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Nano Research 2023, 16(8): 11176-11185 https://doi.org/10.1007/s12274-023-5810-z
Research Article | Issue | Published: 13 June 2023

MicroRNA-208a silencing against myocardial ischemia/reperfusion injury mediated by reversibly camouflaged biomimetic nanocomplexes

Show Author's Information Jianhui Lu1,§,  Jiaheng Zhang1,§,  Wen Yan2,§,  Chenglong Ge3,  Yang Zhou3( ),  Rongying Zhu1,  Shanzhou Duan1,  Lichen Yin3( ),  Yongbing Chen1( )
Department of Thoracic Surgery, Suzhou Key Laboratory of Thoracic Oncology, The Second Affiliated Hospital of Soochow University, Suzhou 215004, China
Center of Stomatology, The Second Affiliated Hospital of Soochow University, Suzhou 215004, China
Jiangsu Key Laboratory for Carbon-Based Functional Materials and Devices, Institute of Functional Nano & Soft Materials (FUNSOM), Collaborative Innovation Center of Suzhou Nano Science & Technology, Soochow University, Suzhou 215123, China

§ Jianhui Lu, Jiaheng Zhang, and Wen Yan contributed equally to this work.

Keywords:
myocardial ischemia/reperfusion (IR) injury, reversible membrane coating, microRNA-208a silencing, red blood cell membrane, H2O2 responsiveness, membrane-penetrating α-helical polypeptide
Topics:
Cardiovascular system Controlled drug deliveryGene therapy NanobiotechnologyNucleic acids
Cite this article:
Lu J, Zhang J, Yan W, et al. MicroRNA-208a silencing against myocardial ischemia/reperfusion injury mediated by reversibly camouflaged biomimetic nanocomplexes. Nano Research, 2023, 16(8): 11176-11185. https://doi.org/10.1007/s12274-023-5810-z
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Abstract Full text Electronic supplementary material About this article

MicroRNA-208a (miR-208a) plays critical roles in the severe fibrosis and heart failure post myocardial ischemia/reperfusion (IR) injury. MiR-208a inhibitor (mI) with complementary RNA sequence can silence the expression of miR-208a, while it is challenging to achieve efficient and myocardium-targeted delivery. Herein, biomimetic nanocomplexes (NCs) reversibly coated with red blood cell membrane (RM) were developed for the myocardial delivery of mI. To construct the NCs, membrane-penetrating helical polypeptide (PG) was first adopted to condense mI and form the cationic inner core, which subsequently adsorbed catalase (CAT) via electrostatic interaction followed by surface coating with RM. The membrane-coated NCs enabled prolonged blood circulation after systemic administration, and could accumulate in the injured myocardium via passive targeting. In the oxidative microenvironment of injured myocardium, CAT decomposed H2O2 to produce O2 bubbles, which drove the shedding of the outer RM to expose the positively charged inner core, thus facilitated effective internalization by cardiac cells. Based on the combined contribution of mI-mediated miR-208a silencing and CAT-mediated alleviation of oxidative stress, NCs effectively ameliorated the myocardial microenvironment, hence reducing the infarct size as well as fibrosis and promoting recovery of cardiac functions. This study provides an effective strategy for the cytosolic delivery of nucleic acid cargoes in the myocardium, and it renders an enlightened approach to resolve the blood circulation/cell internalization dilemma of cell membrane-coated delivery systems.


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Electronic supplementary material
About this article

MicroRNA-208a silencing against myocardial ischemia/reperfusion injury mediated by reversibly camouflaged biomimetic nanocomplexes

Show Author's information Jianhui Lu1,§, Jiaheng Zhang1,§, Wen Yan2,§, Chenglong Ge3, Yang Zhou3( ), Rongying Zhu1, Shanzhou Duan1, Lichen Yin3( ), Yongbing Chen1( )
Department of Thoracic Surgery, Suzhou Key Laboratory of Thoracic Oncology, The Second Affiliated Hospital of Soochow University, Suzhou 215004, China
Center of Stomatology, The Second Affiliated Hospital of Soochow University, Suzhou 215004, China
Jiangsu Key Laboratory for Carbon-Based Functional Materials and Devices, Institute of Functional Nano & Soft Materials (FUNSOM), Collaborative Innovation Center of Suzhou Nano Science & Technology, Soochow University, Suzhou 215123, China

§ Jianhui Lu, Jiaheng Zhang, and Wen Yan contributed equally to this work.

Abstract

MicroRNA-208a (miR-208a) plays critical roles in the severe fibrosis and heart failure post myocardial ischemia/reperfusion (IR) injury. MiR-208a inhibitor (mI) with complementary RNA sequence can silence the expression of miR-208a, while it is challenging to achieve efficient and myocardium-targeted delivery. Herein, biomimetic nanocomplexes (NCs) reversibly coated with red blood cell membrane (RM) were developed for the myocardial delivery of mI. To construct the NCs, membrane-penetrating helical polypeptide (PG) was first adopted to condense mI and form the cationic inner core, which subsequently adsorbed catalase (CAT) via electrostatic interaction followed by surface coating with RM. The membrane-coated NCs enabled prolonged blood circulation after systemic administration, and could accumulate in the injured myocardium via passive targeting. In the oxidative microenvironment of injured myocardium, CAT decomposed H2O2 to produce O2 bubbles, which drove the shedding of the outer RM to expose the positively charged inner core, thus facilitated effective internalization by cardiac cells. Based on the combined contribution of mI-mediated miR-208a silencing and CAT-mediated alleviation of oxidative stress, NCs effectively ameliorated the myocardial microenvironment, hence reducing the infarct size as well as fibrosis and promoting recovery of cardiac functions. This study provides an effective strategy for the cytosolic delivery of nucleic acid cargoes in the myocardium, and it renders an enlightened approach to resolve the blood circulation/cell internalization dilemma of cell membrane-coated delivery systems.

Keywords: myocardial ischemia/reperfusion (IR) injury, reversible membrane coating, microRNA-208a silencing, red blood cell membrane, H2O2 responsiveness, membrane-penetrating α-helical polypeptide

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Publication history
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Acknowledgements

Publication history

Received: 29 March 2023
Revised: 01 May 2023
Accepted: 05 May 2023
Published: 13 June 2023
Issue date: August 2023

Copyright

© Tsinghua University Press 2023

Acknowledgements

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 82172076, 52273144, and 52033006), 111 project, Collaborative Innovation Center of Suzhou Nano Science & Technology, Joint International Research Laboratory of Carbon-Based Functional Materials and Devices, and Suzhou Key Laboratory of Nanotechnology and Biomedicine.

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