Apolipoprotein E mediation of neuro-inflammation in a murine model of multiple sclerosis

Shin, Soomin; Walz, Katharine A.; Archambault, Angela S.; Sim, Julia; Bollman, Bryan P.; Koenigsknecht-Talboo, Jessica; Cross, Anne H.; Holtzman, David M.; Wu, Gregory F.

doi:10.1016/j.jneuroim.2014.03.010

Cited by 32Multiple Sclerosis Research StudiesNeuroinflammation and Neurodegeneration MechanismsT-cell and B-cell Immunology

Apolipoprotein E mediation of neuro-inflammation in a murine model of multiple sclerosis

Open access

Shin, Soomin, Walz, Katharine A., Archambault, Angela S., Sim, Julia, Bollman, Bryan P., Koenigsknecht-Talboo, Jessica, Cross, Anne H., Holtzman, David M. +1 more·2014·Journal of Neuroimmunology

DOI 10.1016/j.jneuroim.2014.03.010PMC PMC4042395

Open this paper in CoChat — free account

Abstract

Apolipoprotein E (ApoE) functions as a ligand in receptor-mediated endocytosis of lipoprotein particles and has been demonstrated to play a role in antigen presentation. To explore the contribution of ApoE during autoimmune central nervous system (CNS) demyelination, we examined the clinical, cellular immune function, and pathologic consequences of experimental autoimmune encephalomyelitis (EAE) induction in ApoE knockout (ApoE(-/-)) mice. We observed reduced clinical severity of EAE in ApoE(-/-) mice in comparison to WT mice that was concomitant with an early reduction of dendritic cells (DCs) followed by a reduction of additional innate cells in the spinal cord at the peak of disease without any differences in axonal damage. While T cell priming was enhanced in ApoE(-/-) mice, reduced severity of EAE was also observed in ApoE(-/-) recipients of encephalitogenic wild type T cells. Expression of ApoE during EAE was elevated within the CNS of wild type mice, particularly by innate cells such as DCs. Overall, ApoE promotes clinical EAE, likely by mediation of inflammation localized within the CNS.

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

Crossref · 10.1016/j.jneuroim.2014.03.010

Cites

63 of 63 references verified0 citation errors · 0 not checkable

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?

