Activated Microglia Desialylate and Phagocytose Cells via Neuraminidase, Galectin-3, and Mer Tyrosine Kinase
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Activated microglia can phagocytose dying, stressed, or excess neurons and synapses via the phagocytic receptor Mer tyrosine kinase (MerTK). Galectin-3 (Gal-3) can cross-link surface glycoproteins by binding galactose residues that are normally hidden below terminal sialic acid residues. Gal-3 was recently reported to opsonize cells via activating MerTK. We found that LPS-activated BV-2 microglia rapidly released Gal-3, which was blocked by calcineurin inhibitors. Gal-3 bound to MerTK on microglia and to stressed PC12 (neuron-like) cells, and it increased microglial phagocytosis of PC12 cells or primary neurons, which was blocked by inhibition of MerTK. LPS-activated microglia exhibited a sialidase activity that desialylated PC12 cells and could be inhibited by Tamiflu, a neuraminidase (sialidase) inhibitor. Sialidase treatment of PC12 cells enabled Gal-3 to bind and opsonize the live cells for phagocytosis by microglia. LPS-induced microglial phagocytosis of PC12 was prevented by small interfering RNA knockdown of Gal-3 in microglia, lactose inhibition of Gal-3 binding, inhibition of neuraminidase with Tamiflu, or inhibition of MerTK by UNC569. LPS-induced phagocytosis of primary neurons by primary microglia was also blocked by inhibition of MerTK. We conclude that activated microglia release Gal-3 and a neuraminidase that desialylates microglial and PC12 surfaces, enabling Gal-3 binding to PC12 cells and their phagocytosis via MerTK. Thus, Gal-3 acts as an opsonin of desialylated surfaces, and inflammatory loss of neurons or synapses may potentially be blocked by inhibiting neuraminidases, Gal-3, or MerTK.
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The absence of ramified microglial cells may stem from BV-2 cells being a transformed microglia cell line with different morphology compared to microglia directly isolated from animals.
“This may stem from the BV-2 cells, a transformed microglia cell line with differed morphology compared to microglia directly isolated from the animals,48 which was reported previously.51–53”
From Acoustofluidic assembly of 3D neurospheroids to model Alzheimer's disease (2020) · cites this paper as [53]
The Materials and methods section (page unavailable) identifies BV-2 as a murine microglial cell line, and the References list its immortalization. The paper does not say that BV-2 cells differ morphologically from microglia isolated from animals or that this explains an absence of ramified cells. (LLM, conf=0.85)
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Towbin, H., Staehelin, T., & Gordon, J. (1979) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.76.9.4350 · Cited by 51,421 · see citing works
Raza, H., John, A., & Nemmar, A. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350087 · Cited by 47,311 · see citing works
Greene, L., & Tischler, A. S. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.7.2424 · Cited by 5,594 · see citing works
Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways
Chung, W.-S., Clarke, L. E., Wang, G. X., Stafford, B. K., Sher, A., Chakraborty, C., Joung, J., Foo, L. C., Thompson, A., Chen, C., et al. (2013) · Nature · doi:10.1038/nature12776 · Cited by 1,377 · see citing works
Phagocytosis and clearance of apoptotic cells is mediated by MER
Scott, R. S., McMahon, E. J., Pop, S. M., Reap, E. A., Caricchio, R., Cohen, P. L., Earp, H. S., & Matsushima, G. K. (2001) · Nature · doi:10.1038/35075603 · Cited by 1,215 · see citing works
Immortalization of murine microglial cells by a v-raf / v-myc carrying retrovirus
Blasi, E., Barluzzi, R., Bocchini, V., Mazzolla, R., & Bistoni, F. (1990) · Journal of Neuroimmunology · doi:10.1016/0165-5728(90)90073-v · Cited by 1,053 · see citing works
Microglial Phagocytosis of Live Neurons
Brown, G. C., & Neher, J. J. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3710 · Cited by 853 · see citing works
Self-citationSecretion of the galectin family of mammalian carbohydrate-binding proteins
Hughes, R. C. (1999) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(99)00177-4 · Cited by 639 · see citing works
Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis
Sierra, A., Abiega, O., Shahraz, A., & Neumann, H. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00006 · Cited by 574 · see citing works
