Published May 17, 2023 | Version v1
Journal article Open

Ribonucleotide reductase regulatory subunit M2 drives glioblastoma TMZ resistance through modulation of dNTP production

Description

During therapy, adaptations driven by cellular plasticity are partly responsible for driving the inevitable recurrence of glioblastoma (GBM). To investigate plasticity-induced adaptation during standard-of-care chemotherapy temozolomide (TMZ), we performed in vivo single-cell RNA sequencing in patient-derived xenograft (PDX) tumors of GBM before, during, and after therapy. Comparing single-cell transcriptomic patterns identified distinct cellular populations present during TMZ therapy. Of interest was the increased expression of ribonucleotide reductase regulatory subunit M2 (RRM2), which we found to regulate dGTP and dCTP production vital for DNA damage response during TMZ therapy. Furthermore, multidimensional modeling of spatially resolved transcriptomic and metabolomic analysis in patients' tissues revealed strong correlations between RRM2 and dGTP. This supports our data that RRM2 regulates the demand for specific dNTPs during therapy. In addition, treatment with the RRM2 inhibitor 3-AP (Triapine) enhances the efficacy of TMZ therapy in PDX models. We present a previously unidentified understanding of chemoresistance through critical RRM2-mediated nucleotide production.

Data availability

The results published here are in part based on data generated by the TCGA Research Network (www.cancer.gov/tcga) and were further analyzed through GlioVis. In addition, these results use data generated by the Human Protein Atlas and GBMSeq (Gephart Laboratory, www.gbmseq.org). Figures, in part, were generated using BioRender (www.biorender.com). All relevant sequencing files were deposited into the GEO repository, accession number: GSE227348. All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.

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Additional details

Identifiers

DOI
10.1126/sciadv.ade7236
Other
oai:uchicago.tind.io:9777

Funding

National Institute of Neurological Disorders and Stroke
1R01NS096376
National Institute of Neurological Disorders and Stroke
1R01NS112856
National Institute of Neurological Disorders and Stroke
P50CA221747
National Institute of Neurological Disorders and Stroke
R01GM135587
National Institute of Neurological Disorders and Stroke
R01GM143334
Else Kröner-Fresenius Foundation
Germany Ministry of Education and Research
MEPHISTO project BMBF

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Medicine