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One Responsive Stone, Three Birds: Mn(III)-Hemoporfin Frameworks with Glutathione-Enhanced Degradation, MRI, and
Peng Geng1, Nuo Yu1, Jiulong Zhang2
1State Key Laboratory for Modification of Chemical Fibers and Polymer Materials, College of Materials Science and Engineering, Donghua University, Shanghai, 201620, China.
Abstract:
Ultrasound-driven sonodynamic therapy (SDT) catches numerous attentions for destroying deep-seated tumors, but its applications suffer from unsatisfactory therapeutic effects and metabolism. Furthermore, SDT is usually weakened by the complex tumor microenvironment, such as the overexpression of glutathione (GSH). To address these issues, Mn(III)-hemoporfin frameworks (Mn(III)-HFs) are reported as nanosonosensitizers by using biocompatible hematoporphyrin monomethyl-ether (HMME) to coordinate with Mn(III) ions. Mn(III)-HFs/PEG can react with GSH to produce Mn(II) ions and oxidized glutathione (GSSG), resulting in three fascinating features: 1) the redox reaction facilitates the decomposition of Mn(III)-HFs/PEG and then collapse of nanostructures, improving the biodegradability; 2) Mn(II) ions with five unpaired 3d-electrons exhibit better magnetic resonance imaging (MRI) ability compared to Mn(III) ions with four electrons; 3) both the depletion of endogenous GSH and the dissociated HMME boost 1 O2 generation ability under US irradiation. As a result, when Mn(III)-HFs/PEG dispersion is intravenously administered into mice, it exhibits high-contrast T1 /T2 dual-modal MRI and significant suppression for the growth rate of the deep-seated tumor. Furthermore, Mn(III)-HFs/PEG can be efficiently metabolized from the mice. Therefore, Mn(III)-HFs/PEG exhibit GSH-enhanced degradation, MRI, and SDT effects, which provide some insights on the developments of other responsive nanosonosensitizers.
Insights
Manganese-hemoporfin frameworks (Mn(III)-HFs) enhance sonodynamic therapy (SDT) by degrading in the tumor microenvironment. This improves biodegradability, boosts magnetic resonance imaging (MRI) contrast, and increases therapeutic efficacy against deep-seated tumors.
Area of Science:
- Biomaterials Science
- Nanotechnology
- Cancer Therapy
Background:
- Ultrasound-driven sonodynamic therapy (SDT) shows promise for deep-seated tumors but faces challenges from the tumor microenvironment, particularly glutathione (GSH).
- Existing nanosonosensitizers often exhibit limited therapeutic effects and poor biodegradability, hindering clinical translation.
Purpose of the Study:
- To develop novel nanosonosensitizers that overcome the limitations of traditional SDT in complex tumor microenvironments.
- To engineer a system that enhances biodegradability, improves imaging capabilities, and increases therapeutic efficacy through GSH responsiveness.
Main Methods:
- Synthesis of Mn(III)-hemoporfin frameworks (Mn(III)-HFs) using biocompatible hematoporphyrin monomethyl-ether (HMME) and Mn(III) ions, further functionalized with PEG.
- Investigation of the redox reaction between Mn(III)-HFs/PEG and GSH, leading to Mn(II) release and nanostructure decomposition.
- Evaluation of the dual-modal magnetic resonance imaging (MRI) capabilities (T1/T2) and sonodynamic therapeutic effects in a mouse tumor model.
Main Results:
- Mn(III)-HFs/PEG demonstrated GSH-triggered degradation, enhancing biodegradability and improving Mn(II) ion release for superior MRI contrast.
- The depletion of GSH and release of HMME significantly boosted singlet oxygen (1O2) generation under ultrasound irradiation, enhancing SDT efficacy.
- Intravenous administration in mice resulted in significant tumor growth suppression and efficient metabolism of the nanostructures.
Conclusions:
- Mn(III)-HFs/PEG represent a promising GSH-responsive nanosonosensitizer with enhanced degradation, MRI, and SDT capabilities.
- This work provides valuable insights for designing other responsive nanosonosensitizers for improved cancer therapy.
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