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Apolipoprotein E4 impairs the response of neurodegenerative retinal microglia and prevents neuronal loss in glaucoma
Open accessAbstract
The apolipoprotein E4 (APOE4) allele is associated with an increased risk of Alzheimer disease and a decreased risk of glaucoma, but the underlying mechanisms remain poorly understood. Here, we found that in two mouse glaucoma models, microglia transitioned to a neurodegenerative phenotype characterized by upregulation of Apoe and Lgals3 (Galectin-3), which were also upregulated in human glaucomatous retinas. Mice with targeted deletion of Apoe in microglia or carrying the human APOE4 allele were protected from retinal ganglion cell (RGC) loss, despite elevated intraocular pressure (IOP). Similarly to Apoe-/- retinal microglia, APOE4-expressing microglia did not upregulate neurodegeneration-associated genes, including Lgals3, following IOP elevation. Genetic and pharmacologic targeting of Galectin-3 ameliorated RGC degeneration, and Galectin-3 expression was attenuated in human APOE4 glaucoma samples. These results demonstrate that impaired activation of APOE4 microglia is protective in glaucoma and that the APOE-Galectin-3 signaling can be targeted to treat this blinding disease.
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“Thus, APOE4 converges to impair the MGnD response to neurodegeneration, which plays a protective role in glaucoma 14 and is detrimental in AD.”
From APOE4 impairs the microglial response in Alzheimer’s disease by inducing TGFβ-mediated checkpoints (2023) · cites this paper as [14]
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“We recently showed impaired MGnD responses in APOE4 -KI glaucoma mice, similar to Apoe -/-mice 14 .”
From APOE4 impairs the microglial response in Alzheimer’s disease by inducing TGFβ-mediated checkpoints (2023) · cites this paper as [14]
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“We recently demonstrated that APOE4 impairs the response of neurodegenerative retinal microglia via LGALS3 signaling associated with neuroprotection in glaucoma 14 .”
From APOE4 impairs the microglial response in Alzheimer’s disease by inducing TGFβ-mediated checkpoints (2023) · cites this paper as [14]
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Neurotoxic reactive astrocytes are induced by activated microglia
Liddelow, S. A., Guttenplan, K. A., Clarke, L. E., Bennett, F. C., Bohlen, C. J., Schirmer, L., Bennett, M. L., Münch, A. E., Chung, W.-S., Peterson, T. C., et al. (2017) · Nature · doi:10.1038/nature21029 · Cited by 7,971
Global Prevalence of Glaucoma and Projections of Glaucoma Burden through 2040
Tham, Y.-C., Li, X., Wong, T. Y., Quigley, H. A., Aung, T., & Cheng, C.-Y. (2014) · Ophthalmology · doi:10.1016/j.ophtha.2014.05.013 · Cited by 7,159
A Unique Microglia Type Associated with Restricting Development of Alzheimer’s Disease
Keren-Shaul, H., Spinrad, A., Weiner, A., Matcovitch-Natan, O., Dvir-Szternfeld, R., Ulland, T. K., David, E., Baruch, K., Lara-Astaiso, D., Toth, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.018 · Cited by 5,493
Strittmatter, W. J., Saunders, A. M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G. S., & Roses, A. D. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.5.1977 · Cited by 4,268
Association of apolipoprotein E allele ϵ4 with late‐onset familial and sporadic Alzheimer's disease
Saunders, A. M., Strittmatter, W. J., Schmechel, D., St. George-Hyslop, P. H., Pericak-Vance, M. A., Joo, S. H., Rosi, B. L., Gusella, J. F., Crapper-MacLachlan, D. R., Alberts, M. J., et al. (1993) · Neurology · doi:10.1212/wnl.43.8.1467 · Cited by 3,786
TREM2 Variants in Alzheimer's Disease
Guerreiro, R., Wojtas, A., Bras, J., Carrasquillo, M., Rogaeva, E., Majounie, E., Cruchaga, C., Sassi, C., Kauwe, J. S. K., Younkin, S., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211851 · Cited by 3,020
Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O’Loughlin, E., Xu, Y., Fanek, Z., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.008 · Cited by 2,979
Self-citationMicroglia Function in the Central Nervous System During Health and Neurodegeneration
Colonna, M., & Butovsky, O. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-051116-052358 · Cited by 2,894
Self-citationMicroglia promote learning-dependent synapse formation through brain-derived neurotrophic factor
Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R., Lafaille, J. J., Hempstead, B. L., Littman, D. R., & Gan, W.-B. (2013) · Cell · doi:10.1016/j.cell.2013.11.030 · Cited by 2,599
Variant of TREM2 Associated with the Risk of Alzheimer's Disease
Jonsson, T., Stefansson, H., Steinberg, S., Jonsdottir, I., Jonsson, P. V., Snaedal, J., Bjornsson, S., Huttenlocher, J., Levey, A. I., Lah, J. J., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1211103 · Cited by 2,558
Identification of a unique TGF-β–dependent molecular and functional signature in microglia
Butovsky, O., Jedrychowski, M. P., Moore, C. S., Cialic, R., Lanser, A. J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P. M., Doykan, C. E., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3599 · Cited by 2,543
Self-citationMicroglia and macrophages in brain homeostasis and disease
Li, Q., & Barres, B. A. (2018) · Nature Reviews Immunology · doi:10.1038/nri.2017.125 · Cited by 1,999
TREM2 Lipid Sensing Sustains the Microglial Response in an Alzheimer’s Disease Model
Wang, Y., Cella, M., Mallinson, K., Ulrich, J. D., Young, K. L., Robinette, M. L., Gilfillan, S., Krishnan, G. M., Sudhakar, S., Zinselmeyer, B. H., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.049 · Cited by 1,736
Self-citationDepletion of microglia and inhibition of exosome synthesis halt tau propagation
Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S., & Ikezu, T. (2015) · Nature Neuroscience · doi:10.1038/nn.4132 · Cited by 1,591
Self-citationNLRP3 inflammasome activation drives tau pathology
Ising, C., Venegas, C., Zhang, S., Scheiblich, H., Schmidt, S. V., Vieira-Saecker, A., Schwartz, S., Albasset, S., McManus, R. M., Tejera, D., et al. (2019) · Nature · doi:10.1038/s41586-019-1769-z · Cited by 1,487
Marschallinger, J., Iram, T., Zardeneta, M., Lee, S. E., Lehallier, B., Haney, M. S., Pluvinage, J. V., Mathur, V., Hahn, O., Morgens, D. W., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0566-1 · Cited by 1,384
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
Microglial control of astrocytes in response to microbial metabolites
Rothhammer, V., Borucki, D. M., Tjon, E. C., Takenaka, M. C., Chao, C.-C., Ardura-Fabregat, A., de Lima, K. A., Gutiérrez-Vázquez, C., Hewson, P., Staszewski, O., et al. (2018) · Nature · doi:10.1038/s41586-018-0119-x · Cited by 1,051
Microglial signatures and their role in health and disease
Butovsky, O., & Weiner, H. L. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0057-5 · Cited by 1,046
Self-citationSpangenberg, E., Severson, P. L., Hohsfield, L. A., Crapser, J., Zhang, J., Burton, E. A., Zhang, Y., Spevak, W., Lin, J., Phan, N. Y., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11674-z · Cited by 939
Single-cell profiling identifies myeloid cell subsets with distinct fates during neuroinflammation
Jordão, M. J. C., Sankowski, R., Brendecke, S. M., Sagar, Locatelli, G., Tai, Y.-H., Tay, T. L., Schramm, E., Armbruster, S., Hagemeyer, N., et al. (2019) · Science · doi:10.1126/science.aat7554 · Cited by 843
Bruttger, J., Karram, K., Wörtge, S., Regen, T., Marini, F., Hoppmann, N., Klein, M., Blank, T., Yona, S., Wolf, Y., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.06.012 · Cited by 634
Loss of TREM2 function increases amyloid seeding but reduces plaque-associated ApoE
Parhizkar, S., Arzberger, T., Brendel, M., Kleinberger, G., Deussing, M., Focke, C., Nuscher, B., Xiong, M., Ghasemigharagoz, A., Katzmarski, N., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0296-9 · Cited by 555
Self-citationA combination of ontogeny and CNS environment establishes microglial identity
