Microglial transglutaminase-2 drives myelination and myelin repair via GPR56/ADGRG1 in oligodendrocyte precursor cells
Open accessAbstract
In the central nervous system (CNS), myelin formation and repair are regulated by oligodendrocyte (OL) lineage cells, which sense and integrate signals from their environment, including from other glial cells and the extracellular matrix (ECM). The signaling pathways that coordinate this complex communication, however, remain poorly understood. The adhesion G protein-coupled receptor ADGRG1 (also known as GPR56) is an evolutionarily conserved regulator of OL development in humans, mice, and zebrafish, although its activating ligand for OL lineage cells is unknown. Here, we report that microglia-derived transglutaminase-2 (TG2) signals to ADGRG1 on OL precursor cells (OPCs) in the presence of the ECM protein laminin and that TG2/laminin-dependent activation of ADGRG1 promotes OPC proliferation. Signaling by TG2/laminin to ADGRG1 on OPCs additionally improves remyelination in two murine models of demyelination. These findings identify a novel glia-to-glia signaling pathway that promotes myelin formation and repair, and suggest new strategies to enhance remyelination.
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?
Microglia express Transglutaminase 2, which is essential for OPC differentiation.
“Furthermore, microglia express factors like Transglutaminase 2, which is essential for OPCs differentiation (13).”
From Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination (2025) · cites this paper as [13]
The Introduction identifies TG2 as microglia-derived and reports that deleting it reduces OPC division and the number of mature oligodendrocytes. The Discussion says the study supports a role in OPC proliferation, while a possible role in OPC differentiation remains for future investigation. Thus, the claim that TG2 is essential for differentiation is not established. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAdgrg1 (Gpr56) is conserved in human, mouse, and zebrafish and is associated with development of oligodendrocytes.
“Among them is Adgrg1 (Gpr56), demonstrated previously to be conserved in human, mouse, and zebrafish, which is associated with development of oligodendrocytes”
From Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program (2019) · cites this paper as Giera et al., 2018
Microglia have been previously shown to promote remyelination independent of debris clearance.
“Whether this prolonged inflammatory response is beneficial for remyelination remains unclear, but microglia have been previously shown to promote remyelination independent of debris clearance55–57.”
From A comparative transcriptomic analysis of mouse demyelination models and multiple sclerosis lesions (2026) · cites this paper as [55]
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
1 retracted
Bialas, A. R., & Stevens, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3560 · Cited by 519 · see citing works
Self-citationRetractedZhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., Phatnani, H. P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1860-14.2014 · Cited by 4,875 · see citing works
Fate Mapping Reveals Origins and Dynamics of Monocytes and Tissue Macrophages under Homeostasis
Yona, S., Kim, K.-W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2012.12.001 · Cited by 3,245 · see citing works
High-resolution in situ hybridization to whole-mount zebrafish embryos
Thisse, C., & Thisse, B. (2007) · Nature Protocols · doi:10.1038/nprot.2007.514 · Cited by 2,587 · see citing works
M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination
Miron, V. E., Boyd, A., Zhao, J.-W., Yuen, T. J., Ruckh, J. M., Shadrach, J. L., van Wijngaarden, P., Wagers, A. J., Williams, A., Franklin, R. J. M., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3469 · Cited by 1,788 · see citing works
The central nervous system and the gut microbiome
Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016) · Cell · doi:10.1016/j.cell.2016.10.027 · Cited by 1,513 · see citing works
Transglutaminases: crosslinking enzymes with pleiotropic functions
Lorand, L., & Graham, R. M. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1014 · Cited by 1,439 · 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
Myelination of the Nervous System: Mechanisms and Functions
Nave, K., & Werner, H. B. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013101 · Cited by 1,000 · see citing works
Oligodendrocyte Dynamics in the Healthy Adult CNS: Evidence for Myelin Remodeling
Young, K. M., Psachoulia, K., Tripathi, R. B., Dunn, S.-J., Cossell, L., Attwell, D., Tohyama, K., & Richardson, W. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.006 · Cited by 872 · see citing works
Kang, S., Fukaya, M., Yang, J. K., Rothstein, J., & Bergles, D. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.009 · Cited by 778 · see citing works
Myelin Impairs CNS Remyelination by Inhibiting Oligodendrocyte Precursor Cell Differentiation
Kotter, M. R., Li, W.-W., Zhao, C., & Franklin, R. J. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2615-05.2006 · Cited by 768 · see citing works
Regulation of oligodendrocyte differentiation and myelination
Emery, B. (2010) · Science · doi:10.1126/science.1190927 · Cited by 653 · see citing works
Hagemeyer, N., Hanft, K.-M., Akriditou, M.-A., Unger, N., Park, E. S., Stanley, E. R., Staszewski, O., Dimou, L., & Prinz, M. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1747-1 · Cited by 558 · see citing works
