Cited by 467Neuroinflammation and Neurodegeneration MechanismsPhagocytosis and Immune RegulationAutophagy in Disease and Therapy

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CD22 blockade restores homeostatic microglial phagocytosis in ageing brains

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Pluvinage, John V., Haney, Michael S., Smith, Benjamin A. H., Sun, Jerry, Iram, Tal, Bonanno, Liana, Li, Lulin, Lee, Davis P., Morgens, David W., Yang, Andrew C., Shuken, Steven R., Gate, David, Scott, Madeleine, Khatri, Purvesh, Luo, Jian, Bertozzi, Carolyn R., Bassik, Michael C., Wyss-Coray, Tony·2019·Nature

DOI 10.1038/s41586-019-1088-4PMC PMC6574119

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Abstract

Microglia maintain homeostasis in the central nervous system through phagocytic clearance of protein aggregates and cellular debris. This function deteriorates during ageing and neurodegenerative disease, concomitant with cognitive decline. However, the mechanisms of impaired microglial homeostatic function and the cognitive effects of restoring this function remain unknown. We combined CRISPR-Cas9 knockout screens with RNA sequencing analysis to discover age-related genetic modifiers of microglial phagocytosis. These screens identified CD22, a canonical B cell receptor, as a negative regulator of phagocytosis that is upregulated on aged microglia. CD22 mediates the anti-phagocytic effect of α2,6-linked sialic acid, and inhibition of CD22 promotes the clearance of myelin debris, amyloid-β oligomers and α-synuclein fibrils in vivo. Long-term central nervous system delivery of an antibody that blocks CD22 function reprograms microglia towards a homeostatic transcriptional state and improves cognitive function in aged mice. These findings elucidate a mechanism of age-related microglial impairment and a strategy to restore homeostasis in the ageing brain.