Hirabayashi, J., & Kasai, K.-I. (1993) · Glycobiology · doi:10.1093/glycob/3.4.297 · Cited by 529 · see citing works
Ho, M., & Springer, T. A. (1982) · The Journal of Immunology · doi:10.4049/jimmunol.128.3.1221 · Cited by 427 · see citing works
Liu, F., Hsu, D. K., Zuberi, R. I., Kuwabara, I., Chi, E. Y., & Henderson, W. R. (1995) · Europe PMC (PubMed Central) · Cited by 403 · see citing works
Mammalian sialidases: Physiological and pathological roles in cellular functions
Miyagi, T., & Yamaguchi, K. (2012) · Glycobiology · doi:10.1093/glycob/cws057 · Cited by 395 · see citing works
Inhibition of Microglial Phagocytosis Is Sufficient To Prevent Inflammatory Neuronal Death
Neher, J. J., Neniskyte, U., Zhao, J.-W., Bal-Price, A., Tolkovsky, A. M., & Brown, G. C. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003600 · Cited by 373 · see citing works
Self-citationBurguillos, M. A., Svensson, M., Schulte, T., Boza-Serrano, A., Garcia-Quintanilla, A., Kavanagh, E., Santiago, M., Viceconte, N., Oliva-Martin, M. J., Osman, A. M., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.012 · Cited by 365 · see citing works
Phagocytosis executes delayed neuronal death after focal brain ischemia
Neher, J. J., Emmrich, J., Fricker, M., Mander, P. K., Théry, C., & Brown, G. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308679110 · Cited by 350 · see citing works
Self-citationEaten alive! Cell death by primary phagocytosis: ‘phagoptosis’
Brown, G. C., & Neher, J. J. (2012) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2012.05.002 · Cited by 320 · see citing works
Self-citationBrown, G. C., & Vilalta, A. (2015) · Brain Research · doi:10.1016/j.brainres.2015.08.031 · Cited by 306 · see citing works
Self-citationNeumann, J. H. L., Sauerzweig, S., Rönicke, R., Gunzer, F., Dinkel, K., Ullrich, O., Gunzer, M., & Reymann, K. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0060-08.2008 · Cited by 255 · see citing works
Microglia function during brain development: New insights from animal models
Bilimoria, P. M., & Stevens, B. (2015) · Brain Research · doi:10.1016/j.brainres.2014.11.032 · Cited by 204 · see citing works
Amith, S. R., Jayanth, P., Franchuk, S. L., Finlay, T. M., Seyrantepe, V., Beyaert, R., Pshezhetsky, A. V., & Szewczuk, M. R. (2009) · Cellular Signalling · doi:10.1016/j.cellsig.2009.09.038 · Cited by 194 · see citing works
Galectin-3 is a new MerTK-specific eat-me signal
Caberoy, N. B., Alvarado, G., Bigcas, J., & Li, W. (2012) · Journal of Cellular Physiology · doi:10.1002/jcp.22955 · Cited by 176 · see citing works
Emerging Role of α2,6-Sialic Acid as a Negative Regulator of Galectin Binding and Function
Zhuo, Y., & Bellis, S. L. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.r110.191429 · Cited by 174 · see citing works
Grommes, C., Lee, C. Y. D., Wilkinson, B. L., Jiang, Q., Koenigsknecht-Talboo, J. L., Varnum, B., & Landreth, G. E. (2008) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-007-9090-2 · Cited by 162 · see citing works
Fricker, M., Oliva-Martín, M. J., & Brown, G. C. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-196 · Cited by 153 · see citing works
Self-citationGalectin-3 contributes to neonatal hypoxic–ischemic brain injury
Doverhag, C., Hedtjärn, M., Poirier, F., Mallard, C. E., Hagberg, H., Karlsson, A., & Sävman, K. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.12.024 · Cited by 140 · see citing works
Yip, P. K., Carrillo-Jiménez, A., King, P., Vilalta, A., Nomura, K., Chau, C. C. C., Scott-Egerton, A. M., Liu, Z., Shetty, A. J., Tremoleda, J. L., et al. (2017) · Scientific Reports · doi:10.1038/srep41689 · Cited by 140 · see citing works
Self-citationLinnartz, B., Kopatz, J., Tenner, A. J., & Neumann, H. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3830-11.2012 · Cited by 134 · see citing works
Galectin-3 mediates post-ischemic tissue remodeling
Yan, Y., Lang, B. T., Vemuganti, R., & Dempsey, R. J. (2009) · Brain Research · doi:10.1016/j.brainres.2009.06.073 · Cited by 130 · see citing works
Eat‐me signals: Keys to molecular phagocyte biology and “Appetite” control
Li, W. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22815 · Cited by 117 · see citing works
Rotshenker, S. (2009) · Journal of Molecular Neuroscience · doi:10.1007/s12031-009-9186-7 · Cited by 111 · see citing works
