Methotrexate chemotherapy induces persistent tri-glial dysregulation that underlies chemotherapy-related cognitive impairment
Open accessAbstract
Chemotherapy results in a frequent yet poorly understood syndrome of long-term neurological deficits. Neural precursor cell dysfunction and white matter dysfunction are thought to contribute to this debilitating syndrome. Here, we demonstrate persistent depletion of oligodendrocyte lineage cells in humans who received chemotherapy. Developing a mouse model of methotrexate chemotherapy-induced neurological dysfunction, we find a similar depletion of white matter OPCs, increased but incomplete OPC differentiation, and a persistent deficit in myelination. OPCs from chemotherapy-naive mice similarly exhibit increased differentiation when transplanted into the microenvironment of previously methotrexate-exposed brains, indicating an underlying microenvironmental perturbation. Methotrexate results in persistent activation of microglia and subsequent astrocyte activation that is dependent on inflammatory microglia. Microglial depletion normalizes oligodendroglial lineage dynamics, myelin microstructure, and cognitive behavior after methotrexate chemotherapy. These findings indicate that methotrexate chemotherapy exposure is associated with persistent tri-glial dysregulation and identify inflammatory microglia as a therapeutic target to abrogate chemotherapy-related cognitive impairment. VIDEO ABSTRACT.
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Reactive microglia and brain-infiltrating macrophages impair mechanisms of cellular homeostasis and plasticity such as the ongoing generation of myelin-forming oligodendrocytes, myelin plasticity, and new neuron generation in the hippocampus.
“Reactive microglia and brain-infiltrating macrophages impair mechanisms of cellular homeostasis and plasticity such as the ongoing generation of myelin-forming oligodendrocytes (Gibson et al., 2019), myelin plasticity (Geraghty et al., 2019), and new neuron generation in the hippocampus (Monje et al., 2002, 2003, 2007).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
Microglia become persistently reactive following exposure to certain chemotherapy drugs, after cranial radiation, or after systemic inflammatory challenge with low-dose lipopolysaccharide.
“Microglia, brain-resident macrophages, become persistently reactive following exposure to certain chemotherapy drugs, after cranial radiation, or after systemic inflammatory challenge with low-dose lipopolysaccharide (Geraghty et al., 2019; Gibson et al., 2019; Monje et al., 2002, 2003, 2007).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
A distinct subpopulation of microglia that reside in white matter are selectively activated by systemic insults such as exposure to the chemotherapy drug methotrexate.
“A distinct subpopulation of microglia that reside in white matter (Hammond et al., 2019) are selectively activated by systemic insults such as exposure to the chemotherapy drug methotrexate (Gibson et al., 2019).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
Anti-inflammatory strategies correct multicellular dysregulation and rescue cognition in disease states such as those occurring after exposure to neurotoxic cancer therapies and in aging.
“This complex cellular dysregulation is thought to contribute importantly to cognitive impairment, and anti-inflammatory strategies correct this multicellular dysregulation and rescue cognition in disease states such as those occurring after exposure to neurotoxic cancer therapies (Geraghty et al., 2019; Gibson et al., 2019; Monje et al., 2003) and in aging (Villeda et al., 2011).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
This complex cellular dysregulation is thought to contribute importantly to cognitive impairment.
“This complex cellular dysregulation is thought to contribute importantly to cognitive impairment, and anti-inflammatory strategies correct this multicellular dysregulation and rescue cognition in disease states such as those occurring after exposure to neurotoxic cancer therapies (Geraghty et al., 2019; Gibson et al., 2019; Monje et al., 2003) and in aging (Villeda et al., 2011).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
Changes in myelin sheath thickness relative to axon diameter (g ratio) were not conclusively identified in remaining myelin sheaths after mild respiratory COVID, in contrast to methotrexate chemotherapy exposure.
“In contrast to methotrexate chemotherapy exposure (Geraghty et al., 2019; Gibson et al., 2019), changes in myelin sheath thickness relative to axon diameter (g ratio) were not conclusively identified in the remaining myelin sheaths after mild respiratory COVID (Figures S7C–S7F).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
White-matter-selective/enriched microglial reactivity is associated with impaired hippocampal neurogenesis, dysregulation of the oligodendroglial lineage, and myelin loss in other disease contexts.
“Such neuroinflammatory changes—particularly white-matter-selective/enriched microglial reactivity—are associated with impaired hippocampal neurogenesis, dysregulation of the oligodendroglial lineage, and myelin loss in other disease contexts (Geraghty et al., 2019; Gibson et al., 2019; Guttenplan et al., 2021; Liddelow et al., 2017; Monje et al., 2003; Villeda et al., 2011).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
The microglial reactivity present after mild respiratory SARS-CoV-2 infection may also induce neurotoxic astrocyte reactivity and aberrant microglial pruning of synapses.
