Differential Phagocytic Properties of CD45low Microglia and CD45high Brain Mononuclear Phagocytes—Activation and Age-Related Effects
Open accessAbstract
In the central nervous system (CNS), microglia are innate immune mononuclear phagocytes (CNS MPs) that can phagocytose infectious particles, apoptotic cells, neurons and pathological protein aggregates such as Aβ in Alzheimer’s disease (AD). While CD11b+CD45low microglia account for the majority of CNS MPs, a small population of CD11b+CD45high CNS MPs is also recognized in AD that surround Aβ plaques. These transcriptionally-distinct and pathologically-relevant CD45high cells have unclear origin and undefined phagocytic characteristics. We have comprehensively validated rapid flow cytometric assays of bulk-phase and amyloid β fibril (fAβ) phagocytosis and applied these to study acutely isolated CNS MPs. Using these methods, we provide novel insights into differential abilities of CD11b+ CD45low and CD45high CNS MPs to phagocytose macroparticles and fAβ under normal, acute and chronic neuroinflammatory states. CD45high CNS MPs also highly upregulate TREM2, CD11c and several disease-associated-microglia (DAM) signature genes, and have a higher phagocytic capacity for Aβ as compared to CD45low microglia in the 5xFAD mouse model of AD that becomes more apparent with ageing. Our data suggest an overall pro-phagocytic and protective role for CD11b+CD45high CNS MPs in neurodegeneration, which if promoted, could be beneficial.
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?
Cytochalasin D inhibits the second peak of fluorescence in the Aβ42 phagocytosis assay, suggesting that the first peak represents non-specific binding of Aβ42 to cells and the second peak represents true actin-dependent uptake.
“We have found that Cytochalasin D inhibits the second peak of fluorescence in this assay, suggesting that the first peak represent non-specific binding of Aβ42 to cells while the second peak represents true uptake in an actin-dependent manner [31].”
From Identification and therapeutic modulation of a pro-inflammatory subset of disease-associated-microglia in Alzheimer’s disease (2018) · cites this paper as [31]
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
Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
A Unique Microglia Type Associated with Restricting Development of Alzheimer’s Disease
Keren-Shaul, H., Spinrad, A., Weiner, A., Matcovitch-Natan, O., Dvir-Szternfeld, R., Ulland, T. K., David, E., Baruch, K., Lara-Astaiso, D., Toth, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.018 · Cited by 5,493 · see citing works
Cox, J., Hein, M. Y., Luber, C. A., Paron, I., Nagaraj, N., & Mann, M. (2014) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m113.031591 · Cited by 5,180 · see citing works
Oakley, H., Cole, S. L., Logan, S., Maus, E., Shao, P., Craft, J., Guillozet-Bongaarts, A., Ohno, M., Disterhoft, J., Van Eldik, L., et al. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1202-06.2006 · Cited by 3,530 · cited 2× · see citing works
“Therefore, we studied phagocytic profiles of acutely isolated CNS MPs in the 5xFAD mouse model of AD pathology in which rapid accumulation of Aβ plaques begins at 3 months of age followed by neurodegeneration and neurobehavioral deficits by 8–10 months of age (59).”
BackgroundGene Ontology Consortium: going forward
The Gene Ontology Consortium (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1179 · Cited by 3,492 · see citing works
Hyman, B. T., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Carrillo, M. C., Dickson, D. W., Duyckaerts, C., Frosch, M. P., Masliah, E., et al. (2012) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.10.007 · Cited by 3,092 · see citing works
Variant of <i>TREM2</i> 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 · see citing works
Self-citationDifferential Roles of M1 and M2 Microglia in Neurodegenerative Diseases
Tang, Y., & Le, W. (2016) · Molecular Neurobiology · doi:10.1007/s12035-014-9070-5 · Cited by 2,190 · see citing works
Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration
Qin, L., Wu, X., Block, M. L., Liu, Y., Breese, G. R., Hong, J., Knapp, D. J., & Crews, F. T. (2007) · Glia · doi:10.1002/glia.20467 · Cited by 2,144 · see citing works
Microglial <scp>M1/M2</scp> polarization and metabolic states
Orihuela, R., McPherson, C. A., & Harry, G. J. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13139 · Cited by 2,070 · see citing works
New tools for studying microglia in the mouse and human CNS
Bennett, M. L., Bennett, F. C., Liddelow, S. A., Ajami, B., Zamanian, J. L., Fernhoff, N. B., Mulinyawe, S. B., Bohlen, C. J., Adil, A., Tucker, A., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525528113 · Cited by 1,804 · see citing works
Neuroinflammation and M2 Microglia: The Good, the Bad, and the Inflamed
Cherry, J. D., Olschowka, J. A., & O’Banion, M. K. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-98 · Cited by 1,748 · see citing works
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 · see citing works
A polarizing question: do M1 and M2 microglia exist?
Ransohoff, R. M. (2016) · Nature Neuroscience · doi:10.1038/nn.4338 · Cited by 1,573 · see citing works
The microglial sensome revealed by direct RNA sequencing
Hickman, S. E., Kingery, N. D., Ohsumi, T. K., Borowsky, M. L., Wang, L.-C., Means, T. K., & El Khoury, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3554 · Cited by 1,511 · see citing works
An environment-dependent transcriptional network specifies human microglia identity
Gosselin, D., Skola, D., Coufal, N. G., Holtman, I. R., Schlachetzki, J. C. M., Sajti, E., Jaeger, B. N., O’Connor, C., Fitzpatrick, C., Pasillas, M. P., et al. (2017) · Science · doi:10.1126/science.aal3222 · Cited by 1,220 · see citing works
ARUK Consortium, Sims, R., GERAD/PERADES, C., van der Lee, S. J., Naj, A. C., Bellenguez, C., Badarinarayan, N., Jakobsdottir, J., Kunkle, B. W., Boland, A., et al. (2017) · Nature Genetics · doi:10.1038/ng.3916 · Cited by 1,126 · see citing works
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
TREM2-mediated early microglial response limits diffusion and toxicity of amyloid plaques
Wang, Y., Ulland, T. K., Ulrich, J. D., Song, W., Tzaferis, J. A., Hole, J. T., Yuan, P., Mahan, T. E., Shi, Y., Gilfillan, S., et al. (2016) · Journal of Experimental Medicine · doi:10.1084/jem.20151948 · Cited by 840 · see citing works
Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia
Rosas‐Ballina, M., Ochani, M., Parrish, W. R., Ochani, K., Harris, Y., Huston, J. M., Chavan, S. S., & Tracey, K. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803237105 · Cited by 757 · see citing works
Phagocytosis and the actin cytoskeleton
May, R. C., & Machesky, L. M. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.6.1061 · Cited by 715 · see citing works
Jay, T. R., Miller, C. M., Cheng, P. J., Graham, L. C., Bemiller, S., Broihier, M. L., Xu, G., Margevicius, D., Karlo, J. C., Sousa, G. L., et al. (2015) · Journal of Experimental Medicine · doi:10.1084/jem.20142322 · Cited by 682 · cited 2× · see citing works
“who also found that 5xFAD CD45high CNS MPs selectively upregulated TREM2 expression in an age-dependent manner (69).”