Transglutaminase 2: an enigmatic enzyme with diverse functions
Fésüs, L., & Piacentini, M. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(02)02182-5 · Cited by 556 · see citing works
G h : a GTP-Binding Protein with Transglutaminase Activity and Receptor Signaling Function
Nakaoka, H., Perez, D. M., Baek, K. J., Das, T., Husain, A., Misono, K. S., Im, M.-J., & Graham, R. M. (1994) · Science · doi:10.1126/science.7911253 · Cited by 547 · see citing works
A novel microglial subset plays a key role in myelinogenesis in developing brain
Wlodarczyk, A., Holtman, I. R., Krueger, M., Yogev, N., Bruttger, J., Khorooshi, R., Benmamar‐Badel, A., de Boer‐Bergsma, J. J., Martin, N. A., Karram, K., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201696056 · Cited by 535 · see citing works
Dicer1 and miR-219 Are Required for Normal Oligodendrocyte Differentiation and Myelination
Dugas, J. C., Cuellar, T. L., Scholze, A., Ason, B., Ibrahim, A., Emery, B., Zamanian, J. L., Foo, L. C., McManus, M. T., & Barres, B. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.027 · Cited by 527 · see citing works
G Protein-Coupled Receptor-Dependent Development of Human Frontal Cortex
Piao, X., Hill, R. S., Bodell, A., Chang, B. S., Basel-Vanagaite, L., Straussberg, R., Dobyns, W. B., Qasrawi, B., Winter, R. M., Innes, A. M., et al. (2004) · Science · doi:10.1126/science.1092780 · Cited by 517 · see citing works
Self-citationMicroglia Enhance Neurogenesis and Oligodendrogenesis in the Early Postnatal Subventricular Zone
Shigemoto‐Mogami, Y., Hoshikawa, K., Goldman, J. E., Sekino, Y., & Sato, K. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1619-13.2014 · Cited by 499 · see citing works
International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G Protein–Coupled Receptors
Hamann, J., Aust, G., Araç, D., Engel, F. B., Formstone, C. J., Fredriksson, R., Hall, R. A., Harty, B. L., Kirchhoff, C., Knapp, B., et al. (2015) · Pharmacological Reviews · doi:10.1124/pr.114.009647 · Cited by 489 · see citing works
Self-citationTransglutaminase 2 Undergoes a Large Conformational Change upon Activation
Pinkas, D. M., Strop, P., Brünger, A. T., & Khosla, C. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050327 · Cited by 452 · see citing works
Chen, Y., Wu, H., Wang, S., Koito, H., Li, J., Ye, F., Hoang, J., Escobar, S. S., Gow, A., Arnett, H. A., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2410 · Cited by 346 · see citing works
Gene Disruption of Tissue Transglutaminase
Laurenzi, V. D., & Melino, G. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.1.148-155.2001 · Cited by 338 · see citing works
erbb3 and erbb2 Are Essential for Schwann Cell Migration and Myelination in Zebrafish
Lyons, D. A., Pogoda, H., Voas, M. G., Woods, I. G., Diamond, B., Nix, R., Arana, N., Jacobs, J., & Talbot, W. S. (2005) · Current Biology · doi:10.1016/j.cub.2005.02.030 · Cited by 338 · see citing works
A G Protein–Coupled Receptor Is Essential for Schwann Cells to Initiate Myelination
Monk, K. R., Naylor, S. G., Glenn, T. D., Mercurio, S., Perlin, J. R., Dominguez, C. X., Moens, C. B., & Talbot, W. S. (2009) · Science · doi:10.1126/science.1173474 · Cited by 326 · see citing works
Self-citationFunctional Genomic Analysis of Oligodendrocyte Differentiation
Dugas, J. C., Tai, Y. C., Speed, T. P., Ngai, J., & Barres, B. A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2572-06.2006 · Cited by 324 · see citing works
Roy, K., Murtie, J. C., El-Khodor, B. F., Edgar, N., Sardi, S. P., Hooks, B. M., Benoit-Marand, M., Chen, C., Moore, H., O'Donnell, P., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702157104 · Cited by 319 · see citing works
Watkins, T. A., Emery, B., Mulinyawe, S. B., & Barres, B. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.011 · Cited by 317 · see citing works
Targeted Inactivation of Gh/Tissue Transglutaminase II
Nanda, N., Iismaa, S. E., Owens, W. A., Husain, A., Mackay, F., & Graham, R. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010846200 · Cited by 292 · see citing works
Luo, R., Jeong, S.-J., Jin, Z., Strokes, N., Li, S., & Piao, X. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104821108 · Cited by 290 · see citing works
Self-citationPetersen, S. C., Luo, R., Liebscher, I., Giera, S., Jeong, S., Mogha, A., Ghidinelli, M., Feltri, M. L., Schöneberg, T., Piao, X., et al. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.057 · Cited by 283 · see citing works
Self-citationXu, L., Begum, S., Hearn, J., & Hynes, R. O. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602681103 · Cited by 278 · see citing works
Remyelination in Experimental Models of Toxin-Induced Demyelination
Blakemore, W. F., & Franklin, R. J. M. (2008) · Current Topics in Microbiology and Immunology · doi:10.1007/978-3-540-73677-6_8 · Cited by 275 · see citing works
Sticky Signaling—Adhesion Class G Protein–Coupled Receptors Take the Stage
Langenhan, T., Aust, G., & Hamann, J. (2013) · Science Signaling · doi:10.1126/scisignal.2003825 · Cited by 263 · see citing works
A Role for the Helix-Loop-Helix Protein Id2 in the Control of Oligodendrocyte Development
Wang, S., Sdrulla, A. D., Johnson, J. E. B., Yokota, Y., & Barres, B. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00237-9 · Cited by 261 · see citing works
Mechanisms regulating the development of oligodendrocytes and central nervous system myelin.
