Changes in nucleosome occupancy associated with metabolic alterations in aged mammalian liver
Open accessAbstract
Aging is accompanied by physiological impairments, which, in insulin-responsive tissues, including the liver, predispose individuals to metabolic disease. However, the molecular mechanisms underlying these changes remain largely unknown. Here, we analyze genome-wide profiles of RNA and chromatin organization in the liver of young (3 months) and old (21 months) mice. Transcriptional changes suggest that derepression of the nuclear receptors PPARα, PPARγ, and LXRα in aged mouse liver leads to activation of targets regulating lipid synthesis and storage, whereas age-dependent changes in nucleosome occupancy are associated with binding sites for both known regulators (forkhead factors and nuclear receptors) and candidates associated with nuclear lamina (Hdac3 and Srf) implicated to govern metabolic function of aging liver. Winged-helix transcription factor Foxa2 and nuclear receptor corepressor Hdac3 exhibit a reciprocal binding pattern at PPARα targets contributing to gene expression changes that lead to steatosis in aged liver.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Nucleosome occupancy changes are associated with global upregulation of gene expression with age in yeast and increased FOXA2 binding in aged mammalian livers.
“Interestingly, nucleosome occupancy changes have also been demonstrated to be associated with the global upregulation of gene expression with age in yeast (Hu et al., 2014) and increased transcription factor (FOXA2) binding in aged mammalian livers (Bochkis et al., 2014).”
From The Aging Epigenome (2016) · cites this paper as Bochkis et al., 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
Li, B., & Dewey, C. N. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-323 · Cited by 22,179 · see citing works
Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., & Mesirov, J. P. (2011) · Nature Biotechnology · doi:10.1038/nbt.1754 · Cited by 15,390 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
MEME SUITE: tools for motif discovery and searching
Bailey, T. L., Boden, M., Buske, F. A., Frith, M., Grant, C. E., Clementi, L., Ren, J., Li, W. W., & Noble, W. S. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp335 · Cited by 10,648 · 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
TRANSFAC(R) and its module TRANSCompel(R): transcriptional gene regulation in eukaryotes
Matys, V. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj143 · Cited by 2,142 · see citing works
Nuclear Lamin-A Scales with Tissue Stiffness and Enhances Matrix-Directed Differentiation
Swift, J., Ivanovska, I. L., Buxboim, A., Harada, T., Dingal, P. C. D. P., Pinter, J., Pajerowski, J. D., Spinler, K. R., Shin, J., Tewari, M., et al. (2013) · Science · doi:10.1126/science.1240104 · Cited by 1,998 · see citing works
Regulation of aging and age-related disease by DAF-16 and heat-shock factor
Hsu, A.-L., Murphy, C. T., & Kenyon, C. (2003) · Science · doi:10.1126/science.1083701 · Cited by 1,513 · see citing works
Lamin A-Dependent Nuclear Defects in Human Aging
Scaffidi, P., & Misteli, T. (2006) · Science · doi:10.1126/science.1127168 · Cited by 1,224 · see citing works
Peroxisome proliferator-activated receptor a target genes
Mandard, S., M�ller, M., & Kersten, S. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-3216-3 · Cited by 1,222 · see citing works
Peroxisome Proliferator-Activated Receptor Alpha Target Genes
Rakhshandehroo, M., Knoch, B., Müller, M., & Kersten, S. (2010) · PPAR Research · doi:10.1155/2010/612089 · Cited by 1,020 · see citing works
Histone variants — ancient wrap artists of the epigenome
Talbert, P. B., & Henikoff, S. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2861 · Cited by 844 · see citing works
PPARγ and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scalePreprint
