5szb Citations

Identification of H3K4me1-associated proteins at mammalian enhancers.

Abstract

Enhancers act to regulate cell-type-specific gene expression by facilitating the transcription of target genes. In mammalian cells, active or primed enhancers are commonly marked by monomethylation of histone H3 at lysine 4 (H3K4me1) in a cell-type-specific manner. Whether and how this histone modification regulates enhancer-dependent transcription programs in mammals is unclear. In this study, we conducted SILAC mass spectrometry experiments with mononucleosomes and identified multiple H3K4me1-associated proteins, including many involved in chromatin remodeling. We demonstrate that H3K4me1 augments association of the chromatin-remodeling complex BAF to enhancers in vivo and that, in vitro, H3K4me1-marked nucleosomes are more efficiently remodeled by the BAF complex. Crystal structures of the BAF component BAF45C indicate that monomethylation, but not trimethylation, is accommodated by BAF45C's H3K4-binding site. Our results suggest that H3K4me1 has an active role at enhancers by facilitating binding of the BAF complex and possibly other chromatin regulators.

Reviews - 5szb mentioned but not cited (1)

  1. Conserved Structure and Evolution of DPF Domain of PHF10-The Specific Subunit of PBAF Chromatin Remodeling Complex. Chugunov AO, Potapova NA, Klimenko NS, Tatarskiy VV, Georgieva SG, Soshnikova NV. Int J Mol Sci 22 11134 (2021)

Articles - 5szb mentioned but not cited (3)

  1. Identification of H3K4me1-associated proteins at mammalian enhancers. Local A, Huang H, Albuquerque CP, Singh N, Lee AY, Wang W, Wang C, Hsia JE, Shiau AK, Ge K, Corbett KD, Wang D, Zhou H, Ren B. Nat Genet 50 73-82 (2018)
  2. Methyl-Induced Polarization Destabilizes the Noncovalent Interactions of N-Methylated Lysines. Rahman S, Wineman-Fisher V, Nagy PR, Al-Hamdani Y, Tkatchenko A, Varma S. Chemistry 27 11005-11014 (2021)
  3. An in silico study of how histone tail conformation affects the binding affinity of ING family proteins. Gül N, Yıldız A. PeerJ 10 e14029 (2022)


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  1. Assessing sufficiency and necessity of enhancer activities for gene expression and the mechanisms of transcription activation. Catarino RR, Stark A. Genes Dev 32 202-223 (2018)
  2. Targeting epigenetic mechanisms in diabetic wound healing. den Dekker A, Davis FM, Kunkel SL, Gallagher KA. Transl Res 204 39-50 (2019)
  3. Histone H3 lysine K4 methylation and its role in learning and memory. Collins BE, Greer CB, Coleman BC, Sweatt JD. Epigenetics Chromatin 12 7 (2019)
  4. Chromatin Regulation of Neuronal Maturation and Plasticity. Gallegos DA, Chan U, Chen LF, West AE. Trends Neurosci 41 311-324 (2018)
  5. Transcriptional Control of Circadian Rhythms and Metabolism: A Matter of Time and Space. Kim YH, Lazar MA. Endocr Rev 41 bnaa014 (2020)
  6. The Promise for Histone Methyltransferase Inhibitors for Epigenetic Therapy in Clinical Oncology: A Narrative Review. Rugo HS, Jacobs I, Sharma S, Scappaticci F, Paul TA, Jensen-Pergakes K, Malouf GG. Adv Ther 37 3059-3082 (2020)