Mitew, S., Hay, C., Peckham, H., Xiao, J., Koenning, M., & Emery, B. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.11.029 · Cited by 259 · see citing works
CNS integrins switch growth factor signalling to promote target-dependent survival
Colognato, H., Baron, W., Avellana‐Adalid, V., Relvas, J. B., Evercooren, A. B., Georges‐Labouesse, E., & ffrench‐Constant, C. (2002) · Nature Cell Biology · doi:10.1038/ncb865 · Cited by 246 · see citing works
GPR56 Regulates Pial Basement Membrane Integrity and Cortical Lamination
Li, S., Jin, Z., Koirala, S., Bu, L., Xu, L., Hynes, R. O., Walsh, C. A., Corfas, G., & Piao, X. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.0853-08.2008 · Cited by 241 · see citing works
Self-citationIsolation of murine microglial cells for RNA analysis or flow cytometry
Cardona, A. E., Huang, D., Sasse, M. E., & Ransohoff, R. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.327 · Cited by 236 · see citing works
Lysolecithin induces demyelination in vitro in a cerebellar slice culture system
Birgbauer, E., Rao, T. S., & Webb, M. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20248 · Cited by 190 · see citing works
The Adhesion GPCR Latrophilin/CIRL Shapes Mechanosensation
Scholz, N., Gehring, J., Guan, C., Ljaschenko, D., Fischer, R., Lakshmanan, V., Kittel, R. J., & Langenhan, T. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.04.008 · Cited by 189 · see citing works
Extracellular TG2: emerging functions and regulation
Belkin, A. M. (2011) · FEBS Journal · doi:10.1111/j.1742-4658.2011.08346.x · Cited by 184 · see citing works
The N Terminus of the Adhesion G Protein-coupled Receptor GPR56 Controls Receptor Signaling Activity
Paavola, K. J., Stephenson, J. R., Ritter, S. L., Alter, S. P., & Hall, R. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.247973 · Cited by 184 · see citing works
Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development
Colognato, H., Ramachandrappa, S., Olsen, I. M. L., & ffrench‐Constant, C. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200404076 · Cited by 177 · see citing works
Genotype–phenotype analysis of human frontoparietal polymicrogyria syndromes
Piao, X., Chang, B. S., Bodell, A., Woods, K., Ben‐Zeev, B., Topçu, M., Guerrini, R., Goldberg‐Stern, H., Sztriha, L., Dobyns, W. B., et al. (2005) · Annals of Neurology · doi:10.1002/ana.20616 · Cited by 151 · see citing works
Self-citationThe adhesion GPCR Gpr56 regulates oligodendrocyte development via interactions with Gα12/13 and RhoA
Ackerman, S. D., Garcia, C. M., Piao, X., Gutmann, D. H., & Monk, K. R. (2015) · Nature Communications · doi:10.1038/ncomms7122 · Cited by 149 · see citing works
Self-citationGlial Cell Development and Function in ZebrafishPreprint
Lyons, D. A., & Talbot, W. S. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020586 · Cited by 143 · see citing works
Giera, S., Deng, Y., Luo, R., Ackerman, S. D., Mogha, A., Monk, K. R., Ying, Y., Jeong, S., Makinodan, M., Bialas, A. R., et al. (2015) · Nature Communications · doi:10.1038/ncomms7121 · Cited by 141 · see citing works
Self-citationMechanical Environment Modulates Biological Properties of Oligodendrocyte Progenitor Cells
Jagielska, A., Norman, A. L., Whyte, G., Vliet, K. J. V., Guck, J. R., & Franklin, R. J. M. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0189 · Cited by 128 · see citing works
Structural Basis for Regulation of GPR56/ADGRG1 by Its Alternatively Spliced Extracellular Domains
Salzman, G., Ackerman, S. D., Ding, C., Koide, A., Leon, K., Luo, R., Stoveken, H. M., Fernandez, C., Tall, G. G., Piao, X., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.022 · Cited by 128 · see citing works
Self-citationRho GTPases as regulators of mitosis and cytokinesis in mammalian cells
Chircop, M. (2014) · Small GTPases · doi:10.4161/sgtp.29770 · Cited by 125 · see citing works
Clemente, D., Ortega, M. C., Melero‐Jerez, C., & de Castro, F. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00268 · Cited by 122 · see citing works
Myelinating glia differentiation is regulated by extracellular matrix elasticity
Urbanski, M. M., Kingsbury, L., Moussouros, D., Kassim, I., Mehjabeen, S., Paknejad, N., & Melendez‐Vasquez, C. V. (2016) · Scientific Reports · doi:10.1038/srep33751 · Cited by 120 · see citing works
Adhesion G protein-coupled receptors in nervous system development and disease
Langenhan, T., Piao, X., & Monk, K. R. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.86 · Cited by 115 · see citing works
Self-citationColognato, H., Galvin, J. W., Wang, Z., Relucio, J. L. V., Nguyen, T., Harrison, D., Yurchenco, P. D., & ffrench‐Constant, C. (2007) · Development · doi:10.1242/dev.02819 · Cited by 108 · see citing works
O’Meara, R. W., Ryan, S. D., Colognato, H., & Kothary, R. (2011) · Journal of Visualized Experiments · doi:10.3791/3324 · Cited by 103 · see citing works
Aeschlimann, D. P., Paulsson, M., & Mann, K. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)49912-2 · Cited by 100 · see citing works
Stacey, M. A., Chang, G.-W., Sanos, S. L., Chittenden, L. R., Stubbs, L. J., Gordon, S., & Lin, H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204306200 · Cited by 99 · see citing works
Jablonska, B., Aguirre, A. A., Vandenbosch, R., Belachew, S. M., Berthet, C., Kaldis, P., & Gallo, V. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200702031 · Cited by 92 · see citing works
Glia unglued: How signals from the extracellular matrix regulate the development of myelinating glia
Colognato, H., & Tzvetanova, I. D. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20966 · Cited by 90 · see citing works
Zebrafish as a model to investigate CNS myelination
Preston, M., & Macklin, W. B. (2014) · Glia · doi:10.1002/glia.22755 · Cited by 89 · see citing works
Relucio, J. L. V., Menezes, M. J., Miyagoe‐Suzuki, Y., Takeda, S., & Colognato, H. (2012) · Glia · doi:10.1002/glia.22365 · Cited by 87 · see citing works
The cell biology of CNS myelination
Hughes, E. G., & Appel, B. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.013 · Cited by 84 · see citing works
Extracellular cues influencing oligodendrocyte differentiation and (re)myelination
Wheeler, N. A., & Fuss, B. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.03.019 · Cited by 78 · see citing works
Dihydromunduletone Is a Small-Molecule Selective Adhesion G Protein–Coupled Receptor Antagonist
Stoveken, H. M., Bahr, L. L., Anders, M. W., Wojtovich, A. P., Smrcka, A. V., & Tall, G. G. (2016) · Molecular Pharmacology · doi:10.1124/mol.116.104828 · Cited by 69 · see citing works
Self-citationGPR56/ADGRG1 regulates development and maintenance of peripheral myelin
Ackerman, S. D., Luo, R., Poitelon, Y., Mogha, A., Harty, B. L., D’Rozario, M., Sanchez, N., Lakkaraju, A. K., Gamble, P. G., Li, J., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20161714 · Cited by 68 · see citing works
Self-citationThe scales and tales of myelination: using zebrafish and mouse to study myelinating glia
Ackerman, S. D., & Monk, K. R. (2015) · Brain Research · doi:10.1016/j.brainres.2015.10.011 · Cited by 65 · see citing works
Self-citationFibronectin as a carrier for the transglutaminase from human erythrocytes.
