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Dido3 PHD modulates cell differentiation and division.

Gatchalian J, Fütterer A, Rothbart SB, Tong Q, Rincon-Arano H, Sánchez de Diego A, Groudine M, Strahl BD, Martínez-A C, van Wely KH, Kutateladze TG
Cell Rep 4 148-58 (2013)
Cited: 38 times
EuropePMC logo PMID: 23831028

Abstract

Death Inducer Obliterator 3 (Dido3) is implicated in the maintenance of stem cell genomic stability and tumorigenesis. Here, we show that Dido3 regulates the expression of stemness genes in embryonic stem cells through its plant homeodomain (PHD) finger. Binding of Dido3 PHD to histone H3K4me3 is disrupted by threonine phosphorylation that triggers Dido3 translocation from chromatin to the mitotic spindle. The crystal structure of Dido3 PHD in complex with H3K4me3 reveals an atypical aromatic-cage-like binding site that contains a histidine residue. Biochemical, structural, and mutational analyses of the binding mechanism identified the determinants of specificity and affinity and explained the inability of homologous PHF3 to bind H3K4me3. Together, our findings reveal a link between the transcriptional control in embryonic development and regulation of cell division.

Reviews - 4l7x mentioned but not cited (1)

  1. Atypical histone targets of PHD fingers. Black JC, Kutateladze TG. J Biol Chem 299 104601 (2023)

Articles - 4l7x mentioned but not cited (6)

  1. Dido3 PHD modulates cell differentiation and division. Gatchalian J, Fütterer A, Rothbart SB, Tong Q, Rincon-Arano H, Sánchez de Diego A, Groudine M, Strahl BD, Martínez-A C, van Wely KH, Kutateladze TG. Cell Rep 4 148-158 (2013)
  2. Chromatin condensation and recruitment of PHD finger proteins to histone H3K4me3 are mutually exclusive. Gatchalian J, Gallardo CM, Shinsky SA, Ospina RR, Liendo AM, Krajewski K, Klein BJ, Andrews FH, Strahl BD, M van Wely KH, Kutateladze TG. Nucleic Acids Res. 44 6102-6112 (2016)
  3. Regulation of Methyllysine Readers through Phosphorylation. Andrews FH, Gatchalian J, Krajewski K, Strahl BD, Kutateladze TG. ACS Chem. Biol. 11 547-553 (2016)
  4. A Unique pH-Dependent Recognition of Methylated Histone H3K4 by PPS and DIDO. Tencer AH, Gatchalian J, Klein BJ, Khan A, Zhang Y, Strahl BD, van Wely KHM, Kutateladze TG. Structure 25 1530-1539.e3 (2017)
  5. Contributions of methionine to recognition of trimethyllysine in aromatic cage of PHD domains: implications of polarizability, hydrophobicity, and charge on binding. Albanese KI, Waters ML. Chem Sci 12 8900-8908 (2021)
  6. Searching for methyllysine-binding aromatic cages. Vann KR, Vishweshwaraiah YL, Dokholyan NV, Kutateladze TG. Biochem J 478 3613-3619 (2021)


Reviews citing this publication (5)

  1. Interpreting the language of histone and DNA modifications. Rothbart SB, Strahl BD. Biochim. Biophys. Acta 1839 627-643 (2014)
  2. Hitting the 'mark': interpreting lysine methylation in the context of active transcription. Wozniak GG, Strahl BD. Biochim. Biophys. Acta 1839 1353-1361 (2014)
  3. Towards understanding methyllysine readout. Musselman CA, Khorasanizadeh S, Kutateladze TG. Biochim Biophys Acta 1839 686-693 (2014)
  4. Functional proteomics of the epigenetic regulators ASXL1, ASXL2 and ASXL3: a convergence of proteomics and epigenetics for translational medicine. Katoh M. Expert Rev Proteomics 12 317-328 (2015)
  5. SPOC domain proteins in health and disease. Appel LM, Benedum J, Engl M, Platzer S, Schleiffer A, Strobl X, Slade D. Genes Dev 37 140-170 (2023)

Articles citing this publication (26)

