Conserved Structure and Evolution of DPF Domain of PHF10—The Specific Subunit of PBAF Chromatin Remodeling Complex
Abstract
:1. Introduction
2. PHF10 Gene Is Essential for Mammalian Development and Encodes Four Evolutionary Conserved Isoforms
3. The Role of PHF10 Isoforms in Gene Transcription
4. Structure of the PHF10 DPF Domain: Similar, but Different
5. DPF Domain of PHF10 Differentiates H3K14ac and H3K4me3 Active Chromatin Marks
6. Evolution of the PHF10 Protein and Its DPF Domain
7. Conclusions
Supplementary Materials
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Jain, K.; Fraser, C.S.; Marunde, M.R.; Parker, M.M.; Sagum, C.; Burg, J.M.; Hall, N.; Popova, I.K.; Rodriguez, K.L.; Vaidya, A.; et al. Characterization of the Plant Homeodomain (PHD) Reader Family for Their Histone Tail Interactions. Epigenetics Chromatin 2020, 13, 3. [Google Scholar] [CrossRef]
- Morrison, E.A.; Musselman, C.A. The Role of PHD Fingers in Chromatin Signaling: Mechanisms and Functional Consequences of the Recognition of Histone and Non-histone Targets. In Chromatin Signaling and Diseases; Academic Press: London, UK, 2016; pp. 127–147. [Google Scholar]
- Soshnikova, N.V.; Sheynov, A.A.; Tatarskiy, E.V.; Georgieva, S.G. The DPF Domain as a Unique Structural Unit Participating in Transcriptional Activation, Cell Differentiation, and Malignant Transformation. Acta Nat. 2020, 12, 57–65. [Google Scholar] [CrossRef]
- Yang, X.-J. MOZ and MORF Acetyltransferases: Molecular Interaction, Animal Development and Human Disease. Biochim. Biophys. Acta 2015, 1853, 1818–1826. [Google Scholar] [CrossRef] [Green Version]
- Huang, F.; Abmayr, S.M.; Workman, J.L. Regulation of KAT6 Acetyltransferases and Their Roles in Cell Cycle Progression, Stem Cell Maintenance, and Human Disease. Mol. Cell. Biol. 2016, 36, 1900–1907. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ribeiro-Silva, C.; Vermeulen, W.; Lans, H. SWI/SNF: Complex Complexes in Genome Stability and Cancer. DNA Repair 2019, 77, 87–95. [Google Scholar] [CrossRef] [PubMed]
- Toto, P.C.; Puri, P.L.; Albini, S. SWI/SNF-Directed Stem Cell Lineage Specification: Dynamic Composition Regulates Specific Stages of Skeletal Myogenesis. Cell. Mol. Life Sci. 2016, 73, 3887–3896. [Google Scholar] [CrossRef]
- Sokpor, G.; Xie, Y.; Rosenbusch, J.; Tuoc, T. Chromatin Remodeling BAF (SWI/SNF) Complexes in Neural Development and Disorders. Front. Mol. Neurosci. 2017, 10, 243. [Google Scholar] [CrossRef] [Green Version]
- Centore, R.C.; Sandoval, G.J.; Soares, L.M.M.; Kadoch, C.; Chan, H.M. Mammalian SWI/SNF Chromatin Remodeling Complexes: Emerging Mechanisms and Therapeutic Strategies. Trends Genet. 2020, 36, 936–950. [Google Scholar] [CrossRef]
- Huber, F.M.; Greenblatt, S.M.; Davenport, A.M.; Martinez, C.; Xu, Y.; Vu, L.P.; Nimer, S.D.; Hoelz, A. Histone-Binding of DPF2 Mediates Its Repressive Role in Myeloid Differentiation. Proc. Natl. Acad. Sci. USA 2017, 114, 6016–6021. [Google Scholar] [CrossRef] [Green Version]
- Local, A.; Huang, H.; Albuquerque, C.P.; Singh, N.; Lee, A.Y.; Wang, W.; Wang, C.; Hsia, J.E.; Shiau, A.K.; Ge, K.; et al. Identification of H3K4me1-Associated Proteins at Mammalian Enhancers. Nat. Genet. 2018, 50, 73–82. [Google Scholar] [CrossRef]
- Zeng, L.; Zhang, Q.; Li, S.; Plotnikov, A.N.; Walsh, M.J.; Zhou, M.-M. Mechanism and Regulation of Acetylated Histone Binding by the Tandem PHD Finger of DPF3b. Nature 2010, 466, 258–262. [Google Scholar] [CrossRef] [Green Version]
- Xiong, X.; Panchenko, T.; Yang, S.; Zhao, S.; Yan, P.; Zhang, W.; Xie, W.; Li, Y.; Zhao, Y.; Allis, C.D.; et al. Selective Recognition of Histone Crotonylation by Double PHD Fingers of MOZ and DPF2. Nat. Chem. Biol. 2016, 12, 1111–1118. [Google Scholar] [CrossRef] [Green Version]