Lorand, L., Dailey, J. E., & Turner, P. M. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.4.1057 · Cited by 65 · see citing works
Belachew, S. M., Aguirre, A. A., Wang, H., Vautier, F., Yuan, X. Q., Anderson, S. M., Kirby, M., & Gallo, V. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-19-08553.2002 · Cited by 63 · see citing works
Hammond, T. R., Mcellin, B. M., Morton, P. D., Raymond, M., Dupree, J. L., & Gallo, V. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.11.002 · Cited by 61 · see citing works
Shin, D., Lin, S., Fu, Y., & Ptáček, L. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318501110 · Cited by 61 · see citing works
Role of tissue transglutaminase-2 (TG2)-mediated aminylation in biological processes
Lai, T., Lin, C., & Greenberg, C. S. (2016) · Amino Acids · doi:10.1007/s00726-016-2270-8 · Cited by 54 · see citing works
Jeong, S., Luo, R., Li, S., Strokes, N., & Piao, X. (2012) · Journal of Comparative Neurology · doi:10.1002/cne.23076 · Cited by 36 · see citing works
Self-citationThe environment rules: spatiotemporal regulation of oligodendrocyte differentiation
Mayoral, S. R., & Chan, J. R. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.002 · Cited by 35 · see citing works
van Strien, M. E., Baron, W., Bakker, E. N. T. P., Bauer, J., Bol, J. G. J. M., Brevé, J. J. P., Binnekade, R., van der Laarse, W. J., Drukarch, B., & van Dam, A. (2011) · Glia · doi:10.1002/glia.21204 · Cited by 29 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cross-Species Single-Cell Analysis Reveals Divergence of the Primate Microglia Program
Geirsdottir, L., David, E., Keren-Shaul, H., Weiner, A., Bohlen, S. C., Neuber, J., Balic, A., Giladi, A., Sheban, F., Dutertre, C.-A., et al. (2019) · Cell · doi:10.1016/j.cell.2019.11.010 · Cited by 461 · see citing works
Treg cell-derived osteopontin promotes microglia-mediated white matter repair after ischemic stroke
Shi, L., Sun, Z., Su, W., Xu, F., Xie, D., Zhang, Q. C., Dai, X., Iyer, K., Hitchens, T. K., Foley, L. M., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.04.022 · Cited by 430 · see citing works
Immune cell regulation of glia during CNS injury and disease
Greenhalgh, A. D., David, S., & Bennett, F. C. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0263-9 · Cited by 398 · see citing works
The pro-remyelination properties of microglia in the central nervous system
Lloyd, A. F., & Miron, V. E. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0184-2 · Cited by 381 · see citing works
Microglia phagocytose myelin sheaths to modify developmental myelination
Hughes, A. N., & Appel, B. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0654-2 · Cited by 344 · see citing works
The benefits of neuroinflammation for the repair of the injured central nervous system
Yong, H. Y. F., Rawji, K. S., Ghorbani, S., Xue, M., & Yong, V. W. (2019) · Cellular & Molecular Immunology · doi:10.1038/s41423-019-0223-3 · Cited by 190 · see citing works
Mechanisms of adhesion G protein–coupled receptor activation
Vizurraga, A., Adhikari, R., Yeung, J., Yu, M., & Tall, G. G. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.007423 · Cited by 179 · see citing works
Self-citationA splicing isoform of GPR56 mediates microglial synaptic refinement via phosphatidylserine binding
Li, T., Chiou, B., Gilman, C. K., Luo, R., Koshi, T., Yu, D., Oak, H. C., Giera, S., Johnson‐Venkatesh, E., Muthukumar, A. K., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019104136 · Cited by 177 · see citing works
Self-citationRegulation of myelination by microglia
Santos, E. N., & Fields, R. D. (2021) · Science Advances · doi:10.1126/sciadv.abk1131 · Cited by 137 · see citing works
Roles and regulation of microglia activity in multiple sclerosis: insights from animal models
Distéfano‐Gagné, F., Bitarafan, S., Lacroix, S., & Gosselin, D. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00709-6 · Cited by 112 · see citing works
Microglia in the developing retina
Li, F., Jiang, D., & Samuel, M. A. (2019) · Neural Development · doi:10.1186/s13064-019-0137-x · Cited by 109 · see citing works
GPR56/ADGRG1 is a platelet collagen-responsive GPCR and hemostatic sensor of shear force
Yeung, J., Adili, R., Stringham, E. N., Luo, R., Vizurraga, A., Rosselli‐Murai, L. K., Stoveken, H. M., Yu, M., Piao, X., Holinstat, M. A., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2008921117 · Cited by 106 · see citing works
Self-citationPremyelinating Oligodendrocytes: Mechanisms Underlying Cell Survival and Integration
Hughes, E. G., & Stockton, M. E. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.714169 · Cited by 98 · see citing works
Microglia‐dependent remodeling of neuronal circuits
Guedes, J. R., Ferreira, P. A., Costa, J. M., Cardoso, A. L., & Peça, J. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15689 · Cited by 93 · see citing works