  7. Epigenetic control of transcriptional regulation in pluripotency and early differentiation. Gökbuget D, Blelloch R. Development 146 dev164772 (2019)
  8. Functional mechanisms and abnormalities of the nuclear lamina. Karoutas A, Akhtar A. Nat Cell Biol 23 116-126 (2021)
  9. Enhancers: bridging the gap between gene control and human disease. Karnuta JM, Scacheri PC. Hum Mol Genet 27 R219-R227 (2018)
  10. Enhancer and super-enhancer: Positive regulators in gene transcription. Peng Y, Zhang Y. Animal Model Exp Med 1 169-179 (2018)
  11. Shaping Gene Expression by Landscaping Chromatin Architecture: Lessons from a Master. Sartorelli V, Puri PL. Mol Cell 71 375-388 (2018)
  12. Exploring 3D chromatin contacts in gene regulation: The evolution of approaches for the identification of functional enhancer-promoter interaction. Xu H, Zhang S, Yi X, Plewczynski D, Li MJ. Comput Struct Biotechnol J 18 558-570 (2020)
  13. Unwinding chromatin at the right places: how BAF is targeted to specific genomic locations during development. Ho PJ, Lloyd SM, Bao X. Development 146 dev178780 (2019)
  14. The Unexpected Noncatalytic Roles of Histone Modifiers in Development and Disease. Aubert Y, Egolf S, Capell BC. Trends Genet 35 645-657 (2019)
  15. DNA Methylation of Enhancer Elements in Myeloid Neoplasms: Think Outside the Promoters? Ordoñez R, Martínez-Calle N, Agirre X, Prosper F. Cancers (Basel) 11 E1424 (2019)
  16. The MLL3/4 H3K4 methyltransferase complex in establishing an active enhancer landscape. Wang LH, Aberin MAE, Wu S, Wang SP. Biochem Soc Trans 49 1041-1054 (2021)
  17. Long non-coding RNAs: the tentacles of chromatin remodeler complexes. Neve B, Jonckheere N, Vincent A, Van Seuningen I. Cell Mol Life Sci 78 1139-1161 (2021)
  18. Molecular Basis of the Function of Transcriptional Enhancers. Ibragimov AN, Bylino OV, Shidlovskii YV. Cells 9 E1620 (2020)
  19. Epigenetic Control of Osteogenic Lineage Commitment. Montecino M, Carrasco ME, Nardocci G. Front Cell Dev Biol 8 611197 (2020)
  20. Genetics and epigenetics of autoimmune thyroid diseases: Translational implications. Lee HJ, Stefan-Lifshitz M, Li CW, Tomer Y. Best Pract Res Clin Endocrinol Metab 37 101661 (2023)
  21. Chromatin Structure and Dynamics: Focus on Neuronal Differentiation and Pathological Implication. Nothof SA, Magdinier F, Van-Gils J. Genes (Basel) 13 639 (2022)
  22. Epigenetic Changes and Chromatin Reorganization in Brain Function: Lessons from Fear Memory Ensemble and Alzheimer's Disease. van Zundert B, Montecino M. Int J Mol Sci 23 12081 (2022)
  23. Atypical histone targets of PHD fingers. Black JC, Kutateladze TG. J Biol Chem 299 104601 (2023)
  24. Chemical Biology Approaches to Identify and Profile Interactors of Chromatin Modifications. Nickel GA, Diehl KL. ACS Chem Biol 18 1014-1026 (2023)
  25. Functions and Interactions of Mammalian KDM5 Demethylases. Pavlenko E, Ruengeler T, Engel P, Poepsel S. Front Genet 13 906662 (2022)
  26. Advances in Single-Cell Multi-Omics and Application in Cardiovascular Research. Zhang X, Qiu H, Zhang F, Ding S. Front Cell Dev Biol 10 883861 (2022)
  27. Epigenomic dynamics of early Xenopus Embryos. Zhou JJ, Cho KWY. Dev Growth Differ 64 508-516 (2022)
