Changes in the detergent‐insoluble brain proteome linked to amyloid and tau in Alzheimer's Disease progression

Hales, Chadwick M.; Dammer, Eric B.; Deng, Qiudong; Duong, Duc M.; Gearing, Marla; Troncoso, Juan C.; Thambisetty, Madhav; Lah, James J.; Shulman, Joshua M.; Levey, Allan I.; Seyfried, Nicholas T.

doi:10.1002/pmic.201600057

Cited by 101Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchAdvanced Proteomics Techniques and Applications

Changes in the detergent‐insoluble brain proteome linked to amyloid and tau in Alzheimer's Disease progression

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Hales, Chadwick M., Dammer, Eric B., Deng, Qiudong, Duong, Duc M., Gearing, Marla, Troncoso, Juan C., Thambisetty, Madhav, Lah, James J. +3 more·2016·PROTEOMICS

DOI 10.1002/pmic.201600057PMC PMC5462625

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Abstract

Despite a key role of amyloid‐beta (Aβ) in Alzheimer's disease (AD), mechanisms that link Aβ plaques to tau neurofibrillary tangles and cognitive decline still remain poorly understood. The purpose of this study was to quantify proteins in the sarkosyl‐insoluble brain proteome correlated with Aβ and tau insolubility in the asymptomatic phase of AD (AsymAD) and through mild cognitive impairment (MCI) and symptomatic AD. Employing label‐free mass spectrometry‐based proteomics, we quantified 2711 sarkosyl‐insoluble proteins across the prefrontal cortex from 35 individual cases representing control, AsymAD, MCI and AD. Significant enrichment of Aβ and tau in AD was observed, which correlated with neuropathological measurements of plaque and tau tangle density, respectively. Pairwise correlation coefficients were also determined for all quantified proteins to Aβ and tau, across the 35 cases. Notably, six of the ten most correlated proteins to Aβ were U1 small nuclear ribonucleoproteins (U1 snRNPs). Three of these U1 snRNPs (U1A, SmD and U1‐70K) also correlated with tau consistent with their association with tangle pathology in AD. Thus, proteins that cross‐correlate with both Aβ and tau, including specific U1 snRNPs, may have potential mechanistic roles in linking Aβ plaques to tau tangle pathology during AD progression.

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Aggregated U1 snRNPs have been observed in asymptomatic AD brains.
“these aggregated U1 snRNPs have been observed in asymptomatic AD brains [135]”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [135]
U1 small nuclear ribonucleoproteins and other RNA-binding proteins are associated with tau tangles in the AD brain detergent-insoluble proteome.
“previous analyses of the AD brain detergent-insoluble proteome, which have repeatedly demonstrated the association of U1 small nuclear ribonucleoproteins (U1 snRNPs) and other RNA-binding proteins with tau tangles [133–137].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [135]
Many U1 snRNPs colocalize with neurofibrillary tangles and paired helical filaments in AD brain.
“Interestingly, our previous studies demonstrated that many of the U1 snRNPs colocalize with neurofibrillary tangles and paired helical filaments in AD brain [24, 32–34], and that accumulation of insoluble snRNPs correlates strongly with both amyloid and Tau pathology [32–37].”
From Deep proteomic network analysis of Alzheimer’s disease brain reveals alterations in RNA binding proteins and RNA splicing associated with disease (2018) · cites this paper as [32]
Aggregation of RNA binding proteins that are part of the cellular pre-mRNA splicing machinery, especially U1 snRNPs such as U1-70K, is an early event in AD pathogenesis.
“We have previously reported that aggregation of RNA binding proteins that are a part of the cellular pre-mRNA splicing machinery, especially the U1 small nuclear ribonucleoproteins (snRNPs) such as U1-70K, is an early event in AD pathogenesis [32].”
From Deep proteomic network analysis of Alzheimer’s disease brain reveals alterations in RNA binding proteins and RNA splicing associated with disease (2018) · cites this paper as [32]
Accumulation of insoluble snRNPs correlates strongly with both amyloid and Tau pathology.
“Interestingly, our previous studies demonstrated that many of the U1 snRNPs colocalize with neurofibrillary tangles and paired helical filaments in AD brain [24, 32–34], and that accumulation of insoluble snRNPs correlates strongly with both amyloid and Tau pathology [32–37].”
From Deep proteomic network analysis of Alzheimer’s disease brain reveals alterations in RNA binding proteins and RNA splicing associated with disease (2018) · cites this paper as [32]