Genetic ablation of ApoE in various neurodegenerative mouse models shows a similar protective effect against neurodegeneration and disease severity.
“Notably, genetic ablation of ApoE in various neurodegenerative mouse models — including tauopathy69, synucleinopathy106, and experimental autoimmune encephalomyelitis (EAE)107 — shows a similar protective effect against neurodegeneration and disease severity”
From Interplay between innate immunity and Alzheimer disease: APOE and TREM2 in the spotlight (2018) · cites this paper as [107]
ApoE ablation in EAE mice reduces inflammation and disease severity.
“ApoE ablation in EAE mice also reduces inflammation and disease severity107.”
From Interplay between innate immunity and Alzheimer disease: APOE and TREM2 in the spotlight (2018) · cites this paper as [107]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Analysis of Fractalkine Receptor CX3CR1 Function by Targeted Deletion and Green Fluorescent Protein Reporter Gene Insertion
Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4106-4114.2000 · Cited by 2,632 · see citing works
The role of apolipoprotein E in Alzheimer's disease
Kim, J., Basak, J. M., & Holtzman, D. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.026 · Cited by 1,661 · see citing works
Self-citation
Interleukin-17 and Type 17 Helper T Cells
Miossec, P., Korn, T., & Kuchroo, V. K. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0707449 · Cited by 1,409 · see citing works
A brief history of TH17, the first major revision in the TH1/TH2 hypothesis of T cell–mediated tissue damage
Steinman, L. (2007) · Nature Medicine · doi:10.1038/nm1551 · Cited by 1,367 · see citing works
Apolipoprotein E controls cerebrovascular integrity via cyclophilin A
Bell, R. D., Winkler, E. A., Singh, I., Sagare, A. P., Deane, R., Wu, Z., Holtzman, D. M., Betsholtz, C., Armulik, A., Sallstrom, J., et al. (2012) · Nature · doi:10.1038/nature11087 · Cited by 1,293 · cited 1× · see citing works
“Recent work has shown that ApoE regulates blood–brain barrier integrity and function (Bell et al., 2012).”
BackgroundSelf-citation
Basic Neurochemistry???Molecular, Cellular, and Medical Aspects
Long, D. M. (2006) · Neurosurgery Quarterly · doi:10.1097/01.wnq.0000203279.82150.41 · Cited by 1,288 · see citing works
Dendritic cells in a mature age
Sousa, C. R. E. (2006) · Nature reviews. Immunology · doi:10.1038/nri1845 · Cited by 1,197 · see citing works
CD1: Antigen Presentation and T Cell Function
Brigl, M., & Brenner, M. B. (2004) · Annual Review of Immunology · doi:10.1146/annurev.immunol.22.012703.104608 · Cited by 1,033 · see citing works
Autoimmune T cell responses in the central nervous system
Goverman, J. M. (2009) · Nature reviews. Immunology · doi:10.1038/nri2550 · Cited by 1,025 · see citing works
T cells in multiple sclerosis and experimental autoimmune encephalomyelitis
Fletcher, J. M., Lalor, S. J., Sweeney, C. M., Tubridy, N. J., & Mills, K. H. G. (2010) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2010.04143.x · Cited by 937 · see citing works
Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis
Greter, M., Heppner, F. L., Lemos, M. P., Odermatt, B. M., Goebels, N., Laufer, T., Noelle, R. J., & Becher, B. (2005) · Nature Medicine · doi:10.1038/nm1197 · Cited by 862 · see citing works
Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis
McMahon, E. J., Bailey, S. L., Castenada, C. V., Waldner, H., & Miller, S. D. (2005) · Nature Medicine · doi:10.1038/nm1202 · Cited by 694 · see citing works
Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions.
Bartholomäus, I., Kawakami, N., Odoardi, F., Schläger, C., Miljkovic, D., Ellwart, J. W., Klinkert, W. E. F., Flügel-Koch, C., Issekutz, T. B., Wekerle, H., et al. (2009) · Nature · doi:10.1038/nature08478 · Cited by 685 · see citing works
Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice
Saederup, N., Cardona, A. E., Croft, K., Mizutani, M., Cotleur, A. C., Tsou, C.-L., Ransohoff, R. M., & Charo, I. F. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013693 · Cited by 599 · see citing works
Active induction of experimental allergic encephalomyelitis
Stromnes, I. M., & Goverman, J. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.285 · Cited by 572 · see citing works
Trafficking of immune cells in the central nervous system
Wilson, E. H., Weninger, W., & Hunter, C. A. (2010) · Journal of Clinical Investigation · doi:10.1172/jci41911 · Cited by 521 · see citing works