  28. The chromatin signatures of enhancers and their dynamic regulation. Barral A, Déjardin J. Nucleus 14 2160551 (2023)
  29. Chemical biology approaches to study histone interactors. Burton AJ, Hamza GM, Zhang AX, Muir TW. Biochem Soc Trans 49 2431-2441 (2021)
  30. Interrogating epigenetic mechanisms with chemically customized chromatin. Hananya N, Koren S, Muir TW. Nat Rev Genet (2023)
  31. New insights into inflammatory memory of epidermal stem cells. Cheng D, Zhu X, Yan S, Shi L, Liu Z, Zhou X, Bi X. Front Immunol 14 1188559 (2023)
  32. Novel Biotherapeutics Targeting Biomolecular and Cellular Approaches in Diabetic Wound Healing. Singh SK, Dwivedi SD, Yadav K, Shah K, Chauhan NS, Pradhan M, Singh MR, Singh D. Biomedicines 11 613 (2023)

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  1. UTX-mediated enhancer and chromatin remodeling suppresses myeloid leukemogenesis through noncatalytic inverse regulation of ETS and GATA programs. Gozdecka M, Meduri E, Mazan M, Tzelepis K, Dudek M, Knights AJ, Pardo M, Yu L, Choudhary JS, Metzakopian E, Iyer V, Yun H, Park N, Varela I, Bautista R, Collord G, Dovey O, Garyfallos DA, De Braekeleer E, Kondo S, Cooper J, Göttgens B, Bullinger L, Northcott PA, Adams D, Vassiliou GS, Huntly BJP. Nat Genet 50 883-894 (2018)
  2. The ATPase module of mammalian SWI/SNF family complexes mediates subcomplex identity and catalytic activity-independent genomic targeting. Pan J, McKenzie ZM, D'Avino AR, Mashtalir N, Lareau CA, St Pierre R, Wang L, Shilatifard A, Kadoch C. Nat Genet 51 618-626 (2019)
  3. Zscan4c activates endogenous retrovirus MERVL and cleavage embryo genes. Zhang W, Chen F, Chen R, Xie D, Yang J, Zhao X, Guo R, Zhang Y, Shen Y, Göke J, Liu L, Lu X. Nucleic Acids Res 47 8485-8501 (2019)
  4. Is H3K4me1 at enhancers correlative or causative? Rada-Iglesias A. Nat Genet 50 4-5 (2018)
  5. H3K4me1 Distribution Predicts Transcription State and Poising at Promoters. Bae S, Lesch BJ. Front Cell Dev Biol 8 289 (2020)
  6. Hypoxia-induced lncHILAR promotes renal cancer metastasis via ceRNA for the miR-613/206/ 1-1-3p/Jagged-1/Notch/CXCR4 signaling pathway. Hu G, Ma J, Zhang J, Chen Y, Liu H, Huang Y, Zheng J, Xu Y, Xue W, Zhai W. Mol Ther 29 2979-2994 (2021)
  7. Chromatin landscape signals differentially dictate the activities of mSWI/SNF family complexes. Mashtalir N, Dao HT, Sankar A, Liu H, Corin AJ, Bagert JD, Ge EJ, D'Avino AR, Filipovski M, Michel BC, Dann GP, Muir TW, Kadoch C. Science 373 306-315 (2021)
  8. H3.3K4M destabilizes enhancer H3K4 methyltransferases MLL3/MLL4 and impairs adipose tissue development. Jang Y, Broun A, Wang C, Park YK, Zhuang L, Lee JE, Froimchuk E, Liu C, Ge K. Nucleic Acids Res 47 607-620 (2019)
  9. MLL4-associated condensates counterbalance Polycomb-mediated nuclear mechanical stress in Kabuki syndrome. Fasciani A, D'Annunzio S, Poli V, Fagnocchi L, Beyes S, Michelatti D, Corazza F, Antonelli L, Gregoretti F, Oliva G, Belli R, Peroni D, Domenici E, Zambrano S, Intartaglia D, Settembre C, Conte I, Testi C, Vergyris P, Ruocco G, Zippo A. Nat Genet 52 1397-1411 (2020)