The emerging tale of microglia in psychiatric disorders
Rahimian, R., Wakid, M., O’Leary, L. A., & Mechawar, N. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.023 · Cited by 91 · see citing works
Adhesion G protein-coupled receptors: opportunities for drug discovery
Bassilana, F., Nash, M., & Ludwig, M. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0039-y · Cited by 88 · see citing works
Pepper, R., Pitman, K. A., Cullen, C. L., & Young, K. M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00399 · Cited by 82 · see citing works
Myelination generates aberrant ultrastructure that is resolved by microglia
Djannatian, M., Radha, S., Weikert, U., Safaiyan, S., Wrede, C., Deichsel, C., Kislinger, G., Rhomberg, A., Ruhwedel, T., Campbell, D. S., et al. (2022) · The Journal of Cell Biology · doi:10.1083/jcb.202204010 · Cited by 81 · see citing works
Central Nervous System Remyelination: Roles of Glia and Innate Immune Cells
Baaklini, C. S., Rawji, K. S., Duncan, G. J., Ho, M. F. S., & Plemel, J. R. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00225 · Cited by 80 · see citing works
Microglia and Wnt Pathways: Prospects for Inflammation in Alzheimer’s Disease
Yang, Y., & Zhang, Z. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00110 · Cited by 76 · see citing works
Adhesion G protein-coupled receptors: structure, signaling, physiology, and pathophysiology
Lala, T., & Hall, R. A. (2022) · Physiological Reviews · doi:10.1152/physrev.00027.2021 · Cited by 79 · see citing works
Microglia promote remyelination independent of their role in clearing myelin debris
Baaklini, C. S., Ho, M. F. S., Lange, T., Hammond, B. P., Panda, S. P., Zirngibl, M., Zia, S., Himmelsbach, K., Rana, H., Phillips, B., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113574 · Cited by 73 · see citing works
Adhesion G Protein-Coupled Receptors as Drug Targets for Neurological Diseases
Folts, C. J., Giera, S., Li, T., & Piao, X. (2019) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2019.02.003 · Cited by 70 · see citing works
Self-citationLigands and Beyond: Mechanosensitive Adhesion GPCRs
Lin, H., Ng, K., Chen, T., & Tseng, W.-Y. (2022) · Pharmaceuticals · doi:10.3390/ph15020219 · Cited by 69 · see citing works
Orphan G Protein Coupled Receptors in Affective Disorders
Watkins, L. R., & Orlandi, C. (2020) · Genes · doi:10.3390/genes11060694 · Cited by 67 · see citing works
GPR56/ADGRG1 is associated with response to antidepressant treatment
Belzeaux-R, R., Gorgievski, V., Fiori, L. M., López, J. P., Grenier, J., Lin, R., Nagy, C., Ibrahim, E. C., Gascon, E., Courtet, P., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15423-5 · Cited by 65 · see citing works
Self-citationZhu, B., Luo, R., Jin, P., Li, T., Oak, H. C., Giera, S., Monk, K. R., Lak, P., Shoichet, B. K., & Piao, X. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.008234 · Cited by 62 · see citing works
Self-citationThe role of GPR56/ADGRG1 in health and disease
Singh, A. K., & Lin, H. (2021) · Biomedical Journal · doi:10.1016/j.bj.2021.04.012 · Cited by 60 · see citing works
Yu, D., Li, T., Delpech, J.-C., Zhu, B., Kishore, P., Koshi, T., Luo, R., Pratt, K. J. B., Popova, G., Nowakowski, T. J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm2545 · Cited by 58 · see citing works
Self-citationGlial Cells Promote Myelin Formation and Elimination
Hughes, A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.661486 · Cited by 58 · see citing works
Microglia as therapeutic target in central nervous system disorders
Fatoba, O., Itokazu, T., & Yamashita, T. (2020) · Journal of Pharmacological Sciences · doi:10.1016/j.jphs.2020.07.004 · Cited by 56 · see citing works
Microglia regulate GABAergic neurogenesis in prenatal human brain through IGF1
Yu, D., Jain, S., Wangzhou, A., Zhu, B., Shao, W., Coley, E. J. L., Florencio, S. L. D., Kim, J. Y., Choi, J. J.-Y., Paredes, M. F., et al. (2025) · Nature · doi:10.1038/s41586-025-09362-8 · Cited by 46 · see citing works
Self-citationGlia-Driven Brain Circuit Refinement Is Altered by Early-Life Adversity: Behavioral Outcomes
Milbocker, K. A., Campbell, T. S., Collins, N. J., Kim, S., Smith, E. A., Roth, T. L., & Klintsova, A. Y. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.786234 · Cited by 40 · see citing works
Irfan, M., Evonuk, K. S., & DeSilva, T. M. (2022) · The FEBS Journal · doi:10.1111/febs.16190 · Cited by 39 · see citing works
Raffaele, S., & Fumagalli, M. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.950819 · Cited by 38 · see citing works
A role for microglia in mediating the microbiota–gut–brain axis
Keane, L., Clarke, G. A., & Cryan, J. F. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-025-01188-9 · Cited by 37 · see citing works
Replenishing the Aged Brains: Targeting Oligodendrocytes and Myelination?
