An integrated multi-omics approach identifies epigenetic alterations associated with Alzheimer’s disease
Open accessAbstract
Protein aggregation is the hallmark of neurodegeneration, but the molecular mechanisms underlying late-onset Alzheimer's disease (AD) are unclear. Here we integrated transcriptomic, proteomic and epigenomic analyses of postmortem human brains to identify molecular pathways involved in AD. RNA sequencing analysis revealed upregulation of transcription- and chromatin-related genes, including the histone acetyltransferases for H3K27ac and H3K9ac. An unbiased proteomic screening singled out H3K27ac and H3K9ac as the main enrichments specific to AD. In turn, epigenomic profiling revealed gains in the histone H3 modifications H3K27ac and H3K9ac linked to transcription, chromatin and disease pathways in AD. Increasing genome-wide H3K27ac and H3K9ac in a fly model of AD exacerbated amyloid-β42-driven neurodegeneration. Together, these findings suggest that AD involves a reconfiguration of the epigenome, wherein H3K27ac and H3K9ac affect disease pathways by dysregulating transcription- and chromatin-gene feedback loops. The identification of this process highlights potential epigenetic strategies for early-stage disease treatment.
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Combined analyses of ChIP-seq and RNA-seq data have linked histone acetylation marks, including H3K27ac and H3K9ac, to transcriptional dysregulation affecting synaptic and chromatin-related genes.
“Combined analyses of ChIP-seq and RNA-seq data have linked histone acetylation marks, including H3K27ac and H3K9ac, to transcriptional dysregulation affecting synaptic and chromatin-related genes104.”
From Artificial intelligence-driven multi-omics approaches in Alzheimer's disease: Progress, challenges, and future directions (2025) · cites this paper as [104]
The 832 LOAD spheroid DEGs overlap with bulk RNA-seq datasets from various brain regions in individuals with AD, GO terms related to apoptosis/neurodegeneration, and AD risk genes from Alzgene database, with overlaps ranging from 8 to 135 genes.
“We further compared 832 DEGs with bulk RNA-seq datasets from various brain regions in individuals with AD (80–84), gene members in GO terms related to apoptosis/neurodegeneration, and AD risk genes from Alzgene database, revealing distinct sets of DEGs with overlaps ranging from 8 to 135 genes (Table S7, page 2, 3 and 4).”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [83]
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Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
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
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
BEDTools: a flexible suite of utilities for comparing genomic features
Quinlan, A. R., & Hall, I. M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq033 · Cited by 27,437 · see citing works
An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072 · see citing works
Self-citationSzklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gky1131 · Cited by 17,749 · see citing works
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382 · see citing works
The Human Genome Browser at UCSC
Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., & Haussler, A. D. (2002) · Genome Research · doi:10.1101/gr.229102 · Cited by 10,400 · see citing works
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
GREAT improves functional interpretation of cis-regulatory regions
McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M., & Bejerano, G. (2010) · Nature Biotechnology · doi:10.1038/nbt.1630 · Cited by 4,502 · see citing works
Meta-Analysis of 74,046 Individuals Identifies 11 New Susceptibility Loci for Alzheimer’s Disease
(EADI), E. A. D. I., Lambert, J.-C., (GERAD), G. A. E. R. I. A. D., Alzheimer's Disease Genetic Consortium (ADGC), (CHARGE), C. F. H. A. A. R. I. G. E., Ibrahim-Verbaas, C. A., Harold, D., Naj, A. C., Sims, R., Bellenguez, C., et al. (2013) · Nature Genetics · doi:10.1038/ng.2802 · Cited by 4,336 · see citing works
Histone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302 · see citing works
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398 · see citing works
Braak, H., Alafuzoff, I., Arzberger, T., Kretzschmar, H., & Del Tredici, K. (2006) · Acta Neuropathologica · doi:10.1007/s00401-006-0127-z · Cited by 3,172 · see citing works
Alzheimer Disease Genetics Consortium (ADGC), Kunkle, B. W., The European Alzheimer’s Disease Initiative (EADI), Cohorts for Heart and Aging Research in Genomic Epidemiology Consortium (CHARGE), Genetic and Environmental Risk in AD/Defining Genetic, P. A. E. R. F. A. D. C. (., Grenier-Boley, B., Sims, R., Bis, J. C., Damotte, V., Naj, A. C., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0358-2 · Cited by 2,946 · see citing works
Self-citationChen, X., Han, X., Yuan, P., Fang, F., Huss, M., Vega, V. B., Wong, E., Orlov, Y. L., Zhang, W., Jiang, J., et al. (2008) · Cell · doi:10.1016/j.cell.2008.04.043 · Cited by 2,474 · see citing works
Combinatorial patterns of histone acetylations and methylations in the human genome
Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Peng, W., Zhang, M. Q., et al. (2008) · Nature Genetics · doi:10.1038/ng.154 · Cited by 2,331 · see citing works
Normalization of RNA-seq data using factor analysis of control genes or samples
Risso, D., Ngai, J., Speed, T. P., & Dudoit, S. (2014) · Nature Biotechnology · doi:10.1038/nbt.2931 · Cited by 2,169 · see citing works
Spatio-temporal transcriptome of the human brain
Kang, H. J., Kawasawa, Y. I., Cheng, F., Zhu, Y., Xu, X., Li, M., Sousa, A. M. M., Pletikos, M., Meyer, K. A., Sedmak, G., et al. (2011) · Nature · doi:10.1038/nature10523 · Cited by 2,084 · see citing works
The diverse functions of histone lysine methylation
Martin, C., & Zhang, Y. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1761 · Cited by 2,066 · see citing works
Moreno-Jiménez, E. P., Flor-García, M., Terreros-Roncal, J., Rábano, A., Cafini, F., Pallas-Bazarra, N., Ávila, J., & Llorens-Martín, M. (2019) · Nature Medicine · doi:10.1038/s41591-019-0375-9 · Cited by 1,577 · see citing works
CTCF: Master Weaver of the Genome
Phillips‐Cremins, J. E., & Corces, V. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.001 · Cited by 1,540 · see citing works
Modification of Enhancer Chromatin: What, How, and Why?
Calo, E., & Wysocka, J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.038 · Cited by 1,457 · see citing works
Wyss-Coray (2006) · doi:10.1038/nm1484 · Cited by 1,284 · see citing works
Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP
Petrif, F., Giles, R. H., Dauwerse, H. G., Saris, J. J., Hennekam, R. C. M., Masuno, M., Tommerup, N., van Ommen, G.-J. B., Goodman, R. H., Peters, D. J. M., et al. (1995) · Nature · doi:10.1038/376348a0 · Cited by 1,217 · see citing works
Sibling rivalry in the E2F family
Trimarchi, J. M., & Lees, J. A. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm714 · Cited by 1,158 · see citing works
Acetylation: a regulatory modification to rival phosphorylation?
