Comparative analysis of transcriptome remodeling in plaque-associated and plaque-distant microglia during amyloid-β pathology progression in mice
Open accessAbstract
Background: Research in recent years firmly established that microglial cells play an important role in the pathogenesis of Alzheimer's disease (AD). In parallel, a series of studies showed that, under both homeostatic and pathological conditions, microglia are a heterogeneous cell population. In AD, amyloid-β (Aβ) plaque-associated microglia (PAM) display a clearly distinct phenotype compared to plaque-distant microglia (PCM), suggesting that these two microglia subtypes likely differently contribute to disease progression. So far, molecular characterization of PAM was performed indirectly using single cell RNA sequencing (scRNA-seq) approaches or based on markers that are supposedly up-regulated in this microglia subpopulation. Methods: In this study based on a well-characterized AD mouse model, we combined cell-specific laser capture microdissection and RNA-seq analysis to i) identify, without preconceived notions of the molecular and/or functional changes that would affect these cells, the genes and gene networks that are dysregulated in PAM or PCM at three critical stages of the disease, and ii) to investigate the potential contribution of both plaque-associated and plaque-distant microglia. Results: First, we established that our approach allows selective isolation of microglia, while preserving spatial information and preventing transcriptome changes induced by classical purification approaches. Then, we identified, in PAM and PCM subpopulations, networks of co-deregulated genes and analyzed their potential functional roles in AD. Finally, we investigated the dynamics of microglia transcriptomic remodeling at early, intermediate and late stages of the disease and validated select findings in postmortem human AD brain. Conclusions: Our comprehensive study provides useful transcriptomic information regarding the respective contribution of PAM and PCM across the Aβ pathology progression. It highlights specific pathways that would require further study to decipher their roles across disease progression. It demonstrates that the proximity of microglia to Aβ-plaques dramatically alters the microglial transcriptome and reveals that these changes can have both positive and negative impacts on the surrounding cells. These opposing effects may be driven by local microglia heterogeneity also demonstrated by this study. Our approach leads to molecularly define the less well studied plaque-distant microglia. We show that plaque-distant microglia are not bystanders of the disease, although the transcriptomic changes are far less striking compared to what is observed in plaque-associated microglia. In particular, our results suggest they may be involved in Aβ oligomer detection and in Aβ-plaque initiation, with increased contribution as the disease progresses. Graphical Abstract:
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Spatial transcriptomics allows gene expression patterns to be mapped onto histologically defined regions, linking molecular signatures to specific pathological features such as amyloid plaques and tau tangles.
“It allows gene expression patterns to be mapped onto histologically defined regions, thereby linking molecular signatures to specific pathological features such as amyloid plaques and tau tangles114,121,166,167.”
From Artificial intelligence-driven multi-omics approaches in Alzheimer's disease: Progress, challenges, and future directions (2025) · cites this paper as [121]
The Results describe linking microglial gene expression to amyloid plaques using laser capture microdissection, RNA-seq, and spatial validation by smFISH. The paper does not show gene-expression mapping to tau tangles; its reported spatial analysis concerns amyloid plaques. (LLM, conf=0.86)
Experimental — accuracy not yet measuredSpatial transcriptomics enhances transcriptomic profiling by preserving the spatial context of gene expression.
“Spatial transcriptomics further enhances transcriptomic profiling by preserving the spatial context of gene expression.”