  10. Orphan CpG islands amplify poised enhancer regulatory activity and determine target gene responsiveness. Pachano T, Sánchez-Gaya V, Ealo T, Mariner-Faulí M, Bleckwehl T, Asenjo HG, Respuela P, Cruz-Molina S, Muñoz-San Martín M, Haro E, van IJcken WFJ, Landeira D, Rada-Iglesias A. Nat Genet 53 1036-1049 (2021)
  11. Specific subfamilies of transposable elements contribute to different domains of T lymphocyte enhancers. Ye M, Goudot C, Hoyler T, Lemoine B, Amigorena S, Zueva E. Proc Natl Acad Sci U S A 117 7905-7916 (2020)
  12. H3K4me2 functions as a repressive epigenetic mark in plants. Liu Y, Liu K, Yin L, Yu Y, Qi J, Shen WH, Zhu J, Zhang Y, Dong A. Epigenetics Chromatin 12 40 (2019)
  13. Ligand-induced native G-quadruplex stabilization impairs transcription initiation. Li C, Wang H, Yin Z, Fang P, Xiao R, Xiang Y, Wang W, Li Q, Huang B, Huang J, Liang K. Genome Res 31 1546-1560 (2021)
  14. Mutually suppressive roles of KMT2A and KDM5C in behaviour, neuronal structure, and histone H3K4 methylation. Vallianatos CN, Raines B, Porter RS, Bonefas KM, Wu MC, Garay PM, Collette KM, Seo YA, Dou Y, Keegan CE, Tronson NC, Iwase S. Commun Biol 3 278 (2020)
  15. ARID1A regulates R-loop associated DNA replication stress. Tsai S, Fournier LA, Chang EY, Wells JP, Minaker SW, Zhu YD, Wang AY, Wang Y, Huntsman DG, Stirling PC. PLoS Genet 17 e1009238 (2021)
  16. Interplay of BAF and MLL4 promotes cell type-specific enhancer activation. Park YK, Lee JE, Yan Z, McKernan K, O'Haren T, Wang W, Peng W, Ge K. Nat Commun 12 1630 (2021)
  17. Enhancer decommissioning imposes an epigenetic barrier to sensory hair cell regeneration. Tao L, Yu HV, Llamas J, Trecek T, Wang X, Stojanova Z, Groves AK, Segil N. Dev Cell 56 2471-2485.e5 (2021)
  18. Linking aberrant chromatin features in chronic lymphocytic leukemia to transcription factor networks. Mallm JP, Iskar M, Ishaque N, Klett LC, Kugler SJ, Muino JM, Teif VB, Poos AM, Großmann S, Erdel F, Tavernari D, Koser SD, Schumacher S, Brors B, König R, Remondini D, Vingron M, Stilgenbauer S, Lichter P, Zapatka M, Mertens D, Rippe K. Mol Syst Biol 15 e8339 (2019)
  19. HRP2-DPF3a-BAF complex coordinates histone modification and chromatin remodeling to regulate myogenic gene transcription. Zhu X, Lan B, Yi X, He C, Dang L, Zhou X, Lu Y, Sun Y, Liu Z, Bai X, Zhang K, Li B, Li MJ, Chen Y, Zhang L. Nucleic Acids Res 48 6563-6582 (2020)
  20. The 3' processing of antisense RNAs physically links to chromatin-based transcriptional control. Fang X, Wu Z, Raitskin O, Webb K, Voigt P, Lu T, Howard M, Dean C. Proc Natl Acad Sci U S A 117 15316-15321 (2020)
  21. In situ chromatin interactomics using a chemical bait and trap approach. Burton AJ, Haugbro M, Gates LA, Bagert JD, Allis CD, Muir TW. Nat Chem 12 520-527 (2020)
