Selective induction of astrocytic gliosis generates deficits in neuronal inhibition
Open accessAbstract
Reactive astrocytosis develops in many neurologic diseases, including epilepsy. Astrocytotic contributions to pathophysiology are poorly understood. Studies examining this are confounded by comorbidities accompanying reactive astrocytosis. We found that high-titer transduction of astrocytes with enhanced green fluorescent protein (eGFP) via adeno-associated virus induced reactive astrocytosis without altering the intrinsic properties or anatomy of neighboring neurons. We examined the consequences of selective astrocytosis induction on synaptic transmission in mouse CA1 pyramidal neurons. Neurons near eGFP-labeled reactive astrocytes had reduced inhibitory, but not excitatory, synaptic currents. This inhibitory postsynaptic current (IPSC) erosion resulted from a failure of the astrocytic glutamate-glutamine cycle. Reactive astrocytes downregulated expression of glutamine synthetase. Blockade of this enzyme normally induces rapid synaptic GABA depletion. In astrocytotic regions, residual inhibition lost sensitivity to glutamine synthetase blockade, whereas exogenous glutamine administration enhanced IPSCs. Astrocytosis-mediated deficits in inhibition triggered glutamine-reversible hyperexcitability in hippocampal circuits. Thus, reactive astrocytosis could generate local synaptic perturbations, leading to broader functional deficits associated with neurologic disease.
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Downregulation of SLC1A2 is predicted to increase the excitability of glutamatergic neurons.
“downregulation of SLC1A2 is predicted to increase the excitability of glutamatergic neurons38”
From Astrocyte transcriptomic changes along the spatiotemporal progression of Alzheimer’s disease (2024) · cites this paper as [38]
The Results section, “Virus-induced astrocytosis alters network excitability” (page unavailable), reports hippocampal network hyperexcitability following reactive gliosis. But it attributes that effect to impaired inhibition associated with reduced glutamine synthetase, not to SLC1A2 downregulation. The paper does not establish the claimed SLC1A2-to-excitability link. (LLM, conf=0.82)
Experimental — accuracy not yet measuredAstroglial reactivity impacts astrocyte-dependent glutamate homeostasis.
“As astroglial reactivity impacts astrocyte‐dependent glutamate homeostasis [36, 94, 95, 96, 97]”
From Gliovascular alterations in sporadic and familial Alzheimer's disease: <scp><i>APOE3</i></scp> Christchurch homozygote glioprotection (2023) · cites this paper as [94]
GS decreases in aging, AD, and reactive astrocytes.
“It has been described that GS decreases in aging [47], AD [112], and reactive astrocytes [94].”
From Gliovascular alterations in sporadic and familial Alzheimer's disease: <scp><i>APOE3</i></scp> Christchurch homozygote glioprotection (2023) · cites this paper as [94]
The AAV9-CAG-GFP dose used (1 × 10^10 vg in 3 μl per hemisphere) is a standard dose used for pre-clinical testing and has been shown to induce glial cell activation and brain infiltration in previous mouse studies using the same route of administration.
“This vector dose was chosen as a standard dose used for pre-clinical testing in several settings, independently of toxicity, and because it has been shown to induce glial cell activation and brain infiltration in previous mouse studies using the same route of administration 36,37,100 .”
From AAV vectors trigger DNA damage response-dependent pro-inflammatory signalling in human iPSC-derived CNS models and mouse brain (2025) · cites this paper as [100]
A previous study has shown that high-titer AAV injection resulted in a prominent decrease of astrocytic glutamine synthetase, suggesting that the normal function of astrocytes is disturbed by high-titer AAV.
“Accordingly, a previous study has shown that high-titer AAV injection resulted in a prominent decrease of astrocytic glutamine synthetase,29 suggesting that the normal function of astrocytes is disturbed by the high-titer of AAV.”
From High-titer AAV disrupts cerebrovascular integrity and induces lymphocyte infiltration in adult mouse brain (2023) · cites this paper as [29]
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- Authors
- Ortinski, P. I., Dong, J., Mungenast, A., Yue, C., Takano, H., Watson, D. J., Haydon, P. G., & Coulter, D. A.
- Affiliations
- Children's Hospital of Philadelphia (US)
- Tufts University (US)
- University of Pennsylvania (US)
- Corresponding author
- Coulter, Douglas A
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2010-04-25
- Volume
- 13
- Issue
- 5
- Pages
- 584-591
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3225960
- OpenAlex
- W2050744136
- Cited by
- 495
- References
- 38
- Citations by year
- 2026: 16 · 2025: 22 · 2024: 44 · 2023: 31 · 2022: 36 · 2021: 23 · 2020: 34 · 2019: 22 · 2018: 24 · 2017: 21 · 2016: 37 · 2015: 39 · 2014: 41 · 2013: 30 · 2012: 42
- FWCI
- 13.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (P20MH071705)
- National Institute of Neurological Disorders and Stroke (R01NS038572, R01NS040978, R01NS054770, P01NS054900, R01NS037585)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Keywords
- reactive astrogliosis, astrocytic gliosis, glutamine synthetase, glutamate-glutamine cycle, synaptic inhibition, CA1 pyramidal neurons, hippocampus, hyperexcitability, epilepsy, astrocyte-neuron interaction
- MeSH terms
- Chondroitin Sulfate Proteoglycan 4, Analysis of Variance, Animals, Animals, Newborn, Antigens, Astrocytes, Bromodeoxyuridine, Calcium-Binding Proteins, Electric Stimulation, Gliosis, Glutamate-Ammonia Ligase, Hippocampus, Microfilament Proteins, Nerve Tissue Proteins, Neural Inhibition, Neurons, Phosphinic Acids, Proteoglycans, Pyridazines, Pyridines, Transduction, Genetic, Patch-Clamp Techniques, GABA Antagonists, Green Fluorescent Proteins, Mice, Synaptic Potentials, In Vitro Techniques
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