Alzheimer’s disease-related transcriptional sex differences in myeloid cells
Open accessAbstract
Sex differences have been identified in many diseases associated with dysregulated immune responses, including Alzheimer’s disease (AD), for which approximately two-thirds of patients are women. An accumulating body of research indicates that microglia may play a causal role in the pathogenesis of this disease. We hypothesised that sex differences in the transcriptome of human myeloid cells may contribute to the sex difference observed in AD prevalence. To explore this, we assessed bulk and single-nuclear RNA sequencing data sets generated from four human derived myeloid cell populations: post-mortem microglial nuclei, peripheral monocytes, monocyte-derived macrophages (MDMs) and induced pluripotent stem cell derived microglial-like cells (MGLs). We found that expression of AD risk genes, gene signatures associated with the inflammatory response in AD, and genes related to proinflammatory immune responses were enriched in microglial nuclei isolated from aged female donors without ante-mortem neurological disease, relative to those from males. In addition, these inflammation-associated gene sets were found to be enriched in peripheral monocytes isolated from postmenopausal women and in MDMs obtained from premenopausal individuals relative to age-matched males. Expression of these gene sets did not differ in MDMs derived from women whose blood was sampled across the menstrual cycle or in MGLs cultured with 17β-oestradiol. This suggests that the observed gene set enrichments in myeloid cells from women were not being driven by acute hormonal influences. Together, these data support the hypothesis that the increased prevalence of AD in women may be partly explained by a myeloid cell phenotype biased towards expression of biological processes relevant to AD.
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?
In postmortem human brain tissue, dysregulation of microglial gene signatures is more common in female patients than in male patients.
“Similar observations were made in a study of postmortem human brain tissue, where dysregulation of microglial gene signatures was shown to be more common in female patients than in male patients. 40”
From Loss of <i>Inpp5d</i> has disease‐relevant and sex‐specific effects on glial transcriptomes (2024) · cites this paper as [40]
The Discussion reports that Bonham et al. inferred microglial-gene dysregulation in patients with Alzheimer’s disease to a greater extent in women than men. But this is a finding the cited paper attributes to another study; its own sex-specific gene-signature findings were primarily in postmortem microglia from donors without neurological disease, and its Results say the AD-donor samples showed no significant sex difference for the inflammatory gene sets tested. (LLM, conf=0.86)
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
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458 · see citing works
GSVA: gene set variation analysis for microarray and RNA-Seq data
Hänzelmann, S., Castelo, R., & Guinney, J. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-7 · Cited by 15,440 · see citing works
Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool
Chen, E. Y., Tan, C. M., Kou, Y., Duan, Q., Wang, Z., Meirelles, G. V., Clark, N. R., & Ma’ayan, A. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-128 · Cited by 7,814 · see citing works
Scenic: single-cell regulatory network inference and clustering.
Aibar, S., González-Blas, C. B., Moerman, T., Huynh-Thu, V. A., Imrichova, H., Hulselmans, G., Rambow, F., Marine, J.-C., Geurts, P., Aerts, J., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4463 · Cited by 6,520 · see citing works
Sex differences in immune responses
Klein, S. L., & Flanagan, K. L. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2016.90 · Cited by 6,370 · 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
Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt
Durinck, S., Spellman, P. T., Birney, E., & Huber, W. K. (2009) · Nature Protocols · doi:10.1038/nprot.2009.97 · Cited by 4,081 · see citing works
MAGMA: Generalized Gene-Set Analysis of GWAS Data
de Leeuw, C. A., Mooij, J. M., Heskes, T., & Posthuma, D. (2015) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1004219 · Cited by 3,653 · see citing works
Orchestrating high-throughput genomic analysis with Bioconductor
Huber, W. K., Carey, V. J., Gentleman, R. C., Anders, S., Carlson, M. R. J., Carvalho, B. S., Bravo, H. C., Davis, S. R., Gatto, L., Girke, T., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3252 · Cited by 3,499 · see citing works
Finak, G., McDavid, A., Yajima, M., Deng, J., Gersuk, V., Shalek, A. K., Slichter, C. K., Miller, H. W., McElrath, M. J., Prlic, M., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0844-5 · Cited by 3,159 · see citing works
Alzheimer Disease Genetics Consortium (ADGC), Kunkle, B. W., The European Alzheimer’s Disease Initiative (EADI), Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium (CHARGE), Genetic and Environmental Risk in AD/Defining Genetic, P. A. E. R. F. A. D. C. (., Grenier-Boley, B., Sims, R., Bis, J. C., Damotte, V., Naj, A. C., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0358-2 · Cited by 2,946 · see citing works
Knopman, D. S., Amieva, H., Petersen, R. C., Chételat, G., Holtzman, D. M., Hyman, B. T., Nixon, R. A., & Jones, D. T. (2021) · Nature Reviews Disease Primers · doi:10.1038/s41572-021-00269-y · Cited by 2,606 · see citing works
Single-cell transcriptomic analysis of Alzheimer’s disease
Mathys, H., Davila-Velderrain, J., Peng, Z., Gao, F., Mohammadi, S., Young, J. Z., Menon, M., He, L., Abdurrob, F., Jiang, X., et al. (2019) · Nature · doi:10.1038/s41586-019-1195-2 · Cited by 2,568 · see citing works
Huang, D. W., Sherman, B. T., Tan, Q., Collins, J., Alvord, W. G., Roayaei, J., Stephens, R. D., Baseler, M., Lane, H. C., & Lempicki, R. A. (2007) · Genome biology · doi:10.1186/gb-2007-8-9-r183 · Cited by 2,482 · see citing works
Jansen, I. E., Savage, J. E., Watanabe, K., Bryois, J., Williams, D. M., Steinberg, S., Sealock, J., Karlsson, I. K., Hägg, S., Athanasiu, L., et al. (2019) · Nature Genetics · doi:10.1038/s41588-018-0311-9 · Cited by 2,277 · see citing works
Integrated Systems Approach Identifies Genetic Nodes and Networks in Late-Onset Alzheimer’s Disease
Zhang, B., Gaiteri, C., Bodea, L.-G., Wang, Z., McElwee, J., Podtelezhnikov, A. A., Zhang, C., Xie, T., Tran, L., Dobrin, R., et al. (2013) · Cell · doi:10.1016/j.cell.2013.03.030 · Cited by 1,657 · see citing works
Microglia development follows a stepwise program to regulate brain homeostasis
Matcovitch-Natan, O., Winter, D. R., Giladi, A., Vargas Aguilar, S., Spinrad, A., Sarrazin, S., Ben-Yehuda, H., David, E., Zelada González, F., Perrin, P., et al. (2016) · Science · doi:10.1126/science.aad8670 · Cited by 1,180 · see citing works
The X-files in immunity: sex-based differences predispose immune responses
Fish, E. N. (2008) · Nature reviews. Immunology · doi:10.1038/nri2394 · Cited by 1,164 · see citing works
Landscape of X chromosome inactivation across human tissues
GTEx Consortium, Tukiainen, T., Villani, A.-C., Yen, A., Rivas, M. A., Marshall, J. L., Satija, R., Aguirre, M., Gauthier, L., Fleharty, M., et al. (2017) · Nature · doi:10.1038/nature24265 · Cited by 1,138 · see citing works
ARUK Consortium, Sims, R., GERAD/PERADES, C., van der Lee, S. J., Naj, A. C., Bellenguez, C., Badarinarayan, N., Jakobsdottir, J., Kunkle, B. W., Boland, A., et al. (2017) · Nature Genetics · doi:10.1038/ng.3916 · Cited by 1,126 · see citing works
Estrogen receptors regulate innate immune cells and signaling pathways
Kovats, S. (2015) · Cellular Immunology · doi:10.1016/j.cellimm.2015.01.018 · Cited by 987 · see citing works
Alzheimer's disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci
De Jager, P. L., Srivastava, G., Lunnon, K., Burgess, J., Schalkwyk, L. C., Yu, L., Eaton, M. L., Keenan, B. T., Ernst, J., McCabe, C., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3786 · Cited by 956 · see citing works
Sala 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 · see citing works
Microbiome Influences Prenatal and Adult Microglia in a Sex-Specific Manner
Thion, M. S., Low, D., Silvin, A., Chen, J., Grisel, P., Schulte-Schrepping, J., Blecher, R., Ulas, T., Squarzoni, P., Hoeffel, G., et al. (2018) · Cell · doi:10.1016/j.cell.2017.11.042 · Cited by 779 · 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
Sexual Dimorphism in Innate Immunity
Jaillon, S., Berthenet, K., & Garlanda, C. (2019) · Clinical reviews in allergy and immunology · doi:10.1007/s12016-017-8648-x · Cited by 659 · see citing works
Genetic identification of brain cell types underlying schizophrenia
Major Depressive Disorder Working Group of the Psychiatric Genomics Consortium, Skene, N. G., Bryois, J., Bakken, T. E., Breen, G., Crowley, J. J., Gaspar, H. A., Giusti-Rodriguez, P., Hodge, R. D., Miller, J. A., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0129-5 · Cited by 651 · see citing works
Sex-specific features of microglia from adult mice
Villa, A., Gelosa, P., Castiglioni, L., Cimino, M., Rizzi, N., Pepe, G., Lolli, F., Marcello, E., Sironi, L., Vegeto, E., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.048 · Cited by 651 · see citing works
Gene expression changes in the course of normal brain aging are sexually dimorphic
Berchtold, N. C., Cribbs, D. H., Coleman, P. D., Rogers, J., Head, E., Kim, R., Beach, T., Miller, C., Troncoso, J., Trojanowski, J. Q., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806883105 · Cited by 626 · see citing works
Haenseler, W., Sansom, S. N., Buchrieser, J., Newey, S. E., Moore, C. S., Nicholls, F. J., Chintawar, S., Schnell, C., Antel, J. P., Allen, N. D., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.05.017 · Cited by 593 · see citing works
Methylomic profiling implicates cortical deregulation of ANK1 in Alzheimer's disease
Lunnon, K., Smith, R., Hannon, E., De Jager, P. L., Srivastava, G., Volta, M., Troakes, C., Al-Sarraj, S., Burrage, J., Macdonald, R., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3782 · Cited by 574 · see citing works
Type I interferon response drives neuroinflammation and synapse loss in Alzheimer disease
Roy, E. R., Wang, B., Wan, Y.-W., Chiu, G., Cole, A., Yin, Z., Propson, N. E., Xu, Y., Jankowsky, J. L., Liu, Z., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci133737 · Cited by 563 · see citing works
Late onset Alzheimer’s disease genetics implicates microglial pathways in disease risk
Efthymiou, A. G., & Goate, A. M. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0184-x · Cited by 562 · see citing works
Epidemiology and risk factors of dementia
van der Flier, W. M. (2005) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2005.082867 · Cited by 550 · see citing works
Transcriptional and Translational Differences of Microglia from Male and Female Brains
Guneykaya, D., Ivanov, A., Hernandez, D. P., Haage, V., Wojtas, B., Meyer, N., Maricos, M., Jordan, P., Buonfiglioli, A., Gielniewski, B., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.001 · Cited by 477 · see citing works
Single-cell RNA sequencing reveals functional heterogeneity of glioma-associated brain macrophages
Ochocka, N., Segit, P., Walentynowicz, K. A., Wojnicki, K., Cyranowski, S., Swatler, J., Mieczkowski, J., & Kaminska, B. (2021) · Nature Communications · doi:10.1038/s41467-021-21407-w · Cited by 466 · 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
Hanamsagar, R., Alter, M. D., Block, C. S., Sullivan, H., Bolton, J. L., & Bilbo, S. D. (2017) · Glia · doi:10.1002/glia.23176 · Cited by 384 · see citing works
Wilgenburg, B. V., Browne, C., Vowles, J., & Cowley, S. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071098 · Cited by 353 · see citing works
Jack, C. R., Wiste, H. J., Weigand, S. D., Therneau, T. M., Knopman, D. S., Lowe, V., Vemuri, P., Mielke, M. M., Roberts, R. O., Machulda, M. M., et al. (2017) · The Lancet Neurology · doi:10.1016/s1474-4422(17)30077-7 · Cited by 333 · see citing works
Interpretation of risk loci from genome-wide association studies of Alzheimer's disease
Andrews, S. J., Fulton-Howard, B., & Goate, A. (2020) · The Lancet Neurology · doi:10.1016/s1474-4422(19)30435-1 · Cited by 314 · see citing works
Hanamsagar, R., Alter, M. D., Block, C. L., Sullivan, H. K., Bolton, J. L., & Bilbo, S. D. (2017) · Glia · doi:10.1002/glia.23277 · Cited by 297 · 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
Sex difference in coronavirus disease (COVID-19): a systematic review and meta-analysis
Abate, B. B., Kassie, A. M., Kassaw, M. W., Aragie, T. G., & Masresha, S. A. (2020) · BMJ Open · doi:10.1136/bmjopen-2020-040129 · Cited by 275 · see citing works
ImmGen report: sexual dimorphism in the immune system transcriptome
Gal-Oz, S. T., Maier, B., Yoshida, H., Seddu, K., Elbaz, N., Czysz, C., Zuk, O., Stranger, B. E., Ner-Gaon, H., & Shay, T. (2019) · Nature Communications · doi:10.1038/s41467-019-12348-6 · Cited by 274 · see citing works
VanRyzin, J. W., Marquardt, A. E., Argue, K. J., Vecchiarelli, H. A., Ashton, S. E., Arambula, S. E., Hill, M. N., & McCarthy, M. M. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.006 · Cited by 272 · see citing works
Female Sex and Alzheimer's Risk: The Menopause Connection
Scheyer, O., Rahman, A., Hristov, H., Berkowitz, C., Isaacson, R. S., Diaz Brinton, R., & Mosconi, L. (2018) · The Journal of Prevention of Alzheimer's Disease · doi:10.14283/jpad.2018.34 · Cited by 268 · see citing works
Microglial translational profiling reveals a convergent APOE pathway from aging, amyloid, and tau
Kang, S. S., Ebbert, M. T. W., Baker, K. E., Cook, C., Wang, X., Sens, J. P., Kocher, J.-P., Petrucelli, L., & Fryer, J. D. (2018) · Journal of Experimental Medicine · doi:10.1084/jem.20180653 · Cited by 260 · see citing works
From Menarche to Menopause: Trends among US Women Born from 1912 to 1969
Nichols, H. B., Trentham‐Dietz, A., Hampton, J. M., Titus-Ernstoff, L. T., Egan, K. M., Willett, W. C., & Newcomb, P. A. (2006) · American Journal of Epidemiology · doi:10.1093/aje/kwj282 · Cited by 225 · see citing works
DEAD/H BOX 3 (DDX3) helicase binds the RIG‐I adaptor IPS‐1 to up‐regulate IFN‐β‐inducing potential
Oshiumi, H., Sakai, K., Matsumoto, M., & Seya, T. (2010) · European Journal of Immunology · doi:10.1002/eji.200940203 · Cited by 216 · see citing works
Diverse human astrocyte and microglial transcriptional responses to Alzheimer’s pathology
Smith, A. M., Davey, K., Tsartsalis, S., Khozoie, C., Fancy, N., Tang, S. S., Liaptsi, E., Weinert, M., McGarry, A., Muirhead, R. C. J., et al. (2022) · Acta Neuropathologica · doi:10.1007/s00401-021-02372-6 · Cited by 209 · cited 6× · see citing works
“However, due to the relatively rarity of microglia in the brain, in this un-enriched population only a low resolution of microglia was be obtained (n = 1920 microglial nuclei compared to n = 27,592 in our enriched discovery data set [39] and n = 148,606 in the replication data set [41]).”
BackgroundMethodResultInfluentialSelf-citationSex differences in microglial phagocytosis in the neonatal hippocampus
Nelson, L. H., Warden, S., & Lenz, K. M. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.03.010 · Cited by 189 · see citing works
Wang, S., Yeh, S., Lin, W., Wang, H., Chen, D., & Chen, P. (2009) · Hepatology · doi:10.1002/hep.23163 · Cited by 188 · see citing works
Microglial metabolism is a pivotal factor in sexual dimorphism in Alzheimer's disease
Guillot-Sestier, M.-V., Araiz, A. R., Mela, V., Gaban, A. S., O’Neill, E., Joshi, L., Chouchani, E. T., Mills, E. L., & Lynch, M. A. (2021) · Communications Biology · doi:10.1038/s42003-021-02259-y · Cited by 182 · see citing works
The structural biology of oestrogen metabolism
THOMAS, M. P., & Potter, B. V. L. (2013) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2012.12.014 · Cited by 181 · see citing works
Sex differences in the human peripheral blood transcriptome
Jansen, R., Batista, S., Brooks, A. I., Tischfield, J. A., Willemsen, G. A. H. M., van Grootheest, G., Hottenga, J., Milaneschi, Y., Mbarek, H., Madar, V., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-33 · Cited by 166 · see citing works
Sex differences in tuberculosis
Hertz, D., & Schneider, B. E. (2018) · Seminars in Immunopathology · doi:10.1007/s00281-018-0725-6 · Cited by 148 · see citing works
Exploring Sex-Related Differences in Microglia May Be a Game-Changer in Precision Medicine
Lynch, M. A. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.868448 · Cited by 146 · see citing works
The non-specific and sex-differential effects of vaccines
Aaby, P., Benn, C. S., Flanagan, K. L., Klein, S. L., Kollmann, T. R., Lynn, D. J., & Shann, F. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-0338-x · Cited by 142 · see citing works
Murphy, A. E., Schilder, B. M., & Skene, N. (2021) · Bioinformatics · doi:10.1093/bioinformatics/btab665 · Cited by 135 · see citing works
Yanguas‐Casás, N., Crespo‐Castrillo, A., CEBALLOS, M. L. D., Chowen, J. A., Azcoitia, Í., Arévalo, M., & García‐Segura, L. M. (2017) · Glia · doi:10.1002/glia.23263 · Cited by 116 · see citing works
Bongen, E., Lucian, H. J., Khatri, A., Fragiadakis, G. K., Bjornson, Z. B., Nolan, G. P., Utz, P. J., & Khatri, P. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.019 · Cited by 115 · see citing works
Tsartsalis, S., Sleven, H., Fancy, N., Wessely, F., Smith, A. M., Willumsen, N., Cheung, T. K. D., Rokicki, M. J., Chau, V., Ifie, E., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-46630-z · Cited by 95 · see citing works
Self-citationThe Transcriptional Landscape of Microglial Genes in Aging and Neurodegenerative Disease
Bonham, L. W., Sirkis, D. W., & Yokoyama, J. S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01170 · Cited by 83 · see citing works
Scully, E. P., Schumock, G., Fu, M., Massaccesi, G., Muschelli, J., Betz, J., Klein, E. Y., West, N. E., Robinson, M., Garibaldi, B. T., et al. (2021) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofab448 · Cited by 73 · see citing works
Spolarics, Z., Peña, G., Qin, Y., DONNELLY, R. J., & Livingston, D. H. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01455 · Cited by 72 · see citing works
Beenakker, K. G. M., Westendorp, R. G. J., de Craen, A. J. M., Chen, S., Raz, Y., Ballieux, B. E. P. B., Nelissen, R. G. H. H., Later, A. F. L., Huizinga, T. W., Slagboom, P. E., et al. (2020) · Journal of Innate Immunity · doi:10.1159/000499840 · Cited by 66 · see citing works
Amyloid PET and cognitive decline in cognitively normal individuals: the SCIENCe project
Timmers, T., Ossenkoppele, R., Verfaillie, S. C. J., van der Weijden, C. W. J., Slot, R. E. R., Wesselman, L. M. P., Windhorst, A. D., Wolters, E. E., Yaqub, M., Prins, N. D., et al. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.02.020 · Cited by 63 · see citing works
Modelling microglial function with induced pluripotent stem cells: an update
Pocock, J. M., & Piers, T. M. (2018) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0030-3 · Cited by 57 · see citing works
Sexual dimorphism of monocyte transcriptome in individuals with chronic low-grade inflammation
So, J., Tai, A., Lichtenstein, A. H., Wu, D., & Lamon‐Fava, S. (2021) · Biology of Sex Differences · doi:10.1186/s13293-021-00387-y · Cited by 50 · see citing works
Meneses, G., Rosetti, M., Espinosa, A., Florentino, A., Bautista, M., Díaz, G., Olvera, G., Bárcena, B., Fleury, A., Adalid-Peralta, L. V., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201375 · Cited by 47 · see citing works
Sex-based differences in the activation of peripheral blood monocytes in early Parkinson disease
Carlisle, S. M., Qin, H., Hendrickson, R. C., Muwanguzi, J. E., Lefkowitz, E. J., Kennedy, R., Yan, Z., Yacoubian, T. A., Benveniste, E. N., West, A. B., et al. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00180-z · Cited by 46 · see citing works
Chen, Y., Hong, T., Chen, F., Sun, Y., Wang, Y., & Cui, L. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.631827 · Cited by 39 · see citing works
Osborne, B. F., Turano, A., Caulfield, J. I., & Schwarz, J. M. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.10.044 · Cited by 27 · see citing works
scFlow: A Scalable and Reproducible Analysis Pipeline for Single-Cell RNA Sequencing DataPreprint
Khozoie, C., Fancy, N. N., Marjaneh, M. M., Murphy, A. E., Matthews, P. M., & Skene, N. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.16.456499 · Cited by 21 · see citing works
Self-citationAge and sex differences in primary microglia culture: A comparative study
Ngwa, C., Qi, S., Mamun, A. A., Xu, Y., Sharmeen, R., & Liu, F. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109359 · Cited by 20 · see citing works
Estimating hepatitis C infection acquired in England, 1986–2000
BALOGUN, M. A., Vyse, A., Hesketh, L. M., Kafatos, G., Parry, J. V., & Ramsay, M. E. (2009) · Epidemiology and Infection · doi:10.1017/s0950268809002143 · Cited by 17 · see citing works
Vaughan-Jackson, A., Stodolak, S., Ebrahimi, K. H., Browne, C., Reardon, P. K., Pires, E., Gilbert‐Jaramillo, J., Cowley, S. A., & James, W. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.11.010 · Cited by 8 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [67]Tsartsalis S Fancy N Smith AM Khozoie C Yang X Davey K Single nuclear transcriptional signatures of dysfunctional brain vascular homeostasis in Alzheimer’s disease bioRxiv 2021 10.1101/2021.10.27.465860 · DOI
- [79]Korotkevich G Sukhov V Budin N Shpak B Artyomov MN Sergushichev A Fast gene set enrichment analysis BioRxiv 2021 10.1101/060012v3 · DOI
Cited by
Sorted by citations
An exhausted-like microglial population accumulates in aged and APOE4 genotype Alzheimer’s brains
Millet, A., Ledo, J. H., & Tavazoie, S. F. (2024) · Immunity · doi:10.1016/j.immuni.2023.12.001 · Cited by 132 · see citing works
Sex and Gender Differences in Neurodegenerative Diseases: Challenges for Therapeutic Opportunities
Bianco, A., Antonacci, Y., & Liguori, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076354 · Cited by 88 · see citing works
A single-cell and spatial RNA-seq database for Alzheimer’s disease (ssREAD)
Wang, C., Acosta, D., McNutt, M., Bian, J., Ma, A., Fu, H., & Ma, Q. (2024) · Nature Communications · doi:10.1038/s41467-024-49133-z · Cited by 73 · see citing works
<i>Tlr7</i> drives sex differences in age- and Alzheimer’s disease–related demyelination
Lopez-Lee, C., Kodama, L., Fan, L., Zhu, D., Zhu, J., Wong, M. Y., Ye, P., Norman, K., Foxe, N. R., Ijaz, L., et al. (2024) · Science · doi:10.1126/science.adk7844 · Cited by 49 · see citing works
Cui, S., Jiang, Q., & Chen, S. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101918 · Cited by 30 · see citing works
Martínková, J., Ferretti, M. T., Ferrari, A., Lerch, O., Matušková, V., Sečník, J., Hort, J., & Initiative, A. D. N. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1039239 · Cited by 29 · see citing works
Altered Metabolism and DAM-signatures in Female Brains and Microglia with Aging
Cleland, N. R. W., Potter, G. J., Buck, C., Quang, D., Oldham, D., Neal, M., Saviola, A., Niemeyer, C. S., Dobrinskikh, E., & Bruce, K. D. (2024) · Brain Research · doi:10.1016/j.brainres.2024.148772 · Cited by 26 · see citing works
Complexity of Sex Differences and Their Impact on Alzheimer’s Disease
Kadlecová, M., Freude, K., & Haukedal, H. (2023) · Biomedicines · doi:10.3390/biomedicines11051261 · Cited by 26 · see citing works
Cell type and sex specific mitochondrial phenotypes in iPSC derived models of Alzheimer’s disease
Flannagan, K., Stopperan, J. A., Hauger, B. M., Troutwine, B., Lysaker, C. R., Strope, T. A., Csikós, V., Gilmore, C. A., Swerdlow, N., Draper, J. M., et al. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1201015 · Cited by 24 · see citing works
Relationship between sex biases in gene expression and sex biases in autism and Alzheimer’s disease
Fass, S. B., Mulvey, B., Chase, R., Yang, W. C., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Biology of Sex Differences · doi:10.1186/s13293-024-00622-2 · Cited by 25 · see citing works
Do microbes play a role in Alzheimer's disease?
Williams, Z. A. P., Láng, L., Nicolas, S., Clarke, G. A., Cryan, J. F., Vauzour, D., & Nolan, Y. M. (2024) · Microbial Biotechnology · doi:10.1111/1751-7915.14462 · Cited by 20 · see citing works
Sex differences and the role of estrogens in the immunological underpinnings of Alzheimer's disease
Price, B. R., Walker, K. A., Eissman, J. M., Suryadevara, V., Sime, L. N., Hohman, T. J., & Gordon, M. N. (2025) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1002/trc2.70139 · Cited by 23 · see citing works
A case for seeking sex-specific treatments in Alzheimer’s disease
Lynch, M. A. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1346621 · Cited by 14 · see citing works
Normal-Tension Glaucoma and Potential Clinical Links to Alzheimer’s Disease
Ho, K., Bodi, N. E., & Sharma, T. P. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13071948 · Cited by 14 · see citing works
Distinct transcriptional alterations distinguish Lewy body disease from Alzheimer’s disease
Olney, K. C., Rabichow, B. E., Wojtas, A., Deture, M. A., McLean, P. J., Dickson, D. W., Chang, R. R., Ross, O. A., & Fryer, J. D. (2024) · Brain · doi:10.1093/brain/awae202 · Cited by 14 · see citing works
Chunchai, T., Chinchapo, T., Sripetchwandee, J., Thonusin, C., Chattipakorn, N., & Chattipakorn, S. C. (2024) · Acta Physiologica · doi:10.1111/apha.14130 · Cited by 13 · see citing works
Sex differences in Huntington's disease from a neuroinflammation perspective
Risby-Jones, G., Lee, J. D., Woodruff, T. M., & Fung, J. N. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1384480 · Cited by 13 · see citing works
Ali, M., Garcia, P., Lunkes, L. P., Sciortino, A., Thomas, M. H., Heurtaux, T., Grzyb, K., Halder, R., Coowar, D., Skupin, A., et al. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-01885-9 · Cited by 12 · see citing works
Rahmani, R., Rambarack, N., Singh, J., Constanti, A., & Ali, A. B. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914917 · Cited by 11 · see citing works
TSPO contributes to neuropathology and cognitive deficits in Alzheimer’s disease
Ceyzériat, K., Badina, A. M., Abjean, L., Meyer, L., Bouteldja, F., Bałkota, M., Amossé, Q., Prudhomme, O., Middleton, R. J., Liu, G.-J., et al. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03583-4 · Cited by 12 · see citing works
Self-citationLoss of <i>Inpp5d</i> has disease‐relevant and sex‐specific effects on glial transcriptomes
Dabin, L. C., Kersey, H., Kim, B., Acri, D. J., Sharify, D., Lee‐Gosselin, A., Lasagna‐Reeves, C. A., Oblak, A. L., Lamb, B. T., & Kim, J. (2024) · Alzheimer's & Dementia · doi:10.1002/alz.13901 · Cited by 10 · see citing works
“40 We were also interested in investigating the differences in gene expression in cell types that do not express Inpp5d .”