Bennett, F. C., Bennett, M. L., Yaqoob, F., Mulinyawe, S. B., Grant, G. A., Hayden Gephart, M., Plowey, E. D., & Barres, B. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.014 · Cited by 524
Microglia use TAM receptors to detect and engulf amyloid β plaques
Huang, Y., Happonen, K. E., Burrola, P. G., O’Connor, C., Hah, N., Huang, L., Nimmerjahn, A., & Lemke, G. (2021) · Nature Immunology · doi:10.1038/s41590-021-00913-5 · Cited by 483
Microglial phagocytosis of living photoreceptors contributes to inherited retinal degeneration
Zhao, L., Zabel, M. K., Wang, X., Ma, W., Shah, P., Fariss, R. N., Qian, H., Parkhurst, C. N., Gan, W., & Wong, W. T. (2015) · EMBO Molecular Medicine · doi:10.15252/emmm.201505298 · Cited by 457
Mutations in genes encoding melanosomal proteins cause pigmentary glaucoma in DBA/2J mice
Anderson, M. G., Smith, R. S., Hawes, N. L., Zabaleta, A., Chang, B., Wiggs, J. L., & John, S. W. M. (2001) · Nature Genetics · doi:10.1038/ng794 · Cited by 453
O’Koren, E. G., Yu, C., Klingeborn, M., Wong, A. Y. W., Prigge, C. L., Mathew, R., Kalnitsky, J., Msallam, R. A., Silvin, A., Kay, J. N., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.02.007 · Cited by 440
Early Fate Defines Microglia and Non-parenchymal Brain Macrophage Development
Utz, S. G., See, P., Mildenberger, W., Thion, M. S., Silvin, A., Lutz, M., Ingelfinger, F., Rayan, N. A., Lelios, I., Buttgereit, A., et al. (2020) · Cell · doi:10.1016/j.cell.2020.03.021 · Cited by 436
Nakazawa, T., Nakazawa, C., Matsubara, A., Noda, K., Hisatomi, T., She, H., Michaud, N. A., Hafezi‐Moghadam, A., Miller, J. W., & Benowitz, L. I. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2801-06.2006 · Cited by 432
Inherited glaucoma in DBA/2J mice: Pertinent disease features for studying the neurodegeneration
Libby, R. T., Anderson, M. G., Pang, I., ROBINSON, Z. H., SAVINOVA, O. V., Cosma, I. M., Snow, A., Wilson, L. A., Smith, R. S., Clark, A. F., et al. (2005) · Visual Neuroscience · doi:10.1017/s0952523805225130 · Cited by 410
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Sappington, R. M., Carlson, B. J., Crish, S. D., & Calkins, D. J. (2010) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.09-3947 · Cited by 391
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Griciuc, A., Patel, S., Federico, A. N., Choi, S. H., Innes, B. J., Oram, M. K., Cereghetti, G., McGinty, D., Anselmo, A., Sadreyev, R. I., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.06.010 · Cited by 378
Self-citationInhibition 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
Burguillos, 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
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Butovsky, O., Jedrychowski, M. P., Cialic, R., Krasemann, S., Murugaiyan, G., Fanek, Z., Greco, D. J., Wu, P. M., Doykan, C. E., Kiner, O., et al. (2015) · Annals of Neurology · doi:10.1002/ana.24304 · Cited by 358
Self-citationPhagocytosis 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 357
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
Loss of TREM2 function increases amyloid seeding but reduces plaque-associated ApoE
Parhizkar, S., Arzberger, T., Brendel, M., Kleinberger, G., Deußing, M., Focke, C., Nuscher, B., Xiong, M., Ghasemigharagoz, A., Katzmarski, N., et al. (2019) · doi:10.7892/boris.125653 · Cited by 352
Self-citationEarly microglia activation in a mouse model of chronic glaucoma
Bosco, A., Steele, M. R., & Vetter, M. L. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22516 · Cited by 350
Activated microglia in the human glaucomatous optic nerve head
Yuan, L., & Neufeld, A. H. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.1104 · Cited by 348
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Hammond, T. R., Marsh, S. E., & Stevens, B. (2019) · Immunity · doi:10.1016/j.immuni.2019.03.016 · Cited by 336
TREM2 function impedes tau seeding in neuritic plaques
Leyns, C. E. G., Gratuze, M., Narasimhan, S., Jain, N., Koscal, L. J., Jiang, H., Manis, M., Colonna, M., Lee, V. M. Y., Ulrich, J. D., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0433-0 · Cited by 332
Self-citationBosco, A., Inman, D. M., Steele, M. R., Wu, G., Soto, I., Marsh‐Armstrong, N., Hubbard, W. C., Calkins, D. J., Horner, P. J., & Vetter, M. L. (2008) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-1337 · Cited by 322
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McAlpine, C. S., Park, J., Griciuc, A., Kim, E., Choi, S. H., Iwamoto, Y., Kiss, M. G., Christie, K. A., Vinegoni, C., Poller, W. C., et al. (2021) · Nature · doi:10.1038/s41586-021-03734-6 · Cited by 322
Self-citationSpecification of CNS macrophage subsets occurs postnatally in defined niches
Masuda, T., Amann, L., Monaco, G., Sankowski, R., Staszewski, O., Krueger, M., Del Gaudio, F., He, L., Paterson, N., Nent, E., et al. (2022) · Nature · doi:10.1038/s41586-022-04596-2 · Cited by 294
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Williams, P. A., Marsh-Armstrong, N., Howell, G. R., Bosco, A., Danias, J., Simon, J., Di Polo, A., Kuehn, M. H., Przedborski, S., Raff, M., et al. (2017) · Experimental Eye Research · doi:10.1016/j.exer.2017.02.014 · Cited by 253
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Soto, I., & Howell, G. R. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a017269 · Cited by 253
Lund, H., Pieber, M., Parsa, R., Han, J., Grommisch, D., Ewing, E., Kular, L., Needhamsen, M., Espinosa, A., Nilsson, E., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07295-7 · Cited by 249
Self-citationMicroglia in the Optic Nerve Head and the Region of Parapapillary Chorioretinal Atrophy in Glaucoma
Neufeld, A. H. (1999) · Archives of Ophthalmology · doi:10.1001/archopht.117.8.1050 · Cited by 248
Ganglion cell contributions to the rat full‐field electroretinogram
Bui, B. V., & Fortune, B. A. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.052738 · Cited by 239
Howell, G. R., Soto, I., Zhu, X., Ryan, M. M., Macalinao, D. G., Sousa, G. L., Caddle, L. B., MacNicoll, K. H., Barbay, J. M., Porciatti, V., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci61135 · Cited by 233
Siew, J. J., Chen, H., Chen, H., Chen, H.-L., Chen, C., Soong, B., Wu, Y., Chang, C., Chan, Y., Lin, C., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11441-0 · Cited by 229
Roh, M., Zhang, Y., Murakami, Y., Thanos, A., Lee, S. C., Vavvas, D. G., Benowitz, L. I., & Miller, J. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040065 · Cited by 220
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Gratuze, M., Chen, Y., Parhizkar, S., Jain, N., Strickland, M. R., Serrano, J. R., Colonna, M., Ulrich, J. D., & Holtzman, D. M. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20210542 · Cited by 215
Self-citationGalectin-3 Deficiency Reduces the Severity of Experimental Autoimmune Encephalomyelitis
Jiang, H., Rasbi, Z. A., Mensah‐Brown, E. P. K., Shahin, A., Xu, D., Goodyear, C. S., Fukada, S. Y., Liu, F., Liew, F. Y., & Lukić, M. L. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.2.1167 · Cited by 190
Rojas, B., Gallego, B., Ramirez, A. I., Salazar, J. J., de Hoz, R., Valiente‐Soriano, F. J., Avilés‐Trigueros, M., Villegas‐Pérez, M. P., Vidal‐Sanz, M., Triviño, A., et al. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-133 · Cited by 188
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Chen, H., Wei, X., Cho, K., Chen, G., Sappington, R. M., Calkins, D. J., & Chen, D. F. (2010) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.09-5115 · Cited by 184
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Qin, Y., Garrison, B. S., Ma, W., Wang, R., Jiang, A., Li, J., Mistry, M., Bronson, R. T., Santoro, D., Franco, C., et al. (2018) · Cell · doi:10.1016/j.cell.2018.05.027 · Cited by 180
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Caberoy, N. B., Alvarado, G., Bigcas, J., & Li, W. (2012) · Journal of Cellular Physiology · doi:10.1002/jcp.22955 · Cited by 176
Bosco, A., Romero, C. O., Breen, K., Chagovetz, A. A., Steele, M. R., Ambati, B. K., & Vetter, M. L. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.018788 · Cited by 160
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Neher, J. J., Neniškytė, U., & Brown, G. C. (2012) · Frontiers in Pharmacology · doi:10.3389/fphar.2012.00027 · Cited by 157
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Albalawi, F., Lu, W., Beckel, J. M., Lim, J. C., McCaughey, S. A., & Mitchell, C. H. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00227 · Cited by 155
McKay, G. J., Patterson, C. C., Chakravarthy, U., Dasari, S., Klaver, C. C., Vingerling, J. R., Ho, L., de Jong, P. T. V. M., Fletcher, A. E., Young, I. S., et al. (2011) · Human Mutation · doi:10.1002/humu.21577 · Cited by 151
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Fortune, B. A., Bui, B. V., Morrison, J. C., Johnson, E. C., Dong, J., Cepurna, W. O., Jia, L., Barber, S. L., & Cioffi, G. A. (2004) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.03-1411 · Cited by 145
Levy, O., Calippe, B., Lavalette, S., Hu, S. J., Raoul, W., Dominguez, E., Housset, M., Pâques, M., Sahel, J., Bemelmans, A., et al. (2015) · EMBO Molecular Medicine · doi:10.15252/emmm.201404524 · Cited by 143
Mirzaei, M., Gupta, V. B., Chick, J. M., Greco, T. M., Wu, Y., Chitranshi, N., Wall, R. V., Hone, E., Deng, L., Dheer, Y., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-12858-7 · Cited by 141
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Howell, G. R., Libby, R. T., Marchant, J. K., Wilson, L. A., Cosma, I. M., Smith, R. S., Anderson, M. G., & John, S. W. M. (2007) · BMC Genetics · doi:10.1186/1471-2156-8-45 · Cited by 133
Wieghofer, P., Hagemeyer, N., Sankowski, R., Schlecht, A., Staszewski, O., Amann, L., Gruber, M., Koch, J., Hausmann, A., Zhang, P., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020105123 · Cited by 130
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Johnson, T. V., Bull, N. D., & Martin, K. R. G. (2010) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.09-3884 · Cited by 126
Harder, J. M., Braine, C., Williams, P. A., Zhu, X., MacNicoll, K. H., Sousa, G. L., Buchanan, R. A., Smith, R. S., Libby, R. T., Howell, G. R., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1608769114 · Cited by 114
Liu, Y., Zhao, C., Meng, J., Li, N., Xu, Z., Liu, X., & Hou, S. (2022) · Clinical Immunology · doi:10.1016/j.clim.2022.108939 · Cited by 112
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Almasieh, M., & Levin, L. A. (2017) · Annual Review of Vision Science · doi:10.1146/annurev-vision-102016-061422 · Cited by 111
Bosco, A., Anderson, S., Breen, K., Romero, C. O., Steele, M. R., Chiodo, V. A., Boye, S. L., Hauswirth, W. W., Tomlinson, S., & Vetter, M. L. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2018.08.017 · Cited by 110
Alqawlaq, S., Flanagan, J. G., & Sivak, J. M. (2018) · Experimental Eye Research · doi:10.1016/j.exer.2018.11.005 · Cited by 107
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Howell, G. R., Soto, I., Ryan, M. M., Graham, L. C., Smith, R. S., & John, S. W. M. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-76 · Cited by 97
Lerman, B. J., Hoffman, E. P., Sutherland, M. L., Bouri, K., Hsu, D. K., Liu, F., Rothstein, J. D., & Knoblach, S. M. (2012) · Brain and Behavior · doi:10.1002/brb3.75 · Cited by 93
Ma, W., Silverman, S. M., Zhao, L., Villasmil, R., Campos, M. M., Amaral, J., & Wong, W. T. (2019) · eLife · doi:10.7554/elife.42049 · Cited by 88
Lund, H., Pieber, M., Parsa, R., Grommisch, D., Ewing, E., Kular, L., Han, J., Zhu, K., Nijssen, J., Hedlund, E., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0091-5 · Cited by 86
Self-citationFractalkine receptor regulates microglial neurotoxicity in an experimental mouse glaucoma model
Wang, K., Peng, B., & Lin, B. (2014) · Glia · doi:10.1002/glia.22715 · Cited by 82
Inhibition of monocyte-like cell extravasation protects from neurodegeneration in DBA/2J glaucoma
Williams, P. A., Braine, C., Kizhatil, K., Foxworth, N. E., Tolman, N. G., Harder, J. M., Scott, R. A., Sousa, G. L., Panitch, A., Howell, G. R., et al. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0303-3 · Cited by 79
A Magnetic Microbead Occlusion Model to Induce Ocular Hypertension-Dependent Glaucoma in Mice
Itō, Y., Belforte, N., Vargas, J. L. C., & Polo, A. D. (2016) · Journal of Visualized Experiments · doi:10.3791/53731 · Cited by 77
Inoue, T., Kawaji, T., & Tanihara, H. (2013) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.13-12245 · Cited by 77
Sensing and clearance of apoptotic cells
Nagata, S., & Segawa, K. (2020) · Current Opinion in Immunology · doi:10.1016/j.coi.2020.07.007 · Cited by 71
Chen, W., Cao, Z., Leffler, H., Nilsson, U. J., & Panjwani, N. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-20009 · Cited by 70
Sapienza, A., Raveu, A.-L., Reboussin, É., Roubeix, C., Boucher, C., Dégardin, J., Godefroy, D., Rostène, W. H., Goazigo, A. R.-L., Baudouin, C., et al. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0509-7 · Cited by 70
Microglia modulation by TGF-β1 protects cones in mouse models of retinal degeneration
Wang, S. K., Xue, Y., & Cepko, C. L. (2020) · Journal of Clinical Investigation · doi:10.1172/jci136160 · Cited by 68
Campagno, K. E., Lu, W., Jassim, A. H., Albalawi, F., Cenaj, A., Tso, H., Clark, S. P., Sripinun, P., Gómez, N. M., & Mitchell, C. H. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02251-7 · Cited by 68
Association of Apolipoprotein E Polymorphisms With Normal Tension Glaucoma in a Chinese Population
Lam, C. Y., Fan, B. J., Wang, D. Y., Tam, P. O. S., Yung Tham, C. C., Leung, D. Y. L., Ping Fan, D. S., Chiu Lam, D. S., & Pang, C. P. (2006) · Journal of Glaucoma · doi:10.1097/01.ijg.0000212217.19804.a7 · Cited by 68
Vargas, J. L. C., Belforte, N., & Polo, A. D. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.05.002 · Cited by 60
(2005) · PubMed · Cited by 59
The role of microglia in the progression of glaucomatous neurodegeneration- a review
Zeng, H.-L., & Shi, J. (2018) · International Journal of Ophthalmology · doi:10.18240/ijo.2018.01.22 · Cited by 54
Tribble, J. R., Kokkali, E., Otmani, A., Plastino, F., Lardner, E., Vohra, R., Kolko, M., André, H., Morgan, J. E., & Williams, P. A. (2021) · Translational Vision Science & Technology · doi:10.1167/tvst.10.1.22 · Cited by 53
The Effect of A 2A Receptor Antagonist on Microglial Activation in Experimental Glaucoma
Liu, X., Huang, P. C., Wang, J., Yang, Z., Huang, S., Luo, X., Qi, J., Shen, X. P., & Zhong, Y. (2016) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-18024 · Cited by 52
Association of APOE With Primary Open-Angle Glaucoma Suggests a Protective Effect for APOE ε4
Margeta, M. A., Letcher, S. M., Igo, R. P., Cooke Bailey, J. N., Pasquale, L. R., Haines, J. L., Butovsky, O., Wiggs, J. L., & for the NEIGHBORHOOD consortium (2020) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.61.8.3 · Cited by 51
Self-citationCD163+ macrophages infiltrate axon bundles of postmortem optic nerves with glaucoma
Margeta, M. A., Lad, E. M., & Proia, A. D. (2018) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-018-4081-y · Cited by 49
Self-citationGpnmbR 150Xallele must be present in bone marrow derived cells to mediate DBA/2J glaucoma
Anderson, M. G., Nair, K. S., Amonoo, L. A., Mehalow, A. K., Trantow, C. M., Masli, S., & John, S. W. M. (2008) · BMC Genetics · doi:10.1186/1471-2156-9-30 · Cited by 45
Xiying, M., Wu, W., Fang, W., & Qing-huai, L. (2017) · Archives of Medical Research · doi:10.1016/j.arcmed.2017.08.002 · Cited by 43
A Magnetic Microbead Occlusion Model to Induce Ocular Hypertension-Dependent Glaucoma in Mice
Itō, Y., Belforte, N., Vargas, J. L. C., & Polo, A. D. (2016) · Journal of Visualized Experiments · doi:10.3791/53731-v · Cited by 36
Chidlow, G., Ebneter, A., Wood, J. P. M., & Casson, R. J. (2016) · Journal of Glaucoma · doi:10.1097/ijg.0000000000000447 · Cited by 32
Absence of galectin-3 promotes neuroprotection in retinal ganglion cells after optic nerve injury.
Abreu, C. A., de Lima, S., Mendonça, H. R., Goulart, C. O., & Martinez, A. M. B. (2017) · PubMed · doi:10.14670/hh-11-788 · Cited by 27
Wagner, T., Bartelt, A., Schlein, C., & Heeren, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0145102 · Cited by 21
Omodaka, K., Nishiguchi, K. M., Yasuda, M., Tanaka, Y., Sato, K., Nakamura, O., Maruyama, K., & Nakazawa, T. (2014) · Brain Research · doi:10.1016/j.brainres.2014.08.053 · Cited by 19
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ApoE in Alzheimer’s disease: pathophysiology and therapeutic strategies
Raulin, A.-C., Doss, S. V., Trottier, Z. A., Ikezu, T. C., Bu, G., & Liu, C.-C. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00574-4 · Cited by 756
Lee, S., Devanney, N. A., Golden, L. R., Smith, C. T., Schwartz, J. L., Walsh, A. E., Clarke, H. A., Goulding, D. S., Allenger, E. J., Morillo-Segovia, G., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112196 · Cited by 203
APOE4 impairs the microglial response in Alzheimer’s disease by inducing TGFβ-mediated checkpoints
Yin, Z., Rosenzweig, N., Kleemann, K. L., Zhang, X., Brandão, W., Margeta, M. A., Schroeder, C., Sivanathan, K. N., Silveira, S., Gauthier, C., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01627-6 · Cited by 202
“The reduction in LGALS3 immunoreactivity, a key MGnD marker 4,14 , was also observed in APOE4 mice compared to APOE3 mice in response to apoptotic neuron injection (Fig.”
BackgroundInfluentialSelf-citationImmune checkpoint TIM-3 regulates microglia and Alzheimer’s disease
Kimura, K., Subramanian, A., Yin, Z., Khalilnezhad, A., Wu, Y., He, D., Dixon, K. O., Chitta, U. K., Ding, X., Adhikari, N., et al. (2025) · Nature · doi:10.1038/s41586-025-08852-z · Cited by 85
Self-citationBrioschi, S., Belk, J. A., Peng, V., Molgora, M., Rodrigues, P. F., Nguyen, K. M., Wang, S., Du, S., Wang, W.-L., Grajales‐Reyes, G. E., et al. (2023) · Immunity · doi:10.1016/j.immuni.2023.01.028 · Cited by 86
Metadata
- Authors
- Margeta, M. A., Yin, Z., Madore, C., Pitts, K. M., Letcher, S. M., Tang, J., Jiang, S., Gauthier, C. D., Silveira, S. R., Schroeder, C. M., Lad, E. M., Proia, A. D., Tanzi, R. E., Holtzman, D. M., Krasemann, S., Chen, D. F., & Butovsky, O.
- Affiliations
- Brigham and Women's Hospital (US)
- Massachusetts Eye and Ear Infirmary (US)
- Duke Medical Center (US)
- Campbell University (US)
- Harvard University (US)
- Washington University in St. Louis (US)
- University Medical Center Hamburg-Eppendorf (DE)
- Corresponding author
- Butovsky, Oleg
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2022-09
- Volume
- 55
- Issue
- 9
- Pages
- 1627-1644.e7
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC9488669
- OpenAlex
- W4292055662
- Cited by
- 130
- References
- 104
- Citations by year
- 2026: 33 · 2025: 32 · 2024: 27 · 2023: 31 · 2022: 6
- FWCI
- 21.48
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 629 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion)
- Funders
- BrightFocus Foundation (2020A016806)
- National Multiple Sclerosis Society (5092A1)
- National Institute of Neurological Disorders and Stroke (R01 NS088137)
- National Institute on Aging (R01 AG054672, R01 AG051812)
- American Glaucoma Society
- ALS Association (EY025913, EY025259)
- Cure Alzheimer's Fund
- NIH
- National Eye Institute (K08 EY030160, R01 EY027921, K12 EY016335)
- Research to Prevent Blindness
- National Health and Medical Research Council (RG180378)
- Topics
- Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- APOE ε4, glaucoma, retinal microglia, neurodegeneration, retinal ganglion cell death, galectin-3, intraocular pressure, microglial activation, neuroprotection, ApoE-deficient mice, glaucoma treatment
- MeSH terms
- Animals, Apolipoproteins E, Disease Models, Animal, Glaucoma, Humans, Microglia, Galectin 3, Mice, Apolipoprotein E4
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 ›
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