Li, X., Wang, J., Fang, B., Tan, W., & Ma, H. (2014) · Molecular Brain · doi:10.1186/1756-6606-7-28 · Cited by 102 · see citing works
Claude, J., Linnartz-Gerlach, B., Kudin, A. P., Kunz, W. S., & Neumann, H. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2211-13.2013 · Cited by 98 · see citing works
Where catabolism meets signalling: neuraminidase 1 as a modulator of cell receptors
Pshezhetsky, A. V., & Hinek, A. (2011) · Glycoconjugate Journal · doi:10.1007/s10719-011-9350-5 · Cited by 88 · see citing works
Nuclear transport of galectin-3 and its therapeutic implications
Funasaka, T., Raz, A., & Nangia‐Makker, P. (2014) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2014.03.004 · Cited by 86 · see citing works
Siglec‐h on activated microglia for recognition and engulfment of glioma cells
Kopatz, J., Beutner, C., Welle, K., Bodea, L., Reinhardt, J., Claude, J., Linnartz‐Gerlach, B., & Neumann, H. (2013) · Glia · doi:10.1002/glia.22501 · Cited by 72 · see citing works
Christoph, S., DeRyckere, D., Schlegel, J., Frazer, J. K., Batchelor, L. A., Trakhimets, A. Y., Sather, S., Hunter, D. M., Cummings, C. T., Liu, J., et al. (2013) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-13-0040 · Cited by 72 · see citing works
Feng, C., Zhang, L., Almulki, L., Faez, S., Whitford, M., Hafezi‐Moghadam, A., & Cross, A. S. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.1210708 · Cited by 65 · see citing works
Hornik, T. C., Neniškytė, U., & Brown, G. C. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12477 · Cited by 58 · see citing works
Self-citationJennings, C., Kusler, B., & Jones, P. P. (2009) · Innate Immunity · doi:10.1177/1753425908100928 · Cited by 58 · see citing works
Galectins and Neuroinflammation
Chen, H.-L., Liao, F., Lin, T., & Liu, F. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1154-7_24 · Cited by 57 · see citing works
Satoh, K., Niwa, M., Goda, W., Bình, N. H., Nakashima, M., Takamatsu, M., & Hara, A. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.049 · Cited by 53 · see citing works
Pereira, M. E. A. (1983) · Journal of Immunological Methods · doi:10.1016/0022-1759(83)90206-5 · Cited by 43 · see citing works
Wang, C., Liu, X., Huang, K., Yin, S.-B., Wei, J., Hu, Y., Gu, Y., & Zheng, G. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13611 · Cited by 28 · see citing works
Sweet kiss of dying cell: Sialidase activity on apoptotic cell is able to act toward its neighbors
Shkandina, T., i, M. H., & Bilyy, R. O. (2012) · Autoimmunity · doi:10.3109/08916934.2012.719951 · Cited by 17 · see citing works
Nomura, K., Lee, M., Banks, C., Lee, G. L., & MORRIS, B. J. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.05.045 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
1 of the 48 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [32]Stamatos NM Liang F Nan X Landry K Cross AS Wang LX Pshezhetsky AV Differential expression of endogenous sialidases of human monocytes during cellular differentiation into macrophages FEBS J 2005 272 2545 2556 15885103
Cited by
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Fricker, M., Tolkovsky, A. M., Borutaitė, V., Coleman, M. P., & Brown, G. C. (2018) · Physiological Reviews · doi:10.1152/physrev.00011.2017 · Cited by 1,122 · see citing works
Self-citationDysregulation of brain and choroid plexus cell types in severe COVID-19
Yang, A. C., Kern, F., Losada, P. M., Agam, M. R., Maat, C. A., Schmartz, G. P., Fehlmann, T., Stein, J. A., Schaum, N., Lee, D. P., et al. (2021) · Nature · doi:10.1038/s41586-021-03710-0 · Cited by 620 · see citing works
Myers, K. V., Amend, S. R., & Pienta, K. J. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1022-2 · Cited by 482 · see citing works
Microglia: Agents of the CNS Pro-Inflammatory Response
Rodríguez-Gómez, J. A., Kavanagh, E., Engskog-Vlachos, P., Engskog, M. K. R., Herrera, A. J., Espinosa-Oliva, A. M., Joseph, B., Hajji, N., Venero, J. L., & Burguillos, M. A. (2020) · Cells · doi:10.3390/cells9071717 · Cited by 365 · see citing works
Boza-Serrano, A., Ruiz, R., Sanchez-Varo, R., García-Revilla, J., Yang, Y., Jimenez-Ferrer, I., Paulus, A., Wennström, M., Vilalta, A., Allendorf, D., et al. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-02013-z · Cited by 357 · see citing works
Self-citationMicroglial phagocytosis of neurons in neurodegeneration, and its regulation
Butler, C. A., Popescu, A. S., Kitchener, E. J. A., Allendorf, D. H., Puigdellívol, M., & Brown, G. C. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15327 · Cited by 293 · see citing works
Self-citationVilalta, A., & Brown, G. C. (2017) · FEBS Journal · doi:10.1111/febs.14323 · Cited by 174 · see citing works
Self-citationGalectin-3, a rising star in modulating microglia activation under conditions of neurodegeneration
García-Revilla, J., Boza-Serrano, A., Espinosa-Oliva, A. M., Soto, M. S., Deierborg, T., Ruiz, R., de Pablos, R. M., Burguillos, M. A., & Venero, J. L. (2022) · Cell Death & Disease · doi:10.1038/s41419-022-05058-3 · Cited by 156 · see citing works
Sialylation and Galectin-3 in Microglia-Mediated Neuroinflammation and Neurodegeneration
Puigdellívol, M., Allendorf, D. H., & Brown, G. C. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00162 · Cited by 145 · see citing works
Self-citationThe Role of Microglial Phagocytosis in Ischemic Stroke
Jia, J., Yang, L., Chen, Y., Zheng, L., Chen, Y., Xu, Y., & Zhang, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.790201 · Cited by 136 · see citing works
Kołosowska, N., Keuters, M. H., Wojciechowski, S., Keksa-Goldsteine, V., Laine, M. T., Malm, T., Goldsteins, G., Koıstınaho, J., & Dhungana, H. (2019) · Neurotherapeutics · doi:10.1007/s13311-019-00761-0 · Cited by 133 · see citing works
Modulation of three key innate immune pathways for the most common retinal degenerative diseases
Akhtar‐Schäfer, I., Wang, L., Krohne, T. U., Xu, H., & Langmann, T. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201708259 · Cited by 127 · see citing works
Retinal microglia: Functions and diseases
Fan, W., Huang, W., Chen, J., Li, N., Mao, L., & Hou, S. (2022) · Immunology · doi:10.1111/imm.13479 · Cited by 131 · see citing works
Microglia: Brain cells on the move
Smolders, S., Kessels, S., Vangansewinkel, T., Rigo, J., Legendre, P., & Brône, B. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.04.001 · Cited by 114 · see citing works
The Phagocytic Code Regulating Phagocytosis of Mammalian Cells
Cockram, T. O. J., Dundee, J. M., Popescu, A. S., & Brown, G. C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.629979 · Cited by 111 · see citing works
Self-citationMicroglia 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
Galectin-3: a key player in microglia-mediated neuroinflammation and Alzheimer's disease
Tan, Y., Zheng, Y., Xu, D., Sun, Z., Yang, H., & Yin, Q. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00592-7 · Cited by 100 · see citing works
The P2X7 Receptor in Microglial Cells Modulates the Endolysosomal Axis, Autophagy, and Phagocytosis
Campagno, K. E., & Mitchell, C. H. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.645244 · Cited by 90 · see citing works
The “Phagocytic Synapse” and Clearance of Apoptotic Cells
Barth, N. D., Marwick, J. A., Vendrell, M., Rossi, A. G., & Dransfield, I. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01708 · Cited by 78 · see citing works
Galectin-3: Roles in Neurodevelopment, Neuroinflammation, and Behavior
Srejovic, I. M., Selaković, D., Jovicic, N. U., Jakovljevic, V. L., Lukić, M. L., & Rosic, G. L. (2020) · Biomolecules · doi:10.3390/biom10050798 · Cited by 77 · see citing works
Allendorf, D. H., Puigdellívol, M., & Brown, G. C. (2019) · Glia · doi:10.1002/glia.23757 · Cited by 76 · see citing works
Self-citationGlycobiology and schizophrenia: a biological hypothesis emerging from genomic research
Mealer, R. G., Williams, S., Daly, M. J., Scolnick, E. M., Cummings, R. D., & Smoller, J. W. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0753-1 · Cited by 75 · see citing works
Acoustofluidic assembly of 3D neurospheroids to model Alzheimer's disease
Cai, H., Ao, Z., Hu, L., Moon, Y., Wu, Z., Lu, H.-C., Kim, J., & Guo, F. (2020) · The Analyst · doi:10.1039/d0an01373k · Cited by 70 · see citing works
Rangan, P., Lobo, F., Parrella, E., Rochette, N. C., Morselli, M., Stephen, T., Cremonini, A. L., Tagliafico, L., Persia, A., Caffa, I., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111417 · Cited by 68 · see citing works
Sialylation acts as a checkpoint for innate immune responses in the central nervous system
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Self-citationMicroglia at the Crossroads of Pathogen-Induced Neuroinflammation
Rodríguez, A. M., Rodríguez, J., & Giambartolomei, G. H. (2022) · ASN NEURO · doi:10.1177/17590914221104566 · Cited by 67 · see citing works
Single Cell RNA-Seq Analysis Reveals Compartment-Specific Heterogeneity and Plasticity of Microglia
Zheng, J., Ru, W., Adolacion, J. R. T., Spurgat, M. S., Liu, X., Yuan, S., Liang, R. X., Dong, J., Potter, A. S., Potter, S. S., et al. (2020) · iScience · doi:10.1016/j.isci.2021.102186 · Cited by 63 · see citing works
Extracellular tau induces microglial phagocytosis of living neurons in cell cultures
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Self-citationLipopolysaccharide activates microglia via neuraminidase 1 desialylation of Toll‐like Receptor 4
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Self-citationMicroglial dysfunction as a key pathological change in adrenomyeloneuropathy
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AXL Receptor in Cancer Metastasis and Drug Resistance: When Normal Functions Go Askew
Auyez, A., Sayan, E., Kriajevska, M. V., & Tulchinsky, E. M. (2021) · Cancers · doi:10.3390/cancers13194864 · Cited by 50 · see citing works
Tabel, M., Wolf, A., Szczepan, M., Xu, H., Jägle, H., Moehle, C., Chen, M., & Langmann, T. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02589-6 · Cited by 50 · see citing works
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Liao, H., Klaus, C., & Neumann, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155494 · Cited by 46 · see citing works
García‐Mateo, N., Pascua‐Maestro, R., Pérez‐Castellanos, A., Lillo, C., Sánchez, D., & Ganfornina, M. D. (2017) · Glia · doi:10.1002/glia.23274 · Cited by 44 · see citing works
Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
García‐Revilla, J., Boza‐Serrano, A., Jin, Y., Vadukul, D. M., Soldán-Hidalgo, J., Camprubí-Ferrer, L., García-Cruzado, M., Martinsson, I., Klementieva, O. L., Ruiz, R., et al. (2023) · Acta Neuropathologica · doi:10.1007/s00401-023-02585-x · Cited by 40 · see citing works
Role of the neurovascular unit in the process of cerebral ischemic injury
Zhao, Y. S., Yang, J., Li, C., Zhou, G., Wan, H., Ding, Z., Wan, H., & Zhou, H. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105103 · Cited by 39 · see citing works
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Zhou, L., & Matsushima, G. K. (2021) · International review of cytology · doi:10.1016/bs.ircmb.2021.02.002 · Cited by 35 · see citing works
Allendorf, D. H., & Brown, G. C. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.917884 · Cited by 34 · see citing works
Self-citationButler, C. A., Thornton, P., & Brown, G. C. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15349 · Cited by 35 · see citing works
Self-citationMammalian Neuraminidases in Immune-Mediated Diseases: Mucins and Beyond
Lillehoj, E. P., Luzina, I. G., & Atamas, S. P. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.883079 · Cited by 33 · see citing works
Rotshenker, S. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.949079 · Cited by 35 · see citing works
Galectins in the brain: advances in neuroinflammation, neuroprotection and therapeutic opportunities
Barake, F., Soza, A., & González, A. (2020) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000812 · Cited by 32 · see citing works
Gillispie, G. J., Sah, E., Krishnamurthy, S., Ahmidouch, M. Y., Zhang, B., & Orr, M. E. (2021) · Life · doi:10.3390/life11020153 · Cited by 32 · see citing works
Differential Cellular Expression of Galectin-1 and Galectin-3 After Intracerebral Hemorrhage
Bonsack, F., & Sukumari‐Ramesh, S. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00157 · Cited by 30 · see citing works
Zhao, Q., & Lai, K. (2023) · Experimental Eye Research · doi:10.1016/j.exer.2023.109770 · Cited by 29 · see citing works
Cellular translocation and secretion of sialidases
Aljohani, M. A., Sasaki, H., & Sun, X. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107671 · Cited by 29 · see citing works
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Mijailović, N. R., Vesić, K., Arsenijević, D., Milojević‐Rakić, M., & Borovčanin, M. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.923811 · Cited by 29 · see citing works
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Tian, Y.-K., Ye, D.-W., Ge, M.-M., Chen, N., Zhou, Y.-Q., & Yang, H. (2022) · Current Neuropharmacology · doi:10.2174/1570159x20666220201094547 · Cited by 31 · see citing works
TAM kinase inhibition and immune checkpoint blockade– a winning combination in cancer treatment?
Msaouel, P., Genovese, G., Gao, J., Sen, S., & Tannir, N. M. (2020) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2021.1869212 · Cited by 28 · see citing works
Haupt, M., Gerner, S. T., & Doeppner, T. R. (2024) · Neuroprotection/Neuroprotection (Chichester, England. Print) · doi:10.1002/nep3.39 · Cited by 26 · see citing works
Pérez-Moreno, E., Oyanadel, C., de la Peña, A., Hernández, R., Pérez-Molina, F., Metz, C., González, A., & Soza, A. (2024) · Biological Research · doi:10.1186/s40659-024-00490-5 · Cited by 26 · see citing works
Neurodegenerative phagocytes mediate synaptic stripping in Neuro-HIV
Liberto, G. D., Égervári, K., Kreutzfeldt, M., Schürch, C. M., Hewer, E., Wagner, I., Pasquier, R. D., & Merkler, D. (2022) · Brain · doi:10.1093/brain/awac102 · Cited by 26 · see citing works
Delaveris, C. S., Wang, C. L., Riley, N. M., Li, S., Kulkarni, R. U., & Bertozzi, C. R. (2023) · ACS Central Science · doi:10.1021/acscentsci.3c01066 · Cited by 25 · see citing works
Reactive microglia partially envelop viable neurons in prion diseases
Makarava, N., Safadi, T., Bocharova, O. V., Mychko, O., Pandit, N. P., Molesworth, K., Baiardi, S., Zhang, L., Parchi, P., & Baskakov, I. V. (2024) · Journal of Clinical Investigation · doi:10.1172/jci181169 · Cited by 26 · see citing works
Efferocytosis: the resolution of inflammation in cardiovascular and cerebrovascular disease
Zhang, B., Zou, Y., Yuan, Z., Jiang, K., Zhang, Z., Chen, S., Zhou, X., Wu, Q., & Zhang, X. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1485222 · Cited by 27 · see citing works
Differential Roles of TREM2+ Microglia in Anterograde and Retrograde Axonal Injury Models
Manich, G., Gómez‐López, A. R., Almolda, B., Villacampa, N., Recasens, M., Shrivastava, K., González, B., & Castellano, B. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.567404 · Cited by 26 · see citing works
García‐Revilla, J., Ruiz, R., Espinosa‐Oliva, A. M., Santiago, M., García-Domínguez, I., Camprubí-Ferrer, L., Bachiller, S., Deierborg, T., Joseph, B., de Pablos, R. M., et al. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-07014-9 · Cited by 25 · see citing works
Neel, D. V., Basu, H., Gunner, G., & Chiu, I. M. (2022) · Immunological Reviews · doi:10.1111/imr.13083 · Cited by 22 · see citing works
Wang, F., Ye, J., Zhu, W., Ge, R., Hu, C., Qian, Y., Li, Y., & Peng, Z. (2023) · Inflammation · doi:10.1007/s10753-023-01928-w · Cited by 23 · see citing works
Kafri, N. A., & Hafizi, S. (2020) · Biomolecules · doi:10.3390/biom10071035 · Cited by 22 · see citing works
I’m Infected, Eat Me! Innate Immunity Mediated by Live, Infected Cells Signaling To Be Phagocytosed
Birkle, T. J. Y., & Brown, G. C. (2021) · Infection and Immunity · doi:10.1128/iai.00476-20 · Cited by 22 · see citing works
Self-citationKuo, T., Chen, Y.-H., Wang, V., Wu, J., & Tseng, K.-Y. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.639145 · Cited by 21 · see citing works
Lee, M. J., Wang, C., Carroll, M. J., Brubaker, D. K., Hyman, B. T., & Lauffenburger, D. A. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.727784 · Cited by 18 · see citing works
Potential Use of Nanomedicine for the Anti-inflammatory Treatment of Neurodegenerative Diseases
Otero, M. D. C., Espinosa‐Oliva, A. M., Herrera, A. J., García-Domínguez, I., Arévalo, M. F., Martín‐Banderas, L., & de Pablos, R. M. (2018) · Current Pharmaceutical Design · doi:10.2174/1381612824666180403113015 · Cited by 17 · see citing works
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Jaiswal, S., & Srivastava, K. K. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.03.075 · Cited by 14 · see citing works