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Background
Epigenetic mechanism of carbohydrate sulfotransferase 3 ( CHST3 ) downregulation in the aging brainPreprint
Baidoe‐Ansah, D., Sakib, M. S., Jia, S., Fischer, A., Kaushik, R., & Dityatev, A. E. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/741355 · Cited by 3
“Several studies have shown that there is a gradual age-dependent physiological increase in the neuroinflammation, which is related to activation of astrocytes and microglia (Godbout et al., 2005; Lynch, 2010), and is also thought to be involved in cognitive decline (Pluvinage et al., 2019).”
Background
Oligomeric amyloid beta prevents myelination in a clusterin-dependent mannerPreprint
Beiter, R. M., Raghavan, T. P., Suchocki, O., Ennerfelt, H. E., Rivet-Noor, C. R., Merchak, A. R., Phillips, J. L., Bathe, T., Lukens, J. R., Prokop, S., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-4415143/v1 · Cited by 3
“C57BL/6J mice (8–14 weeks) were injected with CypHer-A β (ipsilateral) and NHS-Fluorescein (contralateral, Thermo Fisher 46410) as previously described [20].”
Method
Microglia aging in the hippocampus advances through intermediate states that drive activation and cognitive declinePreprint
Shea, J. M., & Villeda, S. (2025) · eLife · doi:10.7554/elife.97671.2 · Cited by 2
Heterochronic Myeloid Cell Replacement Reveals the Local Brain Environment as Key Driver of Microglia AgingPreprint
Gizowski, C., Popova, G., Shin, H., Mader, M. M.-D., Craft, W., Kong, W., Shibuya, Y., Wranik, B. J., Fu, Y. H. H., Depp, C., et al. (2025) · SSRN Electronic Journal · doi:10.1101/2025.09.02.673859 · Cited by 4
Age Associated Increase in Microglia Inflammation and Phagocytosis in the Adult Neural Stem Cell NichePreprint
Cutler, R., Harrison, S., Kuhn-Sandoval, N., Tomlinson, S., & Kokovay, E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.10.681517 · Cited by 3
“We further expanded our phagocytosis gene list to include genes identified in prior functional screens (Haney et al., 2018; Pluvinage et al., 2019), and found that all intersecting genes (9/9) were upregulated in aged microglia (Supplementary Figs.”
Remarkable heterogeneity revealed in the genetic architecture of resistance to a key bacterial pathogen in two commercial rainbow trout populations
Pouil, S., Rigaudeau, D., Lee, B.-H., Segret, E., Desgranges, A., D’Ambrosio, J., François, Y., Boudinot, P., Duchaud, É., Phocas, F., et al. (2025) · BMC Genomics · doi:10.1186/s12864-025-12231-3 · Cited by 2
Stability of Myeloid Cell Phenotype and Function Across a Broad Age Range in Humans and Cynomolgus Monkeys, and a Dominant Contribution of Humoral Factors in the Control of Bacterial Infection
Lysakova, E. V., Burak, M., Larin, I. I., Chuvpilo, S. A., Laktyushkin, V. S., Shumeev, A. N., Pismennyi, I. E., Toshchakov, V. Y., Bobrov, M. Y., & Александрович, Р. С. (2025) · Biomedicines · doi:10.3390/biomedicines14010071 · Cited by 2
“As a result, a decline in the phagocytosis of Staphylococcus aureus by human MDMs has been observed, along with reductions in MDM migration and chemotaxis [23,25,26].”
Aurkb deficiency disrupts microglial development, homeostasis and hinders remyelination following cuprizone-induced demyelination
Yan, W., Xiang, D., Du, L., Zhu, D., Jia, Q., Liu, Y., Wang, S., Liu, L., Guan, H., Zhao, Y., et al. (2026) · iScience · doi:10.1016/j.isci.2026.114718 · Cited by 2
TrkB promotes the neuronal secretion of soluble Siglec-2 (CD22) to mitigate microglial activation and alleviate depression-like behaviors in male mice
Shi, X., Cai, S., Chai, J.-L., Xu, C. J., Zhou, B.-Y., Han-qi, L., Marshall, J., & Cao, C. (2026) · Molecular Psychiatry · doi:10.1038/s41380-026-03575-7 · Cited by 3
“The results of this study suggest that antidepressant drugs enhance TrkB-mediated expression of CD22, a negative regulator of microglia phagocytosis and in ﬂ ammation [32], to restore microglia to a homeostatic state required for learning-related synapse formation.”
Microglial heterogeneity in neurological disorders: From dynamic states to druggable targets
Ou, Q., Dai, Z., Zhou, Y., Li, G., Liu, H., Li, J., He, C., Qin, S., & Su, Z. (2026) · Biochemical Pharmacology · doi:10.1016/j.bcp.2026.117994 · Cited by 3
Microglial senescence and epigenetic reprogramming in alzheimer's disease: An immunometabolic perspective
Ma, J., Yang, B., Jiang, X., Wang, L., Wei, W., Cao, Y., & Li, H. (2026) · Experimental Gerontology · doi:10.1016/j.exger.2026.113177 · Cited by 4
Neuroinflammation in Alzheimer’s and Parkinson’s diseases: pathogenic mechanisms and therapeutic strategies
Wang, Q.-Q., Sun, Q.-Q., Guo, Y.-S., Yin, S., & Zhou, J. (2026) · Translational Neurodegeneration · doi:10.1186/s40035-026-00571-3 · Cited by 2
“CD22 is upregulated in aged microglia, and its blockade restores a more homeostatic transcriptional state and improves cognition [322].”