Kouzarides, T. (2000) · The EMBO Journal · doi:10.1093/emboj/19.6.1176 · Cited by 1,155 · see citing works
Alzheimer's disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci
De Jager, P. L., Srivastava, G., Lunnon, K., Burgess, J., Schalkwyk, L. C., Yu, L., Eaton, M. L., Keenan, B. T., Ernst, J., McCabe, C., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3786 · Cited by 956 · see citing works
Epigenetic mechanisms of longevity and aging
Sen, P., Shah, P. P., Nativio, R., & Berger, S. L. (2016) · Cell · doi:10.1016/j.cell.2016.07.050 · Cited by 956 · see citing works
Self-citationAcetylation of Tau Inhibits Its Degradation and Contributes to Tauopathy
Min, S.-W., Cho, S.-H., Zhou, Y., Schroeder, S., Haroutunian, V., Seeley, W. W., Huang, E. J., Shen, Y., Masliah, E., Mukherjee, C., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.044 · Cited by 949 · see citing works
Understanding the language of Lys36 methylation at histone H3
Wagner, E. J., & Carpenter, P. B. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3274 · Cited by 933 · see citing works
Jin, Q., Yu, L., Wang, L., Zhang, Z., Kasper, L. H., Lee, J., Wang, C., Brindle, P. K., Dent, S. Y. R., & Ge, K. (2011) · The EMBO Journal · doi:10.1038/emboj.2010.318 · Cited by 877 · see citing works
Self-citationThe genetic landscape of Alzheimer disease: clinical implications and perspectives
Van Cauwenberghe, C., Van Broeckhoven, C., & Sleegers, K. (2016) · Genetics in Medicine · doi:10.1038/gim.2015.117 · Cited by 863 · see citing works
An epigenetic blockade of cognitive functions in the neurodegenerating brain
Gräff, J., Rei, D., Guan, J.-S., Wang, W.-Y., Seo, J., Hennig, K. M., Nieland, T. J. F., Fass, D. M., Kao, P. F., Kahn, M., et al. (2012) · Nature · doi:10.1038/nature10849 · Cited by 853 · see citing works
Mitochondria and Mitochondrial Cascades in Alzheimer’s disease
Swerdlow, R. H. (2018) · Journal of Alzheimer’s Disease · doi:10.3233/jad-170585 · Cited by 850 · see citing works
Daxx, a Novel Fas-Binding Protein That Activates JNK and Apoptosis
Yang, X., Khosravi‐Far, R., Chang, H. Y., & Baltimore, D. (1997) · Cell · doi:10.1016/s0092-8674(00)80294-9 · Cited by 830 · see citing works
CBP Histone Acetyltransferase Activity Is a Critical Component of Memory Consolidation
Korzus, E., Rosenfeld, M. G., & Mayford, M. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.002 · Cited by 823 · see citing works
REST and stress resistance in ageing and Alzheimer’s disease
Lu, T., Aron, L., Zullo, J., Pan, Y., Kim, H., Chen, Y., Yang, T.-H., Kim, H., Drake, D., Liu, X., et al. (2014) · Nature · doi:10.1038/nature13163 · Cited by 760 · see citing works
Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis.
Qin, X. Q., Livingston, D. M., Kaelin, W. G., & Adams, P. D. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.23.10918 · Cited by 753 · see citing works
Therapeutics of Alzheimer's disease: Past, present and future
Anand, R., Gill, K. D., & Mahdi, A. A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.07.004 · Cited by 748 · see citing works
JMJD6 Is a Histone Arginine Demethylase
Chang, B., Chen, Y., Zhao, Y., & Bruick, R. K. (2007) · Science · doi:10.1126/science.1145801 · Cited by 746 · see citing works
Histone acetylation: molecular mnemonics on the chromatin
Gräff, J., & Tsai, L.-H. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3427 · Cited by 680 · see citing works
Epigenetic regulation of ageing: linking environmental inputs to genomic stability
Benayoun, B. A., Pollina, E. A., & Brunet, A. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm4048 · Cited by 610 · see citing works
Mehta, D. G., Jackson, R., Paul, G., Shi, J., & Sabbagh, M. N. (2017) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2017.1323868 · Cited by 603 · see citing works
Conserved epigenomic signals in mice and humans reveal immune basis of Alzheimer's disease
Gjoneska, E., Pfenning, A. R., Mathys, H., Quon, G., Kundaje, A., Tsai, L.-H., & Kellis, M. (2015) · Nature · doi:10.1038/nature14252 · Cited by 576 · see citing works
CBP-mediated acetylation of histone H3 lysine 27 antagonizesDrosophilaPolycomb silencing
Tie, F., Banerjee, R., Stratton, C. A., Prasad-Sinha, J., Stepanik, V. A., Zlobin, A., Dı́az, M. O., Scacheri, P. C., & Harte, P. J. (2009) · Development · doi:10.1242/dev.037127 · Cited by 575 · see citing works
Methylomic profiling implicates cortical deregulation of ANK1 in Alzheimer's disease
Lunnon, K., Smith, R., Hannon, E., De Jager, P. L., Srivastava, G., Volta, M., Troakes, C., Al-Sarraj, S., Burrage, J., Macdonald, R., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3782 · Cited by 574 · see citing works
Deregulated Expression of E2F-1 Induces S-Phase Entry and Leads to Apoptosis
Shan, B., & Lee, W. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.8166 · Cited by 529 · see citing works
Tau promotes neurodegeneration through global chromatin relaxation
Frost, B., Hemberg, M., Lewis, J., & Feany, M. B. (2014) · Nature Neuroscience · doi:10.1038/nn.3639 · Cited by 519 · see citing works
Time-Resolved Analysis Reveals Rapid Dynamics and Broad Scope of the CBP/p300 Acetylome
Weinert, B. T., Narita, T., Satpathy, S., Srinivasan, B., Hansen, B. K., Scholz, C. W., Hamilton, W. B., Zucconi, B. E., Wang, W., Liu, W. R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.033 · Cited by 514 · see citing works
Wang, M., Beckmann, N. D., Roussos, P., Wang, E., Zhou, X., Wang, Q., Ming, C., Neff, R., Ma, W., Fullard, J. F., et al. (2018) · Scientific Data · doi:10.1038/sdata.2018.185 · Cited by 502 · see citing works
Expression quantitative trait loci: present and future
Nica, A. C., & Dermitzakis, E. T. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0362 · Cited by 498 · see citing works
Roelfsema, J. H., White, S. J., Ariyürek, Y., Bartholdi, D., Niedrist, D., Papadia, F., Bacino, C. A., den Dunnen, J. T., van Ommen, G. B., Breuning, M. H., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/429130 · Cited by 481 · see citing works
Alteration of the microRNA network during the progression of Alzheimer's disease
Lau, P., Bossers, K., Janky, R., Salta, E., Frigerio, C. S., Barbash, S., Rothman, R., Sierksma, A. S. R., Thathiah, A., Greenberg, D., et al. (2013) · EMBO Molecular Medicine · doi:10.1002/emmm.201201974 · Cited by 474 · see citing works
5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells
Stroud, H., Feng, S., Kinney, S. R. M., Pradhan, S., & Jacobsen, S. E. (2011) · Genome biology · doi:10.1186/gb-2011-12-6-r54 · Cited by 466 · see citing works