  22. Meta-analyses identify DNA methylation associated with kidney function and damage. Schlosser P, Tin A, Matias-Garcia PR, Thio CHL, Joehanes R, Liu H, Weihs A, Yu Z, Hoppmann A, Grundner-Culemann F, Min JL, Adeyemo AA, Agyemang C, Ärnlöv J, Aziz NA, Baccarelli A, Bochud M, Brenner H, Breteler MMB, Carmeli C, Chaker L, Chambers JC, Cole SA, Coresh J, Corre T, Correa A, Cox SR, de Klein N, Delgado GE, Domingo-Relloso A, Eckardt KU, Ekici AB, Endlich K, Evans KL, Floyd JS, Fornage M, Franke L, Fraszczyk E, Gao X, Gào X, Ghanbari M, Ghasemi S, Gieger C, Greenland P, Grove ML, Harris SE, Hemani G, Henneman P, Herder C, Horvath S, Hou L, Hurme MA, Hwang SJ, Jarvelin MR, Kardia SLR, Kasela S, Kleber ME, Koenig W, Kooner JS, Kramer H, Kronenberg F, Kühnel B, Lehtimäki T, Lind L, Liu D, Liu Y, Lloyd-Jones DM, Lohman K, Lorkowski S, Lu AT, Marioni RE, März W, McCartney DL, Meeks KAC, Milani L, Mishra PP, Nauck M, Navas-Acien A, Nowak C, Peters A, Prokisch H, Psaty BM, Raitakari OT, Ratliff SM, Reiner AP, Rosas SE, Schöttker B, Schwartz J, Sedaghat S, Smith JA, Sotoodehnia N, Stocker HR, Stringhini S, Sundström J, Swenson BR, Tellez-Plaza M, van Meurs JBJ, van Vliet-Ostaptchouk JV, Venema A, Verweij N, Walker RM, Wielscher M, Winkelmann J, Wolffenbuttel BHR, Zhao W, Zheng Y, Estonian Biobank Research Team, Genetics of DNA Methylation Consortium, Loh M, Snieder H, Levy D, Waldenberger M, Susztak K, Köttgen A, Teumer A. Nat Commun 12 7174 (2021)
  23. 3D landscape of Hepatitis B virus interactions with human chromatins. Yang B, Li B, Jia L, Jiang Y, Wang X, Jiang S, Du S, Ji X, Yang P. Cell Discov 6 95 (2020)
  24. HNF4A defines tissue-specific circadian rhythms by beaconing BMAL1::CLOCK chromatin binding and shaping the rhythmic chromatin landscape. Qu M, Qu H, Jia Z, Kay SA. Nat Commun 12 6350 (2021)
  25. Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups. Giles KA, Gould CM, Du Q, Skvortsova K, Song JZ, Maddugoda MP, Achinger-Kawecka J, Stirzaker C, Clark SJ, Taberlay PC. Epigenetics Chromatin 12 12 (2019)
  26. Effect of Histone Lysine Methylation on DNA Lesion Reactivity in Nucleosome Core Particles. Yang K, Prasse C, Greenberg MM. Chem Res Toxicol 32 910-916 (2019)
  27. Enhancer-associated H3K4 methylation safeguards in vitro germline competence. Bleckwehl T, Crispatzu G, Schaaf K, Respuela P, Bartusel M, Benson L, Clark SJ, Dorighi KM, Barral A, Laugsch M, van IJcken WFJ, Manzanares M, Wysocka J, Reik W, Rada-Iglesias Á. Nat Commun 12 5771 (2021)
  28. KDM6B promotes activation of the oncogenic CDK4/6-pRB-E2F pathway by maintaining enhancer activity in MYCN-amplified neuroblastoma. D'Oto A, Fang J, Jin H, Xu B, Singh S, Mullasseril A, Jones V, Abu-Zaid A, von Buttlar X, Cooke B, Hu D, Shohet J, Murphy AJ, Davidoff AM, Yang J. Nat Commun 12 7204 (2021)
  29. Nasal DNA methylation differentiates severe from non-severe asthma in African-American children. Zhu T, Zhang X, Chen X, Brown AP, Weirauch MT, Guilbert TW, Khurana Hershey GK, Biagini JM, Ji H. Allergy 76 1836-1845 (2021)
  30. shRNA-interfering LSD1 inhibits proliferation and invasion of gastric cancer cells via VEGF-C/PI3K/AKT signaling pathway. Pan HM, Lang WY, Yao LJ, Wang Y, Li XL. World J Gastrointest Oncol 11 622-633 (2019)
  31. Differential microRNA Expression in USP8-Mutated and Wild-Type Corticotroph Pituitary Tumors Reflect the Difference in Protein Ubiquitination Processes. Bujko M, Kober P, Boresowicz J, Rusetska N, Zeber-Lubecka N, Paziewska A, Pekul M, Zielinski G, Styk A, Kunicki J, Ostrowski J, Siedlecki JA, Maksymowicz M. J Clin Med 10 375 (2021)