Axonal damage correlates with disability in patients with relapsing- remitting multiple sclerosis. Results of a longitudinal magnetic resonance spectroscopy study
Stefano, N. D. (1998) · Brain · doi:10.1093/brain/121.8.1469 · Cited by 491 · see citing works
Recognition of CD1d-restricted antigens by natural killer T cells
Rossjohn, J., Pellicci, D. G., Patel, O., Gapin, L., & Godfrey, D. I. (2012) · Nature reviews. Immunology · doi:10.1038/nri3328 · Cited by 462 · see citing works
Pathogenesis of axonal and neuronal damage in multiple sclerosis
Dutta, R., & Trapp, B. (2007) · Neurology · doi:10.1212/01.wnl.0000275229.13012.32 · Cited by 450 · see citing works
Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease–like pathology and cognitive decline
vom Berg, J., Prokop, S., Miller, K. R., Obst, J., Kälin, R. E., Lopategui-Cabezas, I., Wegner, A., Mair, F., Schipke, C. G., Peters, O., et al. (2012) · Nature Medicine · doi:10.1038/nm.2965 · Cited by 416 · see citing works
Apolipoprotein-mediated pathways of lipid antigen presentation
Elzen, P. V. D., Garg, S., León, L., Brigl, M., Leadbetter, E. A., Gumperz, J. E., Dascher, C. C., Cheng, T.-Y., Sacks, F. M., Illarionov, P. A., et al. (2005) · Nature · doi:10.1038/nature04001 · Cited by 380 · see citing works
T Cell Response in Experimental Autoimmune Encephalomyelitis (EAE): Role of Self and Cross-Reactive Antigens in Shaping, Tuning, and Regulating the Autopathogenic T Cell Repertoire
Kuchroo, V. K., Anderson, A. C., Waldner, H., Munder, M., Bettelli, E., & Nicholson, L. B. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.081701.141316 · Cited by 366 · see citing works
Cutting edge: activation of NK T cells by CD1d and alpha-galactosylceramide directs conventional T cells to the acquisition of a Th2 phenotype.
Singh, N., Hong, S., Scherer, D. C., Serizawa, I., Burdin, N., Kronenberg, M., Koezuka, Y., & Kaer, L. V. (1999) · PubMed · Cited by 358 · see citing works
Microglial cell activation and proliferation precedes the onset of CNS autoimmunity
Ponomarev, E. D., Shriver, L. P., Maresz, K., & Dittel, B. N. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20488 · Cited by 349 · see citing works
Cutting Edge: Activation of NK T Cells by CD1d and α-Galactosylceramide Directs Conventional T Cells to the Acquisition of a Th2 Phenotype
Singh, N., Hong, S., Scherer, D. C., Serizawa, I., Burdin, N., Kronenberg, M., Koezuka, Y., & Kaer, L. V. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.5.2373 · Cited by 311 · see citing works
Overexpression of Low-Density Lipoprotein Receptor in the Brain Markedly Inhibits Amyloid Deposition and Increases Extracellular Aβ Clearance
Kim, J., Castellano, J. M., Jiang, H., Basak, J. M., Parsadanian, M., Pham, V., Mason, S. M., Paul, S. M., & Holtzman, D. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.11.013 · Cited by 274 · cited 3× · see citing works
“Apolipoprotein E (ApoE) is a glycoprotein that functions as a ligand in receptor-mediated endocytosis of lipoprotein particles (Kim et al., 2009a).”
BackgroundSelf-citation
Myelin Formation, Structure and Biochemistry
Morell, P., & Quarles, R. H. (1999) · Cited by 272 · see citing works
The role of antigen presenting cells in multiple sclerosis
Chastain, E. M. L., Duncan, D. S., Rodgers, J. M., & Miller, S. D. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.07.008 · Cited by 264 · see citing works
Antigen presentation in autoimmunity and CNS inflammation: how T lymphocytes recognize the brain
Becher, B., Bechmann, I., & Greter, M. (2006) · Journal of Molecular Medicine · doi:10.1007/s00109-006-0065-1 · Cited by 230 · see citing works
Passive induction of experimental allergic encephalomyelitis
Stromnes, I. M., & Goverman, J. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.284 · Cited by 221 · see citing works
De Novo Central Nervous System Processing of Myelin Antigen Is Required for the Initiation of Experimental Autoimmune Encephalomyelitis1
Tompkins, S., Padilla, J., Canto, M. C. D., Ting, J., Kaer, L. V., & Miller, S. D. (2002) · Journal of Immunology · doi:10.4049/jimmunol.168.8.4173 · Cited by 219 · see citing works
Flt3L controls the development of radiosensitive dendritic cells in the meninges and choroid plexus of the steady-state mouse brain
