Microglial Beclin 1 Regulates Retromer Trafficking and Phagocytosis and Is Impaired in Alzheimer’s Disease
Open accessAbstract
Phagocytosis controls CNS homeostasis by facilitating the removal of unwanted cellular debris. Accordingly, impairments in different receptors or proteins involved in phagocytosis result in enhanced inflammation and neurodegeneration. While various studies have identified extrinsic factors that modulate phagocytosis in health and disease, key intracellular regulators are less understood. Here we show that the autophagy protein beclin 1 is required for efficient phagocytosis in vitro and in mouse brains. Furthermore, we show that beclin 1-mediated impairments in phagocytosis are associated with dysfunctional recruitment of retromer to phagosomal membranes, reduced retromer levels, and impaired recycling of phagocytic receptors CD36 and Trem2. Interestingly, microglia isolated from human Alzheimer's disease (AD) brains show significantly reduced beclin 1 and retromer protein levels. These findings position beclin 1 as a link between autophagy, retromer trafficking, and receptor-mediated phagocytosis and provide insight into mechanisms by which phagocytosis is regulated and how it may become impaired in AD.
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Although beads are not physiological substrates of phagocytes, they serve as experimental substrates to probe phagocytic response under in vitro experimental conditions.
“Although the beads are not physiological substrates of phagocytes, they serve as experimental substrates to probe phagocytic response under in vitro experimental conditions [37].”
From Multifaceted response of microglia in the cuprizone model of demyelination (2026) · cites this paper as [37]
Microglial phagocytosis of Aβ deposits in Alzheimer disease models requires the autophagy-related factors BECN1, ATG7 and LC3.
“microglial phagocytosis of Aβ deposits in Alzheimer disease models [430,431] requires the autophagy-related factors BECN1, ATG7 and LC3 [432,433].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [433]
Autophagy may enhance microglial clearance of Aβ, as it does in neurons.
“autophagy may also enhance microglial clearance of Aβ”
From TREM2 Maintains Microglial Metabolic Fitness in Alzheimer’s Disease (2017) · cites this paper as Lucin et al., 2013
Beclin 1 protein levels are decreased in microglia from Alzheimer's disease brains.
“and that this protein is decreased in microglia from AD brains [153].”
From Microglial dysfunction in brain aging and Alzheimer's disease (2014) · cites this paper as [153]
Reducing beclin 1 genetically disrupted phagocytosis and retromer-mediated recycling of the phagocytic receptors CD36 and TREM2 in microglia.
“a study from our laboratory recently demonstrated that genetic-reduction of beclin 1, a protein classically associated with the autophagy degradation pathway, disrupted phagocytosis and retromer-mediated recycling of the phagocytic receptors CD36 and TREM2 in microglia”
From Microglial dysfunction in brain aging and Alzheimer's disease (2014) · cites this paper as [153]
Expression of several autophagy proteins, particularly Beclin1, ATG5, and ATG7, declines with age and is exacerbated in Alzheimer's disease.
“The expression of several autophagy proteins, in particular Beclin1, ATG5, and ATG7, decline with age, and is exacerbated in AD (Lipinski et al., 2010; Lucin et al., 2013; Pickford et al., 2008; Rubinsztein et al., 2011).”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Lucin et al., 2013
RavZ prevented receptor recycling.
“The Legionella-derived protease, RavZ, which irreversibly cleaves lipidated LC3 (Choy et al., 2012; Kwon et al., 2017) also prevented this receptor recycling, again, as defined by this method (Lucin et al., 2013; Yin et al., 2016).”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Lucin et al., 2013
A previous study showed that recycling of CD36 and TREM2 is dependent on Beclin1 and VPS34.
“A previous study had shown that this recycling of CD36 and TREM2 is dependent on Beclin1 and VPS34 (Lucin et al., 2013), which we confirmed in primary BMDM (Fig. 3).”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Lucin et al., 2013
LANDO is required for the recycling of putative Aβ receptors (CD36, TREM2, and TLR4) from internalized endosomes to the plasma membrane.
“According to the receptor-recycling method we employed and established by others (Lucin et al., 2013; Yin et al., 2016), we found that LANDO is required for the recycling of putative Aβ receptors (CD36, TREM2, and TLR4) from internalized endosomes to the plasma membrane.”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Lucin et al., 2013
The receptor recycling method is well-established and was used as previously reported by Lucin et al. (2013).