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Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888 · see citing works
Neuropathological stageing of Alzheimer-related changes.
Braak, H., & Braak, E. (1991) · Acta Neuropathologica · doi:10.1007/bf00308809 · Cited by 16,123 · 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
Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease
Sperling, R. A., Aisen, P. S., Beckett, L. A., Bennett, D. A., Craft, S., Fagan, A. M., Iwatsubo, T., Jack, C. R., Kaye, J., Montine, T. J., et al. (2011) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.03.003 · Cited by 7,155 · see citing works
The Consortium to Establish a Registry for Alzheimer's Disease (CERAD): Part II. Standardization of the neuropathologic assessment of Alzheimer's disease
Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M., Crain, B. J., Brownlee, L. M., Vogel, F. S., Hughes, J. P., Belle, G. V., Berg, L., et al. (1991) · Neurology · doi:10.1212/wnl.41.4.479 · Cited by 4,961 · see citing works
An RNA-Sequencing Transcriptome and Splicing Database of Glia, Neurons, and Vascular Cells of the Cerebral Cortex
Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., Phatnani, H. P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1860-14.2014 · Cited by 4,875 · see citing works
Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry
Elias, J. E., & Gygi, S. P. (2007) · Nature Methods · doi:10.1038/nmeth1019 · Cited by 3,925 · see citing works
Protein aggregation and neurodegenerative disease
Ross, C. A., & Poirier, M. A. (2004) · Nature Medicine · doi:10.1038/nm1066 · Cited by 3,454 · see citing works
Neuropathological alterations in Alzheimer disease
Serrano-Pozo, A., Frosch, M. P., Masliah, E., & Hyman, B. T. (2011) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006189 · Cited by 3,345 · see citing works
Complement and microglia mediate early synapse loss in Alzheimer mouse models
Hong, S., Beja-Glasser, V. F., Nfonoyim, B. M., Frouin, A., Li, S., Ramakrishnan, S., Merry, K. M., Shi, Q., Rosenthal, A., Barres, B. A., et al. (2016) · Science · doi:10.1126/science.aad8373 · Cited by 3,343 · cited 1× · see citing works
“Complement C3 in the brain is primarily expressed by microglia [60], and is essential in the process of microglial-mediated early synaptic loss in AD models [61].”
Background
Phase Separation by Low Complexity Domains Promotes Stress Granule Assembly and Drives Pathological Fibrillization
Molliex, A., Temirov, J. P., Lee, J., Coughlin, M., Kanagaraj, A., Kim, H. J., Mittag, T., & Taylor, J. P. (2015) · Cell · doi:10.1016/j.cell.2015.09.015 · Cited by 2,658 · see citing works
Amyloid deposition as the central event in the aetiology of Alzheimer’s disease
Hardy, J., & Allsop, D. (1991) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(91)90609-v · Cited by 2,538 · see citing works
Adapting Proteostasis for Disease Intervention
Balch, W. E., Morimoto, R. I., Dillin, A., & Kelly, J. W. (2008) · Science · doi:10.1126/science.1141448 · Cited by 2,495 · see citing works
The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics
Karran, E., Mercken, M., & Strooper, B. D. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3505 · Cited by 2,188 · cited 5× · see citing works
“Alzheimer’s disease (AD) is characterized by extracellular deposition of detergent-insoluble -amyloid (A ) as senile plaques, as well as intracellular accumulation of neurofibrillary tangles (NFTs) composed of aggregated tau [3, 4].”
BackgroundInfluential
Absolute Quantification of Proteins by LCMSE
Silva, J. C., Gorenstein, M. V., Li, G.-Z., Vissers, J. P. C., & Geromanos, S. J. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m500230-mcp200 · Cited by 1,529 · see citing works
Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS
Kim, H. J., Kim, N. C., Wang, Y., Scarborough, E. A., Moore, J., Diaz, Z., MacLea, K. S., Freibaum, B. D., Li, S., Molliex, A., et al. (2013) · Nature · doi:10.1038/nature11922 · Cited by 1,476 · see citing works
ABAD Directly Links Aß to Mitochondrial Toxicity in Alzheimer's Disease
Lustbader, J. W., Cirilli, M., Lin, C., Xu, H. W., Takuma, K., Wang, N., Caspersen, C., Chen, X., Pollak, S., Chaney, M., et al. (2004) · Science · doi:10.1126/science.1091230 · Cited by 1,303 · see citing works
Fast R Functions for Robust Correlations and Hierarchical Clustering
Langfelder, P., & Horvath, S. (2012) · Journal of Statistical Software · doi:10.18637/jss.v046.i11 · Cited by 1,297 · see citing works
Toxic Proteins in Neurodegenerative Disease
Taylor, J. P., Hardy, J., & Fischbeck, K. H. (2002) · Science · doi:10.1126/science.1067122 · Cited by 1,251 · see citing works