Anandasabapathy, N., Victora, G. D., Meredith, M. M., Feder, R. E., Dong, B., Kluger, C., Yao, K.-H., Dustin, M. L., Nussenzweig, M. C., Steinman, R. M., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20102657 · Cited by 206 · see citing works
Rat and Human Myelin Oligodendrocyte Glycoproteins Induce Experimental Autoimmune Encephalomyelitis by Different Mechanisms in C57BL/6 Mice
Oliver, A. R., Lyon, G. M., & Ruddle, N. H. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.1.462 · Cited by 171 · see citing works
ApoE Deficiency Compromises the Blood Brain Barrier Especially After Injury
Methia, N., André, P., Hafezi-Moghadam, A., Economopoulos, M., Thomas, K. L., & Wagner, D. D. (2001) · Molecular Medicine · doi:10.1007/bf03401973 · Cited by 150 · see citing works
Initiation and progression of axonopathy in experimental autoimmune encephalomyelitis
Soulika, A., Lee, E., Mccauley, E., Miers, L., Bannerman, P., & Pleasure, D. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3794-09.2009 · Cited by 146 · see citing works
Activation of invariant NKT cells by αGalCer administration protects mice from MOG35–55‐induced EAE: critical roles for administration route and IFN‐γ
Furlan, R., Bergami, A., Cantarella, D., Brambilla, E., Taniguchi, M., Dellabona, P., Casorati, G., & Martino, G. (2003) · European Journal of Immunology · doi:10.1002/eji.200323885 · Cited by 126 · see citing works
Apolipoprotein E modulates immune activation by acting on the antigen‐presenting cell
Tenger, C., & Zhou, X. (2003) · Immunology · doi:10.1046/j.1365-2567.2003.01665.x · Cited by 125 · see citing works
Dendritic Cells: Arbiters of Immunity and Immunological TolerancePreprint
Lewis, K. L., & Reizis, B. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007401 · Cited by 125 · see citing works
MHC class I–restricted myelin epitopes are cross-presented by Tip-DCs that promote determinant spreading to CD8+ T cells
Ji, Q., Castelli, L., & Goverman, J. M. (2013) · Nature Immunology · doi:10.1038/ni.2513 · Cited by 124 · see citing works
Augmentation of immune-mediated demyelination by lipid haptens.
Raine, C. S., Traugott, U., Farooq, M., Mb, B., & Wt, N. (1981) · PubMed · Cited by 106 · see citing works
Lack of adiponectin leads to increased lymphocyte activation and increased disease severity in a mouse model of multiple sclerosis
Piccio, L. M., Cantoni, C., Henderson, J. G., Hawiger, D., Ramsbottom, M. J., Mikesell, R. J., Ryu, J., Hsieh, C., Cremasco, V., Haynes, W., et al. (2013) · European Journal of Immunology · doi:10.1002/eji.201242836 · Cited by 92 · see citing works
Self-citation
Reversal of Paralysis and Reduced Inflammation from Peripheral Administration of β-Amyloid in T H 1 and T H 17 Versions of Experimental Autoimmune Encephalomyelitis
Grant, J. L., Ghosn, E. E. B., Axtell, R. C., Herges, K., Kuipers, H. F., Woodling, N. S., Andreasson, K., Herzenberg, L. A., Herzenberg, L. A., & Steinman, L. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004145 · Cited by 92 · see citing works
Requirement for endocytic antigen processing and influence of invariant chain and H-2M deficiencies in CNS autoimmunity
Slavin, A., Soos, J. M., Stüve, O., Patarroyo, J. C., Weiner, H. L., Fontana, A., Bikoff, E. K., & Zamvil, S. S. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13360 · Cited by 91 · see citing works
Cutting Edge: CNS CD11c+ Cells from Mice with Encephalomyelitis Polarize Th17 cells and Support CD25+CD4+ T cell-Mediated Immunosuppression, Suggesting Dual Roles in the Disease Process
Deshpande, P., King, I. L., & Segal, B. M. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.11.6695 · Cited by 74 · see citing works
Invariant NKT Cells Regulate Experimental Autoimmune Encephalomyelitis and Infiltrate the Central Nervous System in a CD1d-Independent Manner
Mars, L. T., Gautron, A.-S., Novák, J., Beaudoin, L., Diana, J., Liblau, R., & Lehuen, A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.4.2321 · Cited by 72 · see citing works
Apolipoprotein E isoform‐dependent microglia migration
Cudaback, E., Li, X., Montine, K. S., Montine, T. J., & Keene, C. D. (2011) · The FASEB Journal · doi:10.1096/fj.10-176891 · Cited by 58 · see citing works
Experimental Autoimmune Encephalomyelitis (EAE)
Racke, M. K. (2001) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0907s14 · Cited by 55 · see citing works
Limited sufficiency of antigen presentation by dendritic cells in models of central nervous system autoimmunity