BackgroundFriedman, B. A., Srinivasan, K., Ayalon, G., Meilandt, W. J., Lin, H., Huntley, M. A., Cao, Y., Lee, S.-H., Haddick, P. C. G., Ngu, H., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.066 · Cited by 662 · cited 1× · see citing works
“inflammatory activated Microglial states Microglia and CNS MPs adopt a diverse and complex array of activation states with distinct transcriptomic profiles that are now being revealed by RNA sequencing studies (12, 37, 51).”
BackgroundChiu, I. M., Morimoto, E. T. A., Goodarzi, H., Liao, J. T., O’Keeffe, S., Phatnani, H. P., Muratet, M., Carroll, M. C., Levy, S., Tavazoie, S., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.018 · Cited by 651 · see citing works
Chhor, V., Charpentier, T. L., Lebon, S., Oré, M. V., Lara‐Celador, I., Josserand, J., Degos, V., Jacotot, E. D., Hagberg, H., Sävman, K., et al. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.02.005 · Cited by 647 · see citing works
Phagocytosis of Microglia in the Central Nervous System Diseases
Fu, R., Shen, Q., Xu, P., Luo, J. J., & Tang, Y. (2014) · Molecular Neurobiology · doi:10.1007/s12035-013-8620-6 · Cited by 646 · see citing works
Quantitative proteomics reveals subset-specific viral recognition in dendritic cells
Luber, C. A., Cox, J., Lauterbach, H., Fancke, B., Selbach, M., Tschopp, J., Akira, S., Wiegand, M., Hochrein, H., O'Keeffe, M., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.01.013 · Cited by 576 · 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
A Cell Surface Receptor Complex for Fibrillar β-Amyloid Mediates Microglial Activation
Bamberger, M. E., Harris, M. E., McDonald, D. R., Husemann, J., & Landreth, G. E. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02665.2003 · Cited by 501 · see citing works
Casella, J. F., Flanagan, M. D., & Lin, S. (1981) · Nature · doi:10.1038/293302a0 · Cited by 488 · see citing works
Koenigsknecht-Talboo, J., & Landreth, G. E. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1808-05.2005 · Cited by 477 · see citing works
Seyfried, N. T., Dammer, E. B., Swarup, V., Nandakumar, D., Duong, D. M., Yin, L., Deng, Q., Nguyen, T., Hales, C. M., Wingo, T., et al. (2017) · Cell Systems · doi:10.1016/j.cels.2016.11.006 · Cited by 477 · see citing works
Self-citationA role for TREM2 ligands in the phagocytosis of apoptotic neuronal cells by microglia
Hsieh, C. L., Koike, M., Spusta, S. C., Niemi, E. C., Yenari, M., Nakamura, M. C., & Seaman, W. E. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06042.x · Cited by 475 · see citing works
Microglial Phagocytosis of Fibrillar β-Amyloid through a β1Integrin-Dependent Mechanism
Koenigsknecht-Talboo, J., & Landreth, G. E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2557-04.2004 · Cited by 444 · see citing works
Pavlov, V. A., Parrish, W. R., Rosas‐Ballina, M., Ochani, M., Gallowitsch‐Puerta, M., Ochani, K., Chavan, S. S., Al‐Abed, Y., & Tracey, K. J. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2008.06.011 · Cited by 437 · see citing works
Chen, Z., Jalabi, W., Shpargel, K. B., Farabaugh, K. T., Dutta, R., Yin, X., Kidd, G. J., Bergmann, C. C., Stohlman, S. A., & Trapp, B. D. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0730-12.2012 · Cited by 432 · see citing works
High-dimensional, single-cell characterization of the brain's immune compartment
Korin, B., Ben-Shaanan, T. L., Schiller, M., Dubovik, T., Azulay‐Debby, H., Boshnak, N., Koren, T., & Rolls, A. (2017) · Nature Neuroscience · doi:10.1038/nn.4610 · Cited by 423 · see citing works
Stansley, B., Post, J., & Hensley, K. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-115 · Cited by 419 · see citing works
TREM2 variants: new keys to decipher Alzheimer disease pathogenesis
Colonna, M., & Wang, Y. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.7 · Cited by 418 · see citing works
Sleep Loss Promotes Astrocytic Phagocytosis and Microglial Activation in Mouse Cerebral Cortex
Bellesi, M., de Vivo, L., Chini, M., Gilli, F., Tononi, G., & Cirelli, C. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3981-16.2017 · Cited by 417 · see citing works
Marsh, S. E., Abud, E. M., Lakatos, A., Karimzadeh, A., Yeung, S. T., Davtyan, H., Fote, G. M., Lau, L., Weinger, J. G., Lane, T. E., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525466113 · Cited by 411 · see citing works
Reactive astrocytes function as phagocytes after brain ischemia via ABCA1-mediated pathway
Morizawa, Y. M., Hirayama, Y., Ohno, N., Shibata, S., Shigetomi, E., Sui, Y., Nabekura, J., Sato, K., Okajima, F., Takebayashi, H., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00037-1 · Cited by 411 · see citing works
Fadok, V. A., Warner, M. L., Bratton, D. L., & Henson, P. M. (1998) · PubMed · Cited by 406 · see citing works
Fadok, V. A., Warner, M. L., Bratton, D. L., & Henson, P. M. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.11.6250 · Cited by 353 · see citing works
Monocyte subpopulations and their differentiation patterns during infection
Strauss‐Ayali, D., Conrad, S. M., & Mosser, D. M. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.0307191 · Cited by 348 · see citing works
Microglial Physiology and Pathophysiology: Insights from Genome-wide Transcriptional Profiling
Crotti, A., & Ransohoff, R. M. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.013 · Cited by 323 · see citing works
