Single nucleus transcriptomics, pharmacokinetics, and pharmacodynamics of CDK4/6 and mTOR inhibition in a phase 0/1 trial of recurrent high-grade glioma

Authors

Kevin C. Johnson, Department of Neurosurgery, Yale School of Medicine, New Haven, CT, USA.
An-Chi Tien, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Jun Jiang, Karmanos Cancer Institute, Detroit, MI, USA.
James McNamara, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Yu-Wei Chang, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Chelsea Montgomery, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Anita DeSantis, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Leonel Elena-Sanchez, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Yoko Fujita, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Seongho Kim, Karmanos Cancer Institute, Detroit, MI, USA.
Avishay Spitzer, Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.
Paul Gabriel, The Jackson Laboratory for Genomic Medicine, Farmington, USA, CT.
William F. Flynn, The Jackson Laboratory for Genomic Medicine, Farmington, USA, CT.
Elise T. Courtois, The Jackson Laboratory for Genomic Medicine, Farmington, USA, CT.
Amy Hong, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Jocelyn Harmon, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Yoshie Umemura, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Artak Tovmasyan, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Jing Li, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Shwetal Mehta, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.
Roel G. Verhaak, Department of Neurosurgery, Yale School of Medicine, New Haven, CT, USA.
Nader Sanai, Ivy Brain Tumor Center at Barrow, Neurological Institute Phoenix, AZ, USA.

Document Type

Article

Abstract

BACKGROUND: Outcomes for adult patients with high-grade glioma (HGG) remain poor, necessitating new treatment strategies. Key challenges include poor drug penetration in the brain and malignant cell state plasticity. Phase 0 studies identify agents that achieve target modulation through pharmacologically relevant brain concentrations. METHODS: A Phase 0/1 clinical trial combined the two targeted inhibitors ribociclib (CDK4/6 inhibitor) and everolimus (mTOR inhibitor) in recurrent HGG patients, aiming to identify brain-penetrant combinations and assess their impact on malignant cell states. We enrolled 24 patients with recurrent HGG, characterized by CDKN2A/B deletion or CDK4/6 amplification, PTEN loss or PIK3CA mutations, and wildtype retinoblastoma protein (Rb). Tumors were evaluated for pharmacokinetics, pharmacodynamics, and single nucleus transcriptomics. RESULTS: Median unbound ribociclib concentrations in Gadolinium non-enhancing tumor regions were significantly above the biochemical IC50 for CDK4/6 inhibition at 400 and 600 mg QD doses. Unbound everolimus concentrations were undetectable (< 0.1 nM) in tumor regions across all dose levels. Ribociclib treatment was associated with significantly decreased Ki-67 positive cells. Single nucleus RNA sequencing of 17 on-trial IDH-wildtype recurrences and 88 standard-of-care treated recurrences showed a significantly lower fraction of cycling and neural progenitor-like malignant cell populations in ribociclib-everolimus treated tumors. CDK4/6 inhibitor-directed malignant cell state shifts were validated using three patient-derived cell lines. CONCLUSIONS: This trial underscores the value of integrating pharmacokinetics, pharmacodynamics, and single nucleus transcriptomics in Phase 0/1 surgical studies to assess treatment effects, including malignant cell state shifts. ClinicalTrials.gov identifier: NCT03834740.

Keywords

CDK4, glioma, ribociclib, single cell, targeted therapy

Publication Date

11-8-2025

Publication Title

Neuro-oncology

E-ISSN

1523-5866

PubMed ID

41206763

Digital Object Identifier (DOI)

10.1093/neuonc/noaf257

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