  32. The genomic distribution of histone H3K4me2 in spermatogonia is highly conserved in sperm†. Lambrot R, Siklenka K, Lafleur C, Kimmins S. Biol Reprod 100 1661-1672 (2019)
  33. Establishment and function of chromatin modification at enhancers. Tafessu A, Banaszynski LA. Open Biol 10 200255 (2020)
  34. Predictive QM/MM Modeling of Modulations in Protein-Protein Binding by Lysine Methylation. Rahman S, Wineman-Fisher V, Al-Hamdani Y, Tkatchenko A, Varma S. J Mol Biol 433 166745 (2021)
  35. An integrated multi-omics approach to identify regulatory mechanisms in cancer metastatic processes. Ghaffari S, Hanson C, Schmidt RE, Bouchonville KJ, Offer SM, Sinha S. Genome Biol 22 19 (2021)
  36. Nuclear RIPK1 promotes chromatin remodeling to mediate inflammatory response. Li W, Shan B, Zou C, Wang H, Zhang MM, Zhu H, Naito MG, Xu D, Manuel VJ, Mifflin L, Hou Z, Ravits J, Yuan J. Cell Res 32 621-637 (2022)
  37. The Trithorax group protein dMLL3/4 instructs the assembly of the zygotic genome at fertilization. Prudêncio P, Guilgur LG, Sobral J, Becker JD, Martinho RG, Navarro-Costa P. EMBO Rep 19 e45728 (2018)
  38. Histone 3 lysine 4 monomethylation supports activation of transcription in S. cerevisiae during nutrient stress. Deshpande N, Jordan R, Henderson Pozzi M, Bryk M. Curr Genet 68 181-194 (2022)
  39. Polycomb contraction differentially regulates terminal human hematopoietic differentiation programs. Lorzadeh A, Hammond C, Wang F, Knapp DJHF, Wong JC, Zhu JYA, Cao Q, Heravi-Moussavi A, Carles A, Wong M, Sharafian Z, Steif J, Moksa M, Bilenky M, Lavoie PM, Eaves CJ, Hirst M. BMC Biol 20 104 (2022)
  40. Comprehensive characterization of three classes of Arabidopsis SWI/SNF chromatin remodelling complexes. Guo J, Cai G, Li YQ, Zhang YX, Su YN, Yuan DY, Zhang ZC, Liu ZZ, Cai XW, Guo J, Li L, Chen S, He XJ. Nat Plants 8 1423-1439 (2022)
  41. Epigenetic Regulation of WNT3A Enhancer during Regeneration of Injured Cortical Neurons. Chang CY, Hung JH, Huang LW, Li J, Fung KS, Kao CF, Chen L. Int J Mol Sci 21 E1891 (2020)
  42. Epigenome-wide association study of serum urate reveals insights into urate co-regulation and the SLC2A9 locus. Tin A, Schlosser P, Matias-Garcia PR, Thio CHL, Joehanes R, Liu H, Yu Z, Weihs A, Hoppmann A, Grundner-Culemann F, Min JL, Kuhns VLH, Adeyemo AA, Agyemang C, Ärnlöv J, Aziz NA, Baccarelli A, Bochud M, Brenner H, Bressler J, Breteler MMB, Carmeli C, Chaker L, Coresh J, Corre T, Correa A, Cox SR, Delgado GE, Eckardt KU, Ekici AB, Endlich K, Floyd JS, Fraszczyk E, Gao X, Gào X, Gelber AC, Ghanbari M, Ghasemi S, Gieger C, Greenland P, Grove ML, Harris SE, Hemani G, Henneman P, Herder C, Horvath S, Hou L, Hurme MA, Hwang SJ, Kardia SLR, Kasela S, Kleber ME, Koenig W, Kooner JS, Kronenberg F, Kühnel B, Ladd-Acosta C, Lehtimäki T, Lind L, Liu D, Lloyd-Jones DM, Lorkowski S, Lu AT, Marioni RE, März W, McCartney DL, Meeks KAC, Milani L, Mishra PP, Nauck M, Nowak C, Peters A, Prokisch H, Psaty BM, Raitakari OT, Ratliff SM, Reiner AP, Schöttker B, Schwartz J, Sedaghat S, Smith JA, Sotoodehnia N, Stocker HR, Stringhini S, Sundström J, Swenson BR, van Meurs JBJ, van Vliet-Ostaptchouk JV, Venema A, Völker U, Winkelmann J, Wolffenbuttel BHR, Zhao W, Zheng Y, Estonian Biobank Research Team, Genetics of DNA Methylation Consortium, Loh M, Snieder H, Waldenberger M, Levy D, Akilesh S, Woodward OM, Susztak K, Teumer A, Köttgen A. Nat Commun 12 7173 (2021)