From Artificial intelligence-driven multi-omics approaches in Alzheimer's disease: Progress, challenges, and future directions (2025) · cites this paper as [121]
The Results section ('Validation in mouse and human brain tissue'; page unavailable) says laser capture microdissection preserves spatial information, and the Discussion says combining it with RNA-seq enables transcriptome analysis of spatially distinct microglia. This supports the value of spatial context in profiling, but the paper describes its own method as LCM plus RNA-seq and refers to a separate spatial-transcriptomic study; it does not directly establish the claim about spatial transcriptomics as a method. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · see citing works
The Amyloid Hypothesis of Alzheimer’s Disease: Progress and Problems on the Road to Therapeutics
Hardy, J., & Selkoe, D. J. (2002) · Science · doi:10.1126/science.1072994 · Cited by 13,864 · see citing works
Trapnell, C., Roberts, A., Goff, L. A., Pertea, G. M., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., & Pachter, L. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.016 · Cited by 11,930 · see citing works
FactoMineR : An R Package for Multivariate Analysis
Lê, S., Josse, J., & Husson, F. (2008) · Journal of Statistical Software · doi:10.18637/jss.v025.i01 · Cited by 11,682 · see citing works
Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
A General Framework for Weighted Gene Co-Expression Network Analysis
Zhang, B., & Horvath, S. (2005) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1128 · Cited by 5,684 · see citing works
A Unique Microglia Type Associated with Restricting Development of Alzheimer’s Disease
Keren-Shaul, H., Spinrad, A., Weiner, A., Matcovitch-Natan, O., Dvir-Szternfeld, R., Ulland, T. K., David, E., Baruch, K., Lara-Astaiso, D., Toth, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.018 · Cited by 5,493 · see citing works
Rab proteins as membrane organizers
Zerial, M., & McBride, H. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35052055 · Cited by 3,381 · see citing works
Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O’Loughlin, E., Xu, Y., Fanek, Z., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.008 · Cited by 2,979 · see citing works
Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4106-4114.2000 · Cited by 2,632 · see citing works
Hammond, T. R., Dufort, C., Dissing-Olesen, L., Giera, S., Young, A., Wysoker, A., Walker, A. J., Segel, M., Nemesh, J., Saunders, A., et al. (2018) · doi:10.1101/406140 · Cited by 2,225 · see citing works
The reactome pathway knowledgebase
Jassal, B., Matthews, L. R., Viteri, G., Gong, C., Lorente, P., Fabregat, A., Sidiropoulos, K., Cook, J., Gillespie, M. E., Haw, R., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1031 · Cited by 2,111 · see citing works
Reimand, J., Isserlin, R., Voisin, V., Kucera, M., Tannus-Lopes, C., Rostamianfar, A., Wadi, L., Meyer, M., Wong, J., Xu, C., et al. (2019) · Nature Protocols · doi:10.1038/s41596-018-0103-9 · Cited by 1,970 · see citing works
Microglia in Alzheimer’s disease
Hansen, D. V., Hanson, J. E., & Sheng, M. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201709069 · Cited by 1,935 · see citing works
TREM2 Lipid Sensing Sustains the Microglial Response in an Alzheimer’s Disease Model
Wang, Y., Cella, M., Mallinson, K., Ulrich, J. D., Young, K. L., Robinette, M. L., Gilfillan, S., Krishnan, G. M., Sudhakar, S., Zinselmeyer, B. H., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.049 · Cited by 1,736 · see citing works
The microglial sensome revealed by direct RNA sequencing
Hickman, S. E., Kingery, N. D., Ohsumi, T. K., Borowsky, M. L., Wang, L.-C., Means, T. K., & El Khoury, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3554 · Cited by 1,511 · see citing works
Microglia in physiology and disease
Wolf, S. A., Boddeke, H. W. G. M., & Kettenmann, H. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034406 · Cited by 1,426 · see citing works
The ins and outs of MHC class II-mediated antigen processing and presentation
Roche, P. A., & Furuta, K. (2015) · Nature reviews. Immunology · doi:10.1038/nri3818 · Cited by 1,207 · see citing works