Jiang, T., Tan, L., Zhu, X.-C., Zhang, Q.-Q., Cao, L., Tan, M.-S., Gu, L.-Z., Wang, H.-F., Ding, Z.-Z., Zhang, Y.-D., et al. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.164 · Cited by 320 · see citing works
Is the class A macrophage scavenger receptor (SR-A) multifunctional? — The mouse’s tale
Platt, N., & Gordon, S. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13903 · Cited by 313 · see citing works
Is the class A macrophage scavenger receptor (SR-A) multifunctional? — The mouse’s tale
Platt, N., & Gordon, S. (2001) · Journal of Clinical Investigation · doi:10.1172/jci200113903 · Cited by 265 · see citing works
Differences in the Mode of Phagocytosis with Fc and C3 Receptors in Macrophages
Kaplan, G. (1977) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.1977.tb02153.x · Cited by 244 · see citing works
Intrahippocampal LPS injections reduce Aβ load in APP+PS1 transgenic mice
DiCarlo, G. (2001) · Neurobiology of Aging · doi:10.1016/s0197-4580(01)00292-5 · Cited by 223 · see citing works
Brain macrophages: questions of origin and interrelationship
Jordan, F. L., & Thomas, W. E. (1988) · Brain Research Reviews · doi:10.1016/0165-0173(88)90019-7 · Cited by 222 · see citing works
Arredouani, M. S., Palecanda, A., Koziel, H., Huang, Y.-C., Imrich, A., Sulahian, T. H., Ning, Y. Y., Yang, Z., Pikkarainen, T., Sankala, M., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.9.6058 · Cited by 222 · see citing works
MFG-E8 Mediates Primary Phagocytosis of Viable Neurons during Neuroinflammation
Fricker, M., Neher, J. J., Zhao, J.-W., Théry, C., Tolkovsky, A. M., & Brown, G. C. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4837-11.2012 · Cited by 218 · see citing works
Coppolino, M. G., Krause, M., Hagendorff, P., Monner, D. A., Trimble, W. S., Grinstein, S., Wehland, J., & Sechi, A. S. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.23.4307 · Cited by 200 · see citing works
Greenberg, S., el Khoury, J., di Virgilio, F., Kaplan, E. M., & Silverstein, S. C. (1991) · The Journal of cell biology · doi:10.1083/jcb.113.4.757 · Cited by 171 · see citing works
Das, A., Kim, S. H., Arifuzzaman, S., Yoon, T., Chai, J. C., Lee, Y. S., Park, K. S., Jung, K. H., & Chai, Y. G. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0644-1 · Cited by 171 · see citing works
Genetics ignite focus on microglial inflammation in Alzheimer’s disease
Malik, M., Parikh, I., Vasquez, J. B., Smith, C., Tai, L., Bu, G., LaDu, M. J., Fardo, D. W., Rebeck, G. W., & Estus, S. (2015) · Molecular Neurodegeneration · doi:10.1186/s13024-015-0048-1 · Cited by 161 · see citing works
Savage, J. C., Jay, T., Goduni, E., Quigley, C., Mariani, M. M., Malm, T., Ransohoff, R. M., Lamb, B. T., & Landreth, G. E. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4586-14.2015 · Cited by 154 · cited 1× · see citing works
“The presence of CD45+ TREM2+ CNS MPs around Aβ plaques in AD mouse models suggest a pro-phagocytic and Aβ-clearing role for CD45high cells (68), but direct functional characterization of phagocytic properties of CD45high CNS MPs, in contrast to CD45low CNS MPs, has not been performed.”
BackgroundFricker, 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
Primary Phagocytosis of Neurons by Inflamed Microglia: Potential Roles in Neurodegeneration
Neher, J. J., Neniškytė, U., & Brown, G. C. (2012) · Frontiers in Pharmacology · doi:10.3389/fphar.2012.00027 · Cited by 151 · see citing works
Woo, M., Yang, J., Beltran, C., & Cho, S. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.750018 · Cited by 136 · see citing works
Ryan, T. M., Caine, J. M., Mertens, H. D. T., Kirby, N. M., Nigro, J., Breheney, K., Waddington, L. J., Streltsov, V. A., Curtain, C. C., Masters, C. L., et al. (2013) · PeerJ · doi:10.7717/peerj.73 · Cited by 126 · see citing works
Tse, S. M. L., Furuya, W., Gold, E., Schreiber, A. D., Sandvig, K., Inman, R. D., & Grinstein, S. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m207966200 · Cited by 124 · see citing works
Isolation of highly enriched primary human microglia for functional studies
Rustenhoven, J., Park, T. I.-H., Schweder, P., Scotter, J., Correia, J., Smith, A. M., Gibbons, H. M., Oldfield, R. L., Bergin, P. S., Mee, E. W., et al. (2016) · Scientific Reports · doi:10.1038/srep19371 · Cited by 99 · see citing works
Multiparameter Flow Cytometry: Advances in High Resolution Analysis
O'Donnell, E. A., Ernst, D. N., & Hingorani, R. (2013) · Immune Network · doi:10.4110/in.2013.13.2.43 · Cited by 95 · see citing works
Microglia display modest phagocytic capacity for extracellular tau oligomers
Majerova, P., Zilkova, M., Kazmerova, Z., Kovac, A., Paholikova, K., Kovacech, B., Zilka, N., & Novak, M. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0161-z · Cited by 90 · see citing works
Takahashi, T., Takahashi, K., Mernaugh, R. L., Tsuboi, N., Liu, H., & Daniel, T. O. (2006) · Blood · doi:10.1182/blood-2005-10-4296 · Cited by 82 · see citing works
Migration of blood cells to β-amyloid plaques in Alzheimer's disease
Hohsfield, L. A., & Humpel, C. (2015) · Experimental Gerontology · doi:10.1016/j.exger.2015.03.002 · Cited by 79 · see citing works
Single-cell RNA sequencing identifies distinct mouse medial ganglionic eminence cell types
