Blood–Brain Barrier-Penetrative Fluorescent Anticancer Agents Triggering Paraptosis and Ferroptosis for Glioblastoma Therapy

Currently used drugs for glioblastoma (GBM) treatments are ineffective, primarily due to the significant challenges posed by strong drug resistance, poor blood-brain barrier (BBB) permeability, and the lack of tumor specificity. Here, we report two cationic fluorescent anticancer agents (TriPEX-ClO<sub>4</sub> and TriPEX-PF<sub>6</sub>) capable of BBB penetration for efficient GBM therapy via paraptosis and ferroptosis induction. These aggregation-induced emission (AIE)-active agents specifically target mitochondria, effectively triggering ATF4/JNK/Alix-regulated paraptosis and GPX4-mediated ferroptosis. Specifically, they rapidly induce substantial mitochondria-derived vacuolation, accompanied by reactive oxygen species generation, decreased mitochondrial membrane potential, and intracellular Ca<sup>2+</sup> overload, thereby disrupting metabolisms and inducing nonapoptotic cell death. In vivo imaging revealed that TriPEX-ClO<sub>4</sub> and TriPEX-PF<sub>6</sub> successfully traversed the BBB to target orthotopic glioma and initiated effective synergistic therapy postintravenous injection. Our AIE drugs emerged as the pioneering paraptosis inducers against drug-resistant GBM, significantly extending survival up to 40 days compared to Temozolomide (20 days) in drug-resistant GBM-bearing mice. These compelling results open up new venues for the development of fluorescent anticancer drugs and innovative treatments for brain diseases.

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Publication Details

Journal
Journal of the American Chemical Society
Published
2024-10-11
DOI
https://doi.org/10.1021/jacs.4c07785
Citations
46
Primary Topic
Nanoplatforms for cancer theranostics
Type
article
Field-Weighted Citation Impact
8.48

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article

Blood–Brain Barrier-Penetrative Fluorescent Anticancer Agents Triggering Paraptosis and Ferroptosis for Glioblastoma Therapy

Herman H. Y. Sung, Chaoyue Chen, Gaoyang Wang, Bingyang Shi et al.
46 citations
Journal of the American Chemical Society
Nanoplatforms for cancer theranostics
8.48
article

Blood–Brain Barrier-Penetrative Fluorescent Anticancer Agents Triggering Paraptosis and Ferroptosis for Glioblastoma Therapy

Herman H. Y. Sung, Chaoyue Chen, Gaoyang Wang, Bingyang Shi, Yong Zhong, Mu He, Ping Shangguan, Guangle Niu, Mingyue Cao, Jacky W. Y. Lam, Lulu Han, Ben Zhong Tang, Xiaoyu Chen, Jiefei Wang, Yi‐Sheng Liu, Ming‐Wei Lin, Zhengqun Luo, Mengya Lu
article en
46 citations

Abstract

Currently used drugs for glioblastoma (GBM) treatments are ineffective, primarily due to the significant challenges posed by strong drug resistance, poor blood-brain barrier (BBB) permeability, and the lack of tumor specificity. Here, we report two cationic fluorescent anticancer agents (TriPEX-ClO<sub>4</sub> and TriPEX-PF<sub>6</sub>) capable of BBB penetration for efficient GBM therapy via paraptosis and ferroptosis induction. These aggregation-induced emission (AIE)-active agents specifically target mitochondria, effectively triggering ATF4/JNK/Alix-regulated paraptosis and GPX4-mediated ferroptosis. Specifically, they rapidly induce substantial mitochondria-derived vacuolation, accompanied by reactive oxygen species generation, decreased mitochondrial membrane potential, and intracellular Ca<sup>2+</sup> overload, thereby disrupting metabolisms and inducing nonapoptotic cell death. In vivo imaging revealed that TriPEX-ClO<sub>4</sub> and TriPEX-PF<sub>6</sub> successfully traversed the BBB to target orthotopic glioma and initiated effective synergistic therapy postintravenous injection. Our AIE drugs emerged as the pioneering paraptosis inducers against drug-resistant GBM, significantly extending survival up to 40 days compared to Temozolomide (20 days) in drug-resistant GBM-bearing mice. These compelling results open up new venues for the development of fluorescent anticancer drugs and innovative treatments for brain diseases.

Journal of the American Chemical SocietyVol. 146(42)
Beijing Institute of Technology (CN), Shandong University (CN), Henan University (CN), Hong Kong University of Science and Technology (HK), Chinese University of Hong Kong, Shenzhen (CN), State Key Laboratory of Crystal Materials, University of Hong Kong (HK)
National Natural Science Foundation of China, Innovation and Technology Commission, Beijing Institute of Technology, Science and Technology Department of Henan Province, Science and Technology Innovation Talents in Universities of Henan Province
Openalex Percentile: Top 1%
Nanoplatforms for cancer theranostics
8.48
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