Wu, G. F., Shindler, K. S., Allenspach, E. J., Stephen, T. L., Thomas, H. L., Mikesell, R. J., Cross, A. H., & Laufer, T. M. (2010) · Journal of Autoimmunity · doi:10.1016/j.jaut.2010.10.006 · Cited by 52 · see citing works
Self-citation
Listeriolysin O Is Strongly Immunogenic Independently of Its Cytotoxic Activity
Carrero, J. A., Vivanco-Cid, H., & Unanue, E. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032310 · Cited by 41 · see citing works
Apolipoprotein E and its mimetic peptide suppress Th1 and Th17 responses in experimental autoimmune encephalomyelitis
Wei, J., Zheng, M., Liang, P., Wei, Y., Yin, X., Tang, Y., & Xue, Y. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.04.009 · Cited by 38 · see citing works
Lack of apolipoprotein-E exacerbates experimental allergic encephalomyelitis
Karussis, D. M., Michaelson, D. M., Grigoriadis, N., Korezyn, A. D., Mizrachi-Koll, R., Chapman, S., Abramsky, O., & Chapman, J. (2003) · Multiple Sclerosis Journal · doi:10.1191/1352458503ms950oa · Cited by 36 · see citing works
Chemokine receptor CX3CR1 promotes dendritic cell development under steady‐state conditions
Łyszkiewicz, M., Witzlau, K., Pommerencke, J., & Krueger, A. (2011) · European Journal of Immunology · doi:10.1002/eji.201040977 · Cited by 34 · see citing works
Closing the case of APOE in multiple sclerosis: no association with disease risk in over 29 000 subjects: Figure 1
Lill, C. M., Liu, T., Schjeide, B. M., Roehr, J. T., Akkad, D. A., Damotte, V., Alcina, A., Ortiz, M. A., Arroyo, R., de Lapuente, A. L., et al. (2012) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2012-101175 · Cited by 33 · see citing works
Serial MR imaging of experimental autoimmune encephalomyelitis induced by human white matter or by chimeric myelin-basic and proteolipid protein in the common marmoset.
Jordan, E. K., McFarland, H., Lewis, B. K., Tresser, N. J., Gates, M. A., Johnson, M., Lenardo, M. J., Matis, L. A., McFarland, H. F., & Frank, J. A. (1999) · PubMed Central · Cited by 33 · see citing works
Chromoxane cyanine R. II. Staining of animal tissues by the dye and its iron complexes
Kiernan, J. A. (1984) · Journal of Microscopy · doi:10.1111/j.1365-2818.1984.tb00501.x · Cited by 32 · see citing works
Region-specific regulation of inflammation and pathogenesis in experimental autoimmune encephalomyelitis
Archambault, A. S., Sim, J. E., McCandless, E. E., Klein, R. S., & Russell, J. H. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.08.012 · Cited by 28 · see citing works
Self-citation
The role of dendritic cells in multiple sclerosis
Wu, G. F., & Laufer, T. M. (2007) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-007-0037-z · Cited by 26 · see citing works
Self-citation
A mighty mouse: building a better model of multiple sclerosis
Ransohoff, R. M. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29834 · Cited by 25 · see citing works
APOE ε4 Is Associated With Exacerbation of Cognitive Decline in Patients With Multiple Sclerosis
Shi, J., Tu, J.-L., Gale, S. D., Baxter, L. C., Vollmer, T. L., Campagnolo, D. I., Tyry, T. M., Zhuang, Y., & Kuniyoshi, S. M. (2011) · Cognitive and Behavioral Neurology · doi:10.1097/wnn.0b013e31823380b5 · Cited by 24 · see citing works
Association between apolipoprotein E gene polymorphism and the risk of multiple sclerosis: A meta-analysis of 6977 subjects
Yin, Y.-W., Zhang, Y., Wang, J., Li, B., Yang, Q., Fang, C., Gao, C., Li, J.-C., & Zhang, L. (2012) · Gene · doi:10.1016/j.gene.2012.09.010 · Cited by 20 · see citing works
Paradoxical effects of apolipoprotein E on cognitive function and clinical progression in mice with experimental autoimmune encephalomyelitis
Dayger, C. A., Rosenberg, J. S., Winkler, C. W., Foster, S. C., Witkowski, E. D., Benice, T. S., Sherman, L. S., & Raber, J. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.11.010 · Cited by 15 · see citing works
Myelin basic protein in lipid-bound form induces experimental allergic encephalomyelitis and demyelination in Lewis rat.
Zehetbauer, B., Massacesi, L., Liuzzi, G. M., Vergelli, M., Olivotto, J., Grassi, L., Riccio, P., & Amaducci, L. A. (1991) · PubMed · Cited by 6 · see citing works
Polymorphism of Apo lipoprotein E gene and the risk of multiple sclerosis.
Hamid, M., Sabzghabaee, A. M., Mousavian, Z., Saadatnia, M., Shirani, S., & Moazen, F. (2011) · PubMed Central · Cited by 3 · see citing works