The Reactome pathway Knowledgebase
Fabregat, A., Sidiropoulos, K., Garapati, P., Gillespie, M., Hausmann, K., Haw, R., Jassal, B., Jupe, S., Korninger, F., McKay, S., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkv1351 · Cited by 1,201 · see citing works
Spatial Transcriptomics and In Situ Sequencing to Study Alzheimer’s Disease
Chen, W.-T., Lu, A., Craessaerts, K., Pavie, B., Sala Frigerio, C., Corthout, N., Qian, X., Laláková, J., Kühnemund, M., Voytyuk, I., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.038 · Cited by 949 · cited 13× · see citing works
“Microglia gene signature enrichment To assess the extent of which list of pre-selected genes overlapped with mouse and/or human microglia gene signatures that were previously defined, we performed overrepresentation analysis (Sensome [36]; DAM [11]; microglial neurodegenerative phenotype (MGnD) [5]; Reactome & New-Sen…”
BackgroundMethodResultInfluentialSala Frigerio, C., Wolfs, L., Fattorelli, N., Thrupp, N., Voytyuk, I., Schmidt, I., Mancuso, R., Chen, W.-T., Woodbury, M. E., Srivastava, G., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.099 · Cited by 926 · cited 8× · see citing works
“Microglia gene signature enrichment To assess the extent of which list of pre-selected genes overlapped with mouse and/or human microglia gene signatures that were previously defined, we performed overrepresentation analysis (Sensome [36]; DAM [11]; microglial neurodegenerative phenotype (MGnD) [5]; Reactome & New-Sen…”
BackgroundMethodResultInfluentialCo-expression of multiple transgenes in mouse CNS: a comparison of strategies
Jankowsky, J. L., Slunt, H. H., Ratovitski, T., Jenkins, N. A., Copeland, N. G., & Borchelt, D. (2001) · Biomolecular Engineering · doi:10.1016/s1389-0344(01)00067-3 · Cited by 819 · see citing works
Temporal Tracking of Microglia Activation in Neurodegeneration at Single-Cell Resolution
Mathys, H., Adaikkan, C., Gao, F., Young, J. Z., Manet, E., Hemberg, M., De Jager, P. L., Ransohoff, R. M., Regev, A., & Tsai, L.-H. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.039 · Cited by 740 · see citing works
GWAS on family history of Alzheimer’s disease
Marioni, R. E., Harris, S. E., Zhang, Q., McRae, A. F., Hagenaars, S. P., Hill, W. D., Davies, G., Ritchie, C. W., Gale, C. R., Starr, J. M., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0150-6 · Cited by 564 · see citing works
Microglia use TAM receptors to detect and engulf amyloid β plaques
Huang, Y., Happonen, K. E., Burrola, P. G., O’Connor, C., Hah, N., Huang, L., Nimmerjahn, A., & Lemke, G. (2021) · Nature Immunology · doi:10.1038/s41590-021-00913-5 · Cited by 483 · see citing works
Distinct amyloid-β and tau-associated microglia profiles in Alzheimer’s disease
Gerrits, E., Brouwer, N., Kooistra, S. M., Woodbury, M. E., Vermeiren, Y., Lambourne, M., Mulder, J., Kummer, M., Möller, T., Biber, K., et al. (2021) · Acta Neuropathologica · doi:10.1007/s00401-021-02263-w · Cited by 441 · see citing works
Marsh, S. E., Walker, A. J., Kamath, T., Dissing-Olesen, L., Hammond, T. R., de Soysa, T. Y., Young, A. M. H., Murphy, S., Abdulraouf, A., Nadaf, N., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01022-8 · Cited by 432 · see citing works
Alzheimer’s Patient Microglia Exhibit Enhanced Aging and Unique Transcriptional Activation
Srinivasan, K., Friedman, B. A., Etxeberria, A., Huntley, M. A., van der Brug, M. P., Foreman, O., Paw, J. S., Modrusan, Z., Beach, T. G., Serrano, G. E., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107843 · Cited by 427 · see citing works
An early and late peak in microglial activation in Alzheimer’s disease trajectory
Fan, Z., Brooks, D. J., Okello, A., & Edison, P. (2017) · Brain · doi:10.1093/brain/aww349 · Cited by 422 · see citing works
Isolation of glia from Alzheimer’s mice reveals inflammation and dysfunction
Orre, M., Kamphuis, W., Osborn, L. M., Jansen, A. H. P., Kooijman, L., Bossers, K., & Hol, E. M. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.06.004 · Cited by 394 · see citing works
Transcriptional signature in microglia associated with Aβ plaque phagocytosis
