Quantitative proteomic analysis of the hippocampus in the 5XFAD mouse model at early stages of Alzheimer’s disease pathology
Abstract
Alzheimer's disease (AD) is characterized by progressive memory loss accompanied by synaptic and neuronal degeneration. Although research has shown that substantial neurodegeneration occurs even during the early stages of AD, the detailed mechanisms of AD pathogenesis are largely unknown because of difficulties in diagnosis and limitations of the analytical methods. The 5XFAD mouse model harbors five early-onset familial AD (FAD) mutations and displays substantial amyloid plaques and neurodegeneration. Here, we use quantitative mass spectrometry to identify proteome-wide changes in the 5XFAD mouse hippocampus during the early stages of AD pathology. A subset of the results was validated with immunoblotting. We found that the 5XFAD mice display higher expression of ApoE, ApoJ (clusterin), and nicastrin, three important proteins in AD that are known to participate in amyloid-β processing and clearance, as well as the neurological damage/glial marker protein GFAP and other proteins. A large subset of the proteins that were up- or downregulated in 5XFAD brains have been implicated in neurological disorders and cardiovascular disease, suggesting an association between cardiovascular disease and AD. Common upstream regulator analysis of upregulated proteins suggested that the XBP1, NRF2, and p53 transcriptional pathways were activated, as was IGF-1R signaling. Protein interactome analysis revealed an interconnected network of regulated proteins, with two major sub-networks centered on AβPP processing membrane complexes and mitochondrial proteins. Together with a recent study on the transcriptome of 5XFAD mice, our study allows a comprehensive understanding of the molecular events occurring in 5XFAD mice during the early stages of AD pathology.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
LCM has been used to micro-dissect neurons from both fresh frozen human brain and formalin-fixed paraffin embedded tissue sections for proteomic analyses.
“LCM has been used to micro-dissect neurons from both fresh frozen human brain and formalin-fixed paraffin embedded tissue sections for proteomic analyses [144, 145].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [145]
Hong et al. (2013) demonstrated activation of the NRF2 transcriptional pathway in 5XFAD mice at four months of age.
“For instance, Hong et al. (2013) used proteomic analysis to demonstrate activation of the NRF2 transcriptional pathway in 5XFAD mice at four months of age [100], which is consistent with ARE activation in Alzheimer’s patients [101].”
From Centella Asiatica Improves Memory and Promotes Antioxidative Signaling in 5XFAD Mice (2019) · cites this paper as [100]
Cites
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890 · see citing works
The Amyloid Hypothesis of Alzheimer’s Disease: Progress and Problems on the Road to Therapeutics
Hardy, J., & Selkoe, D. J. (2002) · Science · doi:10.1126/science.1072994 · Cited by 13,864 · see citing works
Corder, E. H., Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Small, G. W., Roses, A. D., Haines, J. L., & Pericak-Vance, M. A. (1993) · Science · doi:10.1126/science.8346443 · Cited by 9,429 · see citing works
Large-scale analysis of the yeast proteome by multidimensional protein identification technology
Washburn, M. P., Wolters, D. A., & Yates, J. R. (2001) · Nature Biotechnology · doi:10.1038/85686 · Cited by 4,759 · see citing works
Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide
Haass, C., & Selkoe, D. J. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2101 · Cited by 4,744 · see citing works
Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS–ADRDA criteria
Dubois, B., Feldman, H. H., Jacova, C., DeKosky, S. T., Barberger-Gateau, P., Cummings, J., Delacourte, A., Galasko, D., Gauthier, S., Jicha, G., et al. (2007) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70178-3 · Cited by 4,411 · see citing works
Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., & Selkoe, D. J. (2002) · Nature · doi:10.1038/416535a · Cited by 4,291 · see citing works
Clinical and biomarker changes in dominantly inherited Alzheimer's disease
Bateman, R. J., Xiong, C., Benzinger, T. L. S., Fagan, A. M., Goate, A., Fox, N. C., Marcus, D. S., Cairns, N. J., Xie, X., Blazey, T. M., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1202753 · Cited by 3,814 · 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 5× · see citing works
“We focus on the early phase of pathology, when synapse and memory deficits are first detected [22], to elucidate mechanisms that are involved in the onset and development of AD.”
InfluentialSzklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A. C., Mínguez, P., Doerks, T., Stark, M., Muller, J., Bork, P., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq973 · Cited by 3,469 · see citing works
Forecasting the global burden of Alzheimer's disease
Brookmeyer, R., Johnson, E., Ziegler‐Graham, K., & Arrighi, H. M. (2007) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2007.04.381 · Cited by 3,370 · see citing works
Cerebrospinal fluid and plasma biomarkers in Alzheimer disease
Blennow, K., Hampel, H., Weiner, M., & Zetterberg, H. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.4 · Cited by 1,863 · see citing works
Quantitative mass spectrometry in proteomics: a critical review
Bantscheff, M., Schirle, M., Sweetman, G. M. A., Rick, J. M., & Küster, B. (2007) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-007-1486-6 · Cited by 1,659 · see citing works
Amyloid-β and tau — a toxic pas de deux in Alzheimer's disease
Ittner, L. M., & Götz, J. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2967 · Cited by 1,357 · see citing works
Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy
Bu, G. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2620 · Cited by 1,168 · see citing works
Alzheimer's disease: strategies for disease modification
Citron, M. (2010) · Nature Reviews Drug Discovery · doi:10.1038/nrd2896 · Cited by 1,060 · see citing works
AMPAR Removal Underlies Aβ-Induced Synaptic Depression and Dendritic Spine Loss
Hsieh, H., Boehm, J., Sato, C., Iwatsubo, T., Tomita, T., Sisodia, S., & Malinow, R. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.035 · Cited by 1,042 · see citing works
Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and βAPP processing
Yu, G., Nishimura, M., Arawaka, S., Levitan, D. J., Zhang, L., Tandon, A., Song, Y., Rogaeva, E. A., Chen, F., Kawarai, T., et al. (2000) · Nature · doi:10.1038/35024009 · Cited by 906 · see citing works
Iwakoshi, N. N., Lee, A.-H., Vallabhajosyula, P., Otipoby, K. L., Rajewsky, K., & Glimcher, L. H. (2003) · Nature Immunology · doi:10.1038/ni907 · Cited by 880 · see citing works
ApoE Promotes the Proteolytic Degradation of Aβ
Jiang, Q., Lee, C. Y. D., Mandrekar, S., Wilkinson, B., Cramer, P., Zelcer, N., Mann, K., Lamb, B., Willson, T. M., Collins, J. L., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.010 · Cited by 876 · 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
Quantitative, High-Resolution Proteomics for Data-Driven Systems Biology
Cox, J., & Mann, M. (2011) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-061308-093216 · Cited by 685 · see citing works
Options and considerations when selecting a quantitative proteomics strategy
Domon, B., & Aebersold, R. H. (2010) · Nature Biotechnology · doi:10.1038/nbt.1661 · Cited by 601 · see citing works
Interleukin-1 Expression in Different Plaque Types in Alzheimerʼs Disease
Griffin, W. S. T., Sheng, J. G., Roberts, G. W., & Mrak, R. E. (1995) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199503000-00014 · Cited by 546 · see citing works
Resolving controversies on the path to Alzheimer's therapeutics
Selkoe, D. J. (2011) · Nature Medicine · doi:10.1038/nm.2460 · Cited by 494 · see citing works
ApoE and Clusterin Cooperatively Suppress Aβ Levels and Deposition
DeMattos, R. B., Cirrito, J. R., Parsadanian, M., May, P. C., O'Dell, M. A., Taylor, J. W., Harmony, J. A. K., Aronow, B. J., Bales, K. R., Paul, S. M., et al. (2004) · Neuron · doi:10.1016/s0896-6273(03)00850-x · Cited by 459 · see citing works
Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour
Pascoli, V., Turiault, M., & Lüscher, C. (2011) · Nature · doi:10.1038/nature10709 · Cited by 419 · see citing works
Kimura, R., & Ohno, M. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.10.006 · Cited by 333 · see citing works
Cardiovascular disease and Alzheimer's disease: common links
