Memory T cells persisting in the brain following MCMV infection induce long-term microglial activation via interferon-γ
Open accessAbstract
Murine cytomegalovirus (MCMV) brain infection stimulates microglial cell-driven proinflammatory chemokine production which precedes the presence of brain-infiltrating systemic immune cells. Here, we show that in response to MCMV brain infection, antigen-specific CD8(+) T cells migrated into the brain and persisted as long-lived memory cells. The role of these persistent T cells in the brain is unclear because most of our understanding of antimicrobial T cell responses comes from analyses of lymphoid tissue. Strikingly, memory T cells isolated from the brain exhibited an effector phenotype and produced IFN-γ upon restimulation with viral peptide. Furthermore, we observed time-dependent and long-term activation of resident microglia, indicated by chronic MHC class II up-regulation and TNF-α production. The immune response in this immunologically restricted site persisted in the absence of active viral replication. Lymphocyte infiltrates were detected until 30 days post-infection (p.i.), with CD8(+) and CD4(+) T cells present at a 3:1 ratio, respectively. We then investigated the role of IFN-γ in chronic microglial activation by using IFN-γ-knockout (GKO) mice. At 30 days p.i., GKO mice demonstrated a similar phenotypic brain infiltrate when compared to wild-type mice (Wt), however, MHC class II expression on microglia isolated from these GKO mice was significantly lower compared to Wt animals. When IFN-γ producing CD8(+) T cells were reconstituted in GKO mice, MHC class II up-regulation on microglial cells was restored. Taken together, these results suggest that MCMV brain infection results in long-term persistence of antigen-specific CD8(+) T cells which produce IFN-γ and drive chronic microglial cell activation. This response was found to be dependent on IFN-γ production by viral Ag-specific T cells during the chronic phase of disease.
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Interferon gamma (IFN-γ) from memory CD8+ T cells upregulates MHC class II in microglia and keeps them in an activated state.
“and interferon gamma (IFN‐y) from memory CD8+ T cells upregulates MHC class II in microglia and keeps them in an activated state. 25”
From The P522R protective variant of PLCG2 promotes the expression of antigen presentation genes by human microglia in an Alzheimer's disease mouse model (2022) · cites this paper as [25]
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Prasad, S., Sheng, W. S., Hu, S., Chauhan, P., & Lokensgard, J. R. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.686340 · Cited by 7 · see citing works
Self-citationMicroglia in the Physiology and Pathology of Brain
Nagayach, A., Patro, N., & Patro, I. K. (2015) · Proceedings of the National Academy of Sciences India Section B Biological Sciences · doi:10.1007/s40011-015-0585-y · Cited by 6 · see citing works
Ciavarra, R. P., Machida, M., Lundberg, P. S., Gauronskas, P. J., Wellman, L. L., Steel, C., Aflatooni, J. O., & Sanford, L. D. (2018) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2018.02.014 · Cited by 6 · see citing works
Tarhini, S., Crespo-Quiles, C., Buhler, E., Pineau, L., Pallesi‐Pocachard, E., Villain, S., Saha, S., Silvagnoli, L., Stamminger, T., Luche, H., et al. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03276-4 · Cited by 5 · see citing works
Immune responses drive chorioretinitis and retinal pathology after neonatal CMV infection
McCord, J. L., Han, J. Y. S., Staudt, R. E., Philp, N. J., & Snyder, C. M. (2024) · Science Advances · doi:10.1126/sciadv.adn6379 · Cited by 5 · see citing works
Persistent microglial activation following neonatal CMV infection mediates neurodegeneration
McCord, J. L., Chatterjee, D., Han, J. Y. S., Scoles, D., Smeyne, R. J., Philp, N. J., & Snyder, C. M. (2026) · Science Advances · doi:10.1126/sciadv.adz1686 · Cited by 4 · see citing works
Programmed death ligand‐1 induction restrains the cytotoxic T lymphocyte response against microglia
Chauhan, P., Hu, S., Prasad, S., Sheng, W. S., & Lokensgard, J. R. (2020) · Glia · doi:10.1002/glia.23932 · Cited by 4 · see citing works
Self-citationRapid diagnostic test for assessment of cellular immune response in a viral infection as a model
Bernuz, M., Porras, J. C., Egri, N., González‐Navarro, E. A., Juan, M., Pividori, M. I., & Martı́, M. (2024) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2024.136185 · Cited by 3 · see citing works
Living rent free in your head: resident memory T cells
Degefu, H. N., Kleist, S. A., & Rosato, P. C. (2026) · ImmunoHorizons · doi:10.1093/immhor/vlaf074 · Cited by 1 · see citing works
Sosnovenko, D. S., Chemych, O. M., & Chemych, M. D. (2023) · Інфекційні хвороби · doi:10.11603/1681-2727.2022.4.13705 · Cited by 1 · see citing works
Liu, W., Dai, X., Jih, J., Chan, K. K. L., Trang, P., Yu, X., Balogun, R. A., Mei, Y., Liu, F., & Zhou, Z. H. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/420604 · Cited by 1 · see citing works
Nagayach, A., & Patro, I. K. (2015)
Bauer, Š., Tarhini, S., Buhler, E., Saha, S., Stamminger, T., Streblow, D. N., Burnashev, N., Luche, H., & Szepetowski, P. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.11.637423
- Authors
- Mutnal, M. B., Hu, S., Little, M. R., & Lokensgard, J. R.
- Affiliations
- University of Minnesota (US)
- Corresponding author
- Lokensgard, James R.
- Venue
- Journal of NeuroVirology
- Published
- 2011-07-29
- Volume
- 17
- Issue
- 5
- Pages
- 424-437
- ISSN
- 1355-0284 (ISSN-L)
- 1538-2443
- PMC
- PMC3204167
- OpenAlex
- W2068303625
- Cited by
- 51
- References
- 53
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 1 · 2020: 2 · 2019: 5 · 2018: 9 · 2017: 3 · 2016: 4 · 2015: 6 · 2014: 4 · 2013: 3 · 2012: 2
- FWCI
- 1.59
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of NeuroVirology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS038836)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Epidemiology › Cytomegalovirus and herpesvirus research
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- murine cytomegalovirus, memory T cells, CD8+ T cells, microglial activation, interferon-gamma, MHC class II upregulation, TNF-α, neuroinflammation, IFN-gamma knockout mice, chronic viral infection
- MeSH terms
- Animals, Brain, Cytomegalovirus Infections, Female, Genes, MHC Class II, Immunologic Memory, Interferon-gamma, Macrophages, Mice, Inbred BALB C, Neutrophils, Phenotype, Tumor Necrosis Factor-alpha, Virus Replication, CD4-Positive T-Lymphocytes, Up-Regulation, Microglia, Muromegalovirus, Mice, Knockout, CD8-Positive T-Lymphocytes, Mice
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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