Grubman, A., Choo, X. Y., Chew, G., Ouyang, J. F., Sun, G., Croft, N. P., Rossello, F. J., Simmons, R., Buckberry, S., Landin, D. V., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23111-1 · Cited by 357 · see citing works
Yang, T., Li, S., Xu, H., Walsh, D. M., & Selkoe, D. J. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.1698-16.2016 · Cited by 347 · see citing works
Mizutani, M., Pino, P. A., Saederup, N., Charo, I. F., Ransohoff, R. M., & Cardona, A. E. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1100421 · Cited by 346 · see citing works
Novel Alzheimer risk genes determine the microglia response to amyloid-β but not to TAU pathology
Sierksma, A., Lu, A., Mancuso, R., Fattorelli, N., Thrupp, N., Salta, E., Zoco, J., Blum, D., Buée, L., De Strooper, B., et al. (2020) · EMBO Molecular Medicine · doi:10.15252/emmm.201910606 · Cited by 291 · see citing works
Barcoded viral tracing of single-cell interactions in central nervous system inflammation
Clark, I. C., Gutiérrez-Vázquez, C., Wheeler, M. A., Li, Z., Rothhammer, V., Linnerbauer, M., Sanmarco, L. M., Guo, L., Blain, M., Zandee, S. E. J., et al. (2021) · Science · doi:10.1126/science.abf1230 · Cited by 285 · see citing works
Single‐cell transcriptomics reveals distinct inflammation‐induced microglia signatures
Sousa, C., Golebiewska, A., Poovathingal, S. K., Kaoma, T., Pires‐Afonso, Y., Martina, S., Coowar, D., Azuaje, F., Skupin, A., Balling, R., et al. (2018) · The EMBO Reports · doi:10.15252/embr.201846171 · Cited by 281 · see citing works
Syndecans as receptors and organizers of the extracellular matrix
Xian, X., Gopal, S., & Couchman, J. (2009) · Cell and Tissue Research · doi:10.1007/s00441-009-0829-3 · Cited by 264 · see citing works
Sobue, A., Komine, O., Hara, Y., Endo, F., Mizoguchi, H., Watanabe, S., Murayama, S., Saito, T., Saido, T. C., Sahara, N., et al. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01099-x · Cited by 253 · see citing works
Clayton, K., Delpech, J. C., Herron, S., Iwahara, N., Ericsson, M., Saito, T., Saido, T. C., Ikezu, S., & Ikezu, T. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00440-9 · Cited by 245 · see citing works
Emerging Roles for Eph Receptors and Ephrin Ligands in Immunity
Darling, T. K., & Lamb, T. J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01473 · Cited by 239 · see citing works
Immune hyperreactivity of Aβ plaque-associated microglia in Alzheimer's disease
Yin, Z., Raj, D., Saiepour, N., Van Dam, D., Brouwer, N., Holtman, I. R., Eggen, B. J. L., Möller, T., Tamm, J. A., Abdourahman, A., et al. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.03.021 · Cited by 238 · see citing works
Microglia in Alzheimer’s Disease: Activated, Dysfunctional or Degenerative
Navarro, V., Sanchez-Mejias, E., Jimenez, S., Muñoz-Castro, C., Sanchez-Varo, R., Davila, J. C., Vizuete, M., Gutierrez, A., & Vitorica, J. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00140 · Cited by 229 · see citing works
Re-evaluating microglia expression profiles using RiboTag and cell isolation strategies
Haimon, Z., Volaski, A., Orthgiess, J., Boura-Halfon, S., Varol, D., Shemer, A., Yona, S., Zuckerman, B., David, E., Chappell-Maor, L., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0110-6 · Cited by 209 · see citing works
APP processing and amyloid deposition in mice haplo-insufficient for presenilin 1
Jankowsky, J. L., Slunt, H. H., Gonzales, V., Jenkins, N. A., Copeland, N. G., & Borchelt, D. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2003.09.008 · Cited by 189 · see citing works
Polygenic risk score analysis of pathologically confirmed Alzheimer disease
Escott‐Price, V., Myers, A., Huentelman, M. J., & Hardy, J. (2017) · Annals of Neurology · doi:10.1002/ana.24999 · Cited by 178 · see citing works
Hamelin, L., Lagarde, J., Dorothée, G., Potier, M. C., Corlier, F., Kuhnast, B., Caillé, F., Dubois, B., Fillon, L., Chupin, M., et al. (2018) · Brain · doi:10.1093/brain/awy079 · Cited by 177 · see citing works
Microglia limit the expansion of β-amyloid plaques in a mouse model of Alzheimer’s disease
Zhao, R., Hu, W., Tsai, J., Li, W., & Gan, W.-B. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0188-6 · Cited by 151 · see citing works
