Resolvin D1 delivery to lesional macrophages using antioxidative black phosphorus nanosheets for atherosclerosis treatment

doi:10.1038/s41565-024-01687-1

. 2024 Sep;19(9):1386-1398.

doi: 10.1038/s41565-024-01687-1. Epub 2024 Jun 19.

Resolvin D1 delivery to lesional macrophages using antioxidative black phosphorus nanosheets for atherosclerosis treatment

Zhongshan He^#¹, Wei Chen^#², Kuan Hu^#^{3

4

5}, Yaoyao Luo¹, Wanqin Zeng⁶, Xi He¹, Tingting Li¹, Jiang Ouyang³, Yongjiang Li³, Lin Xie⁴, Yiding Zhang⁴, Qin Xu¹, Shuping Yang¹, Mengran Guo¹, Wei Zou¹, Yanfei Li¹, Lingjing Huang¹, Lu Chen⁶, Xingcai Zhang⁷, Qimanguli Saiding³, Rui Wang⁵, Ming-Rong Zhang⁴, Na Kong³, Tian Xie⁸, Xiangrong Song⁹, Wei Tao¹⁰

Affiliations

¹ Department of Critical Care Medicine, Frontiers Science Center for Disease-related Molecular Network, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China.
² Center for Nanomedicine and Department of Anesthesiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. wchen123@gate.sinica.edu.tw.
³ Center for Nanomedicine and Department of Anesthesiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁴ Department of Advanced Nuclear Medicine Sciences, Institute for Quantum Medical Science, Quantum Life and Medical Science Directorate, National Institutes for Quantum Science and Technology, Chiba, Japan.
⁵ State Key Laboratory of Bioactive Substance and Function of Natural Medicines, Institute of Materia Medica, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.
⁶ Key Laboratory of Birth Defects and Related Diseases of Women and Children of MOE, State Key Laboratory of Biotherapy, West China Second Hospital, Sichuan University, Chengdu, China.
⁷ Department of Materials Science and Engineering, Stanford University, Stanford, CA, USA.
⁸ College of Pharmacy, School of Medicine, Hangzhou Normal University, Hangzhou, China.
⁹ Department of Critical Care Medicine, Frontiers Science Center for Disease-related Molecular Network, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China. songxr@scu.edu.cn.
¹⁰ Center for Nanomedicine and Department of Anesthesiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. wtao@bwh.harvard.edu.

^# Contributed equally.

PMID: 38898135
DOI: 10.1038/s41565-024-01687-1

Resolvin D1 delivery to lesional macrophages using antioxidative black phosphorus nanosheets for atherosclerosis treatment

Zhongshan He et al. Nat Nanotechnol. 2024 Sep.

. 2024 Sep;19(9):1386-1398.

doi: 10.1038/s41565-024-01687-1. Epub 2024 Jun 19.

Authors

Affiliations

¹ Department of Critical Care Medicine, Frontiers Science Center for Disease-related Molecular Network, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China.
² Center for Nanomedicine and Department of Anesthesiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. wchen123@gate.sinica.edu.tw.
³ Center for Nanomedicine and Department of Anesthesiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁴ Department of Advanced Nuclear Medicine Sciences, Institute for Quantum Medical Science, Quantum Life and Medical Science Directorate, National Institutes for Quantum Science and Technology, Chiba, Japan.
⁵ State Key Laboratory of Bioactive Substance and Function of Natural Medicines, Institute of Materia Medica, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.
⁶ Key Laboratory of Birth Defects and Related Diseases of Women and Children of MOE, State Key Laboratory of Biotherapy, West China Second Hospital, Sichuan University, Chengdu, China.
⁷ Department of Materials Science and Engineering, Stanford University, Stanford, CA, USA.
⁸ College of Pharmacy, School of Medicine, Hangzhou Normal University, Hangzhou, China.
⁹ Department of Critical Care Medicine, Frontiers Science Center for Disease-related Molecular Network, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China. songxr@scu.edu.cn.
¹⁰ Center for Nanomedicine and Department of Anesthesiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. wtao@bwh.harvard.edu.

^# Contributed equally.

PMID: 38898135
DOI: 10.1038/s41565-024-01687-1

Abstract

The buildup of plaques in atherosclerosis leads to cardiovascular events, with chronic unresolved inflammation and overproduction of reactive oxygen species (ROS) being major drivers of plaque progression. Nanotherapeutics that can resolve inflammation and scavenge ROS have the potential to treat atherosclerosis. Here we demonstrate the potential of black phosphorus nanosheets (BPNSs) as a therapeutic agent for the treatment of atherosclerosis. BPNSs can effectively scavenge a broad spectrum of ROS and suppress atherosclerosis-associated pro-inflammatory cytokine production in lesional macrophages. We also demonstrate ROS-responsive, targeted-peptide-modified BPNS-based carriers for the delivery of resolvin D1 (an inflammation-resolving lipid mediator) to lesional macrophages, which further boosts the anti-atherosclerotic efficacy. The targeted nanotherapeutics not only reduce plaque areas but also substantially improve plaque stability in high-fat-diet-fed apolipoprotein E-deficient mice. This study presents a therapeutic strategy against atherosclerosis, and highlights the potential of BPNS-based therapeutics to treat other inflammatory diseases.

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References

1. Moore, K. J. & Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 145, 341–355 (2011). - PubMed - PMC
1. Tabas, I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10, 36–46 (2010). - PubMed
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[1] Moore, K. J. & Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 145, 341–355 (2011). - PubMed - PMC

[2] Moore, K. J. & Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 145, 341–355 (2011). - PubMed - PMC

[3] Tabas, I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10, 36–46 (2010). - PubMed

[4] Tabas, I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10, 36–46 (2010). - PubMed

[5] Libby, P. The changing landscape of atherosclerosis. Nature 592, 524–533 (2021). - PubMed

[6] Libby, P. The changing landscape of atherosclerosis. Nature 592, 524–533 (2021). - PubMed

[7] Chen, W. et al. Macrophage-targeted nanomedicine for the diagnosis and treatment of atherosclerosis. Nat. Rev. Cardiol. 19, 228–249 (2022). - PubMed

[8] Chen, W. et al. Macrophage-targeted nanomedicine for the diagnosis and treatment of atherosclerosis. Nat. Rev. Cardiol. 19, 228–249 (2022). - PubMed

[9] Bäck, M., Yurdagul, A., Tabas, I., Öörni, K. & Kovanen, P. T. Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities. Nat. Rev. Cardiol. 16, 389–406 (2019). - PubMed - PMC

[10] Bäck, M., Yurdagul, A., Tabas, I., Öörni, K. & Kovanen, P. T. Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities. Nat. Rev. Cardiol. 16, 389–406 (2019). - PubMed - PMC

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Resolvin D1 delivery to lesional macrophages using antioxidative black phosphorus nanosheets for atherosclerosis treatment

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Resolvin D1 delivery to lesional macrophages using antioxidative black phosphorus nanosheets for atherosclerosis treatment

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