Optical blood-brain-tumor barrier modulation expands therapeutic options for glioblastoma treatment

Qi Cai, Xiaoqing Li, Hejian Xiong, Hanwen Fan, Xiaofei Gao, Vamsidhara Vemireddy, Ryan Margolis, Junjie Li, Xiaoqian Ge, Monica Giannotta, Kenneth Hoyt, Elizabeth Maher, Robert Bachoo () and Zhenpeng Qin ()
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Qi Cai: the University of Texas at Dallas
Xiaoqing Li: the University of Texas at Dallas
Hejian Xiong: the University of Texas at Dallas
Hanwen Fan: the University of Texas at Dallas
Xiaofei Gao: University of Texas Southwestern Medical Center
Vamsidhara Vemireddy: University of Texas Southwestern Medical Center
Ryan Margolis: the University of Texas at Dallas
Junjie Li: the University of Texas at Dallas
Xiaoqian Ge: the University of Texas at Dallas
Monica Giannotta: IFOM ETS – The AIRC Institute of Molecular Oncology
Kenneth Hoyt: the University of Texas at Dallas
Elizabeth Maher: University of Texas Southwestern Medical Center
Robert Bachoo: University of Texas Southwestern Medical Center
Zhenpeng Qin: the University of Texas at Dallas

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract The treatment of glioblastoma has limited clinical progress over the past decade, partly due to the lack of effective drug delivery strategies across the blood-brain-tumor barrier. Moreover, discrepancies between preclinical and clinical outcomes demand a reliable translational platform that can precisely recapitulate the characteristics of human glioblastoma. Here we analyze the intratumoral blood-brain-tumor barrier heterogeneity in human glioblastoma and characterize two genetically engineered models in female mice that recapitulate two important glioma phenotypes, including the diffusely infiltrative tumor margin and angiogenic core. We show that pulsed laser excitation of vascular-targeted gold nanoparticles non-invasively and reversibly modulates the blood-brain-tumor barrier permeability (optoBBTB) and enhances the delivery of paclitaxel in these two models. The treatment reduces the tumor volume by 6 and 2.4-fold and prolongs the survival by 50% and 33%, respectively. Since paclitaxel does not penetrate the blood-brain-tumor barrier and is abandoned for glioblastoma treatment following its failure in early-phase clinical trials, our results raise the possibility of reevaluating a number of potent anticancer drugs by combining them with strategies to increase blood-brain-tumor barrier permeability. Our study reveals that optoBBTB significantly improves therapeutic delivery and has the potential to facilitate future drug evaluation for cancers in the central nervous system.

Date: 2023
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DOI: 10.1038/s41467-023-40579-1

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