An early enriched experience drives targeted microglial engulfment of miswired neural circuitry during a restricted postnatal period
Rogerson‐Wood, L., Goldsbury, C. S., Sawatari, A., & Leamey, C. A. (2024) · Glia · doi:10.1002/glia.24522 · Cited by 2
“…been reported in various human neurodevelopmental conditions including autistic spectrum disorders (Openshaw et al., 2023; Takeguchi et al., 2022; Xie et al., 2023) and associated mouse models (Bertero et al., 2018; Carroll et al., 2021; Jain et al., 2020; Kennedy et al., 2020; Smith et al., 2019).”
Background
Improved ESI-MS Sensitivity via an Imidazolium Tag (DAPMI-ITag) for Precise Sialic Acid Detection in Human Serum and CMAH-Null Mouse Tissues
Zhang, Y., Hu, Z.-X., Zhang, S., Liu, L., Galán, M. C., Voglmeir, J., & Ghirardello, M. (2025) · Analytical Chemistry · doi:10.1021/acs.analchem.5c00752 · Cited by 2
Nucleic Acid-Based Therapeutics Relevant to Neuroimmune Conditions
Greenfield, A. L., & Hauser, S. L. (2019) · Neurotherapeutics · doi:10.1007/s13311-019-00740-5 · Cited by 2
Integrative single cell and spatial transcriptomic analysis reveal reciprocal microglia-plasma cell crosstalk in the mouse brain during chronic Trypanosoma brucei infectionPreprint
Quintana, J. F., Chandrasegaran, P. R. G., Sinton, M. C., Briggs, E. M., Otto, T. D., Heslop, R., Bentley-Abbot, C., Loney, C., de Lecea, L., Mabbott, N. A., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.25.485502 · Cited by 2
Mouse peritoneal macrophages undergo female-specific remodeling with aging driven by both hormone-dependent and -independent mechanismsPreprint
Lu, R. J., Chen, S., Kim, M., Sampathkumar, N. K., Lee, E. H., Christensen, A., Wang, E., Lau, I. C. Y., Parihar, S., Ravikumar, C. K., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.11.659200 · Cited by 2
Polysialic Acid-Functionalized MAP Scaffolds Promote Regulatory Immune Responses After Ischemic StrokePreprint
Ouyang, Y., Che, S., Whitehead, E. C., Poysungnoen, K., Agarwal, A., Liu, A., Newman, H., Silinski, P., Becker, M. L., & Segura, T. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.10.674054 · Cited by 2
An Agent-Based Model of Microglia and Neuron Interaction: Implications in Neurodegenerative Disease
Ty, C., Case, A., Mezzulo, E., Penland, A., & Larripa, K. (2025) · Spora A Journal of Biomathematics · doi:10.61403/2473-5493.1097 · Cited by 1
Nuclear localization of platelet activating factor receptor accounts for microglial phagocytosis in ischemic stroke
Zhang, X., Xu, H., Ren, X.-W., Li, Q.-X., Hong, C., Chen, Y.-F., Yang, J., Ji, J., Guo, R., & Sun, X. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.107020 · Cited by 2
“Microglia, the brain ’ s resident phagocytes, clear dead cells, neuronal debris, synapses, and even mildly damaged neurons with potential for recovery(Brown, 2021; Brown and Neher, 2010, 2014; Otxoa-de-Ame-zaga et al., 2019; Pluvinage et al., 2019).”
Glial-mediated pathogenesis and intervention strategies in neuromyelitis optica spectrum disorder
Zhang, Z., Li, F., Li, X., & Wei, H. (2025) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2025.106666 · Cited by 1
Roles of the phagocytosis checkpoint in radiotherapy
Kui, Y., Tong, F., Zhang, R., Wang, J., & Dong, X. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-07921-5 · Cited by 1
“…cluster of differentiation 24(CD24)-sialic acid binding Ig like lectin 10(Siglec-10) (in 2019) [42], cluster of differentiation 22 (CD22) (in 2019) [43], signaling lymphocytic activation molecule family 3/4 (SLAMF3/4) (in 2022) [44] and ganglioside 2 (GD2)-sialic acid binding Ig like lectin 7…”
Sialylation patterns in cerebral amyloid angiopathy
Fastenau, C., Crisp, R., Keating, M., Ochoa, E., Richardson, T. E., Flanagan, M. E., Walker, J. M., Hopp, S. C., & Bieniek, K. F. (2025) · Brain Pathology · doi:10.1111/bpa.70042 · Cited by 2
“SA residues contribute to the biophysical property of repulsion due to the negative charge of cells [15].”
A Drug Screening Targeting Upregulation of Syk Gene Identifies Neochlorogenic Acid and L‐Arabinitol Capable of Inducing the M2 Phenotype of Microglia in Alzheimer's Disease
Hu, D., Li, X., Li, Y., Zhang, Q., Dai, Y., Teng, X., Hou, H., & Li, J. (2025) · ChemBioChem · doi:10.1002/cbic.202500515 · Cited by 1
Ablation of CD22 induces a pro-inflammatory transcriptome shift and endocytic deficits in M2-like macrophages
Kukan, E. N., Fabiano, G. L., Zhou, J. Y., Richard, A. R., Telfer, K., & Cobb, B. A. (2025) · Glycobiology · doi:10.1093/glycob/cwaf076 · Cited by 1
Cellular insights into hydrocephalus: The diverse roles and intricate crosstalk of multiple cell types
Xu, L., Zhou, Y., Yang, H. K., Chen, X., & Ouyang, Q. (2025) · Experimental Neurology · doi:10.1016/j.expneurol.2025.115596 · Cited by 2