  43. Accurate prediction of functional states of cis-regulatory modules reveals common epigenetic rules in humans and mice. Ni P, Moe J, Su Z. BMC Biol 20 221 (2022)
  44. Circadian clock function does not require the histone methyltransferase MLL3. Baxter M, Poolman T, Cunningham P, Hunter L, Voronkov M, Kitchen GB, Goosey L, Begley N, Kay D, Hespe A, Maidstone R, Loudon ASI, Ray DW. FASEB J 36 e22356 (2022)
  45. Developmental Exposure to Psychostimulant Primes Activity-dependent Gene Induction in Frontal Cortex. Ye Y, Liu Q, Zhang W, Mastwal S, Wang KH. Dev Neurobiol 79 96-108 (2019)
  46. EBF2 Links KMT2D-Mediated H3K4me1 to Suppress Pancreatic Cancer Progression via Upregulating KLLN. Yao B, Xing M, Meng S, Li S, Zhou J, Zhang M, Yang C, Qu S, Jin Y, Yuan H, Zen K, Ma C. Adv Sci (Weinh) 11 e2302037 (2024)
  47. Genetic variation in NDFIP1 modifies the metabolic patterns in immune cells of multiple sclerosis patients. López-Cotarelo P, González-Jiménez A, Agudo-Jiménez T, Abarca-Zabalía J, Aladro Y, Pilo B, Comabella M, Espino-Paisán L, Urcelay E. Sci Rep 11 21371 (2021)
  48. Impact of Multiple Sclerosis Risk Polymorphism rs7665090 on MANBA Activity, Lysosomal Endocytosis, and Lymphocyte Activation. González-Jiménez A, López-Cotarelo P, Agudo-Jiménez T, Casanova I, Silanes CL, Martín-Requero Á, Matesanz F, Urcelay E, Espino-Paisán L. Int J Mol Sci 23 8116 (2022)
  49. Loss of MLL3/4 decouples enhancer H3K4 monomethylation, H3K27 acetylation, and gene activation during embryonic stem cell differentiation. Boileau RM, Chen KX, Blelloch R. Genome Biol 24 41 (2023)
  50. Loss of full-length DNA replication regulator Rif1 in two-cell embryos is associated with zygotic transcriptional activation. Yoshizawa-Sugata N, Yamazaki S, Mita-Yoshida K, Ono T, Nishito Y, Masai H. J Biol Chem 297 101367 (2021)
  51. Specialized RSC: Substrate Specificities for a Conserved Chromatin Remodeler. Hainer SJ, Kaplan CD. Bioessays 42 e2000002 (2020)
  52. Enhancer remodeling drives MLL oncogene-dependent transcriptional dysregulation in leukemia stem cells. Pan F, Iwasaki M, Wu W, Jiang Y, Yang X, Zhu L, Zhao Z, Cleary ML. Blood Adv 7 2504-2519 (2023)
  53. Epigenetic signals that direct cell type-specific interferon beta response in mouse cells. Muckenhuber M, Seufert I, Müller-Ott K, Mallm JP, Klett LC, Knotz C, Hechler J, Kepper N, Erdel F, Rippe K. Life Sci Alliance 6 e202201823 (2023)
  54. Genetic Variants in KIR/HLA-C Genes Are Associated With the Susceptibility to HCV Infection in a High-Risk Chinese Population. Shen C, Ge Z, Dong C, Wang C, Shao J, Cai W, Huang P, Fan H, Li J, Zhang Y, Yue M. Front Immunol 12 632353 (2021)
  55. Lysine methyltransferase Kmt2d regulates naive CD8+ T cell activation-induced survival. Kim J, Nguyen T, Cifello J, Ahmad R, Zhang Y, Yang Q, Lee JE, Li X, Kai Y, De S, Peng W, Ge K, Weng NP. Front Immunol 13 1095140 (2022)