  1. Dido3-dependent HDAC6 targeting controls cilium size. Sánchez de Diego A, Alonso Guerrero A, Martínez-A C, van Wely KH. Nat Commun 5 3500 (2014)
  2. Structural plasticity of methyllysine recognition by the tandem tudor domain of 53BP1. Tong Q, Cui G, Botuyan MV, Rothbart SB, Hayashi R, Musselman CA, Singh N, Appella E, Strahl BD, Mer G, Kutateladze TG. Structure 23 312-321 (2015)
  3. Structures of RNA polymerase II complexes with Bye1, a chromatin-binding PHF3/DIDO homologue. Kinkelin K, Wozniak GG, Rothbart SB, Lidschreiber M, Strahl BD, Cramer P. Proc. Natl. Acad. Sci. U.S.A. 110 15277-15282 (2013)
  4. PHF13 is a molecular reader and transcriptional co-regulator of H3K4me2/3. Chung HR, Xu C, Fuchs A, Mund A, Lange M, Staege H, Schubert T, Bian C, Dunkel I, Eberharter A, Regnard C, Klinker H, Meierhofer D, Cozzuto L, Winterpacht A, Di Croce L, Min J, Will H, Kinkley S. Elife 5 (2016)
  5. The essential role of acetyllysine binding by the YEATS domain in transcriptional regulation. Andrews FH, Shanle EK, Strahl BD, Kutateladze TG. Transcription 7 14-20 (2016)
  6. Tandem Histone-Binding Domains Enhance the Activity of a Synthetic Chromatin Effector. Tekel SJ, Vargas DA, Song L, LaBaer J, Caplan MR, Haynes KA. ACS Synth Biol 7 842-852 (2018)
  7. The death-inducer obliterator 1 (Dido1) gene regulates embryonic stem cell self-renewal. Liu Y, Kim H, Liang J, Lu W, Ouyang B, Liu D, Songyang Z. J. Biol. Chem. 289 4778-4786 (2014)
  8. PHD and TFIIS-Like domains of the Bye1 transcription factor determine its multivalent genomic distribution. Pinskaya M, Ghavi-Helm Y, Mariotte-Labarre S, Morillon A, Soutourina J, Werner M. PLoS ONE 9 e102464 (2014)
  9. Molecular structures guide the engineering of chromatin. Tekel SJ, Haynes KA. Nucleic Acids Res. 45 7555-7570 (2017)
  10. Analysis of Histone Antibody Specificity with Peptide Microarrays. Cornett EM, Dickson BM, Rothbart SB. J Vis Exp (2017)
  11. DIDO as a Switchboard that Regulates Self-Renewal and Differentiation in Embryonic Stem Cells. Fütterer A, de Celis J, Navajas R, Almonacid L, Gutiérrez J, Talavera-Gutiérrez A, Pacios-Bras C, Bernascone I, Martin-Belmonte F, Martinéz-A C. Stem Cell Reports 8 1062-1075 (2017)
  12. Mechanically transduced immunosorbent assay to measure protein-protein interactions. Petell CJ, Randene K, Pappas M, Sandoval D, Strahl BD, Harrison JS, Steimel JP. Elife 10 e67525 (2021)
  13. Role of DIDO1 in Progression of Esophageal Squamous Cell Carcinoma. Forghanifard MM, Naeimi Khorasanizadeh P, Abbaszadegan MR, Javdani Mallak A, Moghbeli M. J Gastrointest Cancer 51 83-87 (2020)
  14. Impaired stem cell differentiation and somatic cell reprogramming in DIDO3 mutants with altered RNA processing and increased R-loop levels. Fütterer A, Talavera-Gutiérrez A, Pons T, de Celis J, Gutiérrez J, Domínguez Plaza V, Martínez-A C. Cell Death Dis 12 637 (2021)
  15. Interplay between splicing and transcriptional pausing exerts genome-wide control over alternative polyadenylation. Mora Gallardo C, Sánchez de Diego A, Martínez-A C, van Wely KHM. Transcription 12 55-71 (2021)
  16. The SPOC domain is a phosphoserine binding module that bridges transcription machinery with co- and post-transcriptional regulators. Appel LM, Franke V, Benedum J, Grishkovskaya I, Strobl X, Polyansky A, Ammann G, Platzer S, Neudolt A, Wunder A, Walch L, Kaiser S, Zagrovic B, Djinovic-Carugo K, Akalin A, Slade D. Nat Commun 14 166 (2023)
  17. The ZZ domain of p300 mediates specificity of the adjacent HAT domain for histone H3. Zhang Y, Xue Y, Shi J, Ahn J, Mi W, Ali M, Wang X, Klein BJ, Wen H, Li W, Shi X, Kutateladze TG. Nat. Struct. Mol. Biol. 25 841-849 (2018)
  18. The role of the PZP domain of AF10 in acute leukemia driven by AF10 translocations. Klein BJ, Deshpande A, Cox KL, Xuan F, Zandian M, Barbosa K, Khanal S, Tong Q, Zhang Y, Zhang P, Sinha A, Bohlander SK, Shi X, Wen H, Poirier MG, Deshpande AJ, Kutateladze TG. Nat Commun 12 4130 (2021)
  19. Dido3-dependent SFPQ recruitment maintains efficiency in mammalian alternative splicing. Mora Gallardo C, Sánchez de Diego A, Gutiérrez Hernández J, Talavera-Gutiérrez A, Fischer T, Martínez-A C, van Wely KHM. Nucleic Acids Res. 47 5381-5394 (2019)
  20. Histone H3 N-terminal mimicry drives a novel network of methyl-effector interactions. Chen J, Horton J, Sagum C, Zhou J, Cheng X, Bedford MT. Biochem J 478 1943-1958 (2021)
  21. Improved methods for the detection of histone interactions with peptide microarrays. Petell CJ, Pham AT, Skela J, Strahl BD. Sci Rep 9 6265 (2019)
  22. Phosphorylation of H3-Thr3 by Haspin Is Required for Primary Cilia Regulation. Quadri R, Sertic S, Ghilardi A, Rondelli D, Gallo GR, Del Giacco L, Muzi-Falconi M. Int J Mol Sci 22 7753 (2021)
  23. Release of Histone H3K4-reading transcription factors from chromosomes in mitosis is independent of adjacent H3 phosphorylation. Harris RJ, Heer M, Levasseur MD, Cartwright TN, Weston B, Mitchell JL, Coxhead JM, Gaughan L, Prendergast L, Rico D, Higgins JMG. Nat Commun 14 7243 (2023)
  24. The Eaf3 chromodomain acts as a pH sensor for gene expression by altering its binding affinity for histone methylated-lysine residues. Okuda M, Nishimura Y. Biosci Rep 40 (2020)
  25. The PHD finger of Spp1 mediates histone modification cross-talk. Musselman CA, Kutateladze TG. Biochem J 476 2351-2354 (2019)
  26. The SPOC proteins DIDO3 and PHF3 co-regulate gene expression and neuronal differentiation. Benedum J, Franke V, Appel LM, Walch L, Bruno M, Schneeweiss R, Gruber J, Oberndorfer H, Frank E, Strobl X, Polyansky A, Zagrovic B, Akalin A, Slade D. Nat Commun 14 7912 (2023)


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