Stampfer, M. J. (2006) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2006.01687.x · Cited by 325 · see citing works
Li, Z., Adams, R. M., Chourey, K., Hurst, G. B., Hettich, R. L., & Pan, C. (2011) · Journal of Proteome Research · doi:10.1021/pr200748h · Cited by 302 · see citing works
Toward a Molecular Theory of Early and Late Events in Monomer to Amyloid Fibril Formation
Straub, J. E., & Thirumalai, D. (2011) · Annual Review of Physical Chemistry · doi:10.1146/annurev-physchem-032210-103526 · Cited by 272 · see citing works
Amygdala depotentiation and fear extinction
Kim, J., Lee, S., Park, K., Hong, I., Song, B., Son, G. H., Park, H., Kim, W. R., Park, E. J., Choe, H. K., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710548105 · Cited by 252 · see citing works
Self-citationNovel Research Horizons for Presenilins and γ-Secretases in Cell Biology and Disease
Strooper, B. D., & Annaert, W. G. (2010) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100109-104117 · Cited by 233 · see citing works
Validation of Tandem Mass Spectrometry Database Search Results Using DTASelect
Cociorva, D., Tabb, D. L., & Yates, J. R. (2006) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1304s16 · Cited by 228 · see citing works
Glial-Neuronal Interactions in Alzheimer Disease
Sheng, J. G., Mrak, R. E., & Griffin, W. S. T. (1997) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199703000-00007 · Cited by 215 · see citing works
Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase
Huang, T., Naeemuddin, M., Elchuri, S. V., Yamaguchi, M., Kozy, H. M., Carlson, E. J., & Epstein, C. J. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl034 · Cited by 188 · see citing works
Active γ-Secretase Complexes Contain Only One of Each Component
Sato, T., Diehl, T. S., Narayanan, S., Funamoto, S., Ihara, Y., Strooper, B. D., Steiner, H., Haass, C., & Wolfe, M. S. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705248200 · Cited by 187 · see citing works
Mild cognitive impairment clinical trials
Petersen, R. C. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1155 · Cited by 176 · see citing works
Quantitative proteomics of cerebrospinal fluid from patients with Alzheimer disease
Zhang, J., Goodlett, D. R., Quinn, J. F., Peskind, E. R., Kaye, J. A., Zhou, Y. F., Pan, C., Yi, E. C., Eng, J. K., Wang, Q., et al. (2005) · Journal of Alzheimer s Disease · doi:10.3233/jad-2005-7205 · Cited by 174 · see citing works
p53 is upregulated in Alzheimer's disease and induces tau phosphorylation in HEK293a cells
Hooper, C., Meimaridou, E., Tavassoli, M., Melino, G., Lovestone, S., & Killick, R. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.03.026 · Cited by 165 · see citing works
Grant, C. M., MacIver, F. H., & Dawes, I. W. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00592-9 · Cited by 151 · see citing works
Freude, S., Schilbach, K., & Schubert, M. (2009) · Current Alzheimer Research · doi:10.2174/156720509788486527 · Cited by 147 · see citing works
Gillardon, F., Rist, W., Kußmaul, L., Vogel, J., Berg, M., Danzer, K. M., Kraut, N., & Hengerer, B. (2007) · PROTEOMICS · doi:10.1002/pmic.200600728 · Cited by 137 · see citing works
Toward the Treatment and Prevention of Alzheimer's Disease: Rational Strategies and Recent Progress
Gandy, S., & DeKosky, S. T. (2013) · Annual Review of Medicine · doi:10.1146/annurev-med-092611-084441 · Cited by 110 · see citing works
Hong, I., Song, B., Lee, S., Kim, J., Kim, J., & Choi, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07004.x · Cited by 79 · see citing works
Self-citationMoon, M., Hong, H.-S., Nam, D. W., Baik, S. H., Song, H., Kook, S.-Y., Kim, Y. S., Lee, J., & Mook-Jung, I. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2011-111778 · Cited by 60 · see citing works
Self-citationReactivation of Fear Memory Renders Consolidated Amygdala Synapses Labile
