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.
Authors
- Herman H. Y. Sung (ORCID: https://orcid.org/0000-0002-3370-0332)
- Chaoyue Chen (ORCID: https://orcid.org/0000-0003-4874-0633)
- Gaoyang Wang (ORCID: https://orcid.org/0000-0001-6941-7363)
- Bingyang Shi (ORCID: https://orcid.org/0000-0002-1043-3163)
- Yong Zhong (ORCID: https://orcid.org/0000-0003-1446-3148)
- Mu He
- Ping Shangguan
- Guangle Niu (ORCID: https://orcid.org/0000-0002-5403-6880)
- Mingyue Cao
- Jacky W. Y. Lam (ORCID: https://orcid.org/0000-0001-5754-1703)
- Lulu Han (ORCID: https://orcid.org/0000-0001-6378-7486)
- Ben Zhong Tang (ORCID: https://orcid.org/0000-0002-0293-964X)
- Xiaoyu Chen (ORCID: https://orcid.org/0000-0002-0492-7589)
- Jiefei Wang (ORCID: https://orcid.org/0000-0001-8374-8847)
- Yi‐Sheng Liu (ORCID: https://orcid.org/0000-0002-3279-5878)
- Ming‐Wei Lin (ORCID: https://orcid.org/0000-0003-2026-7178)
- Zhengqun Luo
- Mengya Lu
Institutions
- 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)
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
Funders
- 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