The Cortical Signature of Alzheimer's Disease: Regionally Specific Cortical Thinning Relates to Symptom Severity in Very Mild to Mild AD Dementia and is Detectable in Asymptomatic Amyloid-Positive Individuals
Dickerson, B. C., Bakkour, A., Salat, D. H., Feczko, E., Pacheco, J., Greve, D. N., Grodstein, F., Wright, C. I., Blacker, D., Rosas, H. D., et al. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn113 · Cited by 1,153 · see citing works
Tau pathology and neurodegeneration
Spillantini, M. G., & Goedert, M. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70090-5 · Cited by 1,133 · see citing works
ALS/FTD Mutation-Induced Phase Transition of FUS Liquid Droplets and Reversible Hydrogels into Irreversible Hydrogels Impairs RNP Granule Function
Murakami, T., Qamar, S., Lin, J. Q., Schierle, G. S. K., Rees, E. J., Miyashita, A., Costa, A. R., Dodd, R. B., Chan, F. T. S., Michel, C. H., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.030 · Cited by 848 · see citing works
Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205
Goedert, M., Jakes, R., & Vanmechelen, E. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11484-e · Cited by 608 · see citing works
Longitudinal PET evaluation of cerebral metabolic decline in dementia: a potential outcome measure in Alzheimer’s disease treatment studies
Alexander, G. E., Chen, K., Pietrini, P., Rapoport, S. I., & Reiman, E. M. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.5.738 · Cited by 532 · see citing works
Neocortical Neurofibrillary Tangles Correlate With Dementia Severity in Alzheimer's Disease
Bierer, L. M., Hof, P. R., Purohit, D. P., Carlin, L., Schmeidler, J., Davis, K. L., & Perl, D. P. (1995) · Archives of Neurology · doi:10.1001/archneur.1995.00540250089017 · Cited by 514 · see citing works
Cleavage of tau by asparagine endopeptidase mediates the neurofibrillary pathology in Alzheimer's disease
Zhang, Z., Song, M., Liu, X., Kang, S. S., Kwon, I.-S., Duong, D. M., Seyfried, N. T., Hu, W. T., Liu, Z., Wang, J.-Z., et al. (2014) · Nature Medicine · doi:10.1038/nm.3700 · Cited by 494 · see citing works
Self-citation
Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis
Tennent, G. A., Lovat, L. B., & Pepys, M. B. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4299 · Cited by 438 · see citing works
Ribosome Dysfunction Is an Early Event in Alzheimer's Disease
Ding, Q., Markesbery, W. R., Chen, Q., Li, F., & Keller, J. N. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3040-05.2005 · Cited by 433 · see citing works
A yeast functional screen predicts new candidate ALS disease genes
Couthouis, J., Hart, M. P., Shorter, J., DeJesus‐Hernandez, M., Erion, R., Oristano, R., Liu, A. X., Ramos, D. M., Jethava, N., Hosangadi, D., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109434108 · Cited by 389 · see citing works
Interaction of tau with the RNA-Binding Protein TIA1 Regulates tau Pathophysiology and Toxicity
Vanderweyde, T. E., Apicco, D. J., Youmans-Kidder, K., Ash, P. E. A., Cook, C. N., da Rocha, E. L., Jansen‐West, K. R., Frame, A. A., Citro, A., Leszyk, J., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.045 · Cited by 346 · see citing works
U1 small nuclear ribonucleoprotein complex and RNA splicing alterations in Alzheimer’s disease
Bai, B., Hales, C. M., Chen, P.-C., Gozal, Y., Dammer, E. B., Fritz, J. J., Wang, X., Xia, Q., Duong, D. M., Street, C., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310249110 · Cited by 335 · see citing works
Self-citation
Complement activation in amyloid plaques in Alzheimer’s dementia
Eikelenboom, P., Hack, C. E., Rozemüller, A. J. M., & Stam, F. C. (1988) · Virchows Archiv B Cell Pathology Including Molecular Pathology · doi:10.1007/bf02890024 · Cited by 288 · see citing works
GO-Elite: a flexible solution for pathway and ontology over-representation
Zambon, A. C., Gaj, S., Ho, I., Hanspers, K., VRANIZAN, K. M., Evelo, C. T., Conklin, B. R., Pico, A. R., & Salomonis, N. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts366 · Cited by 263 · see citing works
Systematical Optimization of Reverse-Phase Chromatography for Shotgun Proteomics
Xu, P., Duong, D. M., & Peng, J. (2009) · Journal of Proteome Research · doi:10.1021/pr900251d · Cited by 202 · see citing works
Self-citation
The SMN Complex: An Assembly Machine for RNPsPreprint
Battle, D. J., Kasim, M., Yong, J., Lotti, F., Lau, T. C., Mouaikel, J., Zhang, Z., HAN, K., Wan, L., & Dreyfuss, G. (2006) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2006.71.001 · Cited by 187 · see citing works
Characterization and Molecular Profiling of PSEN1 Familial Alzheimer's Disease iPSC-Derived Neural Progenitors
Sproul, A. A., Jacob, S., Prè, D., Kim, S. H., Nestor, M. W., Navarro-Sobrino, M., Santa‐María, I., Zimmer, M., Aubry, S., Steele, J., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084547 · Cited by 179 · see citing works
Functional screening in Drosophila identifies Alzheimer's disease susceptibility genes and implicates Tau-mediated mechanisms
Shulman, J. M., Imboywa, S., Giagtzoglou, N., Powers, M. P., Hu, Y., Devenport, D., Chipendo, P., Chibnik, L. B., Diamond, A., Perrimon, N., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddt478 · Cited by 167 · see citing works
Self-citation
Neuropathologic Studies of the Baltimore Longitudinal Study of Aging (BLSA)
O'Brien, R. J., Resnick, S. M., Zonderman, A. B., Ferrucci, L., Crain, B. J., Pletnikova, O., Rudow, G., Iacono, D., Riudavets, M. A., Driscoll, I., et al. (2009) · Journal of Alzheimer's Disease · doi:10.3233/jad-2009-1179 · Cited by 137 · see citing works
Self-citation
Coaggregation of RNA-Binding Proteins in a Model of TDP-43 Proteinopathy with Selective RGG Motif Methylation and a Role for RRM1 Ubiquitination
Dammer, E. B., Fallini, C., Gozal, Y. M., Duong, D. M., Rossoll, W., Xu, P., Lah, J. J., Levey, A. I., Peng, J., Bassell, G. J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038658 · Cited by 124 · see citing works
Self-citation
Progressive Infantile Neurodegeneration Caused by 2-Methyl-3-Hydroxybutyryl-CoA Dehydrogenase Deficiency: A Novel Inborn Error of Branched-Chain Fatty Acid and Isoleucine Metabolism
Zschocke, J., Ruiter, J. P. N., Brand, J., Lindner, M. S., Hoffmann, G. F., Wanders, R. J. A., & Mayatepek, E. (2000) · Pediatric Research · doi:10.1203/00006450-200012000-00025 · Cited by 116 · see citing works
Human High Temperature Requirement Serine Protease A1 (HTRA1) Degrades Tau Protein Aggregates
Tennstaedt, A., Poepsel, S., Truebestein, L., Hauske, P., Brockmann, A., Schmidt, N., Irle, I., Saccà, B., Niemeyer, C. M., Brandt, R., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.316232 · Cited by 98 · see citing works
Proteomics Analysis Reveals Novel Components in the Detergent-Insoluble Subproteome in Alzheimer’s Disease
Gozal, Y. M., Duong, D. M., Gearing, M., Cheng, D., Hanfelt, J., Funderburk, C. D., Peng, J., Lah, J. J., & Levey, A. I. (2009) · Journal of Proteome Research · doi:10.1021/pr900474t · Cited by 92 · see citing works
Self-citation
Aggregates of Small Nuclear Ribonucleic Acids ( <scp>snRNAs</scp> ) in <scp>A</scp> lzheimer's Disease
Hales, C. M., Dammer, E. B., Diner, I., Yi, H., Seyfried, N. T., Gearing, M., Glass, J. D., Montine, T. J., Levey, A. I., & Lah, J. J. (2014) · Brain Pathology · doi:10.1111/bpa.12133 · Cited by 89 · see citing works
Self-citation
Serum amyloid P immunoreactivity in hippocampal tangles, plaques and vessels: implications for leakage across the blood-brain barrier in Alzheimer's disease
Kalaria, R. N., & Grahovac, I. (1990) · Brain Research · doi:10.1016/0006-8993(90)90941-4 · Cited by 83 · see citing works
Roles of 17β-hydroxysteroid dehydrogenase type 10 in neurodegenerative disorders
Yang, S., He, X., Isaacs, C. E., Dobkin, C., Miller, D. L., & Philipp, M. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.07.001 · Cited by 82 · see citing works
Analysis of a membrane‐enriched proteome from postmortem human brain tissue in A lzheimer's disease
Donovan, L. E., Higginbotham, L. A., Dammer, E. B., Gearing, M., Rees, H. D., Xia, Q., Duong, D. M., Seyfried, N. T., Lah, J. J., & Levey, A. I. (2012) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201100068 · Cited by 82 · see citing works
Self-citation
Quantitative phosphoproteomics of Alzheimer's disease reveals cross‐talk between kinases and small heat shock proteins
Dammer, E. B., Lee, A. K., Duong, D. M., Gearing, M., Lah, J. J., Levey, A. I., & Seyfried, N. T. (2014) · PROTEOMICS · doi:10.1002/pmic.201400189 · Cited by 80 · see citing works
Self-citation
Retinal Degenerative Diseases
Lavail, M., Ash, J. D., Anderson, R. E., Hollyfield, J., & Grimm, C. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-0631-0 · Cited by 76 · see citing works
Apolipoprotein E Interaction with the Neurofibrillary Tangles and Senile Plaques in Alzheimer Disease: Implications for Disease Pathogenesis
Richey, P. L., Siedlak, S. L., Smith, M. A., & Perry, G. L. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.1389 · Cited by 72 · see citing works
Immunophilin FKBP52 induces Tau-P301L filamentous assembly in vitro and modulates its activity in a model of tauopathy
Giustiniani, J., Chambraud, B., Sardin, E., Dounane, O., Guillemeau, K., Nakatani, H., Paquet, D., Kamah, A., Landrieu, I., Lippens, G. M., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402645111 · Cited by 72 · see citing works
Impaired retrograde transport by the Dynein/Dynactin complex contributes to Tau-induced toxicity
Butzlaff, M., Hannan, S. B., Karsten, P., Lenz, S., Ng, J., Voßfeldt, H., Prüßing, K., Pflanz, R., Schulz, J. B., Rasse, T. M., et al. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv107 · Cited by 72 · see citing works
Neuron Enriched Nuclear Proteome Isolated from Human Brain
Dammer, E. B., Duong, D. M., Diner, I., Gearing, M., Feng, Y., Lah, J. J., Levey, A. I., & Seyfried, N. T. (2013) · Journal of Proteome Research · doi:10.1021/pr400246t · Cited by 70 · see citing works
Self-citation
Asparaginyl endopeptidase cleaves TDP‐43 in brain
Herskowitz, J. H., Gozal, Y. M., Duong, D. M., Dammer, E. B., Gearing, M., Ye, K., Lah, J. J., Peng, J., Levey, A. I., & Seyfried, N. T. (2012) · PROTEOMICS · doi:10.1002/pmic.201200006 · Cited by 69 · see citing works
Self-citation
Quantitative Analysis of the Detergent-Insoluble Brain Proteome in Frontotemporal Lobar Degeneration Using SILAC Internal Standards
Seyfried, N. T., Gozal, Y. M., Donovan, L. E., Herskowitz, J. H., Dammer, E. B., Xia, Q., Ku, L., Chang, J., Duong, D. M., Rees, H. D., et al. (2012) · Journal of Proteome Research · doi:10.1021/pr2010814 · Cited by 64 · see citing works
Self-citation
Aggregation Properties of the Small Nuclear Ribonucleoprotein U1-70K in Alzheimer Disease
Diner, I., Hales, C. M., Bishof, I., Rabenold, L., Duong, D. M., Yi, H., Laur, O., Gearing, M., Troncoso, J., Thambisetty, M., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.562959 · Cited by 63 · see citing works
Self-citation
Proteomics of protein post-translational modifications implicated in neurodegeneration
Ren, R., Dammer, E. B., Wang, G., Seyfried, N. T., & Levey, A. I. (2014) · Translational Neurodegeneration · doi:10.1186/2047-9158-3-23 · Cited by 63 · see citing works
Self-citation
U1 small nuclear ribonucleoproteins (snRNPs) aggregate in Alzheimer’s disease due to autosomal dominant genetic mutations and trisomy 21
Hales, C. M., Seyfried, N. T., Dammer, E. B., Duong, D., Yi, H., Gearing, M., Troncoso, J. C., Mufson, E. J., Thambisetty, M., Levey, A. I., et al. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-15 · Cited by 58 · see citing works
Self-citation
Alzheimer's Aβ interacts with cellular prion protein inducing neuronal membrane damage and synaptotoxicity
Peters, C., Espinoza, M. P., Gallegos, S., Opazo, C., & Aguayo, L. G. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.11.019 · Cited by 56 · see citing works
Membrane-Anchored Aβ Accelerates Amyloid Formation and Exacerbates Amyloid-Associated Toxicity in Mice
Nagarathinam, A., Höflinger, P., Bühler, A., Schäfer, C., McGovern, G., Jeffrey, M., Staufenbiel, M., Jucker, M., & Baumann, F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2542-13.2013 · Cited by 44 · see citing works
Exploring the potential of the platelet membrane proteome as a source of peripheral biomarkers for Alzheimer's disease
Donovan, L. E., Dammer, E. B., Duong, D. M., Hanfelt, J., Levey, A. I., Seyfried, N. T., & Lah, J. J. (2013) · Alzheimer s Research & Therapy · doi:10.1186/alzrt186 · Cited by 43 · see citing works
Self-citation
Expression of Regulatory Proteins in Choroid Plexus Changes in Early Stages of Alzheimer Disease
Krzyzanowska, A., García-Consuegra, I., Pascual, C., Antequera, D., Ferrer, I., & Carro, E. (2015) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000181 · Cited by 42 · see citing works
Evaluation of annexin A5 as a biomarker for Alzheimer's disease and dementia with lewy bodies
Sohma, H., Imai, S.-I., Takei, N., Honda, H., Matsumoto, K., Utsumi, K., Matsuki, K., Hashimoto, E., Saito, T., & Kokai, Y. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2013.00015 · Cited by 37 · see citing works
Association of frailty with the serine protease HtrA1 in older adults
Lorenzi, M., Lorenzi, T., Marzetti, E., Landi, F., Vetrano, D. L., Settanni, S., Antocicco, M., Bonassi, S., Valdiglesias, V., Bernabei, R., et al. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.03.019 · Cited by 36 · see citing works
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Page, R. M., Münch, A., Horn, T. L., Kuhn, P., Colombo, A. V., Reiner, O., Boutros, M., Steiner, H., Lichtenthaler, S. F., & Haass, C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2681-12.2012 · Cited by 33 · see citing works
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Braunger, B. M., & Tamm, E. R. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-0631-0_86 · Cited by 19 · see citing works

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[22]Seyfried NT Gozal YM Donovan LE Herskowitz JH Quantitative analysis of the detergent-insoluble brain proteome in frontotemporal lobar degeneration using SILAC internal standards Journal of proteome research 2012 11 2721 2738 22416763 PMC3357000

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Kordas, G., Rudra, P., Hendricks, A. E., Saba, L. M., & Kechris, K. J. (2019) · BMC Genomics · doi:10.1186/s12864-019-6110-6 · Cited by 5 · see citing works
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Paradise, V., Konrad, K. D., Nguyen, C., Sharif, N. A., Wang, X., Mukim, R. D., Sabu, M., Corjuc, B. T., Bafia, J., Fu, J. M., et al. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02297-x · Cited by 4 · see citing works
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Kawahara, K., Hasegawa, T., Hasegawa, N., Izumi, T., Sato, K., Sakamaki, T., Ando, M., & Maeda, T. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16078 · Cited by 4 · see citing works
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Kavanagh, T., Balcomb, K., Trgovcevic, S., Nementzik, L. R., Kanshin, E., Halliday, G. M., Ueberheide, B. M., & Drummond, E. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70401 · Cited by 5 · see citing works
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Askenazi, M., Kavanagh, T., Pires, G., Ueberheide, B. M., Wısnıewskı, T., & Drummond, E. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.13.536828 · Cited by 4 · see citing works
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Hagemeier, B., Ripkens, K., Schulze, N., Bluemke, A., Strzala, M., Koci, M., Kaschani, F., Kaiser, M., Erkelenz, M., Schluecker, S., et al. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110729 · Cited by 3 · see citing works
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Saleem, T., Möbius, W., Schmitz, M., Correia, A. D. S., Thomas, C., Canaslan, S., Hermann, P., Goebel, S., Zafar, S., Root, E., et al. (2026) · Acta Neuropathologica · doi:10.1007/s00401-026-02998-4 · Cited by 4 · see citing works
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Soares, E. S., Leal, C. B. Q. D. S., Sinatti, V. V. C., Bottos, R. M., & Zimmer, C. G. M. (2025) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.70026 · Cited by 3 · see citing works
Subcellular proteomics insights into Alzheimer's disease development
Liang, Z., Zhuang, H., Cao, X., Ma, G., & Shen, L. (2023) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.202200112 · Cited by 3 · see citing works
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Devitt, G., Hanrahan, N., Moreno, M. R., Mudher, A. K., & Mahajan, S. (2025) · Analytical Chemistry · doi:10.1021/acs.analchem.5c00776 · Cited by 2 · see citing works
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Van, K.-T., Nabeebaccus, F., Lamari, F., Boluda, S., Fenaille, F., Villain, N., & Bécher, F. (2025) · Analytical Biochemistry · doi:10.1016/j.ab.2025.115942 · Cited by 2 · see citing works
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Drummond, E., Werry, E. L., Kavanagh, T., Genoud, S., Cho, A., Chen, S., Du, J., Hibbs, D. E., & Kassiou, M. (2026) · Molecular Neurodegeneration Advances · doi:10.1186/s44477-026-00035-y · Cited by 2 · see citing works
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Molzahn, C. M., Nierves, L. A., Lange, P. F., & Mayor, T. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2124-0_3 · Cited by 2 · see citing works
A Novel Spectral Barcoding and Classification Approach for Complex Biological Samples using Multi-excitation Raman Spectroscopy (MX-Raman)Preprint
Devitt, G., Hanrahan, N., Moreno, M. R., Mudher, A. K., & Mahajan, S. (2025) · ChemRxiv · doi:10.26434/chemrxiv-2024-x0lhh-v2 · Cited by 1 · see citing works
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Adeola, H. A., & Robinson, R. A. S. (2025) · ACS Bio & Med Chem Au · doi:10.1021/acsbiomedchemau.5c00074 · Cited by 1 · see citing works
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Chu, M., Wang, J., Yarbro, J. M., Chen, P.-C., Shrestha, H. K., Sun, H., Niu, M., Wang, Z., Harvey, S., Wu, Z., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.02.703320 · Cited by 1 · see citing works
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Evans, P. R., Gerber, K. J., Dammer, E. B., Duong, D. M., Goswami, D., Lustberg, D. J., Zou, J., Yang, J. J., Dudek, S. M., Griffin, P. R., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/247270
Self-citation
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Gomes, L. C. (2020) · doi:10.53846/goediss-7812
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Kalia, V. (2021) · doi:10.7916/d8-fj0m-bn64
Additional file 1 of Proteomic landscape of Alzheimer’s Disease: novel insights into pathogenesis and biomarker discovery
Bai, B., Vanderwall, D., Li, Y., Wang, X., Poudel, S., Wang, H., Dey, K. K., Chen, P., Yang, K., & Peng, J. (2021) · Figshare · doi:10.6084/m9.figshare.15162179
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Bluemke, A., Hagemeier, B., Ripkens, K., Schulze, N., Strzala, M., Koci, M., Kaschani, F., Kaiser, M., Erkelenz, M., Schluecker, S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.26.605305
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Additional file 1 of Pathological tau drives ectopic nuclear speckle scaffold protein SRRM2 accumulation in neuron cytoplasm in Alzheimer’s disease
McMillan, P. J., Strovas, T. J., Baum, M., Mitchell, B. K., Eck, R. J., Hendricks, N. E., Wheeler, J. M., Latimer, C. S., Keene, C. D., & Kraemer, B. C. (2021) · Figshare · doi:10.6084/m9.figshare.14880602
Additional file 1 of A proteomic network approach resolves stage-specific molecular phenotypes in chronic traumatic encephalopathy
Gutierrez-Quiceno, L., Dammer, E. B., Johnson, A. G., Webster, J. A., Shah, R., Duong, D., Yin, L., Seyfried, N. T., Alvarez, V. E., Stein, T. D., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14850628
Self-citation
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Lumpkin, C. J., Patel, H., Potts, G. K., Chaurasia, S., Gibilisco, L., Srivastava, G. P., Lee, J. Y., Brown, N. J., Amarante, P., Williams, J. D., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25885128
Additional file 1 of Broad proteomics analysis of seeding-induced aggregation of α-synuclein in M83 neurons reveals remodeling of proteostasis mechanisms that might contribute to Parkinson’s disease pathogenesis
Lumpkin, C. J., Patel, H., Potts, G. K., Chaurasia, S., Gibilisco, L., Srivastava, G. P., Lee, J. Y., Brown, N. J., Amarante, P., Williams, J. D., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25884924
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Pires, G. (2021) · theses.fr (ABES) · doi:10.70675/45826fd6zd2c8z4b3dz91e0za5080544cb17
Characterization and quantification of proteins involved in neurodegenerative diseases by mass spectrometry
Van, K. T. (2025) · doi:10.70675/32a1a6cez5dd3z42c0za2eaz2e57807081a6
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Tao, Y., Francis, A. E., Liu, W., Watkins, C., Bennett, D. A., Selkoe, D. J., Flynn, R. A., & Stern, A. M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.02.729610
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Elmkvist, S. B., Thygesen, C., Jensen, P., Pihl, M., Freude, K., Finsen, B. R., & Larsen, M. R. (2026) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5c01160
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Peng, B., Zou, S., Shi, Y., Zhu, X., Liu, M., Li, H., & Zhang, Y. (2026) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2026.153818
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Kallweit, L. M. (2026) · doi:10.56902/etdcrp.2026.63