Kim, J., Song, B., Hong, I., Kim, J., Lee, J. L. C., Park, S., Eom, J. Y., Lee, C. J., Lee, S., & Choi, S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0940-10.2010 · Cited by 55 · see citing works
Self-citationRaso, C., Cosentino, C., Gaspari, M., Malara, N., Han, X., McClatchy, D. B., Park, S. K., Renne, M., Vadalà, N., Prati, U., et al. (2012) · Journal of Proteome Research · doi:10.1021/pr2012347 · Cited by 46 · see citing works
Kim, K. H., Moon, M., Yu, S.-B., Mook‐Jung, I., & Kim, J. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-111793 · Cited by 45 · see citing works
Self-citationElectrophoretic, biosensor, and bioactivity analyses of perlecans of different cellular origins
Knox, S. M., Melrose, J., & Whitelock, J. M. (2001) · PROTEOMICS · doi:10.1002/1615-9861(200111)1:12 · Cited by 44 · see citing works
Hong, I., Kim, J., Lee, J., Park, S., Song, B., Kim, J., An, B., Park, K., Lee, H. W., Lee, S., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024260 · Cited by 27 · see citing works
Self-citationModulation of fear memory by retrieval and extinction: a clue for memory deconsolidation
Hong, I., Kim, J., Song, B., Park, S., Lee, J., Kim, J., An, B., Lee, S., & Choi, S. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.023 · Cited by 13 · see citing works
Self-citationByun, K., Kim, J. Y., Bayarsaikhan, E., Kim, D., Jeong, G., Yun, K. N., Min, H. K., Kim, S. U., Yoo, J. S., & Lee, B. (2012) · Electrophoresis · doi:10.1002/elps.201200345 · Cited by 11 · see citing works
Self-citationHong, I., Kim, J., Song, B., Park, K., Shin, K., Eom, K. D., Han, P., Lee, S., & Choi, S. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.10.063 · Cited by 10 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Landel, V., Baranger, K., Virard, I., Loriod, B., Khrestchatisky, M., Rivera, S., Benech, P., & Féron, F. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-33 · Cited by 176 · see citing works
Impaired Hippocampal Neurogenesis and its Enhancement with Ghrelin in 5XFAD Mice
Moon, M., Cha, M.-Y., & Mook-Jung, I. (2014) · Journal of Alzheimer's Disease · doi:10.3233/jad-132417 · Cited by 119 · see citing works
Self-citationSystems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau
Rayaprolu, S., Higginbotham, L., Bagchi, P., Watson, C. M., Zhang, T., Levey, A. I., Rangaraju, S., & Seyfried, N. T. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-020-00840-3 · Cited by 118 · see citing works
Andersen, J. V., Skotte, N. H., Christensen, S. K., Polli, F. S., Shabani, M., Markussen, K. H., Haukedal, H., Westi, E. W., Diaz-delCastillo, M., Sun, R. C., et al. (2021) · Cell Death & Disease · doi:10.1038/s41419-021-04237-y · Cited by 104 · see citing works
Chen, F., Swartzlander, D. B., Ghosh, A., Fryer, J. D., Wang, B., & Zheng, H. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00426-7 · Cited by 99 · see citing works
Neuner, S. M., Wilmott, L. A., Hoffmann, B. R., Mozhui, K., & Kaczorowski, C. C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.06.002 · Cited by 93 · see citing works
Axonal energy metabolism, and the effects in aging and neurodegenerative diseases
Yang, S., Park, J. H., & Lu, H.-C. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00634-3 · Cited by 94 · see citing works
Bundy, J. L., Vied, C., Badger, C., & Nowakowski, R. S. (2019) · Journal of Comparative Neurology · doi:10.1002/cne.24551 · Cited by 90 · see citing works
Centella Asiatica Improves Memory and Promotes Antioxidative Signaling in 5XFAD Mice
Matthews, D. G., Caruso, M., Murchison, C. F., Zhu, J. Y., Wright, K. M., Harris, C. J., Gray, N. E., Quinn, J. F., & Soumyanath, A. (2019) · Antioxidants · doi:10.3390/antiox8120630 · Cited by 86 · see citing works
“For instance, Hong et al. (2013) used proteomic analysis to demonstrate activation of the NRF2 transcriptional pathway in 5XFAD mice at four months of age [100], which is consistent with ARE activation in Alzheimer’s patients [101].”
MethodKim, D. K., Han, D., Park, J., Choi, H., Park, J., Cha, M.-Y., Woo, J. J., Byun, M. S., Lee, D. Y., Kim, Y., et al. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0326-z · Cited by 86 · see citing works
Self-citationKaya, I., Jennische, E., Lange, S., Baykal, A. T., Malmberg, P., & Fletcher, J. S. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.14999 · Cited by 84 · see citing works
Volkman, R., Ben‐Zur, T., Kahana, A., Garty, B. Z., & Offen, D. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00990 · Cited by 72 · see citing works
Siwek, M. E., Müller, R., Henseler, C., Trog, A., Lundt, A., Wormuth, C., Broich, K., Ehninger, D., Weiergräber, M., & Papazoglou, A. (2015) · Neural Plasticity · doi:10.1155/2015/781731 · Cited by 71 · see citing works
Kim, J. H., Franck, J., Kang, T., Heinsen, H., Ravid, R., Ferrer, I., Cheon, M. H., Lee, J., Yoo, J. S., Steinbusch, H. W. M., et al. (2015) · Scientific Reports · doi:10.1038/srep11138 · Cited by 68 · see citing works
Self-citationMiao, J., Zhang, Y., Chen, S., Zheng, Q., & Guo, J. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04457-1 · Cited by 66 · see citing works
Shin, S. J., Nam, Y., Park, Y. H., Kim, M., Lee, E., Jeon, S. G., Bae, B.-S., Seo, J., Shim, S., Kim, J.-S., et al. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.12.454 · Cited by 62 · see citing works
Self-citationYarbro, J. M., Han, X., Dasgupta, A., Yang, K., Liu, D., Shrestha, H. K., Zaman, M., Wang, Z., Yu, K., Lee, D. G., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-56853-3 · Cited by 41 · see citing works
Carmo, S. D., Crynen, G. C., Paradis, T., Reed, J. M., Iulita, M. F., Ducatenzeiler, A., Crawford, F., & Cuello, A. C. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0580-9 · Cited by 31 · see citing works
Boeddrich, A., Haenig, C., Neuendorf, N., Blanc, E., Ivanov, A., Kirchner, M., Schleumann, P., Bayraktaroğlu, I., Richter, M., Molenda, C., et al. (2023) · Genome Medicine · doi:10.1186/s13073-023-01206-2 · Cited by 27 · see citing works
Aβ42 oligomers modulate β-secretase through an XBP-1s-dependent pathway involving HRD1
Gerakis, Y., Dunys, J., Bauer, C., & Checler, F. (2016) · Scientific Reports · doi:10.1038/srep37436 · Cited by 25 · see citing works
Lassen, P. S., Thygesen, C., Larsen, M. R., & Kempf, S. J. (2017) · Journal of Proteomics · doi:10.1016/j.jprot.2017.04.003 · Cited by 26 · see citing works
Devi, L., & Ohno, M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.08.037 · Cited by 28 · see citing works
Lim, S. H., Kim, Y., Yun, K. N., Kim, J. Y., Jang, J., Han, M., & Lee, J. (2016) · Scientific Reports · doi:10.1038/srep38728 · Cited by 25 · see citing works
Self-citationVera, D. M., Zhao, H., Bereczki, E., Rosell‐Valle, C., Shimozawa, M., Chen, G., de Fonseca, F. R., Nilsson, P., & Tambaro, S. (2023) · Biology · doi:10.3390/biology12060805 · Cited by 22 · see citing works
Histone H3 Ser57 and Thr58 phosphorylation in the brain of 5XFAD mice
Anderson, K. W., Mast, N., Pikuleva, I. A., & Turko, I. V. (2015) · FEBS Open Bio · doi:10.1016/j.fob.2015.06.009 · Cited by 21 · see citing works
New Insight into Neurodegeneration: the Role of Proteomics
Pal, R., Alves, G. W., Larsen, J. P., & Møller, S. G. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8590-8 · Cited by 19 · see citing works
Amyloid-Beta-Activated Human Microglial Cells Through ER-Resident Proteins
Yoo, Y., Byun, K., Kang, T., Bayarsaikhan, D., Kim, J. Y., Oh, S., Kim, Y. H., Kim, S. Y., Chung, W., Kim, S. U., et al. (2014) · Journal of Proteome Research · doi:10.1021/pr500926r · Cited by 17 · see citing works
Self-citationThe Potential of Proteomics in Understanding Neurodegeneration
Pal, R., Larsen, J. P., & Møller, S. G. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.05.002 · Cited by 17 · see citing works
Cyclic microchip assay for measurement of hundreds of functional proteins in single neurons
Yang, L., Ball, A., Liu, J. J., Jain, T., Li, Y., Akhter, F., Zhu, D., & Wang, J. (2022) · Nature Communications · doi:10.1038/s41467-022-31336-x · Cited by 15 · see citing works
