Electrical and synaptic integration of glioma into neural circuits
Open accessAbstract
High-grade gliomas are lethal brain cancers whose progression is robustly regulated by neuronal activity. Activity-regulated release of growth factors promotes glioma growth, but this alone is insufficient to explain the effect that neuronal activity exerts on glioma progression. Here we show that neuron and glioma interactions include electrochemical communication through bona fide AMPA receptor-dependent neuron-glioma synapses. Neuronal activity also evokes non-synaptic activity-dependent potassium currents that are amplified by gap junction-mediated tumour interconnections, forming an electrically coupled network. Depolarization of glioma membranes assessed by in vivo optogenetics promotes proliferation, whereas pharmacologically or genetically blocking electrochemical signalling inhibits the growth of glioma xenografts and extends mouse survival. Emphasizing the positive feedback mechanisms by which gliomas increase neuronal excitability and thus activity-regulated glioma growth, human intraoperative electrocorticography demonstrates increased cortical excitability in the glioma-infiltrated brain. Together, these findings indicate that synaptic and electrical integration into neural circuits promotes glioma progression.
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Tumor cells in hCOs showed higher proliferation rates than PTs across all three samples.
“Tumor cells in hCOs showed higher prolifera- tion rates than PTs across all three samples (Figures S1G and S1H), consistent with recent findings on glutamate regulation of GBM progression.19,20”
From Individualized patient tumor organoids faithfully preserve human brain tumor ecosystems and predict patient response to therapy (2025) · cites this paper as [19]
The distance between IPTOs and PTs is much smaller than that between PDEs and original tumors, demonstrating that IPTO is superior to PDE in maintaining patient tumor heterogeneity.
“We further compared our results with the explant culture model19 and found that the distance between IPTOs and PTs is much smaller than that between PDEs and original tumors, demon- strating that IPTO is superior to PDE in maintaining patient tu- mor heterogeneity (Figure 4F).”
From Individualized patient tumor organoids faithfully preserve human brain tumor ecosystems and predict patient response to therapy (2025) · cites this paper as [19]
The citation is attached to “explant culture model,” while the distance comparison is presented as the citing authors’ own result (Figure 4F). The cited paper’s Methods > Cell Culture describes dissociated tumor tissue grown in culture, not a patient-derived explant model. Neither that section nor the retrieved passages report IPTO–PT or PDE–original-tumor distances or compare their preservation of heterogeneity. (LLM, conf=0.74)
Experimental — accuracy not yet measuredThe tumor microenvironment includes stromal, tumor, endothelial cells, hematopoietic progenitor-derived immune components, and a dense network of adrenergic nerve fibres that influence oncogenesis in brain and non-brain cancers.
“The TME comprises not only stromal, tumor, endothelial cells, and hematopoietic progenitor-derived immune components, but also a dense network of adrenergic nerve fibres that influence oncogenesis in brain and non-brain cancers (94–97).”
From The microbiome and human cancer (2021) · cites this paper as [97]
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- Authors
- Venkatesh, H. S., Morishita, W., Geraghty, A. C., Silverbush, D., Gillespie, S. M., Arzt, M., Tam, L. T., Espenel, C., Ponnuswami, A., Ni, L., Woo, P. J., Taylor, K. R., Agarwal, A., Regev, A., Brang, D., Vogel, H., Hervey-Jumper, S., Bergles, D. E., Suvà, M. L., Malenka, R. C., & Monje, M.
- Affiliations
- Stanford University (US)
- Stanford Medicine (US)
- Broad Institute (US)
- Johns Hopkins University (US)
- University of Michigan (US)
- Corresponding author
- Monje, Michelle
- ORCID
- Venue
- Nature
- Published
- 2019-09-18
- Volume
- 573
- Issue
- 7775
- Pages
- 539-545
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7038898
- OpenAlex
- W2974724557
- Cited by
- 1,366
- References
- 58
- Citations by year
- 2026: 226 · 2025: 238 · 2024: 223 · 2023: 204 · 2022: 162 · 2021: 153 · 2020: 139 · 2019: 20
- FWCI
- 66.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- U.S. Department of Defense (NF140075)
- Howard Hughes Medical Institute
- Robert Wood Johnson Foundation (74259)
- Alex's Lemonade Stand Foundation for Childhood Cancer
- Dr. Miriam and Sheldon G. Adelson Medical Research Foundation
- Virginia and D.K. Ludwig Fund for Cancer Research
- Cure Starts Now Foundation
- Ian's Friends Foundation
- Deutsche Forschungsgemeinschaft
- National Institutes of Health (5f31ca200273-02, MH086403, NS069375)
- Klarman Cell Observatory, Broad Institute
- National Institute of Mental Health (P50MH086403)
- National Cancer Institute (F31 CA200273, T32CA009302)
- National Institute of Neurological Disorders and Stroke (P30NS069375, R01NS092597, DP1NS111132, K08NS110919)
- Common Fund
- Topics
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- high-grade glioma, neuron-glioma interactions, AMPA receptors, electrical coupling, gap junctions, neuronal excitability, cortical excitability, intraoperative electrocorticography, optogenetics, glioma xenografts, tumor progression
- MeSH terms
- Animals, Brain, Cell Membrane, Glioma, Humans, Synaptic Transmission, Neurons, Potassium, Tumor Cells, Cultured, Gene Expression Regulation, Neoplastic, Mice, Inbred NOD, Gap Junctions, Gene Expression Profiling, Cell Proliferation, Mice, Electrical Synapses, Electrophysiological Phenomena, Optogenetics, Heterografts
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