Microglia-Mediated Neuroprotection, TREM2, and Alzheimer’s Disease: Evidence From Optical Imaging
Condello, C., Yuan, P., & Grutzendler, J. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.007 · Cited by 131 · see citing works
Calderón‐Garcidueñas, A. L., & Duyckaerts, C. J. (2017) · Handbook of clinical neurology · doi:10.1016/b978-0-12-802395-2.00023-7 · Cited by 120 · see citing works
Plescher, M., Seifert, G., Hansen, J. N., Bedner, P., Steinhäuser, C., & Halle, A. (2018) · Glia · doi:10.1002/glia.23318 · Cited by 101 · see citing works
Jeanneteau, F. D., Barr�re, C., Vos, M., de Vries, C. J. M., Rouillard, C., Lévesque, D., Dromard, Y., Moisan, M., Đurić, V., Franklin, T., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2793-17.2017 · Cited by 91 · see citing works
Self-citationThe Role of Microglia in Sporadic Alzheimer’s Disease
Streit, W. J., Khoshbouei, H., & Bechmann, I. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201248 · Cited by 84 · see citing works
Global transcriptome analysis of genetically identified neurons in the adult cortex
Rossner, M. J., Hirrlinger, J., Wichert, S. P., Boehm, C., Newrzella, D., Hiemisch, H., Eisenhardt, G., Stuenkel, C., von Ahsen, O., & Nave, K.-A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0468-06.2006 · Cited by 80 · see citing works
Plaque-associated myeloid cells derive from resident microglia in an Alzheimer's disease model
Reed-Geaghan, E. G., Croxford, A. L., Becher, B., & Landreth, G. E. (2020) · Journal of Experimental Medicine · doi:10.1084/jem.20191374 · Cited by 72 · see citing works
Mérienne, N., Meunier, C., Schneider‐Anthony, A., Séguin, J., Nair, S. S., Rocher, A. B., Gras, S. L., Keime, C., Faull, R. L. M., Pellerin, L., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.003 · Cited by 72 · see citing works
Wendt, S., Maricos, M., Vana, N., Meyer, N., Guneykaya, D., Semtner, M., & Kettenmann, H. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.05.027 · Cited by 69 · see citing works
Ginsberg, S. D., Malek‐Ahmadi, M. H., Alldred, M. J., Che, S., Elarova, I., Chen, Y., Jeanneteau, F. D., Kranz, T. M., Chao, M. V., Counts, S., et al. (2017) · Hippocampus · doi:10.1002/hipo.22802 · Cited by 69 · see citing works
Self-citationGene biomarker discovery at different stages of Alzheimer using gene co-expression network approach
Zakeri, N. S. S., Pashazadeh, S., & MotieGhader, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-69249-8 · Cited by 62 · see citing works
Shukla, A., McIntyre, L. L., Marsh, S. E., Schneider, C. A., Hoover, E. M., Walsh, C. M., Lodoen, M. B., Blurton-Jones, M. M., & Inlay, M. A. (2018) · Glia · doi:10.1002/glia.23575 · Cited by 59 · see citing works
Minogue, A. (2017) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.02.008 · Cited by 56 · see citing works
Altered motility of plaque-associated microglia in a model of Alzheimer’s disease
Gyoneva, S., Swanger, S. A., Zhang, J., Weinshenker, D., & Traynelis, S. F. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.061 · Cited by 52 · see citing works
Luna‐Muñoz, J., Peralta‐Ramirez, J., Chávez-Macías, L., Harrington, C. R., Wischik, C. M., & Mena, R. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0431-x · Cited by 50 · see citing works
Blume, T., Focke, C., Peters, F., Deußing, M., Albert, N. L., Lindner, S., Gildehaus, F., von Ungern‐Sternberg, B., Ozmen, L., Baumann, K., et al. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1347-6 · Cited by 45 · see citing works
Gautier, M. K., & Ginsberg, S. D. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.109038 · Cited by 41 · see citing works
Self-citationRothman, S. M., Tanis, K. Q., Gandhi, P., Malkov, V. A., Marcus, J., Pearson, M. S., Stevens, R. C., Gilliland, J., Ware, C. M., Mahadomrongkul, V., et al. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1265-7 · Cited by 40 · see citing works
T he microglial reaction signature revealed by RNA seq from individual mice
Hirbec, H., Marmai, C., Duroux-Richard, I., Roubert, C., Esclangon, A., Croze, S., Lachuer, J., Peyroutou, R., & Rassendren, F. (2018) · Glia · doi:10.1002/glia.23295 · Cited by 38 · see citing works
Self-citationAlldred, M. J., Penikalapati, S. C., Lee, S. H., Heguy, A., Roussos, P., & Ginsberg, S. D. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02453-3 · Cited by 36 · see citing works
Self-citationMicroglia Reactivity: Heterogeneous Pathological Phenotypes
Hirbec, H., Rassendren, F., & Audinat, É. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9658-2_4 · Cited by 24 · see citing works
Self-citationBian, Z., Yamashita, T., Shi, X., Feng, T., Yu, H., Hu, X. F., Hu, X., Bian, Y., Sun, H., Tadokoro, K., et al. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147569 · Cited by 24 · see citing works
Hemonnot-Girard, A.-L., Valverde, A., Hua, J., Delaygue, C., Linck, N., Maurice, T., Rassendren, F., & Hirbec, H. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.10.021 · Cited by 17 · see citing works
Self-citationDromard, Y., Arango-Lievano, M., Borie, A. M., Dedin, M., Fontanaud, P., Torrent, J., Garabedian, M. J., Ginsberg, S. D., & Jeanneteau, F. D. (2022) · Acta Neuropathologica Communications · doi:10.1186/s40478-022-01396-7 · Cited by 17 · see citing works
Self-citation
Flagged first, then by citations
1 of the 73 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [46]Marsh SE, Kamath T, Walker AJ, Dissing-Olesen L, Hammond TR, Young AMH, et al. Single cell sequencing reveals glial specific responses to tissue processing & enzymatic dissociation in mice and humans. BioRxiv. 2020:2020.12.03.408542.
Cited by
Sorted by citations
Ren, F., Wei, J., Chen, Q., Hu, M., Yu, L., Mi, J., Zhou, X., Qin, D., Wu, J., & Wu, A. (2025) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2025.07.030 · Cited by 97 · see citing works
Alzheimer’s genes in microglia: a risk worth investigating
Sudwarts, A., & Thinakaran, G. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00679-4 · Cited by 46 · see citing works
Fadila, S., Beucher, B., Dopeso‐Reyes, I. G., Mavashov, A., Brusel, M., Anderson, K., Ismeurt, C., Goldberg, E. M., Ricobaraza, A., Hernández-Alcoceba, R., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci159316 · Cited by 37 · see citing works
You, Y., Chen, Z., & Hu, W. (2024) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2024.108606 · Cited by 22 · see citing works
Hua, J., Paco, E. G. D., Linck, N., Maurice, T., Desrumaux, C. M., Manoury, B., Rassendren, F., & Ulmann, L. (2023) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-023-04784-x · Cited by 20 · see citing works
Self-citationIanni, M., Corraliza-Gómez, M., Costa-Coelho, T., Ferreira-Manso, M., Inteiro-Oliveira, S., Alemãn-Serrano, N., Sebastião, A. M., Garcia, G., Diógenes, M. J., & Brites, D. M. T. O. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179475 · Cited by 17 · see citing works
Pathogenesis and therapeutic applications of microglia receptors in Alzheimer’s disease
Fu, J., Wang, R., He, J., Liu, X., Wang, X., Yao, J., Liu, Y., Ran, C., Ye, Q., & He, Y. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1508023 · Cited by 16 · see citing works
Microglial Responses to Alzheimer's Disease Pathology: Insights From “Omics” Studies
Reid, A. N., Jayadev, S., & Prater, K. E. (2025) · Glia · doi:10.1002/glia.24666 · Cited by 10 · see citing works
Sterile innate immune mechanisms in neurodegenerative diseases
Ealy, A., Serapiglia, A. M., & Panicker, N. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.111039 · Cited by 7 · see citing works
Early amyloid‐induced changes in microglia gene expression in male APP / PS1 mice
Oshima, T., Kater, M. S. J., Huffels, C. F. M., Wesseling, E. M., Middeldorp, J., Hol, E. M., Verheijen, M. H. G., Smit, A. B., Boddeke, E., & Eggen, B. J. L. (2024) · Journal of Neuroscience Research · doi:10.1002/jnr.25295 · Cited by 8 · see citing works
Izquierdo, P., Jolivet, R., Attwell, D., & Madry, C. (2023) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-023-02871-3 · Cited by 6 · see citing works
Wang, J., Wang, S., Li, Q., Liu, F., Wan, Y., & Liang, H. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1450663 · Cited by 4 · see citing works
Gui, Q., Luo, W., Wu, D., Liu, J., Zhou, D., Zhu, X., Wu, M., & Zhu, L. (2025) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2025.152115 · Cited by 4 · see citing works
Stress and the risk of Alzheimer dementia: Can deconstructed engrams be rebuilt?
Jeanneteau, F. D. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13235 · Cited by 3 · see citing works
Self-citationImpaired TGFβ Signaling in Plaque-Associated Microglia
Krzyzan, O., Kuhla, A., Spittau, B., & Vidovic, N. (2026) · Biomolecules · doi:10.3390/biom16020248 · Cited by 2 · see citing works
Kamińska, M., Dudzinska, N. A. M., Klapper, A., Geißler, S., Taudte, N., Greiser, S., Potempa, J., Cynis, H., & Mydel, P. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.06.658266 · Cited by 1 · see citing works
Murphy, S. M., & Husselbee, K. (2013) · Archives of Disease in Childhood · doi:10.1136/archdischild-2013-304107.191
Amyloidosis and ageing have differential effects on microglial Ca 2+ activity in the mouse brainPreprint
Izquierdo, P., Jolivet, R., Attwell, D., & Madry, C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.10.552670
Podleśny-Drabiniok, A., Romero-Molina, C., Patel, T., Wen, Y.-S., Liu, Y.-Y., Marcora, E., & Goate, A. (2024) · bioRxiv · doi:10.1101/2024.10.24.619910 · Cited by 7 · see citing works
APOE genotype differentially modulates prion pathology in a mouse model
Lizińczyk, A. M., Pankiewicz, J. E., Cullina, W. L., Franco, L. A., Sullivan, P. M., & Sadowski, M. J. (2026) · Acta Neuropathologica Communications · doi:10.1186/s40478-025-02207-5
Methodological developments for omic data integration : applications to oncology and neurosciences
Brière, G. (2022) · theses.fr (ABES) · doi:10.70675/13a03fd5zc563z49a8zb32az6cab055621d9
Biased multi-view contrastive learning with attentive masking for spatial transcriptomic analysis
Fu, L., Cui, W., Chen, Y., Wu, D., & Sun, H. (2026) · Briefings in Bioinformatics · doi:10.1093/bib/bbag215
Expression of GPR34 in microglia remains stable in human Alzheimer’s disease
Seiffer, S., Rotter, J., Brendler, J., Ricken, A. M., Detzer, Z., Braune, M., Schöneberg, T., Schulz, A., Winter, K., & Bechmann, I. (2026) · Acta Neuropathologica · doi:10.1007/s00401-026-03035-0
Neurotrophic Glucocorticoid Signalling
Jeanneteau, F. D. (2026) · Receptors · doi:10.3390/receptors5030024
Self-citation
- Authors
- Hemonnot-Girard, A.-L., Meersseman, C., Pastore, M., Garcia, V., Linck, N., Rey, C., Chebbi, A., Jeanneteau, F., Ginsberg, S. D., Lachuer, J., Reynes, C., Rassendren, F., & Hirbec, H.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Nathan Kline Institute for Psychiatric Research (US)
- Corresponding author
- Hirbec, Hélène
- ORCID
- Venue
- Journal of Neuroinflammation
- Published
- 2022-09-24
- Volume
- 19
- Issue
- 1
- Pages
- 234-234
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC9508749
- OpenAlex
- W4296982912
- Cited by
- 24
- References
- 73
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 5 · 2023: 6 · 2022: 1 · 2013: 1
- FWCI
- 1.58
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Labex ICST (ANR 11-LABX-0015)
- FRM
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- microglia, plaque-associated microglia, amyloid plaques, Alzheimer's disease, transcriptome remodeling, microglial heterogeneity, disease progression, laser capture microdissection, mouse models of Alzheimer's disease, postmortem brain, neuroinflammation
- MeSH terms
- Alzheimer Disease, Animals, Disease Models, Animal, Humans, Mice, Transgenic, Amyloid beta-Peptides, Amyloid beta-Protein Precursor, Microglia, Disease Progression, Mice, Plaque, Amyloid, Transcriptome
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