- Dreveny, I.; Deeves, S.E.; Fulton, J.; Yue, B.; Messmer, M.; Bhattacharya, A.; Collins, H.M.; Heery, D.M. The Double PHD Finger Domain of MOZ/MYST3 Induces α-Helical Structure of the Histone H3 Tail to Facilitate Acetylation and Methylation Sampling and Modification. Nucleic Acids Res. 2014, 42, 822–835. [Google Scholar] [CrossRef] [Green Version]
- Klein, B.J.; Simithy, J.; Wang, X.; Ahn, J.; Andrews, F.H.; Zhang, Y.; Côté, J.; Shi, X.; Garcia, B.A.; Kutateladze, T.G. Recognition of Histone H3K14 Acylation by MORF. Structure 2017, 25, 650–654. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Klein, B.J.; Jang, S.M.; Lachance, C.; Mi, W.; Lyu, J.; Sakuraba, S.; Krajewski, K.; Wang, W.W.; Sidoli, S.; Liu, J.; et al. Histone H3K23-Specific Acetylation by MORF Is Coupled to H3K14 Acylation. Nat. Commun. 2019, 10, 4724. [Google Scholar] [CrossRef]
- Brechalov, A.V.; Georgieva, S.G.; Soshnikova, N.V. Mammalian Cells Contain Two Functionally Distinct PBAF Complexes Incorporating Different Isoforms of PHF10 Signature Subunit. Cell Cycle 2014, 13, 1970–1979. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tatarskiy, V.V.; Simonov, Y.P.; Shcherbinin, D.S.; Brechalov, A.V.; Georgieva, S.G.; Soshnikova, N.V. Stability of the PHF10 Subunit of PBAF Signature Module Is Regulated by Phosphorylation: Role of β-TrCP. Sci. Rep. 2017, 7, 5645. [Google Scholar] [CrossRef] [Green Version]
- Viryasova, G.M.; Tatarskiy, V.V.; Sheynov, A.A.; Tatarskiy, E.V.; Sud’ina, G.F.; Georgieva, S.G.; Soshnikova, N.V. PBAF Lacking PHD Domains Maintains Transcription in Human Neutrophils. Biochim. Biophys. Acta Mol. Cell Res. 2019, 1866, 118525. [Google Scholar] [CrossRef]
- Mittnenzweig, M.; Mayshar, Y.; Cheng, S.; Ben-Yair, R.; Hadas, R.; Rais, Y.; Chomsky, E.; Reines, N.; Uzonyi, A.; Lumerman, L.; et al. A Single-Embryo, Single-Cell Time-Resolved Model for Mouse Gastrulation. Cell 2021, 184, 2825–2842. [Google Scholar] [CrossRef]
- Krasteva, V.; Crabtree, G.R.; Lessard, J.A. The BAF45a/PHF10 Subunit of SWI/SNF-like Chromatin Remodeling Complexes Is Essential for Hematopoietic Stem Cell Maintenance. Exp. Hematol. 2017, 48, 58–71. [Google Scholar] [CrossRef]
- Uhlén, M.; Fagerberg, L.; Hallström, B.M.; Lindskog, C.; Oksvold, P.; Mardinoglu, A.; Sivertsson, Å.; Kampf, C.; Sjöstedt, E.; Asplund, A.; et al. Proteomics. Tissue-Based Map of the Human Proteome. Science 2015, 347, 1260419. [Google Scholar] [CrossRef]
- Sheynov, A.A.; Tatarskiy, V.V.; Azieva, A.M.; Georgieva, S.G.; Soshnikova, N.V. Different Functions of PHF10 Isoforms–Subunits of the PBAF Chromatin Remodeling Complex. Vavilovskii Zhurnal Genet. Selektsii 2019, 23, 184–189. [Google Scholar] [CrossRef]
- Soshnikova, N.V.; Simonov, Y.P.; Brechalov, A.V.; Portseva, T.N.; Pankratova, E.V.; Georgieva, S.G. The Level of the Phf10 Protein, a PBAF Chromatin-Remodeling Complex Subunit, Correlates with the Mts1/S100A4 Expression in Human Cancer Cell Lines. Dokl. Biochem. Biophys. 2016, 467, 162–164. [Google Scholar] [CrossRef]
- Soshnikova, N.V.; Tatarskiy, E.V.; Tatarskiy, V.V.; Klimenko, N.S.; Shtil, A.A.; Nikiforov, M.A.; Georgieva, S.G. PHF10 Subunit of PBAF Complex Mediates Transcriptional Activation by MYC. Oncogene 2021, 1–10. [Google Scholar]
- Banga, S.S.; Peng, L.; Dasgupta, T.; Palejwala, V.; Ozer, H.L. PHF10 Is Required for Cell Proliferation in Normal and SV40-Immortalized Human Fibroblast Cells. Cytogenet. Genome Res. 2009, 126, 227–242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lessard, J.; Wu, J.I.; Ranish, J.A.; Wan, M.; Winslow, M.M.; Staahl, B.T.; Wu, H.; Aebersold, R.; Graef, I.A.; Crabtree, G.R. An Essential Switch in Subunit Composition of a Chromatin Remodeling Complex during Neural Development. Neuron 2007, 55, 201–215. [Google Scholar] [CrossRef] [Green Version]