Chen, Y.-J. J., Friedman, B. A., Ha, C., Durinck, S., Liu, J., Rubenstein, J. L. R., Seshagiri, S., & Modrusan, Z. D. (2017) · Scientific Reports · doi:10.1038/srep45656 · Cited by 79 · see citing works
Rangaraju, S., Raza, S. A., Pennati, A., Deng, Q., Dammer, E. B., Duong, D., Pennington, M. W., Tansey, M. G., Lah, J. J., Betarbet, R., et al. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0906-6 · Cited by 75 · see citing works
Self-citationBiswas, S., Zimman, A., Gao, D., Byzova, T. V., & Podrez, E. A. (2017) · Circulation Research · doi:10.1161/circresaha.117.311069 · Cited by 75 · see citing works
Noristani, H. N., Gerber, Y. N., Sabourin, J.-C., Corre, M. L., Lonjon, N., Mestre‐Francés, N., Hirbec, H., & Perrin, F. E. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00090 · Cited by 73 · see citing works
P2Y6 Receptor-Mediated Microglial Phagocytosis in Radiation-Induced Brain Injury
Xu, Y., Hu, W., Liu, Y., Xu, P., Li, Z., Wu, R., Shi, X., & Tang, Y. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9282-3 · Cited by 58 · see citing works
Bell‐Temin, H., Culver‐Cochran, A. E., Chaput, D., Carlson, C., Kuehl, M. N., Burkhardt, B. R., Bickford, P. C., Liu, B., & Stevens, S. M. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m115.053926 · Cited by 58 · see citing works
Analysis of the Impact of CD200 on Phagocytosis
Lyons, A., Minogue, A. M., Jones, R. S., Fitzpatrick, O. M., Noonan, J., Campbell, V. A., & Lynch, M. A. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0223-6 · Cited by 43 · see citing works
Imaging Microglia in Live Brain Slices and Slice CulturesPreprint
Kurpius, D., & Dailey, M. E. (2007) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot4852 · Cited by 30 · see citing works
Imaging Microglia in Brain Slices and Slice CulturesPreprint
Dailey, M. E., Eyo, U. B., Fuller, L. C., Hass, J., & Kurpius, D. (2013) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot079483 · Cited by 29 · see citing works
αvβ5 Integrin/FAK/PGC-1α Pathway Confers Protective Effects on Retinal Pigment Epithelium
Roggia, M. F., & Ueta, T. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134870 · Cited by 25 · see citing works
Mutzke, E., Chomyshyn, E., Nguyen, K. C., Blahoianu, M., & Tayabali, A. F. (2015) · Analytical Biochemistry · doi:10.1016/j.ab.2015.04.034 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Rangaraju, S., Dammer, E. B., Raza, S. A., Rathakrishnan, P., Xiao, H., Gao, T., Duong, D. M., Pennington, M. W., Lah, J. J., Seyfried, N. T., et al. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0254-8 · Cited by 430 · see citing works
Self-citationMicroglia: 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
The choroid plexus links innate immunity to CSF dysregulation in hydrocephalus
Robert, S. M., Reeves, B. C., Kiziltug, E., Duy, P. Q., Karimy, J. K., Mansuri, M. S., Marlier, A., Allington, G., Greenberg, A. B. W., DeSpenza, T., et al. (2023) · Cell · doi:10.1016/j.cell.2023.01.017 · Cited by 160 · see citing works
Fairley, L. H., Lai, K. O., Wong, J. H., Chong, W. J., Vincent, A. S., D’Agostino, G. A., Wu, X., Naik, R. R., Jayaraman, A., Langley, S. R., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2209177120 · Cited by 127 · see citing works
SARS-CoV-2 Infection of Microglia Elicits Proinflammatory Activation and Apoptotic Cell Death
Jeong, G. U., Lyu, J., Kim, K., Chung, Y. C., Yoon, G. Y., Lee, S., Hwang, I., Shin, W.-H., Ko, J., Lee, J., et al. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01091-22 · Cited by 125 · see citing works
Luk, B., Engevik, M. A., Ganesh, B. P., Lackey, E. P., Lin, T., Balderas, M. A., Major, A. M., Runge, J. K., Luna, R. A., Sillitoe, R. V., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-64173-3 · Cited by 123 · see citing works
Extracellular signal‐regulated kinase regulates microglial immune responses in Alzheimer’s disease
Chen, M. J., Ramesha, S., Weinstock, L. D., Gao, T., Ping, L., Xiao, H., Dammer, E. B., Duong, D. D., Levey, A. I., Lah, J. J., et al. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24829 · Cited by 117 · see citing works
Self-citationBIN1 is a key regulator of proinflammatory and neurodegeneration-related activation in microglia
Sudwarts, A., Ramesha, S., Gao, T., Ponnusamy, M., Wang, S., Hansen, M. T., Kozlova, A., Bitarafan, S., Kumar, P., Beaulieu‐Abdelahad, D., et al. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00535-x · Cited by 107 · see citing works
Self-citationHonarpisheh, P., Lee, J., Banerjee, A., Blasco-Conesa, M. P., Honarpisheh, P., d’Aigle, J., Mamun, A. A., Ritzel, R. M., Chauhan, A., Ganesh, B. P., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02019-5 · Cited by 100 · see citing works
Thomas, A. L., Lehn, M. A., Janssen, E. M., Hildeman, D. A., & Chougnet, C. A. (2022) · Scientific Reports · doi:10.1038/s41598-022-21920-y · Cited by 94 · see citing works
Chen, S.-W., Hung, Y.-S., Fuh, J., Chen, N.-J., Chu, Y., Chen, S.-C., Fann, M., & Wong, Y. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.03.010 · Cited by 78 · see citing works
Decoding the temporal and regional specification of microglia in the developing human brain
Li, Y., Li, Z., Yang, M., Wang, F., Zhang, Y., Li, R., Li, Q., Gong, Y., Wang, B., Fan, B., et al. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.02.004 · Cited by 81 · see citing works
Welcome, M. O. (2019) · NeuroMolecular Medicine · doi:10.1007/s12017-019-08547-5 · Cited by 76 · see citing works
Koizumi, T., Kerkhofs, D., Mizuno, T., Steinbusch, H. W. M., & Foulquier, S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01291 · Cited by 73 · see citing works
Delbridge, A. R. D., Huh, D., Brickelmaier, M., Burns, J. C., Roberts, C., Challa, R., Raymond, N., Cullen, P., Carlile, T. M., Ennis, K. A., et al. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.592005 · Cited by 72 · see citing works
Rayaprolu, S., Gao, T., Xiao, H., Ramesha, S., Weinstock, L. D., Shah, J., Duong, D. M., Dammer, E. B., Webster, J. A., Lah, J. J., et al. (2019) · doi:10.1101/802694 · Cited by 71 · see citing works
Self-citationNeurovascular unit, neuroinflammation and neurodegeneration markers in brain disorders
Kempuraj, D., Dourvetakis, K. D., Cohen, J., Valladares, D. S., Joshi, R. S., Kothuru, S. P., Anderson, T., Chinnappan, B., Cheema, A. K., Klimas, N. G., et al. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1491952 · Cited by 75 · see citing works
Mercurio, D., Fumagalli, S., Schäfer, M., Pedragosa, J., Ngassam, L. D. C., Wilhelmi, V., Winterberg, S., Planas, A. M., Weihe, E., & Simoni, M.-G. D. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.820127 · Cited by 64 · see citing works
Gao, T., Jernigan, J. E., Raza, S. A., Dammer, E. B., Xiao, H., Seyfried, N. T., Levey, A. I., & Rangaraju, S. (2019) · Glia · doi:10.1002/glia.23678 · Cited by 64 · see citing works
Self-citationInterferon β-Mediated Protective Functions of Microglia in Central Nervous System Autoimmunity
Scheu, S., Ali, S., Mann‐Nüttel, R., Richter, L., Arolt, V., Dannlowski, U., Kuhlmann, T., Klotz, L., & Alferink, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20010190 · Cited by 48 · see citing works
Ramesha, S., Rayaprolu, S., Bowen, C. A., Giver, C. R., Bitarafan, S., Nguyen, H. M., Gao, T., Chen, M. J., Nwabueze, N. V., Dammer, E. B., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2013545118 · Cited by 47 · see citing works
Self-citationSaber, M., Giordano, K. R., Hur, Y., Ortiz, J. B., Morrison, H., Godbout, J. P., Murphy, S. M., Lifshitz, J., & Rowe, R. K. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14611 · Cited by 46 · see citing works
Ju, H., Park, K. W., Kim, I., Cave, J. W., & Cho, S. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02552-5 · Cited by 45 · see citing works
Divergent Functions of Tissue-Resident and Blood-Derived Macrophages in the Hemorrhagic Brain
Chang, C.-F., Goods, B. A., Askenase, M. H., Beatty, H. E., Osherov, A., DeLong, J. H., Hammond, M. D., Massey, J., Landreneau, M. J., Love, J. C., et al. (2021) · Stroke · doi:10.1161/strokeaha.120.032196 · Cited by 43 · see citing works
CD11bhigh B Cells Increase after Stroke and Regulate Microglia
Korf, J. M., Honarpisheh, P., Mohan, E. C., Banerjee, A., Blasco-Conesa, M. P., Honarpisheh, P., Guzman, G. U., Khan, R., Ganesh, B. P., Hazen, A. L., et al. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2100884 · Cited by 43 · see citing works
d -mannose suppresses oxidative response and blocks phagocytosis in experimental neuroinflammation
Wang, J., Motlagh, N. J., Wang, C., Wojtkiewicz, G. R., Schmidt, S., Chau, C., Narsimhan, R. P., Kuellenberg, E. G., Zhu, C., Linnoila, J., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2107663118 · Cited by 41 · see citing works
Kutsyr, O., Sánchez‐Sáez, X., Martínez‐Gil, N., de Juan, E., Lax, P., Maneu, V., & Cuenca, N. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.10.1 · Cited by 40 · see citing works
Functional and Metabolic Characterization of Microglia Culture in a Defined Medium
Montilla, A., Zabala, A., Matute, C., & Domercq, M. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00022 · Cited by 39 · see citing works
Sharps, M. C., Baker, B., Guevara, T., Bischof, H., Jones, R. L., Greenwood, S. L., & Heazell, A. E. P. (2020) · American Journal of Reproductive Immunology · doi:10.1111/aji.13267 · Cited by 34 · see citing works
Wu, S.-Y., Sharma, S., Wu, K., Tyagi, A., Zhao, D., Deshpande, R. P., & Watabe, K. (2021) · Breast Cancer Research · doi:10.1186/s13058-021-01412-z · Cited by 34 · see citing works
RetractedHwang, D., Ishikawa, L., Seyedsadr, M. S., Mari, E., Kasimoglu, E., Sahin, Z., Boehm, A., Jang, S., Rasouli, J., Vaccaro, C. N., et al. (2022) · Blood Advances · doi:10.1182/bloodadvances.2022008234 · Cited by 19 · see citing works
Khan, M. A. S., & Chang, S. L. (2023) · Cells · doi:10.3390/cells12202475 · Cited by 28 · see citing works
Schroeter, C. B., Herrmann, A. M., Böck, S., Vogelsang, A., Eichler, S., Albrecht, P., Meuth, S. G., & Ruck, T. (2021) · Cells · doi:10.3390/cells10030651 · Cited by 26 · see citing works
Immunoproteasomes control activation of innate immune signaling and microglial function
Çetin, G., Studencka‐Turski, M., Venz, S., Schormann, E., Junker, H., Hammer, E., Völker, U., Ebstein, F., & Krüger, E. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.982786 · Cited by 27 · see citing works
Sunna, S. N., Bowen, C. A., Zeng, H., Rayaprolu, S., Kumar, P., Bagchi, P., Dammer, E. B., Guo, Q., Duong, D. M., Bitarafan, S., et al. (2023) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2023.100546 · Cited by 25 · see citing works