Flagged first, then by citations

Sorted by citations

The TREM2-APOE Pathway Drives the Transcriptional Phenotype of Dysfunctional Microglia in Neurodegenerative Diseases
Krasemann, S., Madore, C., Cialic, R., Baufeld, C., Calcagno, N., El Fatimy, R., Beckers, L., O’Loughlin, E., Xu, Y., Fanek, Z., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.008 · Cited by 2,979 · see citing works
Self-citation
Interplay between innate immunity and Alzheimer disease: APOE and TREM2 in the spotlight
Shi, Y., & Holtzman, D. M. (2018) · Nature Reviews Immunology · doi:10.1038/s41577-018-0051-1 · Cited by 595 · see citing works
Self-citation
ApoE4: an emerging therapeutic target for Alzheimer’s disease
Safieh, M., Korczyn, A. D., & Michaelson, D. M. (2019) · BMC Medicine · doi:10.1186/s12916-019-1299-4 · Cited by 449 · see citing works
ApoE facilitates the microglial response to amyloid plaque pathology
Ulrich, J. D., Ulland, T. K., Mahan, T. E., Nyström, S., Nilsson, K. P., Song, W. M., Zhou, Y., Reinartz, M., Choi, S., Jiang, H., et al. (2018) · Journal of Experimental Medicine · doi:10.1084/jem.20171265 · Cited by 297 · see citing works
Self-citation
APOE genotype regulates pathology and disease progression in synucleinopathy
Davis, A. A., Inman, C. E., Wargel, Z. M., Dube, U., Freeberg, B. M., Galluppi, A., Haines, J. N., Dhavale, D. D., Miller, R., Choudhury, F. A., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aay3069 · Cited by 177 · see citing works
Self-citation
Baicalein Attenuates Neuroinflammation by Inhibiting NLRP3/Caspase-1/GSDMD Pathway in MPTP-Induced Mice Model of Parkinson’s Disease
Rui, W., Li, S., Xiao, H., Xiao, M., & Shi, J. (2020) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaa060 · Cited by 175 · see citing works
Unique microglia recovery population revealed by single-cell RNAseq following neurodegeneration
Tay, T. L., Sagar, Dautzenberg, J., Grün, D., & Prinz, M. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0584-3 · Cited by 102 · see citing works
B Cell Antigen Presentation Is Sufficient To Drive Neuroinflammation in an Animal Model of Multiple Sclerosis
Harp, C. R. P., Archambault, A. S., Sim, J. E., Ferris, S. T., Mikesell, R. J., Koni, P. A., Shimoda, M., Linington, C., Russell, J. H., & Wu, G. F. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402236 · Cited by 97 · see citing works
Self-citation
Age‐related small vessel disease: a potential contributor to neurodegeneration in multiple sclerosis
Geraldes, R., Esiri, M. M., DeLuca, G. C., & Palace, J. A. (2016) · Brain Pathology · doi:10.1111/bpa.12460 · Cited by 76 · see citing works
Expression profiles of cholesterol metabolism-related genes are altered during development of experimental autoimmune encephalomyelitis in the rat spinal cord
Lavrnja, I., Smiljanic, K., Savic, D., Mladenovic-Djordjevic, A., Tesovic, K., Kanazir, S., & Pekovic, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-02638-8 · Cited by 54 · see citing works
“Disease modifying nutricals” for multiple sclerosis
Schmitz, K., Barthelmes, J., Stolz, L., Beyer, S., Diehl, O., & Tegeder, I. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.11.015 · Cited by 54 · see citing works
Association of plasma YKL-40 with brain amyloid-β levels, memory performance, and sex in subjective memory complainers
Vergallo, A., Lista, S., Lemercier, P., Chiesa, P. A., Zetterberg, H., Blennow, K., Potier, M., Habert, M., Baldacci, F., Cavedo, E., et al. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.07.009 · Cited by 48 · see citing works
A tale of two systems: Lessons learned from female mid-life aging with implications for Alzheimer’s prevention & treatment
Mishra, A., Wang, Y., Yin, F., Vitali, F., Rodgers, K. E., Soto, M., Mosconi, L., Wang, T., & Brinton, R. D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101542 · Cited by 44 · see citing works
Neuroprotective pentapeptide CN-105 improves functional and histological outcomes in a murine model of intracerebral hemorrhage
Lei, B., James, M. L., Liu, J. T., Zhou, G., Venkatraman, T. N., Lascola, C. D., Acheson, S. K., Dubois, L. G., Laskowitz, D. T., & Wang, H. (2016) · Scientific Reports · doi:10.1038/srep34834 · Cited by 44 · see citing works
Skin-derived TSLP systemically expands regulatory T cells
Leichner, T. M., Satake, A., Harrison, V. S., Tanaka, Y., Archambault, A. S., Kim, B., Siracusa, M. C., Leonard, W. J., Naji, A., Wu, G. F., et al. (2017) · Journal of Autoimmunity · doi:10.1016/j.jaut.2017.01.003 · Cited by 39 · see citing works
Self-citation
The progress in epidemiological, diagnosis and treatment of primary hemifacial spasm
Xiang, G., Sui, M., Jiang, N., Luo, R., Xia, J., Wei, X., Lin, Y., Li, X., Cai, Z., Lin, J., et al. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e38600 · Cited by 18 · see citing works
Lowering blood cholesterol does not affect neuroinflammation in experimental autoimmune encephalomyelitis
Vigne, S., Duc, D., Peter, B., Rebeaud, J., Yersin, Y., Ruiz, F., Bressoud, V., Collet, T.-H., & Pot, C. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02409-x · Cited by 16 · see citing works
Investigating the Interplay between Cardiovascular and Neurodegenerative Disease
Cousineau, J., Dawe, A. M., & Alpaugh, M. (2024) · Biology · doi:10.3390/biology13100764 · Cited by 15 · see citing works
Investigation of sex-specific effects of apolipoprotein E on severity of EAE and MS
Schrewe, L., Lill, C. M., Liu, T., Salmen, A., Gerdes, L., Guillot‐Noël, L., Akkad, D. A., Blaschke, P., Graetz, C., Hoffjan, S., et al. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0429-y · Cited by 14 · see citing works
Coronal ApoE Protein Combines with LRP1 to Inactivate GSK3β That Mitigates Silica Nanoparticle-Induced Brain Lesion
Wei, W., Sun, H., Yang, B. V., Song, E., & Song, Y. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00728 · Cited by 10 · see citing works
Demyelination and neurodegeneration early in experimental autoimmune encephalomyelitis contribute to functional deficits in the anterior visual pathway
Sekyi, M. T., Feri, M., Desfor, S., Atkinson, K. C., Golestany, B., Beltran, F., & Tiwari-Woodruff, S. K. (2024) · Scientific Reports · doi:10.1038/s41598-024-73792-z · Cited by 8 · see citing works
Role of APOE in glaucoma.
Yi, W.-H., Lv, D., Sun, Y., Mu, J.-Y., & Lu, X. (2023) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/j.bbrc.2023.149414 · Cited by 7 · see citing works
Analysis of risk factors related to the progression rate of hemifacial spasm
Xu, F., Gu, P., Yuan, H., Jiang, L., Xie, Y., Shi, Q., & Zhan, Y. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1357280 · Cited by 5 · see citing works
Global research trends of Apolipoprotein E in central nervous system: A scientometric analysis
Gong, K., Chen, Y., Liu, W., & Wang, Z. (2021) · International Immunopharmacology · doi:10.1016/j.intimp.2021.107919 · Cited by 5 · see citing works
Association Study of Apolipoprotein E Gene Polymorphism With Incidence and Delayed Resolution of Hemifacial Spasm
Zhou, J., Jiang, L., Yuan, S., Huang, J., Shi, Q., Xie, Y., Deng, B., & Zhan, Y. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.760126 · Cited by 2 · see citing works
Lowering blood cholesterol does not affect neuroinflammation in experimental autoimmune encephalomyelitisPreprint
Vigne, S., Duc, D., Yersin, Y., Rebeaud, J., Ruiz, F., Peter, B., Collet, T., & Pot, C. (2021) · Research Square · doi:10.21203/rs.3.rs-315230/v1 · Cited by 1 · see citing works
DETERMINATION OF APOE GENE EXPRESSION IN MULTIPLE SCLEROSIS PATIENTS
Cakina, S., Yücel, S., & Polat, C. Ç. (2021) · Kocatepe tıp dergisi. · doi:10.18229/kocatepetip.633385
Activation of Microglia and Macrophages in Neurodegenerative Diseases
Salamero‐Boix, A., Schulz, M., & Sevenich, L. (2021) · Neuromethods · doi:10.1007/978-1-0716-1712-0_2
Impact of Listeria monocytogenes on microglia and cerebral homeostasis
Levallois, S. (2023) · theses.fr (ABES) · doi:10.70675/cf058269z5911z4582z94fezcb6761f74ddd
An unrecognized mechanism of neuroprotection by microglial TIA1-mediated stress granules to prevent neuroinflammation and demyelination in experimental autoimmune encephalomyelitis mice through sequestering ApoE mRNA
Fu, Q., Liu, Y., Li, F., Wang, Y., Yue, J., Chen, Y., Wu, S., Zhang, J., Jia, M., He, Y., et al. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03833-z
Apolipoprotein E Deficiency Attenuates Neuroinflammatory Responses and Demyelination in Experimental Autoimmune Encephalomyelitis
Lin, X., Wu, X., Guo, X., Zeng, Y., Ye, Q., & Zhang, J. (2026) · Molecular Neurobiology · doi:10.1007/s12035-026-05929-2
Epidemiology of cranial nerve syndromes
Kevci, R., Alhamdan, M., Ericson, H., Hamdeh, S. A., & Wettervik, T. S. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-44891-1.00011-9

