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Nano Research https://doi.org/10.1007/s12274-024-6595-4
Research Article | Online first | Published: 23 March 2024

Enhanced population of excited single state strategy: irradiation and ultrasound dual-response and host tumor-driven nano-sensitizers construction in triple synergistic therapy

Show Author's Information Yaning Li1,  Mengyan Tian1,  Tianyue Yang1,  Jiayu Cao2,  Hongli Chen3,  Jun Guo2,  Pai Liu1,6( ),  Yi Liu4,5,6( )
State Key Laboratory of Separation Membranes and Membrane Processes, School of Materials Science and Engineering, Tiangong University, Tianjin 300387, China
State Key Laboratory of Separation Membranes and Membrane Processes, School of Chemistry, Tiangong University, Tianjin 300387, China
State Key Laboratory of Separation Membranes and Membrane Processes, School of Life Science, Tiangong University, Tianjin 300387, China
State Key Laboratory of Separation Membrane and Membrane Process & Tianjin Key Laboratory of Green Chemical Technology and Process Engineering, School of Chemistry, Tiangong University, Tianjin 300387, China
School of Chemical and Environmental Engineering, Wuhan Polytechnic University, Wuhan 430023, China
Cangzhou Institute of Tiangong University, Cangzhou 061000, China
Keywords:
aggregation-induced emission, photo-sonodynamic therapy, enhanced excited state population, triphosphate (ATP)-activated nano-sensitizers
Topics:
Controlled drug deliveryTheranosticsTumors
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Li Y, Tian M, Yang T, et al. Enhanced population of excited single state strategy: irradiation and ultrasound dual-response and host tumor-driven nano-sensitizers construction in triple synergistic therapy. Nano Research, 2024, https://doi.org/10.1007/s12274-024-6595-4
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Abstract Full text Electronic supplementary material About this article

Phototheranostics is an emerging field in synergistic antitumor therapy in which irradiation and sensitizers are combined to produce reactive oxygen species (ROS), bio-images, and high temperatures. All of these are arrived from the energy of sensitizers, which located in excited single state (S1). Undeniably, the decentralization of the S1 population indirectly decreases the effect of each individual treatment. In this study, a strategy was proposed for enhancing the S1 population, and a sensitizer with mitochondrial targeting property, 1,4-indolyl iodinated pyrrolo[3,2-b]pyrrole derivative (2I-TPIS), was assembled into adenosine triphosphate (ATP)-responsive nanoparticles (DPA-2I NPs) to achieve dual responses to irradiation and ultrasonication (US) for application to photo-sonodynamic therapy (PSDT). Compared with monotherapies, 2I-TPIS generated more ROS in PSDT, inducing mitochondrial autophagy and apoptosis, which in turn triggered immunogenic cell death (ICD). Subsequently, DPA-2I NPs were constructed and self-assembled with the chemotherapeutic agents DPA-Cd and 2I-TPIS to achieve a triple synergistic strategy involving chemotherapy (CT) and PSDT. DPA-2I NPs exhibited absolute sensitization, intra-tumoral overexpression of ATP, and disassembly. Importantly, the biosafety and potent antitumor efficiency of the DPA-2I NP-based “PSDT + CT” therapy were revealed using a 4T1 tumor model. The study results provide insights into the design of sensitizers possessing a sufficient S1 population and a highly efficient tumor ablation capacity derived from molecular structural modulation, further enabling triple synergistic antitumor therapies, and expanding the clinical application of sensitizers.


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Abstract
Full text
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Electronic supplementary material
About this article

Enhanced population of excited single state strategy: irradiation and ultrasound dual-response and host tumor-driven nano-sensitizers construction in triple synergistic therapy

Show Author's information Yaning Li1, Mengyan Tian1, Tianyue Yang1, Jiayu Cao2, Hongli Chen3, Jun Guo2, Pai Liu1,6( ), Yi Liu4,5,6( )
State Key Laboratory of Separation Membranes and Membrane Processes, School of Materials Science and Engineering, Tiangong University, Tianjin 300387, China
State Key Laboratory of Separation Membranes and Membrane Processes, School of Chemistry, Tiangong University, Tianjin 300387, China
State Key Laboratory of Separation Membranes and Membrane Processes, School of Life Science, Tiangong University, Tianjin 300387, China
State Key Laboratory of Separation Membrane and Membrane Process & Tianjin Key Laboratory of Green Chemical Technology and Process Engineering, School of Chemistry, Tiangong University, Tianjin 300387, China
School of Chemical and Environmental Engineering, Wuhan Polytechnic University, Wuhan 430023, China
Cangzhou Institute of Tiangong University, Cangzhou 061000, China

Abstract

Phototheranostics is an emerging field in synergistic antitumor therapy in which irradiation and sensitizers are combined to produce reactive oxygen species (ROS), bio-images, and high temperatures. All of these are arrived from the energy of sensitizers, which located in excited single state (S1). Undeniably, the decentralization of the S1 population indirectly decreases the effect of each individual treatment. In this study, a strategy was proposed for enhancing the S1 population, and a sensitizer with mitochondrial targeting property, 1,4-indolyl iodinated pyrrolo[3,2-b]pyrrole derivative (2I-TPIS), was assembled into adenosine triphosphate (ATP)-responsive nanoparticles (DPA-2I NPs) to achieve dual responses to irradiation and ultrasonication (US) for application to photo-sonodynamic therapy (PSDT). Compared with monotherapies, 2I-TPIS generated more ROS in PSDT, inducing mitochondrial autophagy and apoptosis, which in turn triggered immunogenic cell death (ICD). Subsequently, DPA-2I NPs were constructed and self-assembled with the chemotherapeutic agents DPA-Cd and 2I-TPIS to achieve a triple synergistic strategy involving chemotherapy (CT) and PSDT. DPA-2I NPs exhibited absolute sensitization, intra-tumoral overexpression of ATP, and disassembly. Importantly, the biosafety and potent antitumor efficiency of the DPA-2I NP-based “PSDT + CT” therapy were revealed using a 4T1 tumor model. The study results provide insights into the design of sensitizers possessing a sufficient S1 population and a highly efficient tumor ablation capacity derived from molecular structural modulation, further enabling triple synergistic antitumor therapies, and expanding the clinical application of sensitizers.

Keywords: aggregation-induced emission, photo-sonodynamic therapy, enhanced excited state population, triphosphate (ATP)-activated nano-sensitizers

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Publication history
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Acknowledgements

Publication history

Received: 14 December 2023
Revised: 20 February 2024
Accepted: 26 February 2024
Published: 23 March 2024

Copyright

© Tsinghua University Press 2024

Acknowledgements

Acknowledgements

The authors are thankful for the financial support from the National Natural Science Foundation of China (Nos. U23A2089, 22205159, and 22103055), Natural Science Foundation of Tianjin (No. 21JCQNJC01450), and Science and Technology Plans of Tianjin (Nos. 22ZYJDSS00070 and 21ZYJDJC00050). The authors also thank the Analytical & Testing Center of Tiangong Univertisy for NMR spectrometer and Transmission Electron Microscope.

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