Multi-scale modeling for systematically understanding the key roles of microglia in AD development
Ji, Z., Liu, C., Zhao, W., Soto, C. A., & Zhou, X. (2021) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2021.104374 · Cited by 10 · see citing works
Jarné‐Ferrer, J., Griñán‐Ferré, C., Bellver‐Sanchís, A., Vázquez, S., Muñoz‐Torrero, D., & Pallàs, M. (2022) · Pharmaceuticals · doi:10.3390/ph15080908 · Cited by 9 · see citing works
Hippocampal proteomic changes in high-fat diet-induced obese mice associated with memory decline
Lu, P., Gao, C.-X., Luo, F.-J., Huang, Y.-T., Gao, M., & Long, Y. (2023) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2023.109554 · Cited by 7 · see citing works
Rahman, M. A., Hossain, S., Abdullah, N., & Aminudin, N. (2019) · AIMS neuroscience · doi:10.3934/neuroscience.2019.4.299 · Cited by 7 · see citing works
Ohno, M. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-231451 · Cited by 5 · see citing works
Xu, H. N., Gourmaud, S., Podsednik, A., Li, X., Zhao, H., Jensen, F. E., Talos, D. M., & Li, L. Z. (2022) · Metabolites · doi:10.3390/metabo12090786 · Cited by 4 · see citing works
Fractionation‐dependent improvements in proteome resolution in the mouse hippocampus by IEF LC‐MS/MS
Bundy, J. L., Inouye, B. D., Mercer, R. S., & Nowakowski, R. S. (2016) · Electrophoresis · doi:10.1002/elps.201600076 · Cited by 3 · see citing works
Boeddrich, A., Haenig, C., Neuendorf, N., Blanc, E., Ivanov, A., Kirchner, M., Schleumann, P., Bayraktaroğlu, I., Richter, M., Molenda, C., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.16.523715 · Cited by 2 · see citing works
Increased astrocyte representation in the hippocampus of 5xFAD mice
Jovanović, V., Despotović, J., Balo, M., Zaletel, I. V., Despotović, S. Z., & Puškaš, N. (2021) · Medicinski podmladak · doi:10.5937/mp72-32451
Boeddrich, A., Haenig, C., Neuendorf, N., Blanc, E., Ivanov, A., Kirchner, M., Schleumann, P., Bayraktaroğlu, I., Richter, M., Molenda, C., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23714235
Chen, F., Swartzlander, D. B., Ghosh, A., Fryer, J. D., Wang, B., & Zheng, H. (2021) · Figshare · doi:10.6084/m9.figshare.13671113
Boeddrich, A., Haenig, C., Neuendorf, N., Blanc, E., Ivanov, A., Kirchner, M., Schleumann, P., Bayraktaroğlu, I., Richter, M., Molenda, C., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23714229
Boeddrich, A., Haenig, C., Neuendorf, N., Blanc, E., Ivanov, A., Kirchner, M., Schleumann, P., Bayraktaroğlu, I., Richter, M., Molenda, C., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23714232
- Authors
- Hong, I., Kang, T., Yoo, Y., Park, R., Lee, J., Lee, S., Kim, J., Song, B., Kim, S.-Y., Moon, M., Yun, K. N., Kim, J. Y., Mook-Jung, I., Park, Y. M., & Choi, S.
- Affiliations
- Seoul National University (KR)
- Chungnam National University (KR)
- Korea Basic Science Institute (KR)
- Department of Biochemistry and Molecular Biology, Seoul National University College of Medicine, Seoul, Korea
- Corresponding author
- Choi, Sukwoo
- ORCID
- Venue
- Journal of Alzheimer s Disease
- Publisher
- SAGE Publications
- Published
- 2013-06-18
- Volume
- 36
- Issue
- 2
- Pages
- 321-334
- ISSN
- 1387-2877 (ISSN-L)
- 1875-8908
- OpenAlex
- W1542220056
- Cited by
- 41
- References
- 54
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 7 · 2022: 3 · 2021: 6 · 2020: 2 · 2019: 4 · 2018: 1 · 2017: 2 · 2016: 4 · 2015: 5 · 2014: 3 · 2013: 1
- FWCI
- 3.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Alzheimer s Disease (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Keywords
- Alzheimer's disease, 5xFAD mice
- MeSH terms
- Alzheimer Disease, Animals, Chromatography, Liquid, Disease Models, Animal, Gene Expression Regulation, Glial Fibrillary Acidic Protein, Hippocampus, Humans, Membrane Glycoproteins, Mutation, Transcription Factors, Signal Transduction, Amyloid beta-Protein Precursor, Proteome, Mice, Tandem Mass Spectrometry, Presenilin-1, Amyloid Precursor Protein Secretases
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