Tseng, K.-Y., Wu, J., Chen, Y.-H., Airavaara, M., Cheng, C., & Ma, K. (2022) · Biomedicines · doi:10.3390/biomedicines10061446 · Cited by 13 · see citing works
Shi, G., Zhang, C., Li, G., Wang, K., Cai, Q., & Huang, M. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.114583 · Cited by 12 · see citing works
Izuo, N., & Nitta, A. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11050371 · Cited by 12 · see citing works
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Esposito, N. J., Mazzoni, F., Vargas, J. A., & Finnemann, S. C. (2021) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.62.2.7 · Cited by 9 · see citing works
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Caridi, B., Doncheva, D., Sivaprasad, S., & Turowski, P. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.687495 · Cited by 8 · see citing works
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Flint, E., Triantafyllou, E., & Bernsmeier, C. (2022) · Livers · doi:10.3390/livers2010002 · Cited by 8 · see citing works
Xie, M., Wang, T., Feng, J., Ma, D., Feng, L., & Hao, Y. (2025) · Current Neuropharmacology · doi:10.2174/1570159x23666250225091729 · Cited by 7 · see citing works
MERTK in the rat trigeminal system: a potential novel target for cluster headache?
Edvinsson, J. C. A., Ran, C., Olofsgård, F. J., Steinberg, A., Edvinsson, L. I., & Belin, A. C. (2024) · The Journal of Headache and Pain · doi:10.1186/s10194-024-01791-6 · Cited by 6 · see citing works
Microglial galectin-3 increases with aging in the mouse hippocampus
Shin, H. J., Lee, S. J., An, H. S., Choi, H. N., Jeong, E. A., Lee, J. W., Kim, K. E., Choi, B.-H., Yun, S. P., Kang, D., et al. (2025) · Korean Journal of Physiology and Pharmacology · doi:10.4196/kjpp.24.196 · Cited by 7 · see citing works
Sweet Aging: Glycocalyx and Galectins in CNS Aging and Neurodegenerative Disorders
Légrádi, Á., & Mir, M. Y. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26104699 · Cited by 5 · see citing works
Unique Glycans in Synaptic Glycoproteins in Mouse Brain
Noël, M., Suttapitugsakul, S., Wei, M., Tilton, C. A., Mehta, A. Y., Matsumoto, Y., Heimburg‐Molinaro, J., Mealer, R. G., & Cummings, R. D. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.4c00399 · Cited by 5 · see citing works
Delaveris, C. S., Wang, C. L., Riley, N. M., Li, S., Kulkarni, R. U., & Bertozzi, C. R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.21.554214 · Cited by 5 · see citing works
Zhou, X., Dai, N., Yu, D., Niu, T., & Wang, S. (2024) · Frontiers in Medicine · doi:10.3389/fmed.2024.1443133 · Cited by 4 · see citing works
Oseltamivir (Tamiflu), a commonly prescribed antiviral drug, mitigates hearing loss in mice
Sailor‐Longsworth, E. J., Lutze, R. D., Ingersoll, M. A., Kelmann, R. G., Ly, K., Currier, D. G., Chen, T., Zuo, J., & Teitz, T. (2024) · Clinical and Translational Medicine · doi:10.1002/ctm2.1803 · Cited by 4 · see citing works
Alzarea, S. I., Alsaidan, O. A., Qasim, S., Alhassan, H. H., Alzarea, A. I., Alsahli, T. G., Alharbi, M., & Almutairi, M. (2025) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2025.111318 · Cited by 3 · see citing works
Zhou, W.-M., Zhang, K., Ma, W.-W., Shi, Y.-Q., Dong, Y.-B., Yuan, Z.-Y., & Zhang, H. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1798053 · Cited by 3 · see citing works
Siew, J. J., & Chern, Y. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107410 · Cited by 2 · see citing works
Impaired Efferocytosis of Pericytes and Vascular Smooth Muscle Cells in Diabetic Retinopathy
Gardiner, T. A., Little, K., & Stitt, A. W. (2025) · Cells · doi:10.3390/cells14171349 · Cited by 2 · see citing works
Yan, L., Chen, C., Wang, L., Hong, H., Wu, C., Huang, J., Jiang, J., Chen, J., Xu, G., & Cui, Z. (2024) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2024.12581 · Cited by 2 · see citing works
de la Peña, A., Retamal, C., Pérez-Molina, F., Díaz-Valdivia, N., Veloso-Bahamondes, F., Tapia, D., Cancino, J., Randow, F., González, A., Oyanadel, C., et al. (2025) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2025.151488 · Cited by 1 · see citing works
Akash, A., Ahamed, M., Porel, P., & Aran, K. R. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149949 · Cited by 2 · see citing works
Zheng, J., Spurgat, M. S., Maurelli, M., Watson, Z., Hossain, S., DiBua, A., Yuan, S., Liu, X., Gelman, B. B., & Tang, S. (2025) · Nature Communications · doi:10.1038/s41467-025-67368-2 · Cited by 1 · see citing works
Exploring the role of sialidases in Galectin-1-associated resistance to cancer therapies
Scheidegger, M. A., Merlo, J. P., Villarreal, S. N., Schattner, M. A., Croci, D. O., Dalotto‐Moreno, T., Mariño, K. V., & Rabinovich, G. A. (2026) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2026.130931 · Cited by 1 · see citing works
Dabagh, M., Ciceu, A., Baltă, C., Trotta, M. C., Ferraro, B., D’Amico, G., Hermenean, A. O., & Voiculescu, V. M. (2026) · Biological Research · doi:10.1186/s40659-026-00695-w · Cited by 1 · see citing works
Yang, W., Chen, Z., Zhang, Y., Peng, C., & Chen, B. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2026.1893517 · Cited by 1 · see citing works
Church, K. A., Cardona, A. E., & Hopp, S. C. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-55529-9_15 · Cited by 1 · see citing works
Maestro, R. P. (2018) · doi:10.35376/10324/33119 · Cited by 1 · see citing works
Engulfment of viable neurons by reactive microglia in prion diseasesPreprint
Makarava, N., Safadi, T., Mychko, O., Pandit, N. P., Molesworth, K., Baiardi, S., Zhang, L., Parchi, P., & Baskakov, I. V. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.06.583759 · Cited by 1 · see citing works
Expression and role of Galectin-3 in the postnatal development of the cerebellumPreprint
González-Calvo, I., & Selimi, F. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/364760
- Authors
- Nomura, K., Vilalta, A., Allendorf, D. H., Hornik, T. C., & Brown, G. C.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Brown, Guy C
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-06
- Volume
- 198
- Issue
- 12
- Pages
- 4792-4801
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC5458330
- OpenAlex
- W2612664982
- Cited by
- 111
- References
- 48
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 14 · 2023: 7 · 2022: 17 · 2021: 17 · 2020: 15 · 2019: 9 · 2018: 7 · 2017: 4
- FWCI
- 4.77
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- The Journal of Immunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- Medical Research Council (MR/L010593/1)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Keywords
- microglia, phagocytosis, galectin-3, MERTK, neuraminidase, sialic acid, desialylation, opsonization, lipopolysaccharide stimulation, PC12 cells, neurons, calcineurin, neuraminidase inhibitors, synaptic loss, neuroinflammation
- MeSH terms
- c-Mer Tyrosine Kinase, Animals, Galactose, Lipopolysaccharides, Macrophages, Neuraminidase, Neurons, Opsonin Proteins, Phagocytosis, Proto-Oncogene Proteins, Pyrazoles, Pyrimidines, PC12 Cells, Microglia, Receptor Protein-Tyrosine Kinases, Galectin 3, Rats, Oseltamivir
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