Organotypic Brain Slice Culture Microglia Exhibit Molecular Similarity to Acutely-Isolated Adult Microglia and Provide a Platform to Study Neuroinflammation
Open accessAbstract
Microglia are central nervous system (CNS) resident immune cells that have been implicated in neuroinflammatory pathogenesis of a variety of neurological conditions. Their manifold context-dependent contributions to neuroinflammation are only beginning to be elucidated, which can be attributed in part to the challenges of studying microglia in vivo and the lack of tractable in vitro systems to study microglia function. Organotypic brain slice cultures offer a tissue-relevant context that enables the study of CNS resident cells and the analysis of brain slice microglial phenotypes has provided important insights, in particular into neuroprotective functions. Here we use RNA sequencing, direct digital quantification of gene expression with nCounter® technology and targeted analysis of individual microglial signature genes, to characterize brain slice microglia relative to acutely-isolated counterparts and 2-dimensional (2D) primary microglia cultures, a widely used in vitro surrogate. Analysis using single cell and population-based methods found brain slice microglia exhibited better preservation of canonical microglia markers and overall gene expression with stronger fidelity to acutely-isolated adult microglia, relative to in vitro cells. We characterized the dynamic phenotypic changes of brain slice microglia over time, after plating in culture. Mechanical damage associated with slice preparation prompted an initial period of inflammation, which resolved over time. Based on flow cytometry and gene expression profiling we identified the 2-week timepoint as optimal for investigation of microglia responses to exogenously-applied stimuli as exemplified by treatment-induced neuroinflammatory changes observed in microglia following LPS, TNF and GM-CSF addition to the culture medium. Altogether these findings indicate that brain slice cultures provide an experimental system superior to in vitro culture of microglia as a surrogate to investigate microglia functions, and the impact of soluble factors and cellular context on their physiology.
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Microglia in organotypic brain slice cultures resemble in vivo microglia more than primary cultured microglia, about 50% are non-homeostatic, and overexpress markers associated with microglia in neurodegenerative disease.
“Furthermore, while microglia in organotypic brain slice cultures resemble in vivo microglia more than primary cultured microglia, about 50% of these cells are non-homeostatic (either proliferative, inflammatory, or reactive), and overexpress markers associated with microglia in neurodegenerative disease [9].”
From Culture shock: microglial heterogeneity, activation, and disrupted single-cell microglial networks in vitro (2022) · cites this paper as [9]
The Results section reports that slice-culture microglia more closely resemble acutely isolated adult microglia than primary cultured microglia, and identifies proliferative, inflammatory, and reactive clusters. It also reports increased expression of neurodegeneration-associated signatures, particularly at three weeks. Our copy does not establish that about 50% of slice-culture microglia are non-homeostatic; cluster proportions vary with culture timepoint, which the claim does not specify. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn general, microglia across in vitro systems suffer from disseminated molecular changes attributed to loss of signaling with other cells in the brain microenvironment that is required to maintain them in a homeostatic state.
“In general, microglia across in vitro systems suffer from disseminated molecular changes attributed to loss of signaling with other cells in the brain microenvironment that is required to maintain them in a homeostatic state.”
From Culture shock: microglial heterogeneity, activation, and disrupted single-cell microglial networks in vitro (2022) · cites this paper as [9]
The Results report extensive gene-expression differences in conventionally cultured microglia, and the Discussion links preservation of microglial identity to interactions with other CNS cells (page numbers unavailable). But the paper describes that link as a proposed explanation, not an established cause. It also finds that organotypic brain-slice cultures—an in vitro system—preserve microglial identity better, so the claim is too broad in applying the changes across in vitro systems. (LLM, conf=0.88)
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Self-citationThe TNF receptor family member CD27 signals to Jun N-terminal kinase via Traf-2
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“Furthermore, while microglia in organotypic brain slice cultures resemble in vivo microglia more than primary cultured microglia, about 50% of these cells are non-homeostatic (either proliferative, inflammatory, or reactive), and overexpress markers associated with microglia in neurodegenerative disease [9].”
BackgroundGarcia, G., Pinto, S., Ferreira, S., Lopes, D., Serrador, M. J., Fernandes, A., Vaz, A. R., Mendonça, A. D., Edenhofer, F., Malm, T., et al. (2022) · Cells · doi:10.3390/cells11213377 · Cited by 55 · see citing works
“Importantly, organotypic HCs have also been successfully used to investigate the pathophysiology of AD [87,88] and as a platform to study neuroinflammation and characterize dynamic phenotypic changes in microglia upon exogenously applied stimuli [89].”
MethodMicroglial Cytokines Mediate Plasticity Induced by 10 Hz Repetitive Magnetic Stimulation
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Microglial TNFα controls daily changes in synaptic GABAARs and sleep slow waves
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Microglia in a Dish—Which Techniques Are on the Menu for Functional Studies?
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Microglia and Astrocytes in Postnatal Neural Circuit Formation
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Dissecting surveying behavior of reactive microglia under chronic neurodegeneration
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Microglial TNFα controls synaptic GABAARs, sleep slow waves and memory consolidationPreprint
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Specificities of Living Human Microglial Cells
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Hewitt, B. J., Roberts, L., Roberts, J. A., Fulton, D. J., Hill, L. J., Kitchen, P., Bill, R. M., & Botfield, H. F. (2026) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1722240 · Cited by 1 · see citing works
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Isolation and Whole-Cell Patch-Clamp Recording of Hippocampal Microglia from Adult Mice
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The Rise of Pluripotent Stem Cell-Derived Glia Models of Neuroinflammation
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An organotypic neocortical slice culture for studying neuroglial interactionsPreprint
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Nano-Based Probes for the Brain Extracellular Environment
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Microglial Inflammatory Response in the Glioblastoma Microenvironment in Preclinical Models
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Microglial ontogeny and in vitro reconstruction: Bridging development and modeling
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Experimental induction of myelin damage in post-mortem human brain slice cultures
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- Authors
- Delbridge, A. R. D., Huh, D., Brickelmaier, M., Burns, J. C., Roberts, C., Challa, R., Raymond, N., Cullen, P., Carlile, T. M., Ennis, K. A., Liu, M., Sun, C., Allaire, N. E., Foos, M., Tsai, H.-H., Franchimont, N., Ransohoff, R. M., Butts, C., & Mingueneau, M.
- Affiliations
- Biogen (United States) (US)
- ORCID
- Venue
- Frontiers in Cellular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2020-12-21
- Volume
- 14
- Pages
- 592005-592005
- ISSN
- 1662-5102 (ISSN-L)
- PMC
- PMC7812919
- OpenAlex
- W3116215660
- Cited by
- 72
- References
- 95
- Citations by year
- 2026: 16 · 2025: 11 · 2024: 17 · 2023: 9 · 2022: 14 · 2021: 5
- FWCI
- 2.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Biogen
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- microglia, organotypic brain slice culture, neuroinflammation, microglial phenotype, microglial gene expression, microglial activation, LPS, TNF-α, GM-CSF
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