Aurka-Bhlhe41 axis prevents premature aging-like microglial dysfunction and promotes remyelination
Yan, W., Zhao, Y., Li, H., Hong, L., Jia, Q., Zhu, D., Xiang, D., Du, L., Hu, L., Bai, R., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-71014-w · Cited by 1
“Targeting CD22 with neutralizing antibodies restores aging microglial function and promotes CNS homeostasis 16 .”
Influential
The Roles of Macrophage Lineage Cells ( MLC s) in Brain Aging
Qin, Q., Zhang, L., Guo, M., Lu, D., Liu, Y., Wang, Z., Hu, M., Wang, S., Kang, X., Yi, H., et al. (2026) · CNS Neuroscience & Therapeutics · doi:10.1002/cns.70873 · Cited by 1
Reprogramming microglia in sepsis-associated encephalopathy: from pathological dysfunction to therapeutic restoration
He, C., Shi, H., Yu, Z., Jiao, Z., Li, J., & Yang, F. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1804207 · Cited by 2
“In the aging brain, there is a change in the transcriptional and epigenetic status of microglia, showing increased baseline expression of in ﬂ amma-tory genes, which is termed the “ aged ” or “ primed ” state of microglia (27).”
Targeting microglia-mediated neuroinflammation in Alzheimer’s disease: mechanisms and therapeutic approaches
Bang-feng, L., Chen, X., Xie, R., Mo, Y.-F., Wu, Y.-Z., Meng, Y., Han, X.-L., Chen, M., & Peng, Y. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1818802 · Cited by 2
“For instance, microglial phagocytosis can be restored by inhibiting the CD22 receptor or hexokinase 2, while targeting EP2/4 receptors can revitalize microglial energy metabolism by reprogramming glucose and glycogen utilization (188 – 190).”
Microglial state transitions are constrained by developmental and metabolic checkpoints
Mesaoudi, A. E., & Kim, D. W. (2026) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2026.1852176 · Cited by 1
“Examples include CD22 blockade, which restores phagocytic function in aged microglia by relieving an age-associated inhibitory signal (Pluvinage et al., 2019), and CD33 modulation, which alters microglial engagement with amyloid (Griciuc et al., 2013).”
T cell-microglial interactions that impair myelin maintenance and regeneration: cellular mechanisms on white-matter associated changes
Song, C., Lee, Y., & Kim, M. S. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1813048 · Cited by 1
“CD22, an inhibitory receptor upregulated in aged microglia in murine models, has been shown to suppress phagocytic capacity including myelin debris clearance (69).”
Microglial ITAM & ITIM Signaling in Neurodegenerative Disease and Brain Aging
Mangalmurti, A., Bonheur, A., & Lukens, J. R. (2026) · Journal of Molecular Biology · doi:10.1016/j.jmb.2026.169910 · Cited by 1
SGK1-mediated deficits in microglial phagocytosis drive pathological progression in amyotrophic lateral sclerosis
He, M., Wu, C., Hu, M., Shi, X., Liu, R., Tong, Y., Wang, H., Hu, H., & Liao, H. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03925-w · Cited by 1
“Although BV2 cells cannot fully recapitulate the features of primary microglia, they exhibit similar phagocytic machinery [37].”
Combating ageing beyond the cell: Emerging roles of extracellular proteostasis
Venkatesh, S. R., Gallotta, I., Olabiyi, B. F., Choi, Y. H., Inglesfield, S., Kumita, J. R., Ewald, C. Y., & David, D. C. (2026) · FEBS Journal · doi:10.1111/febs.70647 · Cited by 2
“With age, the recognition of aggregates and their phagocytosis by microglia is impaired [207,208].”
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CD22 regulates Aβ clearance in microglia through INPP5D signaling
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“Recent work has detected CD22 in aging-associated microglia, where it acts as a negative regulator of phagocytosis (Pluvinage et al., 2019).”
Influential
α2,6-Sialoglycan-regulated antitumor immunity of tumor-infiltrating CD8+ T cells
Liang, S., Tang, Q., Guo, Y., Zhang, S., Song, Q., Dai, P., & Chen, X. (2026) · Nature Chemical Biology · doi:10.1038/s41589-026-02299-7 · Cited by 1
“Concurrently, sialoglycans on immune cells are dynamically regulated, and this has substantial functional implications 17–24 .”
The “Glyco-Remodeling” Hypothesis in Alzheimer’s Disease: Linking Protein N -Glycosylation to Pathogenesis and Translation
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Mouse model of repetitive mild traumatic brain injury (investigating cognitive impairment)
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Self-citation
New Insights into Microglia as Therapeutic Targets in Alzheimer’s Disease
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In situ neuroregeneration: frontiers and therapeutic prospects
Wang, Q., Li, W., Lei, W., Chen, W., Zheng, J., Xiang, Z., MinHui, L. I. U., He, Q., Xu, L., Li, Z., et al. (2021) · Scientia Sinica Vitae · doi:10.1360/ssv-2021-0024 · Cited by 1