- Dang, C.V. MYC on the Path to Cancer. Cell 2012, 149, 22–35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Poole, C.J.; van Riggelen, J. MYC-Master Regulator of the Cancer Epigenome and Transcriptome. Genes 2017, 8, 142. [Google Scholar] [CrossRef]
- Ishizaka, A.; Mizutani, T.; Kobayashi, K.; Tando, T.; Sakurai, K.; Fujiwara, T.; Iba, H. Double Plant Homeodomain (PHD) Finger Proteins DPF3a and -3b Are Required as Transcriptional Co-Activators in SWI/SNF Complex-Dependent Activation of NF-κB RelA/p50 Heterodimer. J. Biol. Chem. 2012, 287, 11924–11933. [Google Scholar] [CrossRef] [Green Version]
- McMahon, S.B.; Wood, M.A.; Cole, M.D. The Essential Cofactor TRRAP Recruits the Histone Acetyltransferase hGCN5 to c-Myc. Mol. Cell. Biol. 2000, 20, 556–562. [Google Scholar] [CrossRef] [Green Version]
- Frank, S.R.; Parisi, T.; Taubert, S.; Fernandez, P.; Fuchs, M.; Chan, H.-M.; Livingston, D.M.; Amati, B. MYC Recruits the TIP60 Histone Acetyltransferase Complex to Chromatin. EMBO Rep. 2003, 4, 575–580. [Google Scholar] [CrossRef]
- Faiola, F.; Liu, X.; Lo, S.; Pan, S.; Zhang, K.; Lymar, E.; Farina, A.; Martinez, E. Dual Regulation of c-Myc by p300 via Acetylation-Dependent Control of Myc Protein Turnover and Coactivation of Myc-Induced Transcription. Mol. Cell. Biol. 2005, 25, 10220–10234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mukherjee, S.P.; Behar, M.; Birnbaum, H.A.; Hoffmann, A.; Wright, P.E.; Ghosh, G. Analysis of the RelA:CBP/p300 Interaction Reveals Its Involvement in NF-κB-Driven Transcription. PLoS Biol. 2013, 11, e1001647. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ogryzko, V.V.; Schiltz, R.L.; Russanova, V.; Howard, B.H.; Nakatani, Y. The Transcriptional Coactivators p300 and CBP Are Histone Acetyltransferases. Cell 1996, 87, 953–959. [Google Scholar] [CrossRef] [Green Version]
- Verdin, E.; Ott, M. 50 Years of Protein Acetylation: From Gene Regulation to Epigenetics, Metabolism and beyond. Nat. Rev. Mol. Cell Biol. 2015, 16, 258–264. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Zhao, A.; Tempel, W.; Loppnau, P.; Liu, Y. Crystal Structure of DPF3b in Complex with an Acetylated Histone Peptide. J. Struct. Biol. 2016, 195, 365–372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qiu, Y.; Liu, L.; Zhao, C.; Han, C.; Li, F.; Zhang, J.; Wang, Y.; Li, G.; Mei, Y.; Wu, M.; et al. Combinatorial Readout of Unmodified H3R2 and Acetylated H3K14 by the Tandem PHD Finger of MOZ Reveals a Regulatory Mechanism for HOXA9 Transcription. Genes Dev. 2012, 26, 1376–1391. [Google Scholar] [CrossRef] [Green Version]
- Kirmizis, A.; Santos-Rosa, H.; Penkett, C.J.; Singer, M.A.; Vermeulen, M.; Mann, M.; Bähler, J.; Green, R.D.; Kouzarides, T. Arginine Methylation at Histone H3R2 Controls Deposition of H3K4 Trimethylation. Nature 2007, 449, 928–932. [Google Scholar] [CrossRef] [Green Version]
- Guccione, E.; Bassi, C.; Casadio, F.; Martinato, F.; Cesaroni, M.; Schuchlautz, H.; Lüscher, B.; Amati, B. Methylation of Histone H3R2 by PRMT6 and H3K4 by an MLL Complex Are Mutually Exclusive. Nature 2007, 449, 933–937. [Google Scholar] [CrossRef]
- Ali, M.; Yan, K.; Lalonde, M.-E.; Degerny, C.; Rothbart, S.B.; Strahl, B.D.; Côté, J.; Yang, X.-J.; Kutateladze, T.G. Tandem PHD Fingers of MORF/MOZ Acetyltransferases Display Selectivity for Acetylated Histone H3 and Are Required for the Association with Chromatin. J. Mol. Biol. 2012, 424, 328–338. [Google Scholar] [CrossRef] [Green Version]
- Torrance, G.M.; Leader, D.P.; Gilbert, D.R.; Milner-White, E.J. A Novel Main Chain Motif in Proteins Bridged by Cationic Groups: The Niