CoChat
Sign Up
Cited by 18Neuroinflammation and Neurodegeneration MechanismsAlzheimer's disease research and treatmentsNeurological Disease Mechanisms and Treatments

Lipopolysaccharide distinctively alters human microglia transcriptomes to resemble microglia from Alzheimer’s disease mouse models

Open access
Monzón-Sandoval, Jimena, Burlacu, Elena, Agarwal, Devika, Handel, Adam E., Wei, Liting, Davis, John, Cowley, Sally A., Cader, M. Zameel +1 more·2022·Disease Models & Mechanisms
DOI 10.1242/dmm.049349PMC PMC9612871
Open this paper in CoChat — free accountOpen PDF

Abstract

Alzheimer's disease (AD) is the most common form of dementia, and risk-influencing genetics implicates microglia and neuroimmunity in the pathogenesis of AD. Induced pluripotent stem cell (iPSC)-derived microglia (iPSC-microglia) are increasingly used as a model of AD, but the relevance of historical immune stimuli to model AD is unclear. We performed a detailed cross-comparison over time on the effects of combinatory stimulation of iPSC-microglia, and in particular their relevance to AD. We used single-cell RNA sequencing to measure the transcriptional response of iPSC-microglia after 24 h and 48 h of stimulation with prostaglandin E2 (PGE2) or lipopolysaccharide (LPS)+interferon gamma (IFN-γ), either alone or in combination with ATPγS. We observed a shared core transcriptional response of iPSC-microglia to ATPγS and to LPS+IFN-γ, suggestive of a convergent mechanism of action. Across all conditions, we observed a significant overlap, although directional inconsistency to genes that change their expression levels in human microglia from AD patients. Using a data-led approach, we identify a common axis of transcriptomic change across AD genetic mouse models of microglia and show that only LPS provokes a transcriptional response along this axis in mouse microglia and LPS+IFN-γ in human iPSC-microglia. This article has an associated First Person interview with the first author of the paper.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1242/dmm.049349

Cites

10 of 10 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Our list of core genes can be interpreted as robust tau-responsive genes for future study.

    “As preclinical studies continue to make direct comparisons between human and mouse transcriptomics (Monzón-Sandoval et al., 2022; Onos et al., 2022), our list of core genes can be interpreted as robust tau-responsive genes for future study.”

    From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Monzón-Sandoval et al., 2022

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

Flagged first, then by citations

Research works printed but not linked: 62

  1. Agarwal, D., Sandor, C., Volpato, V., Caffrey, T. M., Monzón-Sandoval, J., Bowden, R., Alegre-Abarrategui, J., Wade-Martins, R. and Webber, C. (2020). A single-cell atlas of the human substantia nigra reveals cell-specific pathways associated with neurological disorders. Nat. Commun. 11, 4183. 10.1038/s41467-020-17876-0 32826893 PMC7442652 · DOI
  2. Amaradhi, R., Banik, A., Mohammed, S., Patro, V., Rojas, A., Wang, W., Motati, D. R., Dingledine, R. and Ganesh, T. (2020). Potent, selective, water soluble, brain-permeable EP2 receptor antagonist for use in central nervous system disease models. J. Med. Chem. 63, 1032- 1050. 10.1021/acs.jmedchem.9b01218 31904232 PMC7394479 · DOI
  3. Anderson, C. M., Bergher, J. P. and Swanson, R. A. (2004). ATP-induced ATP release from astrocytes. J. Neurochem. 88, 246- 256. 10.1111/j.1471-4159.2004.02204.x 14675168 · DOI
  4. Andreasson, K. (2010). Emerging roles of PGE2 receptors in models of neurological disease. Prostaglandins Other Lipid Mediat. 91, 104- 112. 10.1016/j.prostaglandins.2009.04.003 19808012 PMC2846228 · DOI
  5. Badimon, A., Strasburger, H. J., Ayata, P., Chen, X., Nair, A., Ikegami, A., Hwang, P., Chan, A. T., Graves, S. M., Uweru, J. O. et al. (2020). Negative feedback control of neuronal activity by microglia. Nature 586, 417- 423. 10.1038/s41586-020-2777-8 32999463 PMC7577179 · DOI · Paper page
  6. Bodin, P. and Burnstock, G. (2001). Purinergic signalling: ATP release. Neurochem. Res. 26, 959- 969. 10.1023/A:1012388618693 11699948 · DOI
  7. Bray, N. L., Pimentel, H., Melsted, P. and Pachter, L. (2016). Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525- 527. 10.1038/nbt.3519 27043002 · DOI · Paper page
  8. Buniello, A., Macarthur, J. A. L., Cerezo, M., Harris, L. W., Hayhurst, J., Malangone, C., Mcmahon, A., Morales, J., Mountjoy, E., Sollis, E. et al. (2019). The NHGRI-EBI GWAS catalog of published genome-wide association studies, targeted arrays and summary statistics 2019. Nucleic Acids Res. 47, D1005- D1012. 10.1093/nar/gky1120 30445434 PMC6323933 · DOI · Paper page
  9. Caggiano, A. O. and Kraig, R. P. (1999). Prostaglandin E receptor subtypes in cultured rat microglia and their role in reducing lipopolysaccharide-induced interleukin-1beta production. J. Neurochem. 72, 565- 575. 10.1046/j.1471-4159.1999.0720565.x 9930728 PMC2807136 · DOI
  10. Calvo-Rodriguez, M., Garcia-Rodriguez, C., Villalobos, C. and Nunez, L. (2020). Role of toll like receptor 4 in Alzheimer's disease. Front. Immunol. 11, 1588. 10.3389/fimmu.2020.01588 32983082 PMC7479089 · DOI · Paper page
  11. Carvalho, B. S. and Irizarry, R. A. (2010). A framework for oligonucleotide microarray preprocessing. Bioinformatics 26, 2363- 2367. 10.1093/bioinformatics/btq431 20688976 PMC2944196 · DOI
  12. Chakraborty, S., Datta, S. and Datta, S. (2012). Surrogate variable analysis using partial least squares (SVA-PLS) in gene expression studies. Bioinformatics 28, 799- 806. 10.1093/bioinformatics/bts022 22238271 · DOI
  13. Cho, C. E., Damle, S. S., Wancewicz, E. V., Mukhopadhyay, S., Hart, C. E., Mazur, C., Swayze, E. E. and Kamme, F. (2019). A modular analysis of microglia gene expression, insights into the aged phenotype. BMC Genomics 20, 164. 10.1186/s12864-019-5549-9 30819113 PMC6396472 · DOI
  14. Dafinca, R., Scaber, J., Ababneh, N., Lalic, T., Weir, G., Christian, H., Vowles, J., Douglas, A. G., Fletcher-Jones, A., Browne, C. et al. (2016). C9orf72 hexanucleotide expansions are associated with altered endoplasmic reticulum calcium homeostasis and stress granule formation in induced pluripotent stem cell-derived neurons from patients with amyotrophic lateral sclerosis and frontotemporal dementia. Stem Cells 34, 2063- 2078. 10.1002/stem.2388 27097283 PMC4979662 · DOI
  15. Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L. and Gan, W. B. (2005). ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752- 758. 10.1038/nn1472 15895084 · DOI · Paper page
  16. Dou, Y., Wu, H. J., Li, H. Q., Qin, S., Wang, Y. E., Li, J., Lou, H. F., Chen, Z., Li, X. M., Luo, Q. M. et al. (2012). Microglial migration mediated by ATP-induced ATP release from lysosomes. Cell Res. 22, 1022- 1033. 10.1038/cr.2012.10 22231629 PMC3367529 · DOI · Paper page
  17. Edgar, R., Domrachev, M. and Lash, A. E. (2002). Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207- 210. 10.1093/nar/30.1.207 11752295 PMC99122 · DOI · Paper page
  18. Fabregat, A., Jupe, S., Matthews, L., Sidiropoulos, K., Gillespie, M., Garapati, P., Haw, R., Jassal, B., Korninger, F., May, B. et al. (2018). The reactome pathway knowledgebase. Nucleic Acids Res. 46, D649- D655. 10.1093/nar/gkx1132 29145629 PMC5753187 · DOI
  19. Giurgiu, M., Reinhard, J., Brauner, B., Dunger-Kaltenbach, I., Fobo, G., Frishman, G., Montrone, C. and Ruepp, A. (2019). CORUM: the comprehensive resource of mammalian protein complexes-2019. Nucleic Acids Res. 47, D559- D563. 10.1093/nar/gky973 30357367 PMC6323970 · DOI · Paper page
  20. Guthrie, P. B., Knappenberger, J., Segal, M., Bennett, M. V., Charles, A. C. and Kater, S. B. (1999). ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520- 528. 10.1523/JNEUROSCI.19-02-00520.1999 9880572 PMC6782195 · DOI
  21. 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. (2017a). A highly efficient human pluripotent stem cell microglia model displays a neuronal-co-culture-specific expression profile and inflammatory response. Stem Cell Rep. 8, 1727- 1742. 10.1016/j.stemcr.2017.05.017 PMC5470330 28591653 · DOI · Paper page
  22. Haenseler, W., Zambon, F., Lee, H., Vowles, J., Rinaldi, F., Duggal, G., Houlden, H., Gwinn, K., Wray, S., Luk, K. C. et al. (2017b). Excess α-synuclein compromises phagocytosis in iPSC-derived macrophages. Sci. Rep. 7, 9003. 10.1038/s41598-017-09362-3 28827786 PMC5567139 · DOI
  23. Held, T. K., Weihua, X., Yuan, L., Kalvakolanu, D. V. and Cross, A. S. (1999). Gamma interferon augments macrophage activation by lipopolysaccharide by two distinct mechanisms, at the signal transduction level and via an autocrine mechanism involving tumor necrosis factor alpha and interleukin-1. Infect. Immun. 67, 206- 212. 10.1128/IAI.67.1.206-212.1999 9864217 PMC96298 · DOI
  24. Huttlin, E. L., Bruckner, R. J., Navarrete-Perea, J., Cannon, J. R., Baltier, K., Gebreab, F., Gygi, M. P., Thornock, A., Zarraga, G., Tam, S. et al. (2021). Dual proteome-scale networks reveal cell-specific remodeling of the human interactome. Cell 184, 3022- 3040.e28. 10.1016/j.cell.2021.04.011 33961781 PMC8165030 · DOI · Paper page
  25. Jin, J., Shie, F. S., Liu, J., Wang, Y., Davis, J., Schantz, A. M., Montine, K. S., Montine, T. J. and Zhang, J. (2007). Prostaglandin E2 receptor subtype 2 (EP2) regulates microglial activation and associated neurotoxicity induced by aggregated α-synuclein. J. Neuroinflammation 4, 2. 10.1186/1742-2094-4-2 17204153 PMC1766347 · DOI
  26. Kawahara, K., Hohjoh, H., Inazumi, T., Tsuchiya, S. and Sugimoto, Y. (2015). Prostaglandin E2-induced inflammation: relevance of prostaglandin E receptors. Biochim. Biophys. Acta 1851, 414- 421. 10.1016/j.bbalip.2014.07.008 25038274 · DOI · Paper page
  27. Lalo, U., Palygin, O., Rasooli-Nejad, S., Andrew, J., Haydon, P. G. and Pankratov, Y. (2014). Exocytosis of ATP from astrocytes modulates phasic and tonic inhibition in the neocortex. PLoS Biol. 12, e1001747. 10.1371/journal.pbio.1001747 24409095 PMC3883644 · DOI · Paper page
  28. Li, T., Wernersson, R., Hansen, R. B., Horn, H., Mercer, J., Slodkowicz, G., Workman, C. T., Rigina, O., Rapacki, K., Staerfeldt, H. H. et al. (2017). A scored human protein-protein interaction network to catalyze genomic interpretation. Nat. Methods 14, 61- 64. 10.1038/nmeth.4083 27892958 PMC5839635 · DOI
  29. Liang, X., Wang, Q., Shi, J., Lokteva, L., Breyer, R. M., Montine, T. J. and Andreasson, K. (2008). The prostaglandin E2 EP2 receptor accelerates disease progression and inflammation in a model of amyotrophic lateral sclerosis. Ann. Neurol. 64, 304- 314. 10.1002/ana.21437 18825663 PMC2766522 · DOI
  30. Licata, L., Briganti, L., Peluso, D., Perfetto, L., Iannuccelli, M., Galeota, E., Sacco, F., Palma, A., Nardozza, A. P., Santonico, E. et al. (2012). MINT, the molecular interaction database: 2012 update. Nucleic Acids Res. 40, D857- D861. 10.1093/nar/gkr930 22096227 PMC3244991 · DOI
  31. López, Y., Nakai, K. and Patil, A. (2015). HitPredict version 4: comprehensive reliability scoring of physical protein-protein interactions from more than 100 species. Database 2015, bav117. 10.1093/database/bav117 26708988 PMC4691340 · DOI
  32. Love, M. I., Huber, W. and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. 10.1186/s13059-014-0550-8 25516281 PMC4302049 · DOI · Paper page
  33. Lowenstein, C. J., Alley, E. W., Raval, P., Snowman, A. M., Snyder, S. H., Russell, S. W. and Murphy, W. J. (1993). Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 90, 9730- 9734. 10.1073/pnas.90.20.9730 7692452 PMC47644 · DOI
  34. Mancuso, R., Van Den Daele, J., Fattorelli, N., Wolfs, L., Balusu, S., Burton, O., Liston, A., Sierksma, A., Fourne, Y., Poovathingal, S. et al. (2019). Stem-cell-derived human microglia transplanted in mouse brain to study human disease. Nat. Neurosci. 22, 2111- 2116. 10.1038/s41593-019-0525-x 31659342 PMC7616913 · DOI · Paper page
  35. 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). Single-cell transcriptomic analysis of Alzheimer's disease. Nature 570, 332- 337. 10.1038/s41586-019-1195-2 31042697 PMC6865822 · DOI · Paper page
  36. Melani, A., Turchi, D., Vannucchi, M. G., Cipriani, S., Gianfriddo, M. and Pedata, F. (2005). ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem. Int. 47, 442- 448. 10.1016/j.neuint.2005.05.014 16029911 · DOI
  37. Minhas, P. S., Latif-Hernandez, A., Mcreynolds, M. R., Durairaj, A. S., Wang, Q., Rubin, A., Joshi, A. U., He, J. Q., Gauba, E., Liu, L. et al. (2021). Restoring metabolism of myeloid cells reverses cognitive decline in ageing. Nature 590, 122- 128. 10.1038/s41586-020-03160-0 33473210 PMC8274816 · DOI · Paper page
  38. Mosser, D. M. and Edwards, J. P. (2008). Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958- 969. 10.1038/nri2448 19029990 PMC2724991 · DOI · Paper page
  39. Muhl, L., Genove, G., Leptidis, S., Liu, J., He, L., Mocci, G., Sun, Y., Gustafsson, S., Buyandelger, B., Chivukula, I. V. et al. (2020). Single-cell analysis uncovers fibroblast heterogeneity and criteria for fibroblast and mural cell identification and discrimination. Nat. Commun. 11, 3953. 10.1038/s41467-020-17740-1 32769974 PMC7414220 · DOI
  40. Mukherjee, S., Klaus, C., Pricop-Jeckstadt, M., Miller, J. A. and Struebing, F. L. (2019). A microglial signature directing human aging and neurodegeneration-related gene networks. Front. Neurosci. 13, 2. 10.3389/fnins.2019.00002 30733664 PMC6353788 · DOI
  41. Ohsawa, K., Irino, Y., Nakamura, Y., Akazawa, C., Inoue, K. and Kohsaka, S. (2007). Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 55, 604- 616. 10.1002/glia.20489 17299767 · DOI
  42. Orchard, S., Ammari, M., Aranda, B., Breuza, L., Briganti, L., Broackes-Carter, F., Campbell, N. H., Chavali, G., Chen, C., Del-Toro, N. et al. (2014). The MIntAct project—IntAct as a common curation platform for 11 molecular interaction databases. Nucleic Acids Res. 42, D358- D363. 10.1093/nar/gkt1115 24234451 PMC3965093 · DOI
  43. Orre, M., Kamphuis, W., Osborn, L. M., Jansen, A. H. P., Kooijman, L., Bossers, K. and Hol, E. M. (2014). Isolation of glia from Alzheimer's mice reveals inflammation and dysfunction. Neurobiol. Aging 35, 2746- 2760. 10.1016/j.neurobiolaging.2014.06.004 25002035 · DOI · Paper page
  44. Pankratov, Y., Lalo, U., Verkhratsky, A. and North, R. A. (2006). Vesicular release of ATP at central synapses. Pflugers Arch. 452, 589- 597. 10.1007/s00424-006-0061-x 16639550 · DOI
  45. Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L. et al. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science 333, 1456- 1458. 10.1126/science.1202529 21778362 · DOI · Paper page
  46. Park, B. S. and Lee, J. O. (2013). Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp. Mol. Med. 45, e66. 10.1038/emm.2013.97 24310172 PMC3880462 · DOI
  47. Reyes-Vazquez, C., Prieto-Gomez, B. and Dafny, N. (2012). Interferon modulates central nervous system function. Brain Res. 1442, 76- 89. 10.1016/j.brainres.2011.09.061 22322149 · DOI
  48. Rodrigues, R. J., Tome, A. R. and Cunha, R. A. (2015). ATP as a multi-target danger signal in the brain. Front. Neurosci. 9, 148. 10.3389/fnins.2015.00148 25972780 PMC4412015 · DOI
  49. Roselli, F., Chandrasekar, A. and Morganti-Kossmann, M. C. (2018). Interferons in traumatic brain and spinal cord injury: current evidence for translational application. Front. Neurol. 9, 458. 10.3389/fneur.2018.00458 29971040 PMC6018073 · DOI
  50. Shie, F. S., Breyer, R. M. and Montine, T. J. (2005). Microglia lacking E prostanoid receptor subtype 2 have enhanced Abeta phagocytosis yet lack Abeta-activated neurotoxicity. Am. J. Pathol. 166, 1163- 1172. 10.1016/S0002-9440(10)62336-X 15793296 PMC1602400 · DOI
  51. Song, W. M., Joshita, S., Zhou, Y., Ulland, T. K., Gilfillan, S. and Colonna, M. (2018). Humanized TREM2 mice reveal microglia-intrinsic and -extrinsic effects of R47H polymorphism. J. Exp. Med. 215, 745- 760. 10.1084/jem.20171529 29321225 PMC5839761 · DOI · Paper page
  52. Srinivasan, K., Friedman, B. A., Larson, J. L., Lauffer, B. E., Goldstein, L. D., Appling, L. L., Borneo, J., Poon, C., Ho, T., Cai, F. et al. (2016). Untangling the brain's neuroinflammatory and neurodegenerative transcriptional responses. Nat. Commun. 7, 11295. 10.1038/ncomms11295 27097852 PMC4844685 · DOI · Paper page
  53. Stark, C., Breitkreutz, B. J., Reguly, T., Boucher, L., Breitkreutz, A. and Tyers, M. (2006). BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34, D535- D539. 10.1093/nar/gkj109 16381927 PMC1347471 · DOI · Paper page
  54. Stoeckius, M., Hafemeister, C., Stephenson, W., Houck-Loomis, B., Chattopadhyay, P. K., Swerdlow, H., Satija, R. and Smibert, P. (2017). Simultaneous epitope and transcriptome measurement in single cells. Nat. Methods 14, 865- 868. 10.1038/nmeth.4380 28759029 PMC5669064 · DOI · Paper page
  55. Streit, W. J., Sammons, N. W., Kuhns, A. J. and Sparks, D. L. (2004). Dystrophic microglia in the aging human brain. Glia 45, 208- 212. 10.1002/glia.10319 14730714 · DOI · Paper page
  56. Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., 3rd, Hao, Y., Stoeckius, M., Smibert, P. and Satija, R. (2019). Comprehensive integration of single-cell data. Cell 177, 1888- 1902.e21. 10.1016/j.cell.2019.05.031 31178118 PMC6687398 · DOI · Paper page
  57. Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P. et al. (2019). STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607- D613. 10.1093/nar/gky1131 30476243 PMC6323986 · DOI · Paper page
  58. Walz, W., Ilschner, S., Ohlemeyer, C., Banati, R. and Kettenmann, H. (1993). Extracellular ATP activates a cation conductance and a K+ conductance in cultured microglial cells from mouse brain. J. Neurosci. 13, 4403- 4411. 10.1523/JNEUROSCI.13-10-04403.1993 7692013 PMC6576379 · DOI
  59. 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). TREM2 lipid sensing sustains the microglial response in an Alzheimer's disease model. Cell 160, 1061- 1071. 10.1016/j.cell.2015.01.049 25728668 PMC4477963 · DOI · Paper page
  60. Woodling, N. S., Wang, Q., Priyam, P. G., Larkin, P., Shi, J., Johansson, J. U., Zagol-Ikapitte, I., Boutaud, O. and Andreasson, K. I. (2014). Suppression of Alzheimer-associated inflammation by microglial prostaglandin-E2 EP4 receptor signaling. J. Neurosci. 34, 5882- 5894. 10.1523/JNEUROSCI.0410-14.2014 24760848 PMC3996215 · DOI
  61. Zhang, D., Hu, X., Qian, L., Wilson, B., Lee, C., Flood, P., Langenbach, R. and Hong, J. S. (2009). Prostaglandin E2 released from activated microglia enhances astrocyte proliferation in vitro. Toxicol. Appl. Pharmacol. 238, 64- 70. 10.1016/j.taap.2009.04.015 19397918 PMC2699578 · DOI
  62. 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). Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell 153, 707- 720. 10.1016/j.cell.2013.03.030 23622250 PMC3677161 · DOI · Paper page

Cited by

Sorted by citations

Authors
Monzón-Sandoval, J., Burlacu, E., Agarwal, D., Handel, A. E., Wei, L., Davis, J., Cowley, S. A., Cader, M. Z., & Webber, C.
Affiliations
  • UK Dementia Research Institute, Cardiff University 1 , Cardiff CF24 4HQ , UK
  • John Radcliffe Hospital (GB)
  • University of Oxford (GB)
  • UK Dementia Research Institute (GB)
Corresponding author
  • Cader, M. Zameel
  • Webber, Caleb
ORCID
Venue
Disease Models & Mechanisms
Publisher
The Company of Biologists
Published
2022-10-01
Volume
15
Issue
10
ISSN
  • 1754-8403 (ISSN-L)
  • 1754-8411
DOI
10.1242/dmm.049349
PMC
PMC9612871
OpenAlex
W4306682604
Cited by
18
References
10
Citations by year
2026: 5 · 2025: 1 · 2024: 6 · 2023: 4 · 2022: 2
FWCI
1.14
Type
journal article
Language
en
Open access
Licence
Locations
  • Disease Models & Mechanisms (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Medical Research Council (MC_PC_16034)
  • UK Dementia Research Institute (MC_PC_17112)
  • Oxford Martin School, University of Oxford (LC0910-004)
  • Parkinson's UK (J-1403)
  • Dementias Platform UK (MC_EX_MR/N50192X/1)
  • Innovative Medicines Initiative (807015)
  • NIHR Oxford Biomedical Research Centre
  • Wellcome Trust (100643/Z/12/Z)
  • Cardiff University
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
Alzheimer's disease, microglia, iPSC-derived microglia, lipopolysaccharide, interferon-gamma, prostaglandin E2, ATP gamma S, neuroinflammation, transcriptome, single-cell RNA sequencing, mouse models of Alzheimer's disease, neuroimmunity, gene expression response
MeSH terms
Alzheimer Disease, Animals, Disease Models, Animal, Humans, Interferon-gamma, Lipopolysaccharides, Dinoprostone, Microglia, Mice, 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