Quantitative proteomics of tau and Aβ in detergent fractions from Alzheimer's disease brains
Mukherjee, S., Dubois, C., Perez, K. A., Varghese, S., Birchall, I. E., Leckey, M., Davydova, N., McLean, C., Nisbet, R. M., Roberts, B. R., et al. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15713 · Cited by 21 · see citing works
Distinctive temporal profiles of detergent-soluble and -insoluble tau and Aβ species in human Alzheimer’s disease
Koss, D. J., Dubini, M., Buchanan, H. M., Hull, C. E., & Platt, B. (2018) · Brain Research · doi:10.1016/j.brainres.2018.08.014 · Cited by 22 · see citing works
Proteomics Analysis Identifying New Markers Related to Alzheimer’s Disease Pathology In Vivo
Binette, A. P., Salvadó, G., Spotorno, N., Vogel, J. W., Kumar, A., Strandberg, O. T., Janelidze, S., & Hansson, O. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.074976
Quantitative proteomics of detergent insoluble tangles derived from Alzheimer’s disease brains
Mukherjee, S., Dubois, C., Perez, K. A., Nisbet, R. M., Li, Q., Varghese, S., Lago, L., Klatt, S., Birchall, I. E., Jin, L., et al. (2021) · Alzheimer s & Dementia · doi:10.1002/alz.055040 · Cited by 1 · see citing works
Alzheimer disease pathology and the cerebrospinal fluid proteome
Dayon, L., Núñez Galindo, A., Wojcik, J., Cominetti, O., Corthésy, J., Oikonomidi, A., Henry, H., Kussmann, M., Migliavacca, E., Severin, I., et al. (2018) · Alzheimer's Research & Therapy · doi:10.1186/s13195-018-0397-4 · Cited by 101 · see citing works

Authors: Hales, C. M., Dammer, E. B., Deng, Q., Duong, D. M., Gearing, M., Troncoso, J. C., Thambisetty, M., Lah, J. J., Shulman, J. M., Levey, A. I., & Seyfried, N. T.
Affiliations: Emory University (US)
Johns Hopkins University (US)
National Institutes of Health (US)
Baylor College of Medicine (US)
Corresponding author: Seyfried, Nicholas T.
ORCID: Hales, Chadwick M.
Dammer, Eric B.
Deng, Qiudong
Duong, Duc M.
Gearing, Marla
Troncoso, Juan C.
Thambisetty, Madhav
Lah, James J.
Shulman, Joshua M.
Levey, Allan I.
Seyfried, Nicholas T.
Venue: PROTEOMICS
Publisher: Wiley
Published: 2016-12
Volume: 16
Issue: 23
Pages: 3042-3053
ISSN: 1615-9853 (ISSN-L)
1615-9861
DOI: 10.1002/pmic.201600057
PMC: PMC5462625
OpenAlex: W2529144260
Cited by: 99
References: 66
Citations by year: 2026: 10 · 2025: 13 · 2024: 11 · 2023: 12 · 2022: 9 · 2021: 17 · 2020: 8 · 2019: 6 · 2018: 9 · 2017: 4
FWCI: 5.09
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 5 d)
Locations: PROTEOMICS (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Alzheimer's Disease Research Center, Emory University (P50AG025688)
National Institute of Neurological Disorders and Stroke (K08NS087121)
Alzheimer's Association
Alzheimer’s Research UK
BrightFocus Foundation (A2015332S)
National Institute on Aging (P50AG025688, U01AG046161‐02)
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, amyloid-beta, tau protein, prefrontal cortex, mild cognitive impairment, neurofibrillary tangles, amyloid plaques, U1A, SMD, U1-70K, disease progression, asymptomatic Alzheimer's disease
MeSH terms: Aged, Aged, 80 and over, Alzheimer Disease, Detergents, Female, Humans, Male, Proteins, Case-Control Studies, Amyloid beta-Peptides, tau Proteins, Ribonucleoprotein, U1 Small Nuclear, Proteome, Proteomics, Tandem Mass Spectrometry, Cognitive Dysfunction

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Changes in the detergent‐insoluble brain proteome linked to amyloid and tau in Alzheimer's Disease progression

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