Zhang, X., Huang, N., Xiao, L., Wang, F., & Li, T. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.760200 · Cited by 31 · see citing works
Regulators of Oligodendrocyte DifferentiationPreprint
Emery, B., & Wood, T. L. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041358 · Cited by 35 · see citing works
Role of ADGRG1/GPR56 in Tumor Progression
Ng, K., Chen, T., Stacey, M. A., & Lin, H. (2021) · Cells · doi:10.3390/cells10123352 · Cited by 33 · see citing works
Szondy, Z., Al‐Zaeed, N., Tarban, N., Fige, É., Garabuczi, É., & Sarang, Z. (2022) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13024 · Cited by 33 · see citing works
Differential Modulators of NG2-Glia Differentiation into Neurons and Glia and Their Crosstalk
Du, X., Zhang, Z., Zhou, H., & Zhou, J. (2020) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-020-00843-0 · Cited by 32 · see citing works
Kordon, S. P., Dutka, P., Adamska, J. M., Bandekar, S. J., Leon, K., Erramilli, S. K., Adams, B., Li, J., Kossiakoff, A. A., & Araç, D. (2023) · Nature Communications · doi:10.1038/s41467-023-36312-7 · Cited by 31 · see citing works
GPR56: An adhesion GPCR involved in brain development, neurological disorders and cancer
Ganesh, R. A., Venkataraman, K., & Sirdeshmukh, R. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147055 · Cited by 31 · see citing works
The central role of microglia in major depressive disorder and its potential as a therapeutic target
Xia, X., Li, K., Zou, W., & Wang, L. (2025) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2025.1598178 · Cited by 30 · see citing works
Microglia as therapeutic targets for central nervous system remyelination
Mahmood, A., & Miron, V. E. (2022) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2022.102188 · Cited by 28 · see citing works
Targeting microglia-oligodendrocyte crosstalk in neurodegenerative and psychiatric disorders.
Rahimian, R., Perlman, K., Canonne, C., & Mechawar, N. (2022) · Drug Discovery Today · doi:10.1016/j.drudis.2022.06.015 · Cited by 26 · see citing works
Transglutaminases in Monocytes and Macrophages
Sun, H., & Kaartinen, M. T. (2018) · Medical Sciences · doi:10.3390/medsci6040115 · Cited by 29 · see citing works
Alavi, M. S., Karimi, G., & Roohbakhsh, A. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.03.045 · Cited by 29 · see citing works
Chiou, B., Gao, C., Giera, S., Folts, C. J., Kishore, P., Yu, D., Oak, H. C., Jiang, R., & Piao, X. (2020) · Glia · doi:10.1002/glia.23906 · Cited by 26 · see citing works
Self-citationA Glance at the Molecules That Regulate Oligodendrocyte Myelination
Wang, S.-Q., Wang, Y.-X., & Zou, S.-Q. (2022) · Current Issues in Molecular Biology · doi:10.3390/cimb44050149 · Cited by 23 · see citing works
Making tracks: microglia and the extracellular matrix
Wareham, L. K., & Calkins, D. J. (2025) · Molecular Neurodegeneration · doi:10.1186/s13024-025-00898-x · Cited by 31 · see citing works
Hu, X., Geng, P., Zhao, X., Wang, Q., Liu, C., Guo, C., Dong, W., & Jin, X. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106076 · Cited by 25 · see citing works
Cauley, E. S., Hamed, A. A., Mohamed, I. N., Elseed, M. A., Martinez, S., Yahia, A., Abozar, F., Abubakr, R., Koko, M., Elsayed, L. E. O., et al. (2019) · Neurogenetics · doi:10.1007/s10048-019-00577-2 · Cited by 25 · see citing works
Self-citationPerera, S. N., Williams, R. M., Lyne, R., Stubbs, O., Buehler, D. P., Sauka‐Spengler, T., Noda, M., Micklem, G., Southard‐Smith, E. M., & Baker, C. V. H. (2020) · Glia · doi:10.1002/glia.23870 · Cited by 23 · see citing works
Zhi-qiang, L., Wang, T., Du, S., Miao, Z., Zhao, Y., Tang, Y., Meng, X., Yu, S., Zhang, D., Jiang, H., et al. (2025) · Aging Cell · doi:10.1111/acel.14463 · Cited by 22 · see citing works
Gorina, Y. V., Salmina, A. B., Erofeev, A. I., Gerasimov, E., Bolshakova, A. V., Balaban, P. M., Борисович, Б. И., & Власова, О. Л. (2022) · Biochemistry (Moscow) · doi:10.1134/s0006297922090012 · Cited by 21 · see citing works
NG2 ‐glia crosstalk with microglia in health and disease
Zhang, Z., Li, X., Zhou, H., & Zhou, J. (2022) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13948 · Cited by 20 · see citing works
Acute TREM2 inhibition depletes MAFB-high microglia and hinders remyelination
Hou, J., Magliozzi, R., Chen, Y., Wu, J., Wulf, J., Strout, G., Fang, X., & Colonna, M. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2426786122 · Cited by 20 · see citing works
“Furthermore, microglia express factors like Transglutaminase 2, which is essential for OPCs differentiation ( 13 ).”