“This method is well-established and used as previously reported (Lucin et al., 2013).”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Lucin et al., 2013
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2 retracted
Martinez, J., Almendinger, J., Oberst, A., Ness, R., Dillon, C. P., Fitzgerald, P., Hengartner, M. O., & Green, D. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113421108 · Cited by 655 · cited 1× · see citing works
“Although inhibiting beclin 1 is likely to affect various cellular processes that could influence substrate clearance, including autophagy and potentially phagosomal maturation (which has been described for phagosomes containing apoptotic cells, entotic cells, and bacteria (Berger et al., 2010; Florey et al., 2011; Ma…”
RetractedCrews, L., Spencer, B., Desplats, P., Patrick, C., Paulino, A., Rockenstein, E., Hansen, L., Adame, A., Galasko, D., & Masliah, E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009313 · Cited by 376 · see citing works
Self-citationRetractedResting microglial cells are highly dynamic surveillants of brain parenchyma in vivo
Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005) · Science · doi:10.1126/science.1110647 · Cited by 5,827 · see citing works
Synaptic Pruning by Microglia Is Necessary for Normal Brain Development
Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L., et al. (2011) · Science · doi:10.1126/science.1202529 · Cited by 4,244 · see citing works
Autophagy in immunity and inflammation
Levine, B., Mizushima, N., & Virgin, H. W. (2011) · Nature · doi:10.1038/nature09782 · Cited by 3,289 · see citing works
<i>TREM2</i> 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 · see citing works
NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice
Heneka, M. T., Kummer, M. P., Stutz, A., Delekate, A., Schwartz, S., Vieira-Saecker, A., Griep, A., Axt, D., Remus, A., Tzeng, T.-C., et al. (2013) · Nature · doi:10.1038/nature11729 · Cited by 2,898 · see citing works
The role of autophagy during the early neonatal starvation period
Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., & Mizushima, N. (2004) · Nature · doi:10.1038/nature03029 · Cited by 2,865 · 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
Impairment of starvation-induced and constitutive autophagy in <i>Atg7</i> -deficient mice
Komatsu, M., Waguri, S., Ueno, T., Iwata, J., Murata, S., Tanida, I., Ezaki, J., Mizushima, N., Ohsumi, Y., Uchiyama, Y., et al. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200412022 · Cited by 2,331 · see citing works
Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene
Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.-L., Mizushima, N., Ohsumi, Y., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20039 · Cited by 2,311 · see citing works
Yue, Z., Jin, S., Yang, C., Levine, A. J., & Heintz, N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2436255100 · Cited by 2,116 · see citing works
Bard, F., Cannon, C., Barbour, R., Burke, R.-L., Games, D., Grajeda, H., Guido, T., Hu, K., Huang, J., Johnson-Wood, K., et al. (2000) · Nature Medicine · doi:10.1038/78682 · Cited by 2,012 · see citing works
Network organization of the human autophagy system
Behrends, C., Sowa, M. E., Gygi, S. P., & Harper, J. W. (2010) · Nature · doi:10.1038/nature09204 · Cited by 1,554 · see citing works
Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis
Sanjuan, M. A., Dillon, C. P., Tait, S. W. G., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., et al. (2007) · Nature · doi:10.1038/nature06421 · Cited by 1,347 · see citing works
Lee, J.-H., Yu, W. H., Kumar, A., Lee, S., Mohan, P. S., Peterhoff, C. M., Wolfe, D. M., Martinez-Vicente, M., Massey, A. C., Sovak, G., et al. (2010) · Cell · doi:10.1016/j.cell.2010.05.008 · Cited by 1,212 · see citing works
Pickford, F., Masliah, E., Britschgi, M., Lucin, K. M., Narasimhan, R., Jaeger, P. A., Small, S., Spencer, B., Rockenstein, E., Levine, B., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33585 · Cited by 1,186 · see citing works
Self-citationRapid appearance and local toxicity of amyloid-β plaques in a mouse model of Alzheimer’s disease
Meyer-Luehmann, M., Spires-Jones, T. L., Prada, C., Garcia-Alloza, M., de Calignon, A., Rozkalne, A., Koenigsknecht-Talboo, J., Holtzman, D. M., Bacskai, B. J., & Hyman, B. T. (2008) · Nature · doi:10.1038/nature06616 · Cited by 987 · see citing works
A Mutation in VPS35, Encoding a Subunit of the Retromer Complex, Causes Late-Onset Parkinson Disease
Zimprich, A. A., Benet‐Pagès, A., Struhal, W., Graf, E., Eck, S. H., Offman, M. N., Haubenberger, D., Spielberger, S., Schulte, E. C., Lichtner, P., et al. (2011) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2011.06.008 · Cited by 885 · see citing works
VPS35 Mutations in Parkinson Disease
Vilariño‐Güell, C., Wider, C. W., Ross, O. A., Dächsel, J. C., Kachergus, J. M., Lincoln, S., Soto‐Ortolaza, A. I., Cobb, S. A., Wilhoite, G. J., Bacon, J. A., et al. (2011) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2011.06.001 · Cited by 877 · see citing works
HSV-1 ICP34.5 Confers Neurovirulence by Targeting the Beclin 1 Autophagy Protein
Orvedahl, A., Alexander, D., Tallóczy, Z., Sun, Q., Wei, Y., Zhang, W., Burns, D., Leib, D. A., & Levine, B. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2006.12.001 · Cited by 857 · see citing works
The Beclin 1–VPS34 complex – at the crossroads of autophagy and beyond
Funderburk, S. F., Wang, Q. J., & Yue, Z. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.03.002 · Cited by 785 · see citing works
Moloney, A. M., Griffin, R. J., Timmons, S., O’Connor, R., Ravid, R., & O’Neill, C. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.04.002 · Cited by 764 · see citing works
Homeostatic Regulation of the Immune System by Receptor Tyrosine Kinases of the Tyro 3 Family
Lu, Q., & Lemke, G. (2001) · Science · doi:10.1126/science.1061663 · Cited by 699 · see citing works
Immune activation in brain aging and neurodegeneration: too much or too little?