Self-citationAssaying Microglia Functions In Vitro
Maguire, E., Connor‐Robson, N., Shaw, B., O’Donoghue, R., Stöberl, N., & Hall‐Roberts, H. (2022) · Cells · doi:10.3390/cells11213414 · Cited by 27 · see citing works
Li, H., Zhang, P., Liu, C., Wang, Y., Deng, Y., Dong, W., & Yu, Y. W. (2022) · Cells · doi:10.3390/cells12010008 · Cited by 25 · see citing works
Gao, T., Raza, S. A., Ramesha, S., Nwabueze, N. V., Tomkins, A. J., Cheng, L., Xiao, H., Yepes, M., & Rangaraju, S. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1510-8 · Cited by 23 · see citing works
Self-citationPathology of Amyloid-β (Aβ) Peptide Peripheral Clearance in Alzheimer’s Disease
Tsoy, A., Umbayev, B. A., Kassenova, A., Kaupbayeva, B., & Askarova, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252010964 · Cited by 23 · see citing works
Cho, S. M., Vardi, A., Platt, N., & Futerman, A. H. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14483 · Cited by 21 · see citing works
Strategies and Tools for Studying Microglial-Mediated Synapse Elimination and Refinement
Morini, R., Bizzotto, M., Perrucci, F., Filipello, F., & Matteoli, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.640937 · Cited by 20 · see citing works
Welcome, M. O. (2018) · Dementia and Geriatric Cognitive Disorders Extra · doi:10.1159/000492491 · Cited by 20 · see citing works
Norte‐Muñoz, M., Gallego‐Ortega, A., Lucas‐Ruiz, F., González‐Riquelme, M. J., Changa-Espinoza, Y. I., Galindo‐Romero, C., Ponsaerts, P., Vidal‐Sanz, M., García‐Bernal, D., & Agudo‐Barriuso, M. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03129-y · Cited by 19 · see citing works
Bobotis, B. C., Halvorson, T., Carrier, M., & Tremblay, M. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1317125 · Cited by 21 · see citing works
Myeloid cell subpopulations compensate each other for Ccr2‐deficiency in glioblastoma
Bungert, A. D., Urbantat, R. M., Jelgersma, C., Bekele, B. M., Mueller, S. G., Mueller, A., Felsenstein, M., Dusatko, S., Blank, A., Ghori, A., et al. (2022) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12863 · Cited by 18 · see citing works
Immune response of BV-2 microglial cells is impacted by peroxisomal beta-oxidation
Tawbeh, A., Raas, Q., Tahri-Joutey, M., Keime, C., Kaiser, R., Trompier, D., Nasser, B., Bellanger, E., Dessard, M., Hamon, Y., et al. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1299314 · Cited by 18 · see citing works
Modulation of Innate Immunity by Amyloidogenic Peptides
Westwell-Roper, C. Y., & Verchere, C. B. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.06.005 · Cited by 17 · see citing works
SARS-CoV-2 Infection of Microglia Elicits Pro-inflammatory Activation and Apoptotic Cell DeathPreprint
Jeong, G. U., Lyu, J., Kim, K., Chung, Y. C., Yoon, G. Y., Lee, S., Hwang, I., Shin, W.-H., Ko, J., Lee, J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.04.475015 · Cited by 17 · see citing works
Decoding the role of zebrafish neuroglia in CNS disease modeling.
Zabegalov, K., Wang, D.-M., Yang, L.-E., Wang, J.-T., Hu, G.-J., Serikuly, N., Alpyshov, E. T., Khatsko, S., Zhdanov, A., Demin, K., et al. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.09.020 · Cited by 15 · see citing works
Li, H., Ye, T., Liu, X., Guo, R., Yang, X., Li, Y., Qi, D., Wei, Y., Zhu, Y., Wen, L., et al. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.05.008 · Cited by 15 · see citing works
Novel Microglia Cell Line Expressing the Human EP2 Receptor
Rojas, A., Banik, A., Chen, D., Flood, K., Ganesh, T., & Dingledine, R. J. (2019) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.9b00311 · Cited by 15 · see citing works
Novel protocol for the isolation of highly purified neonatal murine microglia and astrocytes
Zelenka, L., Pägelow, D., Krüger, C., Seele, J., Ebner, F., Rausch, S., Rohde, M., Lehnardt, S., van Vorst, K., & Fulde, M. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109420 · Cited by 15 · see citing works
Jäkel, L., Biemans, E. A. L. M., Klijn, C. J. M., Kuiperij, H. B., & Verbeek, M. M. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01873-x · Cited by 14 · see citing works
Francistiová, L., Vörös, K., Lovász, Z., Dinnyés, A., & Kobolák, J. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.793769 · Cited by 14 · see citing works
Recent Progress in Multiple Sclerosis Treatment Using Immune Cells as Targets
Ma, X., Ma, R., Zhang, M.-Z., Qian, B., Wang, B., & Yang, W.-J. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15030728 · Cited by 12 · see citing works
Advances in proteomic phenotyping of microglia in neurodegeneration
Sunna, S. N., Bowen, C. A., Ramelow, C. C., Santiago, J. V., Kumar, P., & Rangaraju, S. (2023) · PROTEOMICS · doi:10.1002/pmic.202200183 · Cited by 12 · see citing works
Self-citationChirico, F. D., Poeta, E., Babini, G., Piccolino, I., Monti, B., & Massenzio, F. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1038721 · Cited by 11 · see citing works
Chen, J., Chen, H., Wei, Q., Lu, Y., Wang, T., Pang, X., Xing, G., Chen, Z., Cao, X., & Yao, J. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02454-4 · Cited by 11 · see citing works
García‐Juárez, M., García-Rodríguez, A., Cruz-Carrillo, G., Flores-Maldonado, O. E., Becerril-García, M. A., Garza‐Ocañas, L., Torre-Villalvazo, I., & Camacho‐Morales, A. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04340-z · Cited by 10 · see citing works