Functions of G protein‐coupled receptor 56 in health and disease
Su, T., Guan, Q., Cheng, H., Zhu, Z., Jiang, C., Guo, P., Tai, Y., Sun, H., Wang, M., Wei, W., et al. (2022) · Acta Physiologica · doi:10.1111/apha.13866 · Cited by 20 · see citing works
The expanding functional roles and signaling mechanisms of adhesion G protein–coupled receptors
Morgan, R. K., Anderson, G. R., Araç, D., Aust, G., Balenga, N. A. B., Boucard, A. A., Bridges, J. P., Engel, F. B., Formstone, C. J., Glitsch, M. D., et al. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14094 · Cited by 20 · see citing works
Self-citationRudlong, J., Cheng, A., & Johnson, G. V. W. (2019) · Analytical Biochemistry · doi:10.1016/j.ab.2019.113556 · Cited by 20 · see citing works
Salzman, G., Zhang, S., Fernandez, C., Araç, D., & Koide, S. (2020) · Scientific Reports · doi:10.1038/s41598-020-74044-6 · Cited by 20 · see citing works
Liu, J., & Mouradian, M. M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042364 · Cited by 20 · see citing works
Long-term microglia depletion impairs synapse elimination and auditory brainstem function
Chokr, S. M., Milinkeviciute, G., Jimenez, G. A., Abubakr, H., & Cramer, K. S. (2022) · Scientific Reports · doi:10.1038/s41598-022-23250-5 · Cited by 20 · see citing works
Role of Adhesion G Protein-Coupled Receptors in Immune Dysfunction and Disorder
Tseng, W.-Y., Stacey, M. A., & Lin, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065499 · Cited by 19 · see citing works
The Role of Microglia in Inherited White-Matter Disorders and Connections to Frontotemporal Dementia
Sirkis, D. W., Bonham, L. W., & Yokoyama, J. S. (2021) · The Application of Clinical Genetics · doi:10.2147/tacg.s245029 · Cited by 18 · see citing works
Role of Microglia in Central Nervous System Development and PlasticityPreprint
Schafer, D. P., Stevens, B., Bennett, M. L., & Bennett, F. C. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041810 · Cited by 19 · see citing works
Self-citationZhang, N., Zhang, S., Liu, X., Zuo, Y., Cui, Y., Wang, F., Zhang, J.-H., Chang, Y., & Yu, P. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2025.06.055 · Cited by 17 · see citing works
Liu, C., Gao, X., Shi, R., Wang, Y., He, X., Du, H., Hu, B., Jiao, J., Liu, C., & Teng, Z. (2023) · Cell Proliferation · doi:10.1111/cpr.13439 · Cited by 16 · see citing works
Recognizing Alzheimer's disease from perspective of oligodendrocytes: Phenomena or pathogenesis?
Wang, J., Zhen, Y., Yang, J., Yang, S., & Zhu, G. (2024) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14688 · Cited by 16 · see citing works
Tissue Transglutaminase Promotes Early Differentiation of Oligodendrocyte Progenitor Cells
Pinzón, N. E., van Mierlo, H., de Jonge, J. C., Brevé, J. J. P., Bol, J. G. J. M., Drukarch, B., van Dam, A., & Baron, W. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00281 · Cited by 17 · see citing works
Olaniru, O. E., Cheng, J., Ast, J., Arvaniti, A., Atanes, P., Huang, G. C., King, A., Jones, P. M., Broichhagen, J., Hodson, D. J., et al. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101285 · Cited by 16 · see citing works
Ganesh, R. A., Sonpatki, P., Naik, D., John, A. E., Sathe, G. J., Lakshmikantha, A., Chandrachari, K. P., Bauer, L., Knäuper, V., Aeschlimann, D. P., et al. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.841890 · Cited by 14 · see citing works
Microglial responses to CSF1 overexpression do not promote the expansion of other glial lineages
De, I., Maklakova, V. I., Litscher, S. J., Boyd, M. M., Klemm, L. C., Wang, Z., Kendziorski, C. M., & Collier, L. S. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02212-0 · Cited by 14 · see citing works
Basso, M., & Milelli, A. (2019) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000753 · Cited by 13 · see citing works
Exploring the Role of Transglutaminase in Patients with Glioblastoma: Current Perspectives
Katt, W. P., Aplin, C., & Cerione, R. A. (2022) · OncoTargets and Therapy · doi:10.2147/ott.s329262 · Cited by 12 · see citing works
Toro, C. A., Hansen, J., Siddiq, M. M., Johnson, K., Zhao, W., Azulai, D., Das, D. K., Bauman, W. A., Sebra, R., Cai, D., et al. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.626192 · Cited by 12 · see citing works
Adhesion G protein-coupled receptors
Langenhan, T., Anderson, G. R., Araç, D., Aust, G., Avila-Zozaya, M., Bagger, S. M., Barth, P., Berndt, S., Blacklow, S. C., Blanco-Redondo, B., et al. (2026) · Pharmacological Reviews · doi:10.1016/j.pharmr.2026.100116 · Cited by 13 · see citing works
Self-citationVizurraga, A., Robertson, M. J., Yu, M., Skiniotis, G., & Tall, G. G. (2023) · Molecular Pharmacology · doi:10.1124/molpharm.123.000688 · Cited by 11 · see citing works
Self-citationMilinkeviciute, G., Chokr, S. M., & Cramer, K. S. (2021) · eNeuro · doi:10.1523/eneuro.0318-20.2021 · Cited by 11 · see citing works
Pearse, D. D., Hefley, A. B., Morales, A. A., & Ghosh, M. (2022) · Biomedicines · doi:10.3390/biomedicines10061241 · Cited by 11 · see citing works
Gene Expression Profiling in Huntington’s Disease: Does Comorbidity with Depressive Symptoms Matter?
Colpo, G. D., Rocha, N. P., Furr-Stimming, E. E., & Teixeira, A. L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228474 · Cited by 11 · see citing works
Research progress of neurovascular units involved in ischemic stroke
Yang, Y., Tong, H., Ye, Z., Xu, Z., & Tao, T. (2024) · Ibrain · doi:10.1002/ibra.12166 · Cited by 10 · see citing works
GPR56: A potential therapeutic target for neurological and psychiatric disorders
Qi, W., & Guan, W. (2024) · Biochemical Pharmacology · doi:10.1016/j.bcp.2024.116395 · Cited by 10 · see citing works
Glia–glia crosstalk via semaphorins: Emerging implications in neurodegeneration
Palazzo, C., Nutarelli, S., Mastrantonio, R., Tamagnone, L., & Viscomi, M. T. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102618 · Cited by 11 · see citing works
Sobierajski, E., Lauer, G., Aktas, M., Beemelmans, C., Beemelmans, C., Meyer, G., & Wahle, P. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25280 · Cited by 10 · see citing works
GPR56 S4 variant is required for microglia‐mediated synaptic pruning
Li, T., Luo, R., Schmidt, R., D'Alessandro, N., Kishore, P., Zhu, B., Yu, D., & Piao, X. (2022) · Glia · doi:10.1002/glia.24293 · Cited by 10 · see citing works
Self-citationOhtomo, R., & Arai, K. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134650 · Cited by 9 · see citing works
Suzzi, S., Ahrendt, R., Hans, S., Semenova, S. A., Chekuru, A., Wirsching, P., Kroehne, V., Bilican, S., Sayed, S., Winkler, S., et al. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009794 · Cited by 9 · see citing works
Sha, Z., Dong, S., Nie, M., Liu, T., Wu, C., Lv, C., Liu, M., Jiang, W., Yuan, J., Yu, Q., et al. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-07501-7 · Cited by 8 · see citing works
Self-citationMicroglia and Myeloid Cell Populations of the Developing Mouse Retina
Martineau, S., Valdez‐Lopez, J. C., Zarnick, S., & Kay, J. N. (2025) · Glia · doi:10.1002/glia.70115 · Cited by 11 · see citing works
Emerging non-proinflammatory roles of microglia in healthy and diseased brains
Sun, Y., Che, J., & Zhang, J. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.110664 · Cited by 8 · see citing works
Syage, A. R., Pachow, C., Murray, K. M., Henningfield, C. M., Fernandez, K., Du, A. X., Cheng, Y., Olivarria, G. M., Kawauchi, S., MacGregor, G. R., et al. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03153-0 · Cited by 7 · see citing works
Translating Molecular Approaches to Oligodendrocyte-Mediated Neurological Circuit Modulation
Song, J., Saglam, A., Zuchero, J. B., & Buch, V. (2024) · Brain Sciences · doi:10.3390/brainsci14070648 · Cited by 7 · see citing works
DeVries, S. A., Dimovasili, C., Medalla, M., Moore, T. L., & Rosene, D. L. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1426975 · Cited by 7 · see citing works
Zhang, W., Li, S., Yun, H. J., Yu, W., Shi, W., Chen, G., Xu, J., Yang, Y., Qin, L., Ding, Y., et al. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14346 · Cited by 7 · see citing works
Huang, H., Kuang, Y., Chen, Y., Zhang, Y., Zhou, J., Yu, X., Zheng, Y., Cai, L., Hu, W., Gao, L., et al. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03483-7 · Cited by 6 · see citing works
GPR56, an Adhesion GPCR with Multiple Roles in Human Diseases, Current Status and Future Perspective
Fan, Y., Yan, X., & Guan, W. (2024) · Current Drug Targets · doi:10.2174/0113894501298344240507080149 · Cited by 6 · see citing works
Tan, Z., Xia, R., Zhao, X., Yang, Z., Liu, H., & Wang, W. (2024) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2024.103980 · Cited by 7 · see citing works
Nimodipine Exerts Beneficial Effects on the Rat Oligodendrocyte Cell Line OLN-93
Boltz, F., Enders, M., Feigenspan, A., Kirchner, P., Ekici, A. B., & Küerten, S. (2022) · Brain Sciences · doi:10.3390/brainsci12040476 · Cited by 6 · see citing works
- Authors
- Giera, S., Luo, R., Ying, Y., Ackerman, S. D., Jeong, S.-J., Stoveken, H. M., Folts, C. J., Welsh, C. A., Tall, G. G., Stevens, B., Monk, K. R., & Piao, X.
- Affiliations
- Boston Children's Hospital (US)
- University of Oregon (US)
- University of Michigan (US)
- Oregon Health & Science University (US)
- Corresponding author
- Monk, Kelly R
- Piao, Xianhua
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2018-05-29
- Volume
- 7
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5980231
- OpenAlex
- W2805257681
- Cited by
- 145
- References
- 76
- Citations by year
- 2026: 18 · 2025: 18 · 2024: 19 · 2023: 10 · 2022: 20 · 2021: 20 · 2020: 19 · 2019: 17 · 2018: 2
- FWCI
- 5.33
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Neurological Disorders and Stroke (NS085201, NS085201 (R56), NS087801, NS079445)
- National Multiple Sclerosis Society (FG 2063-A1/2, Harry Weaver Neuroscience Fellowship, RG-1501-02577)
- National Research Foundation of Korea (2015M3C7A1029037)
- Ministry of Science, ICT and Future Planning (KBRI Basic Research program 18-BR-02-02)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- tissue transglutaminase, ADGRG1, GPR56, oligodendrocyte precursor cells, myelination, remyelination, demyelination, laminin, extracellular matrix, microglia, OPC proliferation
- MeSH terms
- Oligodendrocyte Precursor Cells, CX3C Chemokine Receptor 1, Remyelination, Protein Glutamine gamma Glutamyltransferase 2, Animals, Cell Differentiation, Cerebellum, Demyelinating Diseases, Female, Humans, Laminin, Male, Oligodendroglia, Transglutaminases, Signal Transduction, Prosencephalon, Microglia, Mice, Knockout, Gene Expression Regulation, Developmental, Cell Lineage, GTP-Binding Proteins, Receptor, Platelet-Derived Growth Factor alpha, Receptors, G-Protein-Coupled, Mice, Neurogenesis
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