Aim: Tumour heterogeneity presents a significant obstacle to identifying effective treatments for brain cancer, explaining the ineffectiveness of standard treatment protocols. Patient-derived brain tumour explant organoids (GBOs) replicate this heterogeneity and can predict a patient's response to therapy, constituting a critical tool in precision Neuro-oncology. However, current methods to generate GBOs are time-consuming, costly, and technically challenging. These limitations preclude the development of larger diverse organoid biobanks that capture the true spectrum of the disease and impede rapid patient-personalised preclinical testing.
Methods: By introducing semi-automated tissue processing, size exclusion chromatography and immediate cryopreservation, we optimized current methods1 for the generation and biobanking of tumour pieces (from low-grade glioma, high-grade glioma and primary/recurrent glioblastoma) that are suitable for GBO culture, reducing processing time from up to 6 hours to less than 60 minutes. We used this biobank to compare the effects of novel idronoxil-conjugated benzopyran compounds (NX786, NX904) on GBO growth, viability, cell death, invasion and senescence utilizing a combination of live and fixed imaging and multi-omics.
Results: We used our optimized protocol to generate 24 GBOs from 33 samples of diverse brain tumour types (low-grade glioma, high-grade glioma and primary/recurrent glioblastoma) and tested the effect of NX786 and NX904 on 9 of these. NX786 and NX904 significantly reduced GBO growth (≥50%) and invasion. Low-grade gliomas were more resistant to these treatments. NX904 induced significant cell death (>60%), while NX786 increased cellular senescence and induction of the mesenchymal-like state, with its effects being reversible.
Conclusions: We developed an efficient method for processing and cryopreserving brain tumour tissues suitable for GBO growth, enabling the capture of more patient samples and the establishment of an extensive biobank collection. We successfully used this biobank for targeted drug screening, highlighting its potential for patient-personalised preclinical testing. We found that through the inhibition of crucial brain cancer hallmarks, including proliferation and invasion, together with the induction of a less aggressive senescence phenotype, NX786 and NX904 have the potential for development as new therapeutic agents for brain cancer.
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