Allen, M., Carrasquillo, M. M., Funk, C., Heavner, B. D., Zou, F., Younkin, C. S., Burgess, J. D., Chai, H.-S., Crook, J., Eddy, J. A., et al. (2016) · Scientific Data · doi:10.1038/sdata.2016.89 · Cited by 439 · see citing works
Perez Ortiz, J. M., & Swerdlow, R. H. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14585 · Cited by 426 · see citing works
Meikrantz, W., & Schlegel, R. (1995) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240580205 · Cited by 421 · see citing works
Sox2, a key factor in the regulation of pluripotency and neural differentiation
Zhang, S. (2014) · World Journal of Stem Cells · doi:10.4252/wjsc.v6.i3.305 · Cited by 399 · see citing works
Epigenetic Regulation in Neurodegenerative Diseases
Berson, A., Nativio, R., Berger, S. L., & Bonini, N. M. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.05.005 · Cited by 386 · see citing works
Self-citationDysregulation of the epigenetic landscape of normal aging in Alzheimer’s disease
Nativio, R., Donahue, G., Berson, A., Lan, Y., Amlie-Wolf, A., Tuzer, F., Toledo, J. B., Gosai, S. J., Gregory, B. D., Torres, C., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0101-9 · Cited by 363 · see citing works
Self-citationSeparation of basal histone synthesis from S-phase histone synthesis in dividing cells
Wu, R. S., & Bonner, W. M. (1981) · Cell · doi:10.1016/0092-8674(81)90415-3 · Cited by 360 · see citing works
The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier–Gorlin syndrome
Kuo, A. J., Song, J., Cheung, P., Ishibe-Murakami, S., Yamazoe, S., Chen, J., Patel, D. J., & Gozani, O. (2012) · Nature · doi:10.1038/nature10956 · Cited by 349 · see citing works
MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer’s disease
Banzhaf‐Strathmann, J., Benito, E., May, S., Arzberger, T., Tahirovic, S., Kretzschmar, H., Fischer, A., & Edbauer, D. (2014) · The EMBO Journal · doi:10.15252/embj.201387576 · Cited by 326 · see citing works
Cohesin Is Required for Higher-Order Chromatin Conformation at the Imprinted IGF2-H19 Locus
Nativio, R., Wendt, K. S., Ito, Y., Huddleston, J. E., Uribe‐Lewis, S., Woodfine, K., Krueger, C., Reik, W., Peters, J., & Murrell, A. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000739 · Cited by 325 · see citing works
Self-citationLessons Learned from Alzheimer Disease: Clinical Trials with Negative Outcomes
Cummings, J. (2018) · Clinical and Translational Science · doi:10.1111/cts.12491 · Cited by 298 · see citing works
The ER stress factor XBP1s prevents amyloid-β neurotoxicity
Casas-Tinto, S., Zhang, Y., Sanchez-Garcia, J., Gomez-Velazquez, M., Rincon-Limas, D. E., & Fernandez-Funez, P. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr100 · Cited by 275 · see citing works
Tropberger, P., Pott, S., Keller, C., Kamieniarz-Gdula, K., Caron, M. J., Richter, F. M., Li, G., Mittler, G., Liu, E. T., Bühler, M., et al. (2013) · Cell · doi:10.1016/j.cell.2013.01.032 · Cited by 272 · see citing works
Klein, H., Aubin, C., Gjoneska, E., Sullivan, S. E., Kaskow, B. J., Tang, A. Y., Smith, R. V., Xu, J., Pfenning, A. R., Bernstein, B., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0291-1 · Cited by 267 · see citing works
Multiple faces of the SAGA complex
Koutelou, E., Hirsch, C. L., & Dent, S. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2010.03.005 · Cited by 258 · see citing works
Caccamo, A., Maldonado, M. A., Bokov, A. F., Majumder, S., & Oddo, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012851108 · Cited by 249 · see citing works
Histone H3 globular domain acetylation identifies a new class of enhancers
Pradeepa, M. M., Grimes, G. R., Kumar, Y., Olley, G., Taylor, G. C. A., Schneider, R., & Bickmore, W. A. (2016) · Nature Genetics · doi:10.1038/ng.3550 · Cited by 240 · see citing works
INRICH: interval-based enrichment analysis for genome-wide association studies
Lee, P. H., O'Dushlaine, C., Thomas, B., & Purcell, S. M. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts191 · Cited by 238 · see citing works
Mirra, S. S. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00058-4 · Cited by 236 · see citing works
Toledo, J. B., Van Deerlin, V. M., Lee, E. B., Suh, E., Baek, Y., Robinson, J. L., Xie, S. X., McBride, J., Wood, E. M., Schuck, T., et al. (2014) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2013.06.003 · Cited by 234 · see citing works
Self-citationMarzi, S. J., Leung, S. K., Ribarska, T., Hannon, E., Smith, A. R., Pishva, E., Poschmann, J., Moore, K., Troakes, C., Al-Sarraj, S., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0253-7 · Cited by 232 · see citing works
Zhang, P., Yao, Q., Lu, L., Li, Y., Chen, P.-J., & Duan, C. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.02.011 · Cited by 232 · see citing works
Probing Nucleosome Function: A Highly Versatile Library of Synthetic Histone H3 and H4 Mutants
Dai, J., Hyland, E. M., Yuan, D., Huang, H., Bader, J. S., & Boeke, J. D. (2008) · Cell · doi:10.1016/j.cell.2008.07.019 · Cited by 229 · see citing works
Patterns of histone variant synthesis can distinguish go from G1 cells
Wu, R. S., Tsai, S., & Bonner, W. M. (1982) · Cell · doi:10.1016/0092-8674(82)90130-1 · Cited by 228 · see citing works
de Bruin, A., Maiti, B., Jakoi, L., Timmers, C., Buerki, R., & Leone, G. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m308105200 · Cited by 221 · see citing works
Brain Expression Genome-Wide Association Study (eGWAS) Identifies Human Disease-Associated Variants
Zou, F., Chai, H. S., Younkin, C. S., Allen, M., Crook, J. E., Pankratz, V. S., Carrasquillo, M. M., Rowley, C. N., Nair, A., Middha, S., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002707 · Cited by 216 · see citing works
Sidoli, S., Bhanu, N. V., Karch, K. R., Wang, X., & Garcia, B. A. (2016) · Journal of Visualized Experiments · doi:10.3791/54112 · Cited by 215 · see citing works
Self-citationBlalock, E. M., Buechel, H. M., Popovic, J., Geddes, J. W., & Landfield, P. W. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.06.007 · Cited by 211 · see citing works
Targeting HDACs: A Promising Therapy for Alzheimer's Disease
Xu, K., Dai, X., Huang, H., & Jiang, Z.-F. (2011) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2011/143269 · Cited by 206 · see citing works
Histone H3 lysine-to-methionine mutants as a paradigm to study chromatin signaling
Herz, H.-M., Morgan, M., Gao, X., Jackson, J., Rickels, R., Swanson, S. K., Florens, L., Washburn, M. P., Eissenberg, J. C., & Shilatifard, A. (2014) · Science · doi:10.1126/science.1255104 · Cited by 199 · see citing works
H3 Lysine 4 Is Acetylated at Active Gene Promoters and Is Regulated by H3 Lysine 4 Methylation
Guillemette, B., Drogaris, P., Lin, H.-H. S., Armstrong, H., Hiragami-Hamada, K., Imhof, A., Bonneil, É., Thibault, P., Verreault, A., & Festenstein, R. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001354 · Cited by 199 · see citing works
NFAT control of immune function: New Frontiers for an Abiding Trooper
Vaeth, M., & Feske, S. (2018) · F1000Research · doi:10.12688/f1000research.13426.1 · Cited by 191 · see citing works
EpiProfile 2.0: A Computational Platform for Processing Epi-Proteomics Mass Spectrometry Data
Yuan, Z., Sidoli, S., Marchione, D. M., Simithy, J., Janssen, K. A., Szurgot, M. R., & Garcia, B. A. (2018) · Journal of Proteome Research · doi:10.1021/acs.jproteome.8b00133 · Cited by 187 · see citing works
Self-citationATAC-king the complexity of SAGA during evolutionPreprint
Spedale, G., Timmers, H. T. M., & Pijnappel, W. W. M. P. (2012) · Genes & Development · doi:10.1101/gad.184705.111 · Cited by 180 · see citing works
A Highly Sensitive and Robust Method for Genome-wide 5hmC Profiling of Rare Cell Populations
Han, D., Lu, X., Shih, A. H., Nie, J., You, Q., Xu, M. M., Melnick, A. M., Levine, R. L., & He, C. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.06.028 · Cited by 167 · see citing works
Self-citationLee, C. S., Lee, C., Hu, T., Nguyen, J. M., Zhang, J., Martin, M. V., Vawter, M. P., Huang, E. J., & Chan, J. Y. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019209108 · Cited by 164 · see citing works
Nagy, Z., Esiri, M. M., & Smith, A. D. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00293-0 · Cited by 157 · see citing works
Wnt signaling in Alzheimer's disease: Up or down, that is the question
Boonen, R. A. C. M., van Tijn, P., & Živković, D. (2008) · Ageing Research Reviews · doi:10.1016/j.arr.2008.11.003 · Cited by 143 · see citing works
Satoh, J., Kawana, N., & Yamamoto, Y. (2013) · Gene Regulation and Systems Biology · doi:10.4137/grsb.s13204 · Cited by 141 · see citing works
Neurons in Vulnerable Regions of the Alzheimer’s Disease Brain Display Reduced ATM Signaling
Shen, X., Chen, J., Li, J., Kofler, J., & Herrup, K. (2016) · eNeuro · doi:10.1523/eneuro.0124-15.2016 · Cited by 118 · see citing works
Role of CBP and SATB-1 in Aging, Dietary Restriction, and Insulin-Like Signaling
Zhang, M., Poplawski, M. M., Yen, K., Cheng, H., Bloss, E. B., Zhu, X., Patel, H., & Mobbs, C. V. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000245 · Cited by 113 · see citing works
A chromodomain switch mediated by histone H3 Lys 4 acetylation regulates heterochromatin assemblyPreprint
Xhemalçe, B., & Kouzarides, T. (2010) · Genes & Development · doi:10.1101/gad.1881710 · Cited by 101 · see citing works
Wnt/β-Catenin Signaling in Alzheimer’s Disease
Ferrari, G., Avila, M., Medina, M., Perez-Palma, E., Bustos, B., & Alarcon, M. (2014) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527312666131223113900 · Cited by 95 · see citing works
From development to diseases: The role of 5hmC in brain
Sun, W., Zang, L., Shu, Q., & Li, X. (2014) · Genomics · doi:10.1016/j.ygeno.2014.08.021 · Cited by 90 · see citing works
CXXC finger protein 1 restricts the Setd1A histone H3K4 methyltransferase complex to euchromatin
Tate, C. M., Lee, J., & Skalnik, D. G. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07475.x · Cited by 73 · see citing works
Anderson, K. W., Chen, J., Wang, M., Mast, N., Pikuleva, I. A., & Turko, I. V. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126592 · Cited by 69 · see citing works
Cutler, T., Sarkar, A., Moran, M. T., Steffensmeier, A. M., Puli, O. R., Mancini, G., Tare, M., Gogia, N., & Singh, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137691 · Cited by 65 · see citing works
Sidoli, S., Simithy, J., Karch, K. R., Kulej, K., & Garcia, B. A. (2015) · Analytical Chemistry · doi:10.1021/acs.analchem.5b03009 · Cited by 61 · see citing works
Self-citationAP-1 Repressor Protein JDP-2: Inhibition of UV-Mediated Apoptosis through p53 Down-Regulation
Piu, F., Aronheim, A., Katz, S., & Karin, M. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.9.3012-3024.2001 · Cited by 61 · see citing works
Benhattar, J., & Jiricny, J. (1988) · Gene · doi:10.1016/0378-1119(88)90458-1 · Cited by 60 · see citing works
An E2F7-dependent transcriptional program modulates DNA damage repair and genomic stability
Mitxelena, J., Apraiz, A., Vallejo-Rodríguez, J., García‐Santisteban, I., Fullaondo, A., Álvarez‐Fernández, M., Malumbres, M., & Zubiaga, A. M. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky218 · Cited by 59 · see citing works
Histone H4 lysine 20 acetylation is associated with gene repression in human cells
Kaimori, J.-Y., Maehara, K., Hayashi‐Takanaka, Y., Harada, A., Fukuda, M., Yamamoto, S., Ichimaru, N., Umehara, T., Yokoyama, S., Matsuda, R., et al. (2016) · Scientific Reports · doi:10.1038/srep24318 · Cited by 56 · see citing works
Wu, Y., Hou, F., Wang, X., Kong, Q., Han, X., & Bai, B. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00114 · Cited by 52 · see citing works
Premature aging with impaired oxidative stress defense in mice lacking TR4
Lee, Y., Liu, S., Liu, N.-C., Wang, R.-S., Chen, L., Lin, W., Ting, H., Ho, H.-C., Li, G., Puzas, E. J., et al. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00701.2010 · Cited by 40 · see citing works
Liu, B.-Y., Shats, I., Angus, S. P., Gatza, M., & Nevins, J. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.467506 · Cited by 36 · see citing works
PLZF mutation alters mouse hematopoietic stem cell function and cell cycle progression
Vincent‐Fabert, C., Platet, N., Vandevelde, A., Poplineau, M., Koubi, M., Finetti, P., Tibéri, G., Imbert, A., Bertucci, F., & Duprez, E. (2016) · Blood · doi:10.1182/blood-2015-09-666974 · Cited by 34 · see citing works
Daxx Is a Transcriptional Repressor of CCAAT/Enhancer-binding Protein β
Wethkamp, N., & Klempnauer, K. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.041186 · Cited by 31 · see citing works
Histone complements of human tissues, carcinomas, and carcinoma-derived cell lines
Gabriellia, F., Aden, D. P., Carrele, S. C., von Bahrd, C., Raned, A., Angelettie, C. A., & Hancockf, R. (1984) · Molecular and Cellular Biochemistry · doi:10.1007/bf00226019 · Cited by 26 · see citing works
Chien, H., Wang, H., Su, Y.-N., Lai, K.-Y., Lu, L.-C., Chen, P., Tsai, S., Wu, C., Hsieh, W., & Shen, C.-K. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047481 · Cited by 14 · see citing works
Flagged first, then by citations
2 of the 116 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- [25]Nagy Z, Esiri MM & Smith AD The cell division cycle and the pathophysiology of Alzheimer’s disease. Neuroscience 87, 731– 9 (1998). 9759963
- [66]De Ferrari GV Wnt/beta-catenin signaling in Alzheimer’s disease. CNS Neurol Disord Drug Targets 13, 745– 54 (2014). 24365184
Cited by
Sorted by citations
Modulation of cellular processes by histone and non-histone protein acetylation
Shvedunova, M., & Akhtar, A. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00441-y · Cited by 975 · see citing works
Biological aging processes underlying cognitive decline and neurodegenerative disease
Gonzales, M. M., Garbarino, V. R., Pollet, E., Palavicini, J. P., Kellogg, D. L., Kraig, E., & Orr, M. E. (2022) · Journal of Clinical Investigation · doi:10.1172/jci158453 · Cited by 394 · see citing works
The role of histone modifications: from neurodevelopment to neurodiseases
Park, J., Lee, K., Kim, K., & Yi, S.-J. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01078-9 · Cited by 321 · see citing works
The human connectome in Alzheimer disease — relationship to biomarkers and genetics
Yu, M., Sporns, O., & Saykin, A. J. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00529-1 · Cited by 265 · see citing works
Deep learning-based approaches for multi-omics data integration and analysis
Ballard, J. L., Wang, Z., Li, W., Shen, L., & Long, Q. (2024) · BioData Mining · doi:10.1186/s13040-024-00391-z · Cited by 287 · see citing works
Gene–environment interactions in Alzheimer disease: the emerging role of epigenetics
Migliore, L., & Coppedè, F. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00714-w · Cited by 217 · see citing works
Dementia in Africa: current evidence, knowledge gaps, and future directions
Akinyemi, R. O., Yaria, J., Ojagbemi, A., Guerchet, M., Okubadejo, N., Njamnshi, A. K., Sarfo, F. S., Akpalu, A., Ogbole, G., Ayantayo, T., et al. (2022) · Alzheimer's & Dementia · doi:10.1002/alz.12432 · Cited by 184 · see citing works
Acetyl-CoA Metabolism and Histone Acetylation in the Regulation of Aging and Lifespan
Bradshaw, P. C. (2021) · Antioxidants · doi:10.3390/antiox10040572 · Cited by 185 · see citing works
A benchmark study of deep learning-based multi-omics data fusion methods for cancer
Leng, D., Zheng, L., Wen, Y., Zhang, Y., Wu, L., Wang, J., Wang, M., Zhang, Z., He, S., & Bo, X. (2022) · Genome biology · doi:10.1186/s13059-022-02739-2 · Cited by 163 · see citing works
Insights from multi-omics integration in complex disease primary tissues
Kreitmaier, P., Katsoula, G., & Zeggini, E. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.08.005 · Cited by 160 · see citing works
Multi-Omics Integration for the Design of Novel Therapies and the Identification of Novel Biomarkers
Ivanisevic, T., & Sewduth, R. (2023) · Proteomes · doi:10.3390/proteomes11040034 · Cited by 118 · see citing works
The interaction between ageing and Alzheimer's disease: insights from the hallmarks of ageing
Liu, Y., Tan, Y., Zhang, Z., Yi, M., Zhu, L., & Peng, W. (2024) · Translational Neurodegeneration · doi:10.1186/s40035-024-00397-x · Cited by 144 · see citing works
Stress, epigenetics, and aging: Unraveling the intricate crosstalk
Wu, Z., Qu, J. T., Zhang, W., & Liu, G. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.10.006 · Cited by 142 · see citing works
Histone Modifications in Alzheimer’s Disease
Santana, D. A., Smith, M. D. A. C., & Chen, E. (2023) · Genes · doi:10.3390/genes14020347 · Cited by 109 · see citing works
Role of Histone Post-Translational Modifications in Inflammatory Diseases
Lin, Y., Qiu, T., Wei, G., Que, Y., Wang, W., Kong, Y., Xie, T., & Chen, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.852272 · Cited by 95 · see citing works
Multiomics technologies: role in disease biomarker discoveries and therapeutics
Dar, M. A., Arafah, A. M., Bhat, K. A., Khan, A., Khan, M. S., Ali, A., Ahmad, S. M., Rashid, S. M., & Rehman, M. U. (2022) · Briefings in Functional Genomics · doi:10.1093/bfgp/elac017 · Cited by 96 · see citing works
Linking environmental risk factors with epigenetic mechanisms in Parkinson’s disease
Tsalenchuk, M., Gentleman, S., & Marzi, S. J. (2023) · npj Parkinson s Disease · doi:10.1038/s41531-023-00568-z · Cited by 90 · see citing works
Ren, F., Wei, J., Chen, Q., Hu, M., Yu, L., Mi, J., Zhou, X., Qin, D., Wu, J., & Wu, A. (2025) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2025.07.030 · Cited by 97 · see citing works
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Liu, J., Fan, Z., Zhao, W., & Zhou, X. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.655536 · Cited by 84 · see citing works
Nuclei isolation of multiple brain cell types for omics interrogation
Nott, A., Schlachetzki, J. C. M., Fixsen, B. R., & Glass, C. K. (2021) · Nature Protocols · doi:10.1038/s41596-020-00472-3 · Cited by 79 · see citing works
Li, T. Y., Sleiman, M. B., Li, H., Gao, A. W., Mottis, A., Bachmann, A. M., Alam, G. E., Li, X., Goeminne, L. J. E., Schoonjans, K., et al. (2021) · Nature Aging · doi:10.1038/s43587-020-00025-z · Cited by 78 · see citing works
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Reyes, C. D. G., Alejo‐Jacuinde, G., Sanchez, B. P., Chávez‐Reyes, J., Onigbinde, S. B., Mogut, D., Hernández‐Jasso, I., Calderón-Vallejo, D., Quintanar, J. L., & Mechref, Y. S. (2024) · Current Issues in Molecular Biology · doi:10.3390/cimb46060345 · Cited by 85 · see citing works
Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming
Sun, Z., Kwon, J.-S., Ren, Y., Chen, S., Walker, C. K., Lu, X., Cates, K., Karahan, H., Sviben, S., Fitzpatrick, J. A. J., et al. (2024) · Science · doi:10.1126/science.adl2992 · Cited by 77 · see citing works
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Wu, Z., Zhang, W., Qu, J. T., & Liu, G. (2024) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2023.12.002 · Cited by 74 · see citing works
Williams, J. B., Cao, Q., & Yan, Z. (2021) · Brain Communications · doi:10.1093/braincomms/fcab123 · Cited by 72 · see citing works
The exposome of healthy and accelerated aging across 40 countries
Hernandez, H., Santamaria-Garcia, H., Moguilner, S., Farina, F. R., Legaz, A., Prado, P., Cuadros, J., Gonzalez, L., Gonzalez-Gomez, R., Migeot, J., et al. (2025) · Nature Medicine · doi:10.1038/s41591-025-03808-2 · Cited by 71 · see citing works
Applied machine learning in Alzheimer's disease research: omics, imaging, and clinical data
Li, Z., Jiang, X., Wang, Y., & Kim, Y. (2021) · Emerging Topics in Life Sciences · doi:10.1042/etls20210249 · Cited by 67 · see citing works
A hyper-quiescent chromatin state formed during aging is reversed by regeneration
Yang, N., Occean, J. R., Melters, D. P., Shi, C., Wang, L., Stransky, S., Doyle, M. E., Cui, C., Delannoy, M. R., Fan, J., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.04.005 · Cited by 71 · see citing works
Self-citationBrain high-throughput multi-omics data reveal molecular heterogeneity in Alzheimer’s disease
Eteleeb, A. M., Novotny, B. C., Tarraga, C. S., Sohn, C., Dhungel, E., Brase, L., Nallapu, A., Buss, J., Farias, F., Bergmann, K., et al. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002607 · Cited by 64 · see citing works
Luo, Y., Yang, L.-L., & Yao, X. (2024) · Molecular Neurodegeneration · doi:10.1186/s13024-024-00720-0 · Cited by 70 · see citing works
Liu, Z., Zhang, S., James, B. T., Galani, K., Mangan, R. J., Fass, S. B., Liang, C., Wagle, M. M., Boix, C. A., Tanigawa, Y., et al. (2025) · Cell · doi:10.1016/j.cell.2025.06.031 · Cited by 65 · see citing works
Lu, B., Qiu, R., Wei, J., Wang, L., Zhang, Q., Li, M., Zhan, X., Chen, J., Hsieh, I.-Y., Yang, C., et al. (2024) · Nature Cancer · doi:10.1038/s43018-024-00816-y · Cited by 62 · see citing works
Self-citationRole of histone modifications in neurogenesis and neurodegenerative disease development
Zhao, A., Xu, W., Han, R., Wei, J., Qi, Y., Wang, M., Li, H., Li, M., & Chi, G. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102324 · Cited by 59 · see citing works
Cummings, J. L., & Kinney, J. W. (2022) · Medicina · doi:10.3390/medicina58070952 · Cited by 58 · see citing works
Epigenetic Regulation of Neuroinflammation in Alzheimer’s Disease
Ma, Y., Wang, W., Liu, S., Qiao, X., Xing, Y., Zhou, Q., & Zhang, Z. (2023) · Cells · doi:10.3390/cells13010079 · Cited by 57 · see citing works
Prasanth, M. I., Sivamaruthi, B. S., Cheong, C. S. Y., Verma, K., Tencomnao, T., Brimson, J. M., & Prasansuklab, A. (2024) · Antioxidants · doi:10.3390/antiox13050606 · Cited by 57 · see citing works
Cognata, V. L., Morello, G., & Cavallaro, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094820 · Cited by 56 · see citing works
Trace elements and Alzheimer dementia in population-based studies: A bibliometric and meta-analysis
Li, K., Li, A., Mei, Y., Zhao, J., Zhou, Q., Li, Y., Yang, M., & Xu, Q. (2022) · Environmental Pollution · doi:10.1016/j.envpol.2022.120782 · Cited by 54 · see citing works
Omics-based biomarkers discovery for Alzheimer's disease
Aerqin, Q., Wang, Z.-T., Wu, K., He, X., Dong, Q., & Yu, J. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04614-6 · Cited by 55 · see citing works
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Balusu, S., Praschberger, R., Lauwers, E., Strooper, B. D., & Verstreken, P. (2023) · Neuron · doi:10.1016/j.neuron.2023.01.016 · Cited by 51 · see citing works
Promoting Alzheimer’s disease research and therapy with stem cell technology
Cao, Z., Kong, F., Ding, J., Chen, C., He, F., & Deng, W. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03737-w · Cited by 59 · see citing works
Zhang, G., Song, C., Yin, M., Liu, L., Zhang, Y., Li, Y., Zhang, J., Guo, M., & Li, C. (2025) · Nature Communications · doi:10.1038/s41467-025-58921-0 · Cited by 55 · see citing works
Role of primary aging hallmarks in Alzheimer´s disease
Zhao, J., & Huai, J. (2022) · Theranostics · doi:10.7150/thno.79535 · Cited by 53 · see citing works
Yang, F., Wang, X., Yang, D., Lu, Y., Wei, G., Yu, W., Liu, X., Zheng, Q., Ying, J., & Hua, F. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.738686 · Cited by 50 · see citing works
Hajjo, R., Sabbah, D. A., Abusara, O. H., & Bawab, A. Q. A. (2022) · Diagnostics · doi:10.3390/diagnostics12122975 · Cited by 55 · see citing works
The role of epigenetic modifications for the pathogenesis of Crohn's disease
Hornschuh, M., Wirthgen, E., Wolfien, M., Singh, K. P., Wolkenhauer, O., & Däbritz, J. (2021) · Clinical Epigenetics · doi:10.1186/s13148-021-01089-3 · Cited by 51 · see citing works
Multi-omics analysis reveals the key factors involved in the severity of the Alzheimer’s disease
Meng, L., Jin, H., Yulug, B., Altay, O., Li, X., Hanoglu, L., Cankaya, S., Coskun, E., Idil, E., Nogaylar, R., et al. (2024) · Alzheimer's Research & Therapy · doi:10.1186/s13195-024-01578-6 · Cited by 49 · see citing works
Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias
Yassine, H. N., Self, W. K., Kerman, B. E., Santoni, G., Shanmugam, N. K. N., Abdullah, L. I., Golden, L. R., Fonteh, A. N., Harrington, M. G., Gräff, J., et al. (2022) · Alzheimer s & Dementia · doi:10.1002/alz.12845 · Cited by 49 · see citing works
A machine learning and deep learning-based integrated multi-omics technique for leukemia prediction
Abbasi, E. Y., Deng, Z., Arain, Q. A., Khan, A., Shaikh, A., Reshan, M. S. A., Sulaiman, A. A., & Alshahrani, H. M. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e25369 · Cited by 49 · see citing works
The hitchhikers’ guide to RNA sequencing and functional analysis
Chen, J.-W., Shrestha, L., Green, G. A., Leier, A., & Marquez‐Lago, T. T. (2023) · Briefings in Bioinformatics · doi:10.1093/bib/bbac529 · Cited by 47 · see citing works
Restoring the epigenome in Alzheimer's disease: advancing HDAC inhibitors as therapeutic agents
Pereira, M. S., Cruz, M. T., Fortuna, A. C., & Bicker, J. (2024) · Drug Discovery Today · doi:10.1016/j.drudis.2024.104052 · Cited by 44 · see citing works
Alexander, D. C., Corman, T. S., Mendoza, M. R., Glass, A., Belity, T., Wu, R., Campbell, R. R., Han, J., Keiser, A. A., Winkler, J. D., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114758119 · Cited by 40 · see citing works
Self-citationThe microglial lysosomal system in Alzheimer’s disease: Guardian against proteinopathy
Acker, Z. P. V., Perdok, A., Bretou, M., & Annaert, W. G. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101444 · Cited by 45 · see citing works
Clearance Systems in the Brain, From Structure to Function
Liu, J., Guo, Y., Zhang, C., Zeng, Y., Luo, Y., & Wang, G. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.729706 · Cited by 42 · see citing works
Clark, C., Rabl, M., Dayon, L., & Popp, J. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1065904 · Cited by 40 · see citing works
Wahl, D., Smith, M. E., McEntee, C. M., Cavalier, A. N., Osburn, S. C., Burke, S. D., Grant, R. A., Nerguizian, D., Lark, D. S., Link, C. D., et al. (2023) · Aging Cell · doi:10.1111/acel.13798 · Cited by 40 · see citing works
Luo, R., Fan, Y., Yang, J., Ye, M., Zhang, D., Guo, K., Li, X., Bi, R., Xu, M., Yang, L.-X., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00748-4 · Cited by 41 · see citing works
Zheng, X., Wang, M., Huang, K., & Zhu, E. (2023) · Information Fusion · doi:10.1016/j.inffus.2023.102077 · Cited by 39 · see citing works
Yoon, J. H., Lee, H., Kwon, D., Lee, D., Lee, S., Cho, E., Kim, J., & Kim, D. (2024) · Brain Communications · doi:10.1093/braincomms/fcae265 · Cited by 39 · see citing works
Epigenetic Regulation of Aging and its Rejuvenation
An, Y., Wang, Q., Gao, K., Zhang, C., Ouyang, Y., Li, R., Zhou, M., Wu, T., Zhou, L., Xie, Z., et al. (2025) · MedComm · doi:10.1002/mco2.70369 · Cited by 44 · see citing works
Pan, X., Yun, J., Coban‐Akdemir, Z., Jiang, X., Wu, E., Huang, J. H., Sahni, N., & Yi, S. S. (2023) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2023.02.004 · Cited by 36 · see citing works
Thrush, K., Bennett, D. A., Gaiteri, C., Horvath, S., van Dyck, C. H., Higgins‐Chen, A., & Levine, M. E. (2022) · Aging · doi:10.18632/aging.204196 · Cited by 38 · see citing works
SMGR: a joint statistical method for integrative analysis of single-cell multi-omics data
Song, Q., Zhu, X., Jin, L., Chen, M., Zhang, W., & Su, J. (2022) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqac056 · Cited by 37 · see citing works
Zhang, C., Tan, G., Zhang, Y., Zhong, X., Zhao, Z., Peng, Y., Cheng, Q., Xue, K., Xu, Y., Li, X., et al. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14280 · Cited by 35 · see citing works
Epigenetic control of microglial immune responses
Scholz, R., Brösamle, D., Yuan, X., Beyer, M., & Neher, J. J. (2024) · Immunological Reviews · doi:10.1111/imr.13317 · Cited by 39 · see citing works
Yang, Y., Liu, Y., Zhang, A.-L., Tang, S., Ming, Q., Ao, C.-Y., Liu, Y., Li, C.-Z., Yu, C. W., Zhao, H. Y., et al. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.113469 · Cited by 36 · see citing works
Dissecting the brain with spatially resolved multi-omics
Fangma, Y., Liu, M., Liao, J., Chen, Z., & Zheng, Y. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.04.003 · Cited by 37 · see citing works
Targeting epigenetics: A novel promise for Alzheimer’s disease treatment
Jeremic, D., Jiménez‐Díaz, L., & Navarro‐López, J. D. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102003 · Cited by 36 · see citing works
Saeedi, M., & Mehranfar, F. (2022) · Recent Patents on Biotechnology · doi:10.2174/1872208316666220302115901 · Cited by 35 · see citing works
Multi-omic integration via similarity network fusion to detect molecular subtypes of ageing
Yang, M., Matan-Lithwick, S., Wang, Y., De Jager, P. L., Bennett, D. A., & Felsky, D. (2023) · Brain Communications · doi:10.1093/braincomms/fcad110 · Cited by 35 · see citing works
CUT&Tag recovers up to half of ENCODE ChIP-seq histone acetylation peaks
Abbasova, L., Urbanaviciute, P., Hu, D., Ismail, J. N., Schilder, B. M., Nott, A., Skene, N., & Marzi, S. J. (2025) · Nature Communications · doi:10.1038/s41467-025-58137-2 · Cited by 32 · see citing works
Histone H3 Lysine 4 and 27 Trimethylation Landscape of Human Alzheimer’s Disease
Persico, G., Casciaro, F., Amatori, S., Rusin, M., Cantatore, F., Perna, A., Alberi, L. A., Fanelli, M., & Giorgio, M. (2022) · Cells · doi:10.3390/cells11040734 · Cited by 35 · see citing works
Thomas, T. A., Salcedo-Tacuma, D., & Smith, D. M. (2023) · Biomolecules · doi:10.3390/biom13091326 · Cited by 33 · see citing works
Patel, P. J., Ren, Y., & Yan, Z. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106192 · Cited by 32 · see citing works
HAT and HDAC: Enzyme with Contradictory Action in Neurodegenerative Diseases
Singh, R., Rathore, A. S., Dilnashin, H., Keshri, P. K., Gupta, N. K., Satyaprakash, S. A., Zahra, W., Singh, S., & Singh, S. P. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04115-6 · Cited by 32 · see citing works
Wang, X., Allen, M., İş, Ö., Reddy, J. S., Tutor‐New, F. Q., Casey, M. C., Carrasquillo, M. M., Oatman, S. R., Min, Y., Asmann, Y. W., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci149904 · Cited by 30 · see citing works
Genetic insights into immune mechanisms of Alzheimer’s and Parkinson’s disease
Nott, A., & Holtman, I. R. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1168539 · Cited by 31 · see citing works
Williams, J. B., Cao, Q., Wang, W., Lee, Y., Qin, L., Zhong, P., Ren, Y., Ma, K., & Yan, Z. (2023) · Nature Communications · doi:10.1038/s41467-022-35749-6 · Cited by 29 · see citing works
Epigenomics and Lipidomics Integration in Alzheimer Disease: Pathways Involved in Early Stages
Peña‐Bautista, C., Álvarez‐Sánchez, L., Martínez, A. J. C., Baquero, M., & Cháfer‐Pericás, C. (2021) · Biomedicines · doi:10.3390/biomedicines9121812 · Cited by 28 · see citing works
Marmolejo-Garza, A., Medeiros-Furquim, T., Rao, R. G., Eggen, B. J. L., Boddeke, E., & Dolga, A. M. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2022.119326 · Cited by 28 · see citing works
Zhang, L., Liu, Y., Lu, Y., & Wang, G. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.115295 · Cited by 27 · see citing works
Neuroepigenetics of ageing and neurodegeneration-associated dementia: An updated review
Mir, F. A., Amanullah, A., Jain, B. P., Hyderi, Z., & Gautam, A. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102067 · Cited by 28 · see citing works
Xu, D. C., Sas‐Nowosielska, H., Donahue, G., Huang, H., Pourshafie, N., Good, C. R., & Berger, S. L. (2024) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01696-6 · Cited by 30 · see citing works
Self-citationGene body DNA hydroxymethylation restricts the magnitude of transcriptional changes during aging
Occean, J. R., Yang, N., Sun, Y., Dawkins, M. S., Munk, R. B., Belair, C., Dar, S. A., Anerillas, C., Wang, L., Shi, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50725-y · Cited by 27 · see citing works
Self-citationDNA methylation, histone acetylation in the regulation of memory and its modulation during aging
Singh, P., & Paramanik, V. (2025) · Frontiers in Aging · doi:10.3389/fragi.2024.1480932 · Cited by 27 · see citing works
Epigenetic regulation in Alzheimer’s disease: is it a potential therapeutic target?
Coppedè, F. (2021) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2021.1916469 · Cited by 27 · see citing works
Disease‐specific interactome alterations via epichaperomics: the case for Alzheimer’s disease
Ginsberg, S. D., Neubert, T. A., Sharma, S., Digwal, C. S., Yan, P., Timbus, C., Wang, T., & Chiosis, G. (2021) · FEBS Journal · doi:10.1111/febs.16031 · Cited by 27 · see citing works
Dai, Y., Wei, T., Huang, Y., Bei, Y., Lin, H., Shen, Z., Yu, L., Yang, M., Xu, H., He, W., et al. (2023) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-023-04945-y · Cited by 22 · see citing works
A Review of the Application of Spatial Transcriptomics in Neuroscience
Zhang, L., Xiong, Z., & Xiao, M. (2024) · Interdisciplinary Sciences: Computational Life Sciences · doi:10.1007/s12539-024-00603-4 · Cited by 29 · see citing works
Using blood transcriptome analysis for Alzheimer's disease diagnosis and patient stratification
Zhong, H., Zhou, X., Uhm, H., Jiang, Y., Cao, H., Chen, Y., Mak, T. T. W., Lo, R. M. N., Wong, B. W. Y., Cheng, E. Y. L., et al. (2024) · Alzheimer's & Dementia · doi:10.1002/alz.13691 · Cited by 25 · see citing works
Distinct regional vulnerability to Aβ and iron accumulation in post mortem AD brains
Yao, J., Li, Z., Zhou, Z., Bao, A., Wang, Z., Wei, H., & He, H. (2024) · Alzheimer s & Dementia · doi:10.1002/alz.14188 · Cited by 24 · see citing works
Epigenetic biomarkers in Alzheimer's disease: Diagnostic and prognostic relevance
Behl, T., Kyada, A., Roopashree, R., Nathiya, D., Arya, R., Kumar, M., Khalid, M., Gulati, M., Sachdeva, M., Fareed, M., et al. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102556 · Cited by 25 · see citing works
Hudson, H. R., Sun, X., & Orr, M. E. (2025) · Neurotherapeutics · doi:10.1016/j.neurot.2024.e00519 · Cited by 26 · see citing works
SIRT6 Through the Brain Evolution, Development, and Aging
García-Venzor, A., & Toiber, D. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.747989 · Cited by 26 · see citing works
Application of Optogenetics in Neurodegenerative Diseases
Zhang, Q., Li, T., Xu, M., Islam, B., & Wang, J. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-024-01486-1 · Cited by 25 · see citing works
Huang, X., Wang, C., Chen, L., Zhang, T., Leung, K. L., & Wong, G. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166203 · Cited by 24 · see citing works
Liu, T., Du, D., Zhao, R., Xie, Q., & Dong, Z. (2023) · Microbiological Research · doi:10.1016/j.micres.2023.127440 · Cited by 24 · see citing works
CCPA: cloud-based, self-learning modules for consensus pathway analysis using GO, KEGG and Reactome
Nguyen, H., Pham, V.-D., Nguyen, H., Tran, B., Petereit, J., & Nguyen, T. (2024) · Briefings in Bioinformatics · doi:10.1093/bib/bbae222 · Cited by 24 · see citing works
Liu, Y., Zeng, J.-M., Zhao, H. Y., Ao, C.-Y., Ao, L.-H., Ban, J.-Q., & Li, J. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.116155 · Cited by 23 · see citing works
Qin, Y., Yang, P. C., He, W., Li, D., Zeng, L., Li, J., Zhou, T., Peng, J., Cao, L., & Huang, W. G. (2024) · Clinical Epigenetics · doi:10.1186/s13148-024-01650-w · Cited by 26 · see citing works
- Authors
- Nativio, R., Lan, Y., Donahue, G., Sidoli, S., Berson, A., Srinivasan, A. R., Shcherbakova, O., Amlie-Wolf, A., Nie, J., Cui, X., He, C., Wang, L.-S., Garcia, B. A., Trojanowski, J. Q., Bonini, N. M., & Berger, S. L.
- Affiliations
- University of Pennsylvania (US)
- Albert Einstein College of Medicine (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Bonini, Nancy M.
- Berger, Shelley L.
- ORCID
- Venue
- Nature Genetics
- Published
- 2020-09-28
- Volume
- 52
- Issue
- 10
- Pages
- 1024-1035
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC8098004
- OpenAlex
- W3089451699
- Cited by
- 380
- References
- 116
- Citations by year
- 2026: 61 · 2025: 79 · 2024: 70 · 2023: 60 · 2022: 58 · 2021: 47 · 2020: 5
- FWCI
- 25.57
- Type
- journal article
- Language
- en
- Update notices
- correction (2020-10-08)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Spiral (Imperial College London) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute on Aging (P01AG031862, P30AG010124, U54AG052427, U24AG041689, T32AG000255)
- National Human Genome Research Institute (R01HG006827)
- National Cancer Institute (P01CA196539)
- National Institute of Allergy and Infectious Diseases (R01AI118891)
- National Institute of Neurological Disorders and Stroke (R35NS097275, R01NS111997)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- Alzheimer's disease, epigenetic modifications, histone acetyltransferase, chromatin regulation, transcriptional dysregulation, amyloid-beta 42, neurodegeneration, Drosophila model, multi-omics integration, postmortem brain
- MeSH terms
- Epigenome, Acetylation, Alzheimer Disease, Chromatin, Histones, Humans, Peptide Fragments, Signal Transduction, Transcriptional Activation, Amyloid beta-Peptides, Proteome, Histone Code, Histone Acetyltransferases, Transcriptome, Protein Aggregation, Pathological
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