Sánchez-García, M. A., Lara-Ureña, N., March‐Díaz, R., Luis, C. O. S., Quiñones-Cañete, S., Mora-Romero, B., Cabello-Rivera, D., Cabello-Rivera, D., Romero‐Molina, C., Romero‐Molina, C., et al. (2025) · Science Advances · doi:10.1126/sciadv.adu2244 · Cited by 9 · see citing works
Zhang, X., Yuan, J., Zhang, S., Li, W., Xu, Y., Li, H., Zhang, L., Chen, X., Ding, W., Zhu, J., et al. (2022) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x221147091 · Cited by 10 · see citing works
Mimouna, S., Rollins, D. A., Shibu, G., Tharmalingam, B., Deochand, D. K., Chen, X., Oliver, D., Chinenov, Y. V., & Rogatsky, I. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20192386 · Cited by 10 · see citing works
He, A., Wang, Y., Shen, Y., Dong, Z., Luo, L., Ge, X., Liu, X., Mao, Y., Zhang, T., Li, X., et al. (2025) · Nature Aging · doi:10.1038/s43587-025-01028-4 · Cited by 9 · see citing works
He, J., Zhao, F., Chen, B., Cui, N., Li, Z., Qin, J., Luo, L., Zhao, C., & Li, L. (2023) · Science China Life Sciences · doi:10.1007/s11427-021-2223-4 · Cited by 9 · see citing works
Interrogation of human microglial phagocytosis by CRISPR genome editing
Chang, J. C.-Y., Wang, C., & Lin, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1169725 · Cited by 9 · see citing works
Method of Microglial DNA-RNA Purification from a Single Brain of an Adult Mouse
Raihan, M. O., McGregor, B. A., Velaris, N. A., Brishti, A., Hur, J., & Porter, J. E. (2021) · Methods and Protocols · doi:10.3390/mps4040086 · Cited by 8 · see citing works
The changing landscape of immune cells in the fetal mouse testis
Hosseini, S., Moody, S. C., Fietz, D., Indumathy, S., Schuppe, H.-C., Hedger, M. P., & Loveland, K. L. (2022) · Histochemistry and Cell Biology · doi:10.1007/s00418-022-02129-6 · Cited by 8 · see citing works
Jahromi, S. R., Haddadi, M., Mousavi, P., & Sanadgol, N. (2022) · Metabolic Brain Disease · doi:10.1007/s11011-022-01083-5 · Cited by 8 · see citing works
Liu, L.-Z., Fan, S., Gao, J., Li, W., & Xian, X. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.110683 · Cited by 9 · see citing works
Gardner, R. S., Kyle, M. M., Hughes, K., & Zhao, L. (2024) · Biomolecules · doi:10.3390/biom14070827 · Cited by 7 · see citing works
Topological Dissection of Proteomic Changes Linked to the Limbic Stage of Alzheimer’s Disease
Velásquez, E., Szeitz, B., Gil, J., Murillo, J. R., Palkovits, M., Renner, É., Hortobágyi, T., Döme, P., Nogueira, F. C. S., Marko‐Varga, G., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.750665 · Cited by 8 · see citing works
The effects of okadaic acid‐treated SH‐SY5Y cells on microglia activation and phagocytosis
Amonruttanapun, P., Chongthammakun, S., & Chamniansawat, S. (2021) · Cell Biology International · doi:10.1002/cbin.11722 · Cited by 8 · see citing works
An anti-inflammatory transcriptional cascade conserved from flies to humans
Pavlidaki, A., Panic, R., Monticelli, S., Riet, C., Yuasa, Y., Cattenoz, P. B., Nait‐Oumesmar, B., & Giangrande, A. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111506 · Cited by 8 · see citing works
Lin, C., Calzarossa, C., Fernández-Zafra, T., Liu, J., Li, X., Ekblad, Å., Vázquez‐Juárez, E., Codeluppi, S., Holmberg, L., Lindskog, M., et al. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01771-y · Cited by 8 · see citing works
Specificity and efficiency of tamoxifen-mediated Cre induction is equivalent regardless of age
Kellogg, C. M., Pham, K. D., Ko, S.-H., Cox, J. E. J., Machalinski, A. H., Stout, M. B., Sharpe, A. L., Beckstead, M. J., Chucair‐Elliott, A. J., Ocañas, S. R., et al. (2023) · iScience · doi:10.1016/j.isci.2023.108413 · Cited by 9 · see citing works
Ni, J.-W., Li, C., Chen, X., & Cai, W. (2022) · Neurology India · doi:10.4103/0028-3886.364080 · Cited by 7 · see citing works
Su, X., Xie, L., Li, J., Tian, X., Bing, L., & Chen, M. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1133106 · Cited by 9 · see citing works
Ramesha, S., Rayaprolu, S., & Rangaraju, S. (2020) · Journal of Visualized Experiments · doi:10.3791/61467 · Cited by 7 · see citing works
Self-citationCrews, F. T., Qin, L., Coleman, L. G., Vidrascu, E. M., & Vetreno, R. P. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.106156 · Cited by 7 · see citing works
Ruiz-Pastor, M. J., Sánchez‐Sáez, X., Kutsyr, O., Albertos‐Arranz, H., Sánchez‐Castillo, C., Ortuño‐Lizarán, I., Martínez‐Gil, N., Vidal‐Gil, L., Méndez, L., Sánchez‐Martín, M., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-06243-8 · Cited by 6 · see citing works
Lin, Y. N., Mao, F., Wong, N.-K., Zhang, X., Liu, K., Huang, M., Ma, H., Xiang, Z., Li, J., Xiao, S., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00416 · Cited by 6 · see citing works
Cheng, J.-J., Guo, Q. H., Wu, X.-G., Ma, S., Gao, Y., & Yazhen, S. (2020) · Combinatorial Chemistry & High Throughput Screening · doi:10.2174/1386207323666201209092358 · Cited by 5 · see citing works
Shin, T. H., Lee, D. Y., Jang, Y. E., Kwon, D. H., Hwang, J. S., Kim, S. G., Seo, C., Paik, M., Lee, J. Y., Kim, J. Y., et al. (2022) · Cells · doi:10.3390/cells11152393 · Cited by 5 · see citing works
Early ultrastructural damage in retina and optic nerve following intraocular pressure elevation
Abreu, C. A., Ferraz, G., dos Santos, R. C., Conde, L., Dantas, D. P., Archanjo, B. S., Linden, R., Pimentel‐Coelho, P. M., & Allodi, S. (2025) · Vision Research · doi:10.1016/j.visres.2025.108544 · Cited by 4 · see citing works
Ting, S., Zhao, X., Sun, G., Ricote, M., & Aronowski, J. A. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0248-25.2025 · Cited by 4 · see citing works
Berríos‐Cárcamo, P., Núñez, S., Castañeda, J., Gallardo, J., Bono, M. R., & Ezquer, F. E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084173 · Cited by 4 · see citing works
Hu, Y., Wang, X., Zhao, Z., Liu, M., Ren, X., Xian, X., Liu, C., & Wang, Q. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-240118 · Cited by 4 · see citing works
Latham, A. S., Geer, C. E., Ackart, D. F., Weninger, K. N., Gross, C. C., Podell, B. K., Basaraba, R. J., & Moreno, J. A. (2024) · PLoS ONE · doi:10.1371/journal.pone.0307577 · Cited by 5 · see citing works
RGS10 attenuates systemic immune dysregulation induced by chronic inflammatory stress
Jernigan, J. E., Staley, H. A., Baty, Z., Bolen, M. L., Gomes, B. N., Holt, J., Cole, C. L., Neighbarger, N. K., Dheeravath, K., Merchak, A. R., et al. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03322-1 · Cited by 4 · see citing works
Improved human hematopoietic reconstitution in HepaRG co-transplanted humanized NSG mice
Kim, J., Ryu, B., Kim, U., Kim, C., Hur, G.-H., Kim, C., & Park, J. (2020) · BMB Reports · doi:10.5483/bmbrep.2020.53.9.304 · Cited by 4 · see citing works
Cho, H., Choi, B. Y., Shin, Y., Suh, S. W., & Park, S. B. (2023) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00508 · Cited by 4 · see citing works
Mitochondrial control of microglial phagocytosis in Alzheimer’s diseasePreprint
Fairley, L. H., Lai, K. O., Wong, J. H., Salvatore, A. V., D’Agostino, G. A., Wu, X., Jayaraman, A., Langley, S. R., Ruedl, C., & Barron, A. M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.01.469111 · Cited by 4 · see citing works
Emerging Techniques for the Study of Microglia: Visualization, Depletion and Fate MappingPreprint
Bobotis, B. C., Halvorson, T., Carrier, M., & Tremblay, M. (2023) · Preprints.org · doi:10.20944/preprints202308.2190.v1 · Cited by 3 · see citing works
Li, R., Zhang, J., Fan, J.-Q., & Lin, B. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03692-8 · Cited by 3 · see citing works
Capes, D. E., Slone, V. K., Winchester, D. K., Salazar, J., Opoku, P., Li, Y., Hash, M. T., Kumari, R., Hawk, G. S., & Stewart, A. N. (2026) · Experimental Neurology · doi:10.1016/j.expneurol.2026.115690 · Cited by 3 · see citing works
Dual immune armies in glaucoma: microglia and monocyte-derived macrophages
Tan, K., Zhang, Y., Jiang, P., Yu, Y., Wu, Z. G., Peng, J. Q., Liu, P., & Peng, Q. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1801497 · Cited by 3 · see citing works
Reconstitution of human microglia and resident T cells in the brain of humanized DRAGA mice
Roy, S. G., Karim, A. F., Brumeanu, T., & Casares, S. A. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1367566 · Cited by 3 · see citing works
Microglia-specificity of different markers is overridden in glioblastoma specimens
Bungert, A. D., Sanchin, A., Blank, A., Jüngst-Mieczkowska, M., Müller, A., Felsenstein, M., Turkowski, K., Zhang, W., Vajkoczy, P., & Brandenburg, S. (2026) · Scientific Reports · doi:10.1038/s41598-026-52315-y · Cited by 2 · see citing works
Dynamics of CD44+ bovine nucleus pulposus cells with inflammation
Ferreira, J. N., Caldeira, J., Sousa, M. M., Barbosa, M. A., Lamghari, M., Almeida-Porada, G. D., & Gonçalves, R. M. (2024) · Scientific Reports · doi:10.1038/s41598-024-59504-7 · Cited by 2 · see citing works
Mimouna, S., Rollins, D. A., Shibu, G., Tharmalingam, B., Deochand, D. K., Chen, X., Oliver, D., Chinenov, Y. V., & Rogatsky, I. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.2019238611162020c · Cited by 3 · see citing works
- Authors
- Rangaraju, S., Raza, S. A., Li, N. X., Betarbet, R., Dammer, E. B., Duong, D., Lah, J. J., Seyfried, N. T., & Levey, A. I.
- Affiliations
- Emory University (US)
- Corresponding author
- Rangaraju, Srikant
- ORCID
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2018-03-02
- Volume
- 9
- Pages
- 405-405
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC5840283
- OpenAlex
- W2792377614
- Cited by
- 126
- References
- 80
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 12 · 2023: 18 · 2022: 35 · 2021: 13 · 2020: 19 · 2019: 8 · 2018: 3 · 2017: 1
- FWCI
- 4.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (P50 AG025688, NS099474-1, P30 NS055077, 1U01AG046161)
- National Science Foundation (CHE-1507932, NSF/DMR-BSF 1610377)
- American Brain Foundation
- Alzheimer’s Association
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- microglia, phagocytosis, amyloid-beta fibrils, Alzheimer's disease, disease-associated microglia, TREM2, CD11c, neuroinflammation, aging, 5xFAD mice, neurodegeneration
- MeSH terms
- Aging, Alzheimer Disease, Animals, Brain, Cell Line, Disease Models, Animal, Humans, Membrane Glycoproteins, Mice, Inbred C57BL, Mice, Mutant Strains, Phagocytes, Phagocytosis, Receptors, Immunologic, Mononuclear Phagocyte System, Amyloid beta-Peptides, Leukocyte Common Antigens, Microglia, Mice
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