Lucin, K. M., & Wyss-Coray, T. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.039 · Cited by 679 · see citing works
Self-citationAutophagy Gene-Dependent Clearance of Apoptotic Cells during Embryonic Development
Qu, X., Zou, Z., Sun, Q., Luby‐Phelps, K., Cheng, P., Hogan, R. N., Gilpin, C. J., & Levine, B. (2007) · Cell · doi:10.1016/j.cell.2006.12.044 · Cited by 655 · see citing works
Andersen, O. M., Reiche, J., Schmidt, V., Gotthardt, M., Spoelgen, R., Behlke, J., von Arnim, C. A. F., Breiderhoff, T., Jansen, P., Wu, X., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503689102 · Cited by 655 · see citing works
Spencer, B., Potkar, R., Trejo, M., Rockenstein, E., Patrick, C., Gindi, R., Adame, A., Wyss-Coray, T., & Masliah, E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4390-09.2009 · Cited by 595 · see citing works
Self-citationTGF-β1 promotes microglial amyloid-β clearance and reduces plaque burden in transgenic mice
Wyss-Coray, T., Lin, C., Yan, F., Yu, G.-Q., Rohde, M., McConlogue, L., Masliah, E., & Mucke, L. (2001) · Nature Medicine · doi:10.1038/87945 · Cited by 587 · see citing works
Self-citationVieira, O. V., Botelho, R. J., Rameh, L. E., Brachmann, S. M., Matsuo, T., Davidson, H. W., Schreiber, A. D., Backer, J., Cantley, L. C., & Grinstein, S. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200107069 · Cited by 530 · see citing works
RAB7L1 Interacts with LRRK2 to Modify Intraneuronal Protein Sorting and Parkinson’s Disease Risk
MacLeod, D. A., Rhinn, H., Kuwahara, T., Zolin, A., Paolo, G. D., McCabe, B. D., Marder, K. S., Honig, L. S., Clark, L. N., Small, S. A., et al. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.033 · Cited by 519 · see citing works
Tyro-3 family receptors are essential regulators of mammalian spermatogenesis
Lu, Q., Gore, M., Zhang, Q., Camenisch, T., Boast, S., Casagranda, F., Lai, C., Skinner, M. K., Klein, R., Matsushima, G. K., et al. (1999) · Nature · doi:10.1038/19554 · Cited by 514 · see citing works
CD36 Mediates the Innate Host Response to β-Amyloid
El Khoury, J. B., Moore, K. J., Means, T. K., Leung, J., Terada, K., Toft, M., Freeman, M. W., & Luster, A. D. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021546 · Cited by 483 · see citing works
Florey, O., Kim, S. E., Sandoval, C. P., Haynes, C. M., & Overholtzer, M. (2011) · Nature Cell Biology · doi:10.1038/ncb2363 · Cited by 459 · see citing works
Bonifacino, J. S., & Hurley, J. H. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.03.009 · Cited by 449 · see citing works
Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice
Wyss-Coray, T., Yan, F., Lin, A. H.-T., Lambris, J. D., Alexander, J. J., Quigg, R. J., & Masliah, E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162350199 · Cited by 446 · see citing works
Self-citationModel‐guided microarray implicates the retromer complex in Alzheimer's disease
Small, S. A., Kent, K., Pierce, A., Leung, C., Kang, M. S., Okada, H., Honig, L., Vonsattel, J., & Kim, T. (2005) · Annals of Neurology · doi:10.1002/ana.20667 · Cited by 440 · see citing works
Blocking TGF-β–Smad2/3 innate immune signaling mitigates Alzheimer-like pathology
Town, T., Laouar, Y., Pittenger, C., Mori, T., Szekely, C. A., Tan, J., Duman, R. S., & Flavell, R. A. (2008) · Nature Medicine · doi:10.1038/nm1781 · Cited by 422 · see citing works
Formation and maintenance of Alzheimer's disease β-amyloid plaques in the absence of microglia
Grathwohl, S. A., Kälin, R. E., Bolmont, T., Prokop, S., Winkelmann, G., Kaeser, S. A., Odenthal, J., Radde, R., Eldh, T., Gandy, S., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2432 · Cited by 401 · see citing works
Neprilysin Gene Transfer Reduces Human Amyloid Pathology in Transgenic Mice
Marr, R. A., Rockenstein, E. M., Mukherjee, A., Kindy, M. S., Hersh, L. B., Gage, F. H., Verma, I. M., & Masliah, E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-01992.2003 · Cited by 391 · see citing works
Self-citationDeficiency in neuronal TGF-β signaling promotes neurodegeneration and Alzheimer’s pathology
Tesseur, I., Zou, K., Esposito, L., Bard, F., Berber, E., Can, J. V., Lin, A. H., Crews, L., Tremblay, P., Mathews, P., et al. (2006) · Journal of Clinical Investigation · doi:10.1172/jci27341 · Cited by 355 · see citing works
Self-citationOsteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice
Kaifu, T., Nakahara, J., Inui, M., Mishima, K., Momiyama, T., Kaji, M., Sugahara, A., Koito, H., Ujike, A., Nakamura, A., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci16923 · Cited by 342 · see citing works
A Novel Protein Complex Linking the δ2 Glutamate Receptor and Autophagy
Yue, Z., Horton, A., Bravin, M., DeJager, P. L., Selimi, F., & Heintz, N. (2002) · Neuron · doi:10.1016/s0896-6273(02)00861-9 · Cited by 306 · see citing works
Shaping Development of Autophagy Inhibitors with the Structure of the Lipid Kinase Vps34
Miller, S., Tavshanjian, B., Oleksy, A., Perišić, O., Houseman, B. T., Shokat, K. M., & Williams, R. L. (2010) · Science · doi:10.1126/science.1184429 · Cited by 290 · see citing works
Liu, Z., Condello, C., Schain, A., Harb, R., & Grutzendler, J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4403-10.2010 · Cited by 276 · see citing works
VPS35 haploinsufficiency increases Alzheimer’s disease neuropathology
Wen, L., Tang, F., Hong, Y., Luo, S.-W., Wang, C.-L., He, W., Shen, C., Jung, J.-U., Xiong, F., Lee, D.-H., et al. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201105109 · Cited by 264 · see citing works
Burda, P., Padilla, S. M., Sarkar, S., & Emr, S. D. (2002) · Journal of Cell Science · doi:10.1242/jcs.00090 · Cited by 216 · see citing works
Mitchell, H., Choudhury, A., Pagano, R. E., & Leof, E. B. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-03-0245 · Cited by 215 · see citing works
Regulation of Amyloid Precursor Protein Processing by the Beclin 1 Complex
Jaeger, P. A., Pickford, F., Sun, C.-H., Lucin, K. M., Masliah, E., & Wyss-Coray, T. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011102 · Cited by 209 · see citing works