Apolipoprotein E Deficiency Attenuates Neuroinflammatory Responses and Demyelination in Experimental Autoimmune Encephalomyelitis
Lin, X., Wu, X., Guo, X., Zeng, Y., Ye, Q., & Zhang, J. (2026) · Molecular Neurobiology · doi:10.1007/s12035-026-05929-2
Effect of apolipoprotein E on inflammation in mice with experimental autoimmune encephalomyelitis
Lei, Y., Wei, J., Tang, Y., Yang, C., Zheng, M., Zhao, W., Wei, Y., & Tao, M. (2016) · Chinese Journal of Neuromedicine · doi:10.3760/cma.j.issn.1671-8925.2016.05.001
Increased Susceptibility to Experimental Autoimmune Neuritis after Upregulation of the Autoreactive T Cell Response to Peripheral Myelin Antigen in Apolipoprotein E-Deficient Mice
Yu, S., Duan, R., Chen, Z., Quezada, H. C., Bao, L., Nennesmo, I., Zhu, S., Winblad, B. G., Ljunggren, H., & Zhu, J. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.2.120 · Cited by 16 · see citing works
The Immune‐Modulatory Role of Apolipoprotein E with Emphasis on Multiple Sclerosis and Experimental Autoimmune Encephalomyelitis
Zhang, H., Wu, J., & Zhu, J. (2010) · Journal of Immunology Research · doi:10.1155/2010/186813 · Cited by 98 · see citing works
Apolipoprotein E and its mimetic peptide suppress Th1 and Th17 responses in experimental autoimmune encephalomyelitis
Wei, J., Zheng, M., Liang, P., Wei, Y., Yin, X., Tang, Y., & Xue, Y. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.04.009 · Cited by 38 · see citing works

