 22192–22200.
Sau, T. K.; Murphy, C. J. Seeded high yield synthesis of short Au nanorods in aqueous solution. Langmuir 2004, 20, 6414–6420.
Ye, J. M.; Li, Z.; Fu, Q. R.; Li, Q. Q.; Zhang, X.; Su, L. C.; Yang, H. H.; Song, J. B. Quantitative photoacoustic diagnosis and precise treatment of inflammation in vivo using activatable theranostic nanoprobe. Adv. Funct. Mater. 2020, 30, 2001771.
Roper, D. K.; Ahn, W.; Hoepfner, M. Microscale heat transfer transduced by surface Plasmon resonant gold nanoparticles. J. Phys. Chem. C 2007, 111, 3636–3641.
Du, Y.; Yang, C.; Li, F. Y.; Liao, H. W.; Chen, Z.; Lin, P. H.; Wang, N.; Zhou, Y.; Lee, J. Y.; Ding, Q. et al. Core–shell–satellite nanomaces as remotely controlled self-fueling Fenton reagents for imaging-guided triple-negative breast cancer-specific therapy. Small 2020, 16, 2002537.
Ma, N. N.; Jiang, Y. W.; Zhang, X. D.; Wu, H.; Myers, J. N.; Liu, P. D.; Jin, H. Z.; Gu, N.; He, N. Y.; Wu, F. G. et al. Enhanced radiosensitization of gold nanospikes via hyperthermia in combined cancer radiation and photothermal therapy. ACS Appl. Mater. Interfaces 2016, 8, 28480–28494.
Wang, Z.; Liu, B.; Sun, Q. Q.; Feng, L. L.; He, F.; Yang, P. P.; Gai, S. L.; Quan, Z. W.; Lin, J. Upconverted metal–organic framework janus architecture for near-infrared and ultrasound co-enhanced high performance tumor therapy. ACS Nano 2021, 15, 12342–12357.
Wei, J. P.; Chen, X. L.; Shi, S. G.; Mo, S. G.; Zheng, N. F. An investigation of the mimetic enzyme activity of two-dimensional Pd-based nanostructures. Nanoscale 2015, 7, 19018–19026.
Speyer, J. L.; Collins, J. M.; Dedrick, R. L.; Brennan, M. F.; Buckpitt, A. R.; Londer, H.; DeVita, V. T. Jr.; Myers, C. E. Phase I and pharmacological studies of 5-fluorouracil administered intraperitoneally. Cancer Res. 1980, 40, 567–572.
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