Authors: Pluvinage, J. V., Haney, M. S., Smith, B. A. H., Sun, J., Iram, T., Bonanno, L., Li, L., Lee, D. P., Morgens, D. W., Yang, A. C., Shuken, S. R., Gate, D., Scott, M., Khatri, P., Luo, J., Bertozzi, C. R., Bassik, M. C., & Wyss-Coray, T.
Affiliations: Stanford Medicine (US)
VA Palo Alto Health Care System (US)
Howard Hughes Medical Institute (US)
ORCID: Pluvinage, John V.
Haney, Michael S.
Smith, Benjamin A. H.
Sun, Jerry
Iram, Tal
Li, Lulin
Morgens, David W.
Yang, Andrew C.
Shuken, Steven R.
Gate, David
Scott, Madeleine
Khatri, Purvesh
Luo, Jian
Bertozzi, Carolyn R.
Bassik, Michael C.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2019-04
Volume: 568
Issue: 7751
Pages: 187-192
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-019-1088-4
PMC: PMC6574119
OpenAlex: W2934339908
Cited by: 459
References: 71
Citations by year: 2026: 44 · 2025: 73 · 2024: 62 · 2023: 70 · 2022: 71 · 2021: 59 · 2020: 54 · 2019: 26
FWCI: 23.14
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (1s10od020141-01)
National Institute on Aging (F30AG060638, R01AG045034, DP1AG053015)
National Human Genome Research Institute (T32HG000044)
National Cancer Institute (R01CA227942)
National Institute of General Medical Sciences (T32GM120007, T32GM007365, R01GM059907)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Keywords: CD22, microglial phagocytosis, brain aging, microglial homeostasis, sialic acid, myelin debris clearance, amyloid-beta oligomers, alpha-synuclein fibrils, cognitive decline, antibody therapy, CRISPR-Cas9 screen, neurodegeneration
MeSH terms: CRISPR-Associated Protein 9, Aging, Animals, Brain, Cognition, Female, Homeostasis, Male, Mice, Inbred C57BL, Phagocytosis, Sequence Analysis, RNA, Microglia, N-Acetylneuraminic Acid, Mice, Sialic Acid Binding Ig-like Lectin 2, CRISPR-Cas Systems

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CD22 blockade restores homeostatic microglial phagocytosis in ageing brains

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