Lefterova, M. I., Zhang, Y., Steger, D. J., Schupp, M., Schug, J., Cristancho, A. G., Feng, D., Zhuo, D. X., Stoeckert, C. J., Liu, X. S., et al. (2008) · Genes & Development · doi:10.1101/gad.1709008 · Cited by 826 · see citing works
Aging Hematopoietic Stem Cells Decline in Function and Exhibit Epigenetic Dysregulation
Chambers, S. M., Shaw, C. A., Gatza, C. E., Fisk, C. J., Donehower, L. A., & Goodell, M. A. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050201 · Cited by 799 · see citing works
Gavrilova, O., Haluzı́k, M., Matsusue, K., Cutson, J. J., Johnson, L. K., Dietz, K. R., Nicol, C. J. B., Vinson, C., Gonzalez, F. J., & Reitman, M. L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300043200 · Cited by 759 · see citing works
LMNA, encoding lamin A/C, is mutated in partial lipodystrophy
Shackleton, S., Lloyd, D. J., Jackson, S. N. J., Evans, R. S., Niermeijer, M. F., Singh, B. M., Schmidt, H., Brabant, G. E., Kumar, S., Durrington, P. N., et al. (2000) · Nature Genetics · doi:10.1038/72807 · Cited by 701 · see citing works
The UCSC Genome Browser database: 2014 update
Karolchik, D., Barber, G. P., Casper, J., Clawson, H., Cline, M. S., Diekhans, M., Dreszer, T. R., Fujita, P. A., Guruvadoo, L., Haeussler, M., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gkt1168 · Cited by 670 · see citing works
A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis
Niedernhofer, L. J., Garinis, G. A., Raams, A., Lalai, A. S., Robinson, A. R., Appeldoorn, E., Odijk, H., Oostendorp, R., Ahmad, A., van Leeuwen, W., et al. (2006) · Nature · doi:10.1038/nature05456 · Cited by 669 · see citing works
The SMRT and N-CoR Corepressors Are Activating Cofactors for Histone Deacetylase 3
Guenther, M. G., Barak, O., & Lazar, M. A. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.18.6091-6101.2001 · Cited by 611 · see citing works
PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls
Rozowsky, J. S., Euskirchen, G. M., Auerbach, R. K., Zhang, Z. D., Gibson, T., Bjornson, R. D., Carriero, N., Snyder, M. P., & Gerstein, M. (2009) · Nature Biotechnology · doi:10.1038/nbt.1518 · Cited by 558 · see citing works
Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging
Liu, L., Cheung, T. H., Charville, G. W., Hurgo, B. M. C., Leavitt, T., Shih, J., Brunet, A., & Rando, T. A. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.05.043 · Cited by 544 · see citing works
Elevated histone expression promotes life span extension
Feser, J., Truong, D., Das, C., Carson, J. J., Kieft, J., Harkness, T., & Tyler, J. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.08.015 · Cited by 435 · see citing works
DANPOS: Dynamic analysis of nucleosome position and occupancy by sequencingPreprint
Chen, K.-F., Xi, Y., Pan, X.-W., Li, Z.-Y., Kaestner, K., Tyler, J. K., Dent, S., He, X.-W., & Li, W. (2013) · Genome Research · doi:10.1101/gr.142067.112 · Cited by 415 · see citing works
Hdac3 is essential for the maintenance of chromatin structure and genome stability
Bhaskara, S., Knutson, S. K., Jiang, G., Chandrasekharan, M. B., Wilson, A. J., Zheng, S., Yenamandra, A., Locke, K., Yuan, J.-L., Bonine-Summers, A. R., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.10.022 · Cited by 353 · see citing works
Hepatic Hdac3 promotes gluconeogenesis by repressing lipid synthesis and sequestration
Sun, Z., Miller, R. A., Patel, R. T., Chen, J., Dhir, R., Wang, H., Zhang, D., Graham, M. J., Unterman, T. G., Shulman, G. I., et al. (2012) · Nature Medicine · doi:10.1038/nm.2744 · Cited by 335 · see citing works
Self-citationTropberger, 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
Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks
Knutson, S. K., Chyla, B. J., Amann, J. M., Bhaskara, S., Huppert, S. S., & Hiebert, S. W. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.51 · Cited by 271 · see citing works
Toll-like receptor signaling links dietary fatty acids to the metabolic syndrome
Fessler, M. B., Rudel, L. L., & Brown, J. M. (2009) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e32832fa5c4 · Cited by 248 · see citing works
Boergesen, M., Pedersen, T. Å., Gross, B. S., van Heeringen, S. J., Hagenbeek, D., Bindesbøll, C., Caron, S., Lalloyer, F., Steffensen, K. R., Nebb, H. I., et al. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.06175-11 · Cited by 237 · see citing works
Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity
Henis‐Korenblit, S., Zhang, P., Hansen, M., McCormick, M. A., Lee, S., Cary, M. P., & Kenyon, C. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002575107 · Cited by 236 · see citing works
Vlieghe, D. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj115 · Cited by 230 · see citing works
Aging, Androgens, and the Metabolic Syndrome in a Longitudinal Study of Aging
Rodríguez, A., Muller, D. C., Metter, E. J., Maggio, M. G., Harman, S. M., Blackman, M. R., & Andres, R. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2764 · Cited by 215 · see citing works
Nucleosome Core Displacement in Vitro via a Metastable Transcription Factor-Nucleosome Complex
Workman, J. L., & Kingston, R. E. (1992) · Science · doi:10.1126/science.1465613 · Cited by 203 · see citing works
Celona, B., Weiner, A., Felice, F. D., Mancuso, F. M., Cesarini, E., Rossi, R. L., Gregory, L., Baban, D. F., Rossetti, G., Grianti, P., et al. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001086 · Cited by 198 · see citing works
Bochkis, I. M., Rubins, N. E., White, P., Furth, E. E., Friedman, J. R., & Kaestner, K. H. (2008) · Nature Medicine · doi:10.1038/nm.1853 · Cited by 186 · see citing works
Self-citationLamin A/C-promoter interactions specify chromatin state–dependent transcription outcomesPreprint
Lund, E. G., Oldenburg, A. R., Delbarre, E., Freberg, C. T., Duband‐Goulet, I., Eskeland, R., Buendia, B., & Collas, P. (2013) · Genome Research · doi:10.1101/gr.159400.113 · Cited by 182 · see citing works
CIDE proteins and metabolic disorders
Gong, J., Sun, Z., & Li, P. (2009) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328328d0bb · Cited by 167 · see citing works
Using Galaxy to Perform Large‐Scale Interactive Data Analyses
Taylor, J., Schenck, I., Blankenberg, D. J., & Nekrutenko, A. (2007) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1005s19 · Cited by 143 · see citing works
Nucleosome-Driven Transcription Factor Binding and Gene Regulation
Ballaré, C., Castellano, G., Gaveglia, L., Althammer, S., González‐Vallinas, J., Eyras, E., Dily, F. L., Zaurín, R., Soronellas, D., Vicent, G. P., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.10.019 · Cited by 140 · see citing works
PPARγ contributes to PKM2 and HK2 expression in fatty liver
Panasyuk, G., Espeillac, C., Chauvin, C., Pradelli, L. A., Horie, Y., Suzuki, A., Annicotte, J., Lluis Fajas, A., Foretz, M., Verdeguer, F., et al. (2012) · Nature Communications · doi:10.1038/ncomms1667 · Cited by 140 · see citing works
DNA Damage Triggers a Chronic Autoinflammatory Response, Leading to Fat Depletion in NER Progeria
Karakasilioti, I., Kamileri, I., Chatzinikolaou, G., Kosteas, T., Vergadi, E., Robinson, A. R., Tsamardinos, I., Rozgaja, T. A., Siakouli, S., Tsatsanis, C., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.08.011 · Cited by 137 · see citing works
Chromatin Opening and Stable Perturbation of Core Histone:DNA Contacts by FoxO1
Hatta, M., & Cirillo, L. A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704735200 · Cited by 127 · see citing works
Jin, J., Iakova, P. A., Jiang, Y., Medrano, E. E., & Timchenko, N. A. (2011) · Hepatology · doi:10.1002/hep.24471 · Cited by 107 · see citing works
Mouse models of inherited lipodystrophy
Savage, D. B. (2009) · Disease Models & Mechanisms · doi:10.1242/dmm.002907 · Cited by 106 · see citing works
Site-Specific Analysis of Histone Methylation and Acetylation
Umlauf, D., Goto, Y., & Feil, R. (2004) · Humana Press eBooks · doi:10.1385/1-59259-828-5:099 · Cited by 95 · see citing works
Zambelli, F., Pesole, G., & Pavesi, G. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt448 · Cited by 86 · see citing works
Role of HDAC1 in senescence, aging, and cancer
Willis-Martinez, D., Richards, H. W., Timchenko, N. A., & Medrano, E. E. (2009) · Experimental Gerontology · doi:10.1016/j.exger.2009.10.001 · Cited by 85 · see citing works
The nucleosome map of the mammalian liver
Li, Z., Schug, J., Tuteja, G., White, P., & Kaestner, K. H. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2060 · Cited by 78 · see citing works
The effect of age and calorie restriction on HIF-1-responsive genes in aged liver
Kang, M. J., Kim, H. J., Kim, H. K., Lee, J. Y., Kim, D. H., Jung, K. J., Kim, K. W., Baik, H. S., Yoo, M. A., Yu, B. P., et al. (2005) · Biogerontology · doi:10.1007/s10522-004-7381-z · Cited by 58 · see citing works
Bochkis, I. M., Schug, J., Ye, D. Z., Kurinna, S. M., Stratton, S. A., Barton, M. C., & Kaestner, K. H. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002770 · Cited by 53 · see citing works
Self-citationUsing Galaxy to Perform Large‐Scale Interactive Data Analyses
Hillman‐Jackson, J., Clements, D., Blankenberg, D. J., Taylor, J., Nekrutenko, A., & Galaxy Zoo Team (2012) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1005s38 · Cited by 48 · see citing works
Sealing the gap between nuclear DNA damage and longevity
Schumacher, B., Hoeijmakers, J. H. J., & Garinis, G. A. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.10.031 · Cited by 43 · see citing works
Jin, J., Wang, G.-L., Timchenko, L., & Timchenko, N. A. (2009) · Aging · doi:10.18632/aging.100060 · Cited by 33 · see citing works
Epigenetic changes play critical role in age‐associated dysfunctions of the liver
Jin, J., Wang, G., Iakova, P. A., Shi, X., Haefliger, S., Finegold, M. J., & Timchenko, N. A. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00617.x · Cited by 32 · see citing works
Sun, K., Battle, M. A., Misra, R. P., & Duncan, S. A. (2009) · Hepatology · doi:10.1002/hep.22834 · Cited by 31 · see citing works
Ding, W., Gao, S. P., & Scott, R. E. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.5.1011 · Cited by 30 · see citing works
Bochkis, I. M., Shin, S., & Kaestner, K. H. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.08.005 · Cited by 28 · see citing works
Self-citation
Flagged first, then by citations
1 of the 60 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Ding W Gao S Scott RE 2012 Senescence represses the nuclear localization of the serum response factor and differentiation regulates its nuclear localization with lineage specificity 11181183
Cited by
Sorted by citations
Pal, S., & Tyler, J. K. (2016) · Science Advances · doi:10.1126/sciadv.1600584 · Cited by 860 · see citing works
Booth, L. N., & Brunet, A. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.013 · Cited by 499 · see citing works
Benayoun, B. A., Pollina, E. A., Singh, P. P., Mahmoudi, S., Harel, I., Casey, K. M., Dulken, B. W., Kundaje, A., & Brunet, A. (2019) · Genome Research · doi:10.1101/gr.240093.118 · Cited by 360 · see citing works
Hallmarks of Aging in the Liver
Hunt, N. J., Kang, S. W., Lockwood, G. P., Couteur, D. G. L., & Cogger, V. C. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.07.021 · Cited by 315 · see citing works
Caloric restriction delays age-related methylation drift
Maegawa, S., Lu, Y., Tahara, T., Lee, J. T., Madžo, J., Liang, S., Jelı́nek, J., Colman, R. J., & Issa, J. J. (2017) · Nature Communications · doi:10.1038/s41467-017-00607-3 · Cited by 278 · see citing works
Biohorology and biomarkers of aging: Current state-of-the-art, challenges and opportunities
Galkin, F., Mamoshina, P., Aliper, A., de Magalhães, J. P., Gladyshev, V. N., & Zhavoronkov, A. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101050 · Cited by 189 · see citing works
Cole, J. J., Robertson, N., Rather, M. I., Thomson, J. P., McBryan, T., Sproul, D., Wang, T., Brock, C., Clark, W. A., Ideker, T. E., et al. (2017) · Genome biology · doi:10.1186/s13059-017-1185-3 · Cited by 182 · see citing works
Genome-wide RNA polymerase stalling shapes the transcriptome during aging
Gyenis, Á., Chang, J., Demmers, J. J. P. G., Bruens, S. T., Barnhoorn, S., Brandt, R. M. C., Baar, M. P., Rašeta, M., Derks, K., Hoeijmakers, J. H. J., et al. (2023) · Nature Genetics · doi:10.1038/s41588-022-01279-6 · Cited by 140 · see citing works
Yang, Z., Jiang, X., Zhao, Z., Zhao, Z., Xing, W., Liu, Y., Jiang, X., & Zhao, H. (2020) · Cancer Gene Therapy · doi:10.1038/s41417-020-0193-8 · Cited by 88 · see citing works
Interaction between epigenetic and metabolism in aging stem cells
Brunet, A., & Rando, T. A. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.12.009 · Cited by 76 · see citing works
Nucleosome positioning: resources and tools online
Teif, V. B. (2015) · Briefings Bioinform. · doi:10.1093/bib/bbv086 · Cited by 66 · see citing works
Oh, G., Ebrahimi, S. B., Carlucci, M., Zhang, A., Nair, A., Groot, D. E., Labrie, V., Jia, P., Oh, E. S., Jeremian, R., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03073-7 · Cited by 64 · see citing works
Developmental and temporal characteristics of clonal sperm mosaicism
Yang, X., Breuss, M. W., Xu, X., Antaki, D., James, K. N., Stanley, V., Ball, L., George, R. D., Wirth, S. A., Cao, B., et al. (2021) · Cell · doi:10.1016/j.cell.2021.07.024 · Cited by 53 · see citing works
Hdac3, Setdb1, and Kap1 mark H3K9me3/H3K14ac bivalent regions in young and aged liver
Price, A. J., Manjegowda, M. C., Kain, J., Anandh, S., & Bochkis, I. M. (2019) · Aging Cell · doi:10.1111/acel.13092 · Cited by 51 · see citing works
Self-citationGreen, C. D., Huang, Y., Dou, X., Liu, Y., Liu, Y., & Han, J. J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.001 · Cited by 47 · see citing works
Insights into the function of HDAC3 and NCoR1/NCoR2 co-repressor complex in metabolic diseases
Paluvai, H., Shanmukha, K. D., Tyedmers, J., & Backs, J. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1190094 · Cited by 44 · see citing works
Multi-level remodeling of transcriptional landscapes in aging and longevity
Lai, R. W., Lu, R. J., Danthi, P. S., Bravo, J. I., Goumba, A., Sampathkumar, N. K., & Benayoun, B. A. (2019) · BMB Reports · doi:10.5483/bmbrep.2019.52.1.296 · Cited by 42 · see citing works
Lin, C., Li, H., Liu, J., Hu, Q., Zhang, S., Zhang, N., Liu, L., Dai, Y., Cao, D., Li, X., et al. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-0562-8 · Cited by 43 · see citing works
The Nuclear Receptor—Co-repressor Complex in Control of Liver Metabolism and Disease
Liang, N., Jakobsson, T., Fan, R., & Treuter, E. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00411 · Cited by 41 · see citing works
Aging is associated with increased chromatin accessibility and reduced polymerase pausing in liver
Bozukova, M., Nikopoulou, C., Kleinenkuhnen, N., Grbavac, D., Goetsch, K., & Tessarz, P. (2022) · Molecular Systems Biology · doi:10.15252/msb.202211002 · Cited by 39 · see citing works
PPARα and NCOR/SMRT corepressor network in liver metabolic regulation
Kang, Z., & Fan, R. (2020) · The FASEB Journal · doi:10.1096/fj.202000055rr · Cited by 37 · see citing works
Capturing and Understanding the Dynamics and Heterogeneity of Gene Expression in the Living Cell
Pascual‐Ahuir, A., Fita‐Torró, J., & Proft, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218278 · Cited by 35 · see citing works
Inflammaging and fatty acid oxidation in monocytes and macrophages
Kruglov, V., Jang, I. H., & Camell, C. D. (2024) · Immunometabolism · doi:10.1097/in9.0000000000000038 · Cited by 38 · see citing works
Wu, J., Bu, D., Wang, H., Shen, D., Chong, D., Zhang, T., Tao, W., Zhao, M., Zhao, Y., Fang, L., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36775-8 · Cited by 35 · see citing works
DNA methylation and histone variants in aging and cancer
Mangelinck, A., & Mann, C. (2021) · International review of cytology · doi:10.1016/bs.ircmb.2021.06.002 · Cited by 33 · see citing works
Unraveling Histone Loss in Aging and Senescence
Dubey, S. K., Dubey, R., & Kleinman, M. E. (2024) · Cells · doi:10.3390/cells13040320 · Cited by 32 · see citing works
Changes at the nuclear lamina alter binding of pioneer factor Foxa2 in aged liver
Whitton, H. J., Singh, L. N., Patrick, M. A., Price, A. J., Osorio, F. G., López-Otı́n, C., & Bochkis, I. M. (2018) · Aging Cell · doi:10.1111/acel.12742 · Cited by 31 · see citing works
Self-citationAgeing and sources of transcriptional heterogeneity
Nikopoulou, C., Parekh, S., & Tessarz, P. (2019) · Biological Chemistry · doi:10.1515/hsz-2018-0449 · Cited by 30 · see citing works
Remodeling of the H3 nucleosomal landscape during mouse aging
Chen, Y., Bravo, J. I., Son, J. M., Lee, C. D., & Benayoun, B. A. (2020) · Translational Medicine of Aging · doi:10.1016/j.tma.2019.12.003 · Cited by 30 · see citing works
Understanding the Unique Microenvironment in the Aging Liver
Zhao, Y., Yang, Y., Li, Q., & Li, . (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.842024 · Cited by 28 · see citing works
Resilience to aging in the regeneration‐capable flatworm Macrostomum lignano
Mouton, S., Grudniewska, M., Glazenburg, L., Guryev, V., & Berezikov, E. (2018) · Aging Cell · doi:10.1111/acel.12739 · Cited by 28 · see citing works
Positive Selection and Enhancer Evolution Shaped Lifespan and Body Mass in Great Apes
Tejada-Martinez, D., Avelar, R., de Magalhães, J. D., Lopes, I., Zhang, B., Novoa, G., & Trizzino, M. (2021) · bioRxiv · doi:10.1093/molbev/msab369 · Cited by 22 · see citing works
Nuclear Receptor Coregulators in Metabolism and Disease
Giudici, M., Goñi, S., Fan, R., & Treuter, E. (2015) · Handbook of experimental pharmacology · doi:10.1007/164_2015_5 · Cited by 27 · see citing works
Pioneer factor Foxa2 enables ligand-dependent activation of type II nuclear receptors FXR and LXRα
Kain, J., Wei, X., Reddy, N. A., Price, A. J., Woods, C. E., & Bochkis, I. M. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101291 · Cited by 23 · see citing works
Self-citationAging Induces Hepatic Oxidative Stress and Nuclear Proteomic Remodeling in Liver from Wistar Rats
Bárcena, B., Salamanca, A., Pintado, C., Mazuecos, L., Villar, M., Moltó, E., Bonzón‐Kulichenko, E., Vázquez, J., Andrés, A., & Gallardo, N. (2021) · Antioxidants · doi:10.3390/antiox10101535 · Cited by 24 · see citing works
Chen, J., Li, E., Zhang, X., Dong, X., Lei, L., Song, W., Zhao, H., & Lai, J. (2017) · Molecular Plant · doi:10.1016/j.molp.2017.05.001 · Cited by 24 · see citing works
Self-citationLi, J., Gan‐Schreier, H., Zhu, X., Wang, W., Tuma‐Kellner, S., Liebisch, G., Stremmel, W., & Chamulitrat, W. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2017.09.001 · Cited by 23 · see citing works
The Significance of Polyploid Hepatocytes During Aging Process
Matsumoto, T., Wakefield, L., & Grompe, M. (2020) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.12.011 · Cited by 16 · see citing works
Shi, Y., Shu, Z.-J., Xue, X., Yeh, C., Katz, M. S., & Kamat, A. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.03.005 · Cited by 19 · see citing works
Porukala, M., & Vinod, P. K. U. (2023) · Scientific Reports · doi:10.1038/s41598-023-31315-2 · Cited by 17 · see citing works
MRT, Functioning with NURF Complex, Regulates Lipid Droplet Size
Yao, Y., Li, X., Wang, W., Liu, Z., Chen, J., Ding, M., & Huang, X. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.026 · Cited by 16 · see citing works
Self-citationTran, K. A., Gilbert, M., Vazquez, B. N., Ianni, A., Garcia, B. A., Vaquero, A., & Berger, S. L. (2025) · Molecular Cell · doi:10.1016/j.molcel.2025.05.025 · Cited by 15 · see citing works
Phua, W. W. T., Tan, W., Yip, Y. S., Hew, I. D., Wee, J. W. K., Cheng, H. S., Leow, M. K., Wahli, W., & Tan, N. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051747 · Cited by 15 · see citing works
Regulation of Age-related Decline by Transcription Factors and Their Crosstalk with the Epigenome
Zhou, X., Sen, I., Lin, X.-X., & Riedel, C. G. (2018) · Current Genomics · doi:10.2174/1389202919666180503125850 · Cited by 14 · see citing works
Age-associated changes in transcriptional elongation and their effects on homeostasis
Papantonis, A., Antebi, A., Partridge, L., & Beyer, A. (2024) · Trends in Cell Biology · doi:10.1016/j.tcb.2024.11.005 · Cited by 13 · see citing works
Ucar, D., & Benayoun, B. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-811060-7.00001-2 · Cited by 12 · see citing works
Coupling between Sequence-Mediated Nucleosome Organization and Genome Evolution
Barbier, J., Vaillant, C., Volff, J., Brunet, F., & Audit, B. (2021) · Genes · doi:10.3390/genes12060851 · Cited by 12 · see citing works
Guo, Y., Zhou, A., Zhang, Y., Chen, Y., Chen, Y., Gao, Y., & Miao, X. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.121824 · Cited by 10 · see citing works
Xie, W., Xue, Y., Zhang, H., Wang, Y., Meng, M., Chang, G., & Shen, X. (2022) · Gene · doi:10.1016/j.gene.2022.146703 · Cited by 10 · see citing works
Functionally analyzing the important roles of hepatocyte nuclear factor 3 (FoxA) in tumorigenesis
Gao, B. X., Xie, W., Wu, X., Wang, L., & Guo, J. (2020) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188365 · Cited by 9 · see citing works
Chen, J., Li, E., & Lai, J. (2017) · Nucleus · doi:10.1080/19491034.2017.1402152 · Cited by 9 · see citing works
Self-citationAge-associated transcriptional stress due to accelerated elongation and increased stalling of RNAPII
Papadakis, A., Gyenis, Á., Pothof, J., Hoeijmakers, J. H. J., Papantonis, A., & Beyer, A. (2023) · Nature Genetics · doi:10.1038/s41588-023-01601-w · Cited by 8 · see citing works
Time makes histone H3 modifications drift in mouse liver
Hillje, R., Luzi, L., Amatori, S., Persico, G., Casciaro, F., Rusin, M., Fanelli, M., Pelicci, P., & Giorgio, M. (2022) · Aging · doi:10.18632/aging.204107 · Cited by 7 · see citing works
Chicken or Egg: Is Clonal Hematopoiesis Primarily Caused by Genetic or Epigenetic Aberrations?
Cypris, O., Božić, T., & Wagner, W. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00785 · Cited by 7 · see citing works
Zeng, H., Wang, B., Huang, Z., Gao, L., Xiao, Y., Liu, X., Xu, Y., Hu, Z., Pang, J., Yu, Y., et al. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03601-5 · Cited by 7 · see citing works
Costa, S. S., Wegmann, D., & Ripperger, J. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0169615 · Cited by 6 · see citing works
Lemus, A. J. J., Tewelde, E., Bhala, R., Guan, A., Xu, A., & Benayoun, B. A. (2026) · Open Biology · doi:10.1098/rsob.250093 · Cited by 5 · see citing works
Fenofibrate induces liver enlargement in aging mice via activating the PPARα-YAP signaling pathway
Li, H., Zhou, Y., Cai, C., Liang, H., Li, X., Huang, M., Fan, S., & Bi, H. (2024) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2024.111286 · Cited by 5 · see citing works
Gene Expression, Epigenetics and Ageing
Maniyadath, B., Shukla, N., & Kolthur‐Seetharam, U. (2018) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-981-13-2835-0_16 · Cited by 5 · see citing works
Lomas‐Soria, C., Rodríguez-González, G. L., Ibáñez, C. A., Reyes‐Castro, L. A., Nathanielsz, P. W., & Zambrano, E. (2023) · Biology · doi:10.3390/biology12091166 · Cited by 5 · see citing works
Stem cell-based therapeutic strategies for liver aging
Niu, H., Wang, Y., Ding, Y. S., Lin, Y., Qin, J., & Wang, J. (2025) · Liver Research · doi:10.1016/j.livres.2025.04.003 · Cited by 4 · see citing works
Progress in understanding how clock genes regulate aging and associated metabolic processes
Su, Y., Wang, M., Chen, J., Bao, Y., Wen, R., Ren, H., & Luan, Z. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2025.1654369 · Cited by 3 · see citing works
Self-citationSwer, P. B., Kharbuli, B., Syiem, D., & Sharma, R. (2024) · Biogerontology · doi:10.1007/s10522-024-10117-7 · Cited by 3 · see citing works
Preparation of Frozen Liver Tissues for Integrated Omics Analysis
Liang, N., Fan, R., Goñi, S., & Treuter, E. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9130-3_13 · Cited by 3 · see citing works
Chen, X., Yang, H., Liu, G., & Zhang, Y. (2021) · BMC Bioinformatics · doi:10.1186/s12859-021-04239-9 · Cited by 3 · see citing works
Liu, J.-F., Wu, S., Liu, C., Chen, H., & Yang, J. (2020) · Research Square · doi:10.21203/rs.3.rs-104808/v1 · Cited by 3 · see citing works
Chromatin Signaling in Aging and Cellular Senescence
Couteau, F., & Mallette, F. A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802389-1.00016-2 · Cited by 1 · see citing works
Histone Deacetylase Functions in Epidermal Development, Homeostasis and Cancer
Brennan-Crispi, D. M., & Millar, S. E. (2018) · Contributions to management science · doi:10.1007/978-3-319-16769-5_5 · Cited by 1 · see citing works
NUCOME : A Comprehensive Database of Nucleosome Organizations in Mammalian GenomesPreprint
Chen, X., Yang, H., & Zhang, Y. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/414094
The role of forkhead box A2 in skeletal muscle
Phua, W. W. T. (2019) · doi:10.32657/10220/49672
Time makes histone H3 modifications driftPreprint
Hillje, R., Luzi, L., Amatori, S., Fanelli, M., Pelicci, P. G., & Giorgio, M. (2021) · Research Square · doi:10.21203/rs.3.rs-369821/v1
Reduced polymerase pausing compensates for increased chromatin accessibility in the aging liverPreprint
Bozukova, M., Grbavac, D., Nikopoulou, C., & Tessarz, P. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.25.481984
Chen, X., Yang, H., Liu, G., & Zhang, Y. (2021) · Figshare · doi:10.6084/m9.figshare.14776523
Structure de la chromatine et éléments transposables : une approche évolutive
Barbier, J. (2022) · theses.fr (ABES) · doi:10.70675/dd1ee9e6z52fez46d7za781ze5573e9c1277
Targeting the liver for longevity
Yu, J., Fan, B., Gao, X., Fan, Y., Wang, S., Huang, C., & Fan, S. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103142
Chromatin signaling in aging and cellular senescence
Gagné, L. M., Couteau, F., & Mallette, F. A. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-19001-8.00018-0
Frank, A., Tierling, S., Czepukojc, B., Kessler, S. M., Hentrich, T., Kohlstedt, M., Haybaeck, J., Wittmann, C., Hoppstädter, J., Schulze-Hentrich, J. M., et al. (2026) · Liver international communications. · doi:10.1002/lci2.70058
- Authors
- Bochkis, I. M., Przybylski, D., Chen, J., & Regev, A.
- Affiliations
- Broad Institute (US)
- Corresponding author
- Bochkis, Irina M.
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2014-11
- Volume
- 9
- Issue
- 3
- Pages
- 996-1006
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC4250828
- OpenAlex
- W2020049638
- Cited by
- 78
- References
- 60
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 6 · 2023: 7 · 2022: 6 · 2021: 10 · 2020: 10 · 2019: 9 · 2018: 8 · 2017: 9 · 2016: 4 · 2015: 2
- FWCI
- 2.05
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- Howard Hughes Medical Institute
- National Human Genome Research Institute (P50HG006193, T32HG002295)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-101633, K01DK101633)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- aging, liver, nucleosome occupancy, chromatin organization, nuclear receptors, PPARα, PPARγ, liver X receptor alpha, lipid metabolism, steatosis, forkhead transcription factor, nuclear lamina, HDAC3, SRF, FOXA2, transcriptional derepression, insulin resistance, metabolic disorders
- MeSH terms
- Histone Deacetylase 3, Aging, Animals, Base Sequence, DNA-Binding Proteins, Fatty Liver, Histone Deacetylases, Inflammation, Liver, Male, Mammals, Mice, Inbred C57BL, Models, Biological, Molecular Sequence Data, Nucleosomes, Protein Binding, Transcription Factors, Gene Expression Regulation, Developmental, Nuclear Lamina, PPAR alpha, Hepatocyte Nuclear Factor 3-beta
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