“As occurs after cancer therapies and in other disease states, the microglial reactivity present after mild respiratory SARS-CoV-2 infection may also induce neurotoxic astrocyte reactivity (Liddelow et al., 2017; Gibson et al., 2019; Guttenplan et al., 2021), as well as aberrant microglial pruning of synapses (Hinkle et al., 2019; Hosseini et al., 2018; Vasek et al., 2016).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
Methotrexate directly stimulates reactivity of microglia.
“While methotrexate directly stimulates reactivity of microglia (Gibson et al., 2019),”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
Microglial depletion strategies can restore similar multicellular deficits and rescue impaired cognitive performance in mouse models of CRCI.
“For example, microglial depletion strategies can restore similar multicellular deficits and rescue impaired cognitive performance in mouse models of CRCI (Acharya et al., 2016; Gibson et al., 2019),”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
Preclinical studies in disease models sharing features with the cellular dysregulation observed here after mild respiratory COVID have identified anti-inflammatory and neuro-regenerative strategies that restore neural plasticity and rescue cognition.
“Preclinical studies in disease models that share numerous features with the cellular dysregulation observed here after mild respiratory COVID have identified anti-inflammatory and neuro-regenerative strategies that restore neural plasticity and rescue cognition (Ayoub et al., 2020; Geraghty et al., 2019; Gibson et al., 2019; Monje et al., 2003; Villeda et al., 2011).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Gibson et al., 2019
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(Re)building the nervous system: A review of neuron–glia interactions from development to disease
Demmings, M. D., Chagas, L. D. S., Traetta, M. E., Rodrigues, R. S., Acutain, M. F., Barykin, E. P., Datusalia, A. K., German‐Castelan, L., Mattera, V. S., Mazengenya, P., et al. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16258 · Cited by 36 · see citing works
Zhu, L., Retana, D., García‐Gómez, P., Álvaro‐Espinosa, L., Priego, N., Masmudi‐Martín, M., Yebra, N., Miarka, L., Hernández-Encinas, E., Blanco‐Aparicio, C., et al. (2022) · EMBO Molecular Medicine · doi:10.15252/emmm.202114552 · Cited by 38 · see citing works
- Authors
- Gibson, E. M., Nagaraja, S., Ocampo, A., Tam, L. T., Wood, L. S., Pallegar, P. N., Greene, J. J., Geraghty, A. C., Goldstein, A. K., Ni, L., Woo, P. J., Barres, B. A., Liddelow, S., Vogel, H., & Monje, M.
- Affiliations
- Stanford University (US)
- New York University (US)
- Institute for Stem Cell Biology and Regenerative Medicine (US)
- Corresponding author
- Monje, Michelle
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2019-01
- Volume
- 176
- Issue
- 1-2
- Pages
- 43-55.e13
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6329664
- OpenAlex
- W2903050755
- Cited by
- 372
- References
- 71
- Citations by year
- 2026: 39 · 2025: 65 · 2024: 38 · 2023: 47 · 2022: 60 · 2021: 52 · 2020: 41 · 2019: 28
- FWCI
- 22.77
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- California Institute for Regenerative Medicine (RB4-06093, RN3-06510)
- Unravel Pediatric Cancer
- McKenna Claire Foundation
- Virginia and D.K. Ludwig Fund for Cancer Research
- National Institutes of Neurological Disorders and Stroke (R01NS092597)
- Stanford Medical Scientist Training Program
- Stanford Neuroscience Institute
- Stanford Maternal and Child Health Research Institute
- Anne T. and Robert M. Bass Endowed Faculty Scholarship in Pediatric Cancer and Blood Diseases
- Stanford CTSA (UL1 RR025744)
- BioX Institute
- McCormick Fellowship
- Stanford MedScholars Program
- Christopher and Dana Reeve Foundation
- Novartis Institute for Biomedical Research
- Dr. Miriam and Sheldon G. Adelson Medical Research Foundation
- JPB Foundation
- Cure Alzheimer's Fund
- Glenn Foundation
- Esther B. O’Keeffe Charitable Foundation
- Australian National Health and Medical Research Council (GNT1052961)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cancer-related cognitive impairment studies
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- methotrexate, chemotherapy-induced cognitive impairment, oligodendrocyte precursor cells, myelination, microglial activation, astrocyte activation, neuroinflammation, cognitive behavior
- MeSH terms
- Animals, Brain, Cell Differentiation, Disease Models, Animal, Drug Therapy, Humans, Methotrexate, Myelin Sheath, Nerve Fibers, Myelinated, Neuroglia, Neurons, Oligodendroglia, Microglia, Cell Lineage, Mice, Neurogenesis, Cognitive Dysfunction, Drug-Related Side Effects and Adverse Reactions, White Matter
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