  56. A novel chromatin-remodeling complex variant, dcPBAF, is involved in maintaining transcription in differentiated neurons. Soshnikova NV, Azieva AM, Klimenko NS, Khamidullina AI, Feoktistov AV, Sheynov AA, Brechalov AV, Tatarskiy VV, Georgieva SG. Front Cell Dev Biol 11 1271598 (2023)
  57. BRWD3 promotes KDM5 degradation to maintain H3K4 methylation levels. Han D, Schaffner SH, Davies JP, Benton ML, Plate L, Nordman JT. Proc Natl Acad Sci U S A 120 e2305092120 (2023)
  58. Cell-specific and shared regulatory elements control a multigene locus active in mammary and salivary glands. Lee HK, Willi M, Liu C, Hennighausen L. Nat Commun 14 4992 (2023)
  59. Contact Inhibition of Proliferation Is Accompanied by Expression of the PHF10D Subunit of the Chromatin Remodeling Complex PBAF in Mouse and Human Cell Lines. Simonov YP, Tatarskiy VV, Georgieva SG, Soshnikova NV. Dokl Biochem Biophys (2024)
  60. Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice. Wu X, Liu H, Lian B, Jiang X, Chen C, Tang T, Ding X, Hu J, Zhao S, Zhang S, Wu J. Front Plant Sci 13 1090794 (2022)
  61. H3K4me1 Modification Functions in Caste Differentiation in Honey Bees. Zhang Y, Li Z, He X, Wang Z, Zeng Z. Int J Mol Sci 24 6217 (2023)
  62. Hi-TrAC detects active sub-TADs and reveals internal organizations of super-enhancers. Cao Y, Liu S, Cui K, Tang Q, Zhao K. Nucleic Acids Res 51 6172-6189 (2023)
  63. Histone H3K4me1 strongly activates the DNase I hypersensitive sites in super-enhancers than those in typical enhancers. Kang Y, Kang J, Kim A. Biosci Rep 41 BSR20210691 (2021)
  64. Identification of Regulatory Elements in Primary Sensory Neurons Involved in Trauma-Induced Neuropathic Pain. Stephens KE, Moore C, Vinson DA, White BE, Renfro Z, Zhou W, Ji Z, Ji H, Zhu H, Guan Y, Taverna SD. Mol Neurobiol (2023)
  65. Identification of pleiotropic loci underlying hip bone mineral density and trunk lean mass. Feng GJ, Wei XT, Zhang H, Yang XL, Shen H, Tian Q, Deng HW, Zhang L, Pei YF. J Hum Genet 66 251-260 (2021)
  66. Impaired histone inheritance promotes tumor progression. Tian C, Zhou J, Li X, Gao Y, Wen Q, Kang X, Wang N, Yao Y, Jiang J, Song G, Zhang T, Hu S, Liao J, Yu C, Wang Z, Liu X, Pei X, Chan K, Liu Z, Gan H. Nat Commun 14 3429 (2023)
  67. Intrinsic catalytic properties of histone H3 lysine-9 methyltransferases preserve monomethylation levels under low S-adenosylmethionine. Haws SA, Miller LJ, La Luz DR, Kuznetsov VI, Trievel RC, Craciun G, Denu JM. J Biol Chem 299 104938 (2023)
  68. Polymorphisms of the GCLC Gene Are Novel Genetic Markers for Susceptibility to Psoriasis Associated with Alcohol Abuse and Cigarette Smoking. Efanova E, Bushueva O, Saranyuk R, Surovtseva A, Churnosov M, Solodilova M, Polonikov A. Life (Basel) 13 1316 (2023)
  69. Prognostic hub gene CBX2 drives a cancer stem cell-like phenotype in HCC revealed by multi-omics and multi-cohorts. Meng Q, Zhou Q, Chen X, Chen J. Aging (Albany NY) 15 12817-12851 (2023)
  70. Role of Non-Coding Regulatory Elements in the Control of GR-Dependent Gene Expression. Borczyk M, Zieba M, Korostyński M, Piechota M. Int J Mol Sci 22 4258 (2021)
  71. The super-enhancer repertoire in porcine liver. Zhang Y, Zhang J, Wang C, Dai H, Du X, Li Q, Pan Z. J Anim Sci 101 skad056 (2023)