Authors: Shin, S., Walz, K. A., Archambault, A. S., Sim, J., Bollman, B. P., Koenigsknecht-Talboo, J., Cross, A. H., Holtzman, D. M., & Wu, G. F.
Affiliations: Washington University in St. Louis (US)
Corresponding author: Wu, Gregory F.
ORCID: Bollman, Bryan P.
Cross, Anne H.
Holtzman, David M.
Wu, Gregory F.
Venue: Journal of Neuroimmunology
Publisher: Elsevier BV
Published: 2014-06
Volume: 271
Issue: 1-2
Pages: 8-17
ISSN: 0165-5728 (ISSN-L)
DOI: 10.1016/j.jneuroim.2014.03.010
PMC: PMC4042395
OpenAlex: W2008256259
Cited by: 32
References: 63
Citations by year: 2026: 3 · 2024: 5 · 2023: 2 · 2022: 1 · 2021: 6 · 2020: 3 · 2019: 1 · 2018: 3 · 2017: 3 · 2016: 2 · 2015: 2 · 2014: 1
FWCI: 1.98
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Journal of Neuroimmunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
McDonnell Center for Cellular and Molecular Neurobiology, Washington University in St. Louis
National Institute on Aging (R01AG013956, R37AG013956, AG13956)
National Institute of Neurological Disorders and Stroke (R01NS083678, K08NS062138)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (P30AR048335)
Topics: Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: apolipoprotein E, neuroinflammation, multiple sclerosis, experimental autoimmune encephalomyelitis, ApoE-deficient mice, dendritic cells, innate immune cells, T cell priming, central nervous system demyelination, antigen presentation
MeSH terms: CX3C Chemokine Receptor 1, Animals, Apolipoproteins E, Central Nervous System, Dendritic Cells, Disease Models, Animal, Dose-Response Relationship, Immunologic, Encephalitis, Encephalomyelitis, Autoimmune, Experimental, Freund's Adjuvant, Leukocytes, Mononuclear, Mice, Inbred C57BL, Mice, Transgenic, Multiple Sclerosis, Spinal Cord, CD4-Positive T-Lymphocytes, Antigen Presentation, Receptors, Chemokine, 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

Apolipoprotein E mediation of neuro-inflammation in a murine model of multiple sclerosis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks