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Reader domain specificity and lysine demethylase-4 family function.

Su Z, Wang F, Lee JH, Stephens KE, Papazyan R, Voronina E, Krautkramer KA, Raman A, Thorpe JJ, Boersma MD, Kuznetsov VI, Miller MD, Taverna SD, Phillips GN, Denu JM
Nat Commun 7 13387 (2016)
Related entries: 4uc4, 5d6x, 5d6y

Cited: 26 times
EuropePMC logo PMID: 27841353

Abstract

The KDM4 histone demethylases are conserved epigenetic regulators linked to development, spermatogenesis and tumorigenesis. However, how the KDM4 family targets specific chromatin regions is largely unknown. Here, an extensive histone peptide microarray analysis uncovers trimethyl-lysine histone-binding preferences among the closely related KDM4 double tudor domains (DTDs). KDM4A/B DTDs bind strongly to H3K23me3, a poorly understood histone modification recently shown to be enriched in meiotic chromatin of ciliates and nematodes. The 2.28 Å co-crystal structure of KDM4A-DTD in complex with H3K23me3 peptide reveals key intermolecular interactions for H3K23me3 recognition. Furthermore, analysis of the 2.56 Å KDM4B-DTD crystal structure pinpoints the underlying residues required for exclusive H3K23me3 specificity, an interaction supported by in vivo co-localization of KDM4B and H3K23me3 at heterochromatin in mammalian meiotic and newly postmeiotic spermatocytes. In vitro demethylation assays suggest H3K23me3 binding by KDM4B stimulates H3K36 demethylation. Together, these results provide a possible mechanism whereby H3K23me3-binding by KDM4B directs localized H3K36 demethylation during meiosis and spermatogenesis.

Articles - 5d6w mentioned but not cited (1)

  1. Reader domain specificity and lysine demethylase-4 family function. Su Z, Wang F, Lee JH, Stephens KE, Papazyan R, Voronina E, Krautkramer KA, Raman A, Thorpe JJ, Boersma MD, Kuznetsov VI, Miller MD, Taverna SD, Phillips GN, Denu JM. Nat Commun 7 13387 (2016)


Reviews citing this publication (9)

  1. Choose and Use Your Chemical Probe Wisely to Explore Cancer Biology. Blagg J, Workman P. Cancer Cell 32 9-25 (2017)
  2. KDM4B: A Nail for Every Hammer? Wilson C, Krieg AJ. Genes (Basel) 10 E134 (2019)
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  7. Control of Intra-Thymic αβ T Cell Selection and Maturation by H3K27 Methylation and Demethylation. Bosselut R. Front Immunol 10 688 (2019)
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  1. Methylglyoxal-derived posttranslational arginine modifications are abundant histone marks. Galligan JJ, Wepy JA, Streeter MD, Kingsley PJ, Mitchener MM, Wauchope OR, Beavers WN, Rose KL, Wang T, Spiegel DA, Marnett LJ. Proc Natl Acad Sci U S A 115 9228-9233 (2018)
  2. EBS is a bivalent histone reader that regulates floral phase transition in Arabidopsis. Yang Z, Qian S, Scheid RN, Lu L, Chen X, Liu R, Du X, Lv X, Boersma MD, Scalf M, Smith LM, Denu JM, Du J, Zhong X. Nat Genet 50 1247-1253 (2018)
  3. Dual recognition of H3K4me3 and H3K27me3 by a plant histone reader SHL. Qian S, Lv X, Scheid RN, Lu L, Yang Z, Chen W, Liu R, Boersma MD, Denu JM, Zhong X, Du J. Nat Commun 9 2425 (2018)
  4. Histone peptide microarray screen of chromo and Tudor domains defines new histone lysine methylation interactions. Shanle EK, Shinsky SA, Bridgers JB, Bae N, Sagum C, Krajewski K, Rothbart SB, Bedford MT, Strahl BD. Epigenetics Chromatin 10 12 (2017)
  5. Cross-talk between Lysine-Modifying Enzymes Controls Site-Specific DNA Amplifications. Mishra S, Van Rechem C, Pal S, Clarke TL, Chakraborty D, Mahan SD, Black JC, Murphy SE, Lawrence MS, Daniels DL, Whetstine JR. Cell 174 803-817.e16 (2018)
  6. Histone H3 binding to the PHD1 domain of histone demethylase KDM5A enables active site remodeling. Longbotham JE, Chio CM, Dharmarajan V, Trnka MJ, Torres IO, Goswami D, Ruiz K, Burlingame AL, Griffin PR, Fujimori DG. Nat Commun 10 94 (2019)
  7. Caenorhabditis elegans nuclear RNAi factor SET-32 deposits the transgenerational histone modification, H3K23me3. Schwartz-Orbach L, Zhang C, Sidoli S, Amin R, Kaur D, Zhebrun A, Ni J, Gu SG. Elife 9 e54309 (2020)
  8. Inhibition of the histone demethylase KDM4B leads to activation of KDM1A, attenuates bacterial-induced pro-inflammatory cytokine release, and reduces osteoclastogenesis. Kirkpatrick JE, Kirkwood KL, Woster PM. Epigenetics 13 557-572 (2018)
  9. Heterozygous Variants in KDM4B Lead to Global Developmental Delay and Neuroanatomical Defects. Duncan AR, Vitobello A, Collins SC, Vancollie VE, Lelliott CJ, Rodan L, Shi J, Seman AR, Agolini E, Novelli A, Prontera P, Guillen Sacoto MJ, Santiago-Sim T, Trimouille A, Goizet C, Nizon M, Bruel AL, Philippe C, Grant PE, Wojcik MH, Stoler J, Genetti CA, van Dooren MF, Maas SM, Alders M, Faivre L, Sorlin A, Yoon G, Yalcin B, Agrawal PB. Am J Hum Genet 107 1170-1177 (2020)
  10. Kinome-Wide RNAi Screen Uncovers Role of Ballchen in Maintenance of Gene Activation by Trithorax Group in Drosophila. Khan MHF, Akhtar J, Umer Z, Shaheen N, Shaukat A, Munir MS, Mithani A, Anwar S, Tariq M. Front Cell Dev Biol 9 637873 (2021)
  11. Trimethylacetic Anhydride-Based Derivatization Facilitates Quantification of Histone Marks at the MS1 Level. Kuchaříková H, Dobrovolná P, Lochmanová G, Zdráhal Z. Mol Cell Proteomics 20 100114 (2021)
  12. A cyclin D1 intrinsically disordered domain accesses modified histone motifs to govern gene transcription. Jiao X, Di Sante G, Casimiro MC, Tantos A, Ashton AW, Li Z, Quach Y, Bhargava D, Di Rocco A, Pupo C, Crosariol M, Lazar T, Tompa P, Wang C, Yu Z, Zhang Z, Aldaaysi K, Vadlamudi R, Mann M, Skordalakes E, Kossenkov A, Du Y, Pestell RG. Oncogenesis 13 4 (2024)
  13. Engineering human JMJD2A tudor domains for an improved understanding of histone peptide recognition. Parkinson J, Hard R, Ainsworth R, Wang W. Proteins 91 32-46 (2023)
  14. Genotype-phenotype correlation study of structural abnormalities in a fetal brain caused by a novel KDM4B variant. Zhao X, Li X, Yu M, Jia JA, Tian R, Zhu F. Mol Biol Rep 51 188 (2024)
  15. KDM4 Demethylases: Structure, Function, and Inhibitors. Jiang Y, Liu L, Yang ZQ. Adv Exp Med Biol 1433 87-111 (2023)
  16. Novel 17-bp Deletion in KDM1B Gene is Significantly Associated with Testis Weight in Male Piglet. Cui Y, Hu T, Chen R, Yu S, Dong W, Lv X, Pan C. Anim Biotechnol 29 252-258 (2018)


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