Self-citationKu, B., Woo, J., Liang, C., Lee, K.-H., Hong, H.-S., Xiaofei, E., Kim, K.-S., Jung, J. U., & Oh, B. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.0040025 · Cited by 190 · see citing works
SLAM is a microbial sensor that regulates bacterial phagosome functions in macrophages
Berger, S. B., Ros, X. R., Ma, C., Wang, G., Faubion, W. A., Liao, G., Compeer, E. B., Keszei, M., Rameh, L. E., Wang, N., et al. (2010) · Nature Immunology · doi:10.1038/ni.1931 · Cited by 182 · see citing works
Modeling microglial activation in Alzheimer's disease with human postmortem microglial cultures
Lue, L. (2001) · Neurobiology of Aging · doi:10.1016/s0197-4580(01)00311-6 · Cited by 165 · see citing works
Time-dependent reduction in Aβ levels after intracranial LPS administration in APP transgenic mice
Herber, D. L., Roth, L. M., Wilson, D. H., Wilson, N., Mason, J. E., Morgan, D., & Gordon, M. N. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.07.007 · Cited by 148 · see citing works
Retromer Is Required for Apoptotic Cell Clearance by Phagocytic Receptor Recycling
Chen, D., Xiao, H., Zhang, K., Wang, B., Gao, Z., Jian, Y., Qi, X., Sun, J., Miao, L., & Yang, C. (2010) · Science · doi:10.1126/science.1184840 · Cited by 123 · see citing works
Ruck, A., Attonito, J. D., Garces, K. T., Núñez, L., Palmisano, N. J., Rubel, Z., Bai, Z., Nguyen, K. C. Q., Sun, L., Grant, B. D., et al. (2011) · Autophagy · doi:10.4161/auto.7.4.14391 · Cited by 114 · see citing works
BACE1 Retrograde Trafficking Is Uniquely Regulated by the Cytoplasmic Domain of Sortilin
Finan, G. M., Okada, H., & Kim, T. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.170217 · Cited by 108 · see citing works
Yanagawa, M., Tsukuba, T., Nishioku, T., Okamoto, Y., Okamoto, K., Takii, R., Terada, Y., Nakayama, K. I., Kadowaki, T., & Yamamoto, K. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604143200 · Cited by 60 · see citing works
Ikonomović, M. D., Mizukami, K., Warde, D., Sheffield, R., Hamilton, R. L., Wenthold, R. J., & Armstrong, D. M. (1999) · Experimental Neurology · doi:10.1006/exnr.1999.7196 · Cited by 57 · see citing works
Prada, I., Naum-Onganı́a, G., Buonsanti, C., Panina‐Bordignon, P., & Meldolesi, J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.03.058 · Cited by 49 · see citing works
Ma, C., Wang, N., Detre, C., Wang, G., O’Keeffe, M. S., & Terhorst, C. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.367060 · Cited by 46 · see citing works
Transfection by Electroporation of RAW 264.7 MacrophagesPreprint
Smale, S. T. (2010) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5374 · Cited by 14 · see citing works
Flagged first, then by citations
1 of the 62 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Neuroinflammation in Alzheimer's disease
Heneka, M. T., Carson, M. J., Khoury, J. E., Landreth, G. E., Brosseron, F., Feinstein, D. L., Jacobs, A. H., Wyss-Coray, T., Vitorica, J., Ransohoff, R. M., et al. (2015) · The Lancet Neurology · doi:10.1016/s1474-4422(15)70016-5 · Cited by 6,226 · see citing works
Self-citationImmune attack: the role of inflammation in Alzheimer disease
Heppner, F. L., Ransohoff, R. M., & Becher, B. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3880 · Cited by 2,134 · see citing works
TREM2 Maintains Microglial Metabolic Fitness in Alzheimer’s Disease
Ulland, T. K., Song, W. M., Huang, S. C.-C., Ulrich, J. D., Sergushichev, A., Beatty, W. L., Loboda, A. A., Zhou, Y., Cairns, N. J., Kambal, A., et al. (2017) · Cell · doi:10.1016/j.cell.2017.07.023 · Cited by 1,263 · see citing works
Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease
Prinz, M., & Priller, J. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3722 · Cited by 1,329 · see citing works
The clearance of dead cells by efferocytosis
Boada-Romero, E., Martinez, J., Heckmann, B. L., & Green, D. R. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0232-1 · Cited by 893 · see citing works
Compromised autophagy and neurodegenerative diseases
Menzies, F. M., Fleming, A., & Rubinsztein, D. C. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3961 · Cited by 851 · see citing works
TREM2 mutations implicated in neurodegeneration impair cell surface transport and phagocytosis
Kleinberger, G., Yamanishi, Y., Suárez-Calvet, M., Czirr, E., Lohmann, E., Cuyvers, E., Struyfs, H., Pettkus, N., Wenninger-Weinzierl, A., Mazaheri, F., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009093 · Cited by 798 · see citing works
Self-citationHistory and progress of hypotheses and clinical trials for Alzheimer’s disease
Liu, P.-P., Xie, Y., Meng, X.-Y., & Kang, J.-S. (2019) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-019-0063-8 · Cited by 723 · see citing works
Macrophages in health and disease
Park, M. D., Silvin, A., Ginhoux, F., & Merad, M. (2022) · Cell · doi:10.1016/j.cell.2022.10.007 · Cited by 644 · see citing works
Microglial dysfunction in brain aging and Alzheimer's disease
Mosher, K. I., & Wyss-Coray, T. (2014) · Biochemical Pharmacology · doi:10.1016/j.bcp.2014.01.008 · Cited by 618 · see citing works
Self-citationInflammatory Response in the CNS: Friend or Foe?
Sochocka, M., Diniz, B. S., & Leszek, J. (2017) · Molecular Neurobiology · doi:10.1007/s12035-016-0297-1 · Cited by 573 · see citing works
Inflammation: the link between comorbidities, genetics, and Alzheimer’s disease
Newcombe, E. A., Camats-Perna, J., Silva, M. L., Valmas, N., Huat, T. J., & Medeiros, R. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1313-3 · Cited by 532 · see citing works
Mechanisms of Aβ Clearance and Degradation by Glial Cells
Ries, M., & Sastre, M. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00160 · Cited by 527 · see citing works
Heckmann, B. L., Teubner, B. J. W., Tummers, B., Boada-Romero, E., Harris, L., Yang, M., Guy, C. S., Zakharenko, S. S., & Green, D. R. (2019) · Cell · doi:10.1016/j.cell.2019.05.056 · Cited by 503 · see citing works
“This method is well-established and used as previously reported (Lucin et al., 2013).”
InfluentialThe different autophagy degradation pathways and neurodegeneration
Fleming, A., Bourdenx, M., Fujimaki, M., Karabiyik, C., Krause, G. J., Lopez, A., Martín‐Segura, A., Puri, C., Scrivo, A., Skidmore, J., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.017 · Cited by 485 · see citing works
Autophagy and Alzheimer’s Disease: From Molecular Mechanisms to Therapeutic Implications
Uddin, M. S., Stachowiak, A., Mamun, A. A., Tzvetkov, N. T., Takeda, S., Atanasov, A. G., Bergantin, L. B., Abdel‐Daim, M. M., & Stankiewicz, A. M. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00004 · Cited by 440 · see citing works
TREM2 in Neurodegenerative Diseases
Jay, T. R., von Saucken, V. E., & Landreth, G. E. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0197-5 · Cited by 427 · see citing works
Layé, S., Nadjar, A., Joffre, C., & Bazinet, R. P. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.014092 · Cited by 420 · see citing works
Autophagy in microglia degrades extracellular β-amyloid fibrils and regulates the NLRP3 inflammasome
Cho, M.-H., Cho, K., Kang, H.-J., Jeon, E.-Y., Kim, H.-S., Kwon, H.-J., Kim, H.-M., Kim, D.-H., & Yoon, S.-Y. (2014) · Autophagy · doi:10.4161/auto.29647 · Cited by 395 · see citing works
Autophagy in Alzheimer’s disease pathogenesis: Therapeutic potential and future perspectives
Zhang, Z., Yang, X., Song, Y., & Tu, J. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101464 · Cited by 378 · see citing works
Systemic inflammation impairs microglial Aβ clearance through NLRP3 inflammasome
Tejera, D., Mercan, D., Sanchez‐Caro, J. M., Hanan, M., Greenberg, D., Soreq, H., Latz, E., Golenbock, D., & Heneka, M. T. (2019) · The EMBO Journal · doi:10.15252/embj.2018101064 · Cited by 351 · see citing works
Luo, R., Su, L.-Y., Li, G., Yang, J., Liu, Q., Yang, L.-X., Zhang, D.-F., Zhou, H., Xu, M., Fan, Y., et al. (2020) · Autophagy · doi:10.1080/15548627.2019.1596488 · Cited by 364 · see citing works
Microglia Phenotypes in Aging and Neurodegenerative Diseases
Wendimu, M. Y., & Hooks, S. B. (2022) · Cells · doi:10.3390/cells11132091 · Cited by 336 · see citing works
Autophagy and neurodegeneration
Frake, R. A., Ricketts, T., Menzies, F. M., & Rubinsztein, D. C. (2015) · Journal of Clinical Investigation · doi:10.1172/jci73944 · Cited by 332 · see citing works
Wang, W., Wang, X., Fujioka, H., Hoppel, C. L., Whone, A. L., Caldwell, M. A., Cullen, P. J., Liu, J., & Zhu, X. (2015) · Nature Medicine · doi:10.1038/nm.3983 · Cited by 324 · see citing works
Autophagy and Microglia: Novel Partners in Neurodegeneration and Aging
Plaza-Zabala, A., Sierra-Torre, V., & Sierra, A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18030598 · Cited by 323 · see citing works
Microglia in Alzheimer’s disease: pathogenesis, mechanisms, and therapeutic potentials
Miao, J., Ma, H., Yang, Y., Liao, Y., Lin, C., Zheng, J., Yu, M., & Lan, J. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1201982 · Cited by 293 · see citing works
Pan, R., Ma, J., Kong, X.-X., Wang, X., Li, S., Qi, X., Yan, Y., Cheng, J., Liu, Q., Jin, W., et al. (2019) · Science Advances · doi:10.1126/sciadv.aau6328 · Cited by 290 · see citing works
Lee, J.-W., Nam, H., Kim, L. E., Jeon, Y., Min, H., Ha, S., Lee, Y., Kim, S.-Y., Lee, S. J., Kim, E.-K., et al. (2019) · Autophagy · doi:10.1080/15548627.2018.1556946 · Cited by 260 · see citing works
Interplay of endoplasmic reticulum stress and autophagy in neurodegenerative disorders
Cai, Y. C., Arikkath, J., Yang, L., Guo, M., Periyasamy, P., & Buch, S. J. (2016) · Autophagy · doi:10.1080/15548627.2015.1121360 · Cited by 258 · see citing works
Autophagy, aging, and age-related neurodegeneration
Palmer, J. E., Wilson, N., Son, S. M., Obrocki, P., Wróbel, L., Rob, M., Takla, M., Korolchuk, V. I., & Rubinsztein, D. C. (2024) · Neuron · doi:10.1016/j.neuron.2024.09.015 · Cited by 255 · see citing works
Davies, D. S., Ma, J., Jegathees, T., & Goldsbury, C. (2017) · Brain Pathology · doi:10.1111/bpa.12456 · Cited by 251 · see citing works
Retromer in Alzheimer disease, Parkinson disease and other neurological disorders
Small, S. A., & Petsko, G. A. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn3896 · Cited by 235 · see citing works
Autophagy in Neurodegenerative Diseases: From Mechanism to Therapeutic Approach
Nah, J., Yuan, J., & Jung, Y. (2015) · Molecules and Cells · doi:10.14348/molcells.2015.0034 · Cited by 229 · see citing works
Membrane recruitment of endogenous LRRK2 precedes its potent regulation of autophagy
Schapansky, J., Nardozzi, J. D., Felizia, F., & LaVoie, M. J. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu138 · Cited by 226 · see citing works
Autophagy in aging and neurodegenerative diseases: implications for pathogenesis and therapy
Tan, C., Yu, J., Tan, M., Jiang, T., Zhu, X., & Tan, L. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.11.019 · Cited by 221 · see citing works
Endo-lysosomal dysregulations and late-onset Alzheimer’s disease: impact of genetic risk factors
Van Acker, Z. P., Bretou, M., & Annaert, W. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0323-7 · Cited by 222 · see citing works
Beclin1‐driven autophagy modulates the inflammatory response of microglia via NLRP3
Houtman, J., Freitag, K., Gimber, N., Schmoranzer, J., Heppner, F. L., & Jendrach, M. (2019) · The EMBO Journal · doi:10.15252/embj.201899430 · Cited by 212 · see citing works
The role of the immune system in Alzheimer disease: Etiology and treatment
Jevtic, S. D., Sengar, A. S., Salter, M. W., & McLaurin, J. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.08.005 · Cited by 218 · see citing works
Autophagy in Neurodegenerative Diseases: A Hunter for Aggregates
Park, H., Kang, J., & Lee, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093369 · Cited by 209 · see citing works
Autophagy in the physiology and pathology of the central nervous system
Nikoletopoulou, V., Papandreou, M. E., & Tavernarakis, N. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.204 · Cited by 206 · see citing works
The Autophagy Lysosomal Pathway and Neurodegeneration
Finkbeiner, S. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a033993 · Cited by 196 · see citing works
Autophagy and ALS: mechanistic insights and therapeutic implications
Chua, J. P., De Calbiac, H., Kabashi, E., & Barmada, S. J. (2022) · Autophagy · doi:10.1080/15548627.2021.1926656 · Cited by 189 · see citing works
“In line with these connections between phagocytosis and autophagy, microglial phagocytosis of Aβ deposits in Alzheimer disease models [430,431] requires the autophagy-related factors BECN1, ATG7 and LC3 [432,433].”
BackgroundWu, A., Zhou, X., Qiao, G., Yu, L., Tang, Y., Yan, L., Qiu, W., Pan, R., Yu, C., Law, B. Y. K., et al. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101202 · Cited by 193 · see citing works
The role of autophagy in modulation of neuroinflammation in microglia
Su, P., Zhang, J., Wang, D., Zhao, F., Cao, Z., Aschner, M., & Luo, W. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.035 · Cited by 183 · see citing works
Microglial Phagocytosis and Its Regulation: A Therapeutic Target in Parkinson’s Disease?
Janda, E., Boi, L., & Carta, A. R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00144 · Cited by 175 · see citing works
Beclin orthologs: integrative hubs of cell signaling, membrane trafficking, and physiology
Levine, B., Liu, R., Dong, X., & Zhong, Q. (2015) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.05.004 · Cited by 177 · see citing works
Astrocytic phagocytosis is a compensatory mechanism for microglial dysfunction
Konishi, H., Okamoto, T., Hara, Y., Komine, O., Tamada, H., Maeda, M., Osako, F., Kobayashi, M., Nishiyama, A., Kataoka, Y., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020104464 · Cited by 179 · see citing works
Hyttinen, J. M. T., Amadio, M., Viiri, J., Pascale, A., Salminen, A., & Kaarniranta, K. (2014) · Ageing Research Reviews · doi:10.1016/j.arr.2014.07.002 · Cited by 165 · see citing works
Endosomal Traffic Jams Represent a Pathogenic Hub and Therapeutic Target in Alzheimer’s Disease
Small, S. A., Simoes, S., Mayeux, R. P., & Petsko, G. A. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.08.003 · Cited by 163 · see citing works
Rocchi, A., Yamamoto, S., Ting, T., Fan, Y., Sadleir, K., Wang, Y., Zhang, W., Huang, S., Levine, B., Vassar, R., et al. (2017) · PLOS Genetics · doi:10.1371/journal.pgen.1006962 · Cited by 166 · see citing works
Melatonin and Autophagy in Aging-Related Neurodegenerative Diseases
Luo, F., Sandhu, A. F., Rungratanawanich, W., Williams, G. E., Akbar, M. D., Zhou, S., Song, B., & Wang, X. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197174 · Cited by 158 · see citing works
Microglia change from a reactive to an age-like phenotype with the time in culture
Caldeira, C., Oliveira, A. F., Cunha, C., Vaz, A. R., Falcão, A. S., Fernandes, A., & Brites, D. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00152 · Cited by 156 · see citing works
Alzheimer’s Disease Pathogenesis: Role of Autophagy and Mitophagy Focusing in Microglia
Eshraghi, M., Adlimoghaddam, A., Mahmoodzadeh, A., Sharifzad, F., Yasavoli-Sharahi, H., Lorzadeh, S., Albensi, B. C., & Ghavami, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073330 · Cited by 158 · see citing works
Cai, Q., Li, Y., & Pei, G. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0839-0 · Cited by 154 · see citing works
Liu, X., Hao, W., Qin, Y., Decker, Y., Wang, X., Burkart, M., Schötz, K., Menger, M. D., Fassbender, K., & Liu, Y. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.01.011 · Cited by 149 · see citing works
Tu, H., Yuan, B., Hou, X., Zhang, X., Pei, C., Ma, Y., Yang, Y., Fan, Y., Qin, Z., Liu, C., et al. (2021) · Aging Cell · doi:10.1111/acel.13522 · Cited by 152 · see citing works
Phosphoinositides in phagocytosis and macropinocytosis
Levin‐Konigsberg, R., Grinstein, S., & Schlam, D. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.09.005 · Cited by 144 · see citing works
Endo-lysosomal dysfunction: a converging mechanism in neurodegenerative diseases
Wang, C., Telpoukhovskaia, M. A., Bahr, B. A., Chen, X., & Gan, L. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.09.005 · Cited by 144 · see citing works
TREM2 promotes Aβ phagocytosis by upregulating C/EBPα-dependent CD36 expression in microglia
Kim, S.-M., Mun, B.-R., Lee, S.-J., Joh, Y., Lee, H.-Y., Ji, K.-Y., Choi, H.-R., Lee, E.-H., Kim, E.-M., Jang, J.-H., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-11634-x · Cited by 143 · see citing works
Macroautophagy in CNS health and disease
Griffey, C. J., & Yamamoto, A. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00588-3 · Cited by 144 · see citing works
Neuroinflammation and fractalkine signaling in Alzheimer’s disease
Finneran, D. J., & Nash, K. R. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1412-9 · Cited by 133 · see citing works
Age- and location-related changes in microglial function
Ritzel, R. M., Patel, A. R., Pan, S., Crapser, J., Hammond, M., Jellison, E., & McCullough, L. D. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.02.016 · Cited by 134 · see citing works
Mitochondria at the interface between neurodegeneration and neuroinflammation
Bader, V., & Winklhofer, K. F. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.05.028 · Cited by 134 · see citing works
Zhong, L., Chen, X.-F., Zhang, Z.-L., Wang, Z., Shi, X.-Z., Xu, K., Zhang, Y.-W., Xu, H., & Bu, G. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.645986 · Cited by 133 · see citing works
Alborixin clears amyloid-β by inducing autophagy through PTEN-mediated inhibition of the AKT pathway
Wani, A., Gupta, M., Ahmad, M. N., Shah, A. M., Ahsan, A. U., Qazi, P. H., Malik, F. A., Singh, G., Sharma, P. R., Kaddoumi, A., et al. (2019) · Autophagy · doi:10.1080/15548627.2019.1596476 · Cited by 129 · see citing works
Microglial phagocytosis in aging and Alzheimer's disease
Gabandé‐Rodríguez, E., Keane, L., & Capasso, M. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24419 · Cited by 127 · see citing works
Extracellular Vesicle as a Source of Alzheimer’s Biomarkers: Opportunities and Challenges
Lee, S., Mankhong, S., & Kang, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20071728 · Cited by 125 · see citing works
Teter, B., Morihara, T., Lim, G. P., Chu, T., Jones, M. R., Zuo, X., Paul, R. M., Frautschy, S. A., & Cole, G. M. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.02.015 · Cited by 125 · see citing works
Autophagy in Age-Associated Neurodegeneration
Metaxakis, A., Ploumi, C., & Tavernarakis, N. (2018) · Cells · doi:10.3390/cells7050037 · Cited by 121 · see citing works
Interferon regulatory factor 7 participates in the M 1‐like microglial polarization switch
Tanaka, T., Murakami, K., Bandô, Y., & Yoshida, S. (2014) · Glia · doi:10.1002/glia.22770 · Cited by 122 · see citing works
Shobin, E., Bowley, M. P., Estrada, L. I., Heyworth, N. C., Orczykowski, M. E., Eldridge, S. A., Calderazzo, S. M., Mortazavi, F., Moore, T. L., & Rosene, D. L. (2017) · GeroScience · doi:10.1007/s11357-017-9965-y · Cited by 121 · see citing works
Mitophagy and cGAS–STING crosstalk in neuroinflammation
Zhou, X., Wang, J., Yu, L., Qiao, G., Qin, D., Yuen-Kwan Law, B., Ren, F., Wu, J., & Wu, A. (2024) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2024.05.012 · Cited by 131 · see citing works
Noncanonical function of an autophagy protein prevents spontaneous Alzheimer’s disease
Heckmann, B. L., Teubner, B. J. W., Boada-Romero, E., Tummers, B., Guy, C., Fitzgerald, P., Mayer, U., Carding, S., Zakharenko, S. S., Wileman, T., et al. (2020) · Science Advances · doi:10.1126/sciadv.abb9036 · Cited by 114 · see citing works
Neuronal autophagy and intercellular regulation of homeostasis in the brain
Kulkarni, A., Chen, J., & Maday, S. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.008 · Cited by 117 · see citing works
Spermidine reduces neuroinflammation and soluble amyloid beta in an Alzheimer’s disease mouse model
Freitag, K., Sterczyk, N., Wendlinger, S., Obermayer, B., Schulz, J., Farztdinov, V. M., Mülleder, M., Ralser, M., Houtman, J., Fleck, L., et al. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02534-7 · Cited by 122 · see citing works
Autophagy in inflammation, infection, neurodegeneration and cancer
Arroyo, D. S., Gaviglio, E. A., Ramos, J. M. P., Bussi, C., Rodriguez‐Galán, M. C., & Iribarren, P. (2013) · International Immunopharmacology · doi:10.1016/j.intimp.2013.11.001 · Cited by 112 · see citing works
Central nervous system myeloid cells as drug targets: current status and translational challenges
Biber, K. P. H., Möller, T., Boddeke, E., & Prinz, M. (2015) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2015.14 · Cited by 111 · see citing works
Kim, K. S., Marcogliese, P. C., Yang, J., Callaghan, S. M., Resende, V., Abdel-Messih, E., Marras, C., Visanji, N. P., Huang, J., Schlossmacher, M. G., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1718946115 · Cited by 111 · see citing works
Microglial efferocytosis: Diving into the Alzheimer’s disease gene pool
Romero-Molina, C., Garretti, F., Andrews, S. J., Marcora, E., & Goate, A. M. (2022) · Neuron · doi:10.1016/j.neuron.2022.10.015 · Cited by 111 · see citing works
Gawriluk, T. R., Ko, C. J., Hong, X., Christenson, L. K., & Rucker, E. B. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1409323111 · Cited by 111 · see citing works
Shibuya, Y., Chang, C. C. Y., Huang, L.-H., Bryleva, E. Y., & Chang, T.-Y. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.2567-14.2014 · Cited by 108 · see citing works
“Impaired microglial clearance of A is partially responsible for AD pathogenesis (Hickman et al., 2008; Griciuc et al., 2013; Lucin et al., 2013).”
BackgroundZádori, D., Veres, G., Szalárdy, L., Klivènyi, P., & Vécsei, L. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-170929 · Cited by 107 · see citing works
Nucleic acid drug vectors for diagnosis and treatment of brain diseases
Lü, Z., Shen, J., Yang, H. J., Wang, J., Zhao, R., Zhang, T.-L., Guo, J. R., & Zhang, X. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01298-z · Cited by 108 · see citing works
ACAT1/SOAT1 as a Therapeutic Target for Alzheimer's Disease
Shibuya, Y., Chang, C. C., & Chang, T.-Y. (2015) · Future Medicinal Chemistry · doi:10.4155/fmc.15.161 · Cited by 113 · see citing works
Alzheimer’s Disease: Mechanism and Approach to Cell Therapy
Amemori, T., Jendelová, P., Růžička, J., Urdzíková, L. M., & Syková, E. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161125961 · Cited by 102 · see citing works
Endosomal sorting and trafficking, the retromer complex and neurodegeneration
Vagnozzi, A. N., & Praticò, D. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0221-3 · Cited by 95 · see citing works
Medrano-Jiménez, E., Jiménez-Ferrer, I., Pedraza‐Escalona, M., Ramírez-Serrano, C. E., Álvarez‐Arellano, L., Cortés‐Mendoza, J., Herrera-Ruiz, M. L., Jiménez‐Ferrer, E., Zamilpa, A., Tortoriello, J., et al. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1515-3 · Cited by 98 · see citing works
Naeem, A., Prakash, R., Kumari, N., Ali Khan, M., Quaiyoom Khan, A., Uddin, S., Verma, S., AB Robertson, A., Boltze, J., & Shadab Raza, S. (2024) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2023.11.031 · Cited by 96 · see citing works
Zhou, R., Shi, X., Bi, D., Fang, W., Wei, G., & Xu, X. (2015) · Marine Drugs · doi:10.3390/md13095828 · Cited by 95 · see citing works
Yan, P., Kim, K.-W., Xiao, Q., Ma, X., Czerniewski, L. R., Liu, H., Rawnsley, D. R., Yan, Y., Randolph, G. J., Epelman, S., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci152565 · Cited by 95 · see citing works
Longitudinal follow-up of autophagy and inflammation in brain of APPswePS1dE9 transgenic mice
François, A., Bilan, A. R., Quellard, N., Fernandez, B., Janet, T., Chassaing, D., Paccalin, M., Terro, F., & Page, G. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0139-x · Cited by 95 · see citing works
Ye, J., Jiang, Z., Chen, X., Liu, M., Li, J., & Liu, N. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14042 · Cited by 92 · see citing works
TREM2 in Alzheimer’s Disease: Microglial Survival and Energy Metabolism
Zheng, H., Cheng, B., Li, Y., Li, X., Chen, X., & Zhang, Y.-W. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00395 · Cited by 94 · see citing works
Savonenko, A. V., Melnikova, T., Wang, Y., Ravert, H. T., Gao, Y., Koppel, J. L., Lee, D., Pletniková, O., Cho, E., Sayyida, N., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129618 · Cited by 93 · see citing works
Exploring the bi‐directional relationship between autophagy and Alzheimer’s disease
Kuang, H., Tan, C., Tian, H., Liu, L., Yang, M.-W., Hong, F., & Yang, S. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13216 · Cited by 92 · see citing works
The Retromer Complex and Sorting Nexins in Neurodegenerative Diseases
Zhang, H., Huang, T. Y., Hong, Y., Yang, W., Zhang, X., Luo, H., Xu, H., & Wang, X. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00079 · Cited by 89 · see citing works
Hellwig, S., Masuch, A., Nestel, S., Katzmarski, N., Meyer-Luehmann, M., & Biber, K. (2015) · Scientific Reports · doi:10.1038/srep14624 · Cited by 91 · see citing works
Vps35-dependent recycling of Trem2 regulates microglial function
Yin, J., Liu, X., He, Q., Zhou, L., Yuan, Z., & Zhao, S. (2016) · Traffic · doi:10.1111/tra.12451 · Cited by 90 · see citing works
Qin, Y., Liu, Y., Hao, W., Decker, Y., Tomic, I., Menger, M. D., Liu, C., & Fassbender, K. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600873 · Cited by 90 · see citing works
- Authors
- Lucin, K. M., O’Brien, C. E., Bieri, G., Czirr, E., Mosher, K. I., Abbey, R. J., Mastroeni, D. F., Rogers, J., Spencer, B., Masliah, E., & Wyss-Coray, T.
- Affiliations
- VA Palo Alto Health Care System (US)
- Banner Sun Health Research Institute (US)
- SRI International (US)
- University of California San Diego (US)
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 79
- Issue
- 5
- Pages
- 873-886
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3779465
- OpenAlex
- W2081014274
- Cited by
- 374
- References
- 62
- Citations by year
- 2026: 11 · 2025: 23 · 2024: 27 · 2023: 34 · 2022: 38 · 2021: 37 · 2020: 30 · 2019: 37 · 2018: 28 · 2017: 24 · 2016: 23 · 2015: 33 · 2014: 27 · 2013: 2
- FWCI
- 15.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Funders
- U.S. Department of Veterans Affairs (I01 BX001319)
- University of California, Irvine
- National Institute on Aging (P30-AG-19610, F31AG040877, R01 AG10435, R01AG18440, R37AG018440, R01AG018440, P50AG005131, R01AG020603, R01AG030144, R01AG045034, P30AG019610, R01AG043384)
- National Institute of Mental Health (T32MH020016)
- National Institute of Neurological Disorders and Stroke (P30NS069375, F31NS078865, U24NS072026)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- Beclin-1, retromer complex, phagocytosis, microglia, Alzheimer's disease, autophagy, CD36, TREM2, receptor recycling, neuroinflammation, neurodegeneration
- MeSH terms
- Beclin-1, Alzheimer Disease, Animals, Autophagy, Brain, Cell Line, Humans, Membrane Glycoproteins, Membrane Proteins, Phagocytosis, Receptors, Immunologic, Amyloid beta-Peptides, Microglia, CD36 Antigens, Vesicular Transport Proteins, Apoptosis Regulatory Proteins, 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 ›
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