Shwab, E. K., Pathak, G. A., Harvey, J., Belloy, M. E., Fischer, C. E., Lutz, M. W., Scholz, S. W., Cook, N., Reid, D. M., Chen, J., et al. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70549 · Cited by 11 · see citing works
Nguyen, T. B., Lac, Q., Abdi, L., Banerjee, D., Deng, Y., & Zhang, Y. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1071243 · Cited by 10 · see citing works
Tournier, B. B., Ceyzériat, K., Badina, A. M., Gloria, Y., Fall, A. B., Amossé, Q., Tsartsalis, S., & Millet, P. (2024) · NeuroImage · doi:10.1016/j.neuroimage.2024.120778 · Cited by 8 · see citing works
Self-citationQiu, C., Zhang, D., Wang, M., Mei, X., Chen, W., Yu, H., Yin, W., Peng, G., & Hu, S. (2025) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.70204 · Cited by 9 · see citing works
Calcines-Rodríguez, L., Noyes-Martel, N., Becker, J. D., Nguyen, S. K., Osabutey, M., Trojanczyk, L., Majewska, A. K., & O’Banion, M. K. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03659-1 · Cited by 7 · see citing works
Microglial states revisited: from homeostasis to disease
Eggen, B. J. L., & Kooistra, S. M. (2026) · Nature Reviews Neuroscience · doi:10.1038/s41583-026-01066-w · Cited by 6 · see citing works
Tharp, M. E., Han, C. Z., Talukdar, M., Balak, C. D., Fitzpatrick, C., O’Connor, C., Preißl, S., Buchanan, J., Nott, A., Escoubet, L., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.06.06.597433 · Cited by 6 · see citing works
Azevedo, C. V., Otaviano, S. F. S. D., Campos, H. C., Figueiredo, E. V., Pereira, A. R., Alves, L., Braga, M., Gimenes, C., Boldarine, V. T., Oyama, L. M., et al. (2025) · Journal of Alzheimer s Disease · doi:10.1177/13872877251389824 · Cited by 5 · see citing works
Genetic and Epigenetic Sexual Dimorphism of Brain Cells during Aging
Shirokova, O. M., Zaborskaya, O., Pchelin, P. V., Kozliaeva, E. V., Pershin, V. I., & Mukhina, I. V. (2023) · Brain Sciences · doi:10.3390/brainsci13020195 · Cited by 5 · see citing works
Multifactorial glial responses and their contributions to Alzheimer's disease continuum
Hijioka, M., Manabe, T., & Saito, T. (2023) · Clinical and Experimental Neuroimmunology · doi:10.1111/cen3.12745 · Cited by 4 · see citing works
Type-1 interferons associated with microglial-mediated neuroinflammation in Alzheimer’s disease
Shippy, D. C., Sande, M. L., & Ulland, T. K. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03828-w · Cited by 3 · see citing works
The complex of gut microbial metabolites and sex hormones in Alzheimer’s disease
Bahar, A., Khazaei, M., & Tahmasebi, H. (2026) · Seminars in Immunopathology · doi:10.1007/s00281-026-01076-x · Cited by 5 · see citing works
Lopez-Lee, C., Kodama, L., Fan, L., Wong, M. Y., Foxe, N. R., Jiaz, L., Yu, F., Ye, P., Zhu, J., Norman, K., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.19.558439 · Cited by 3 · see citing works
Rodriguez, L. C., Noyes-Martel, N., Becker, J. D., Majewska, A. K., & O’Banion, M. K. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.28.646050 · Cited by 3 · see citing works
Figueiredo-Pereira, M. E., Serrano, P. A., & Rockwell, P. (2025) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-25-00256 · Cited by 2 · see citing works
Seijo, M. A., Banerjee, A., & Hernandez, C. M. (2025) · Scientific Reports · doi:10.1038/s41598-025-30561-w · Cited by 2 · see citing works
Sex-dependent interferon signaling contributes to female-biased vulnerability in Alzheimer’s disease
López-López, V., Iniesta, G., Galán-Ganga, M., Exposito-Coca, A., Durán-Laforet, V., Bhojwani-Cabrera, A. M., Navarrón, C. M., Guillot-Fernández, M., Venero, J. L., Sanchez-Mut, J. V., et al. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03840-0 · Cited by 4 · see citing works
Amossé, Q., Tournier, B. B., Badina, A. M., Marchand-Maillet, L., Abjean, L., Lengacher, S., Fancy, N. N., Smith, A. M., Leung, Y.-Y., Santer, V., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.29.564621 · Cited by 2 · see citing works
Self-citationChunchai, T., Pintana, H., Pantiya, P., Kunasol, C., Thonusin, C., Chattipakorn, N., & Chattipakorn, S. C. (2026) · Acta Physiologica · doi:10.1111/apha.70241 · Cited by 1 · see citing works
Fatih, N., Chaturvedi, N., Garfield, V., Sudre, C. H., Silverwood, R. J., Cash, D. M., Malone, I. B., Barnes, J., Richards, M., Schott, J. M., et al. (2025) · medRxiv · doi:10.1101/2025.08.01.25332698 · Cited by 1 · see citing works
Sex-dependent interferon signaling drives female-biased vulnerability in Alzheimer’s diseasePreprint
López-López, V., Iniesta, G., Galán-Ganga, M., Exposito-Coca, A., Bhojwani-Cabrera, A. M., Guillot-Fernández, M., Giralt, A., & López‐Atalaya, J. P. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.22.671724 · Cited by 1 · see citing works
Glial Cells in Alzheimer’s Disease
Verkerke, M. L. (2023) · doi:10.33540/1838
Yu, M., Risacher, S. L., Nho, K. T., Wen, Q., Oblak, A. L., Unverzagt, F. W., Apostolova, L. G., Farlow, M. R., Brosch, J. R., Clark, D. G., et al. (2023) · medRxiv · doi:10.1101/2023.08.12.23294017
Cerebral blood flow in elastin haploinsufficient and 3xTg-AD micePreprint
Cullen, A. E., Reeve, E. H., Winder, N., Henson, G. D., Arora, N., Leonhardt, T., Hogan, A. P., Kumaran, S. K., Setthavongsack, N., Krajbich, V., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.18.670895
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730706
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730724
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730709
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730715
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730730
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730718
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730721
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730727
Fass, S. B., Mulvey, B., Chase, R., Yang, W., Selmanovic, D., Chaturvedi, S. M., Tycksen, E., Weiss, L. A., & Dougherty, J. D. (2024) · Figshare · doi:10.6084/m9.figshare.26730712
Lower cerebral blood flow but not cerebrovascular response in elastin haploinsufficient mice
Cullen, A. E., Reeve, E. H., Winder, N. R., Henson, G. D., Arora, N., Leonhardt, T., Hogan, A., Kumaran, S. K., Setthavonsack, N., Krajbich, V., et al. (2026) · Experimental Physiology · doi:10.1113/ep093234
Fatih, N., Chaturvedi, N., Garfield, V., Sudre, C. H., Silverwood, R. J., Cash, D. M., Malone, I. B., Barnes, J., Richards, M., Schott, J. M., et al. (2026) · PLoS ONE · doi:10.1371/journal.pone.0329046
Sriram, A., Attili, S. M., & Seshaiyer, P. (2026) · Research Square · doi:10.21203/rs.3.rs-10233914/v1
- Authors
- Coales, I., Tsartsalis, S., Fancy, N., Weinert, M., Clode, D., Owen, D., & Matthews, P. M.
- Affiliations
- King's College London (GB)
- University of Geneva (CH)
- Imperial College London (GB)
- Hammersmith Hospital (GB)
- Corresponding author
- Owen, David
- Matthews, Paul M.
- Venue
- Journal of Neuroinflammation
- Published
- 2022-10-05
- Volume
- 19
- Issue
- 1
- Pages
- 247-247
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC9535846
- OpenAlex
- W4302009331
- Cited by
- 49
- References
- 79
- Citations by year
- 2026: 8 · 2025: 12 · 2024: 14 · 2023: 15
- FWCI
- 4.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Research Portal (King's College London) (submittedVersion, cc-by)
- Spiral (Imperial College London) (submittedVersion, cc-by)
- Funders
- Medical Research Council Doctoral Training Programme
- Swiss National Science Foundation (P2GEP3_191446)
- Prof Dr Max Cloëtta Foundation
- University Hospitals of Geneva
- Jean and Madeleine Vachoux Foundation
- MRC Clinical Scientist Award (MR/N008219/1)
- MRC Pathfinder Award (MR/N016343/1)
- Edmond J Safra Foundation
- Lily Safra
- NIHR Senior Investigator Award
- UK Dementia Research Institute
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Keywords
- Alzheimer's disease, sex differences, myeloid cells, microglia, monocytes, monocyte-derived macrophages, transcriptome, postmenopausal women, estrogen, inflammation, menstrual cycle
- MeSH terms
- Aged, Alzheimer Disease, Estradiol, Female, Humans, Male, Sex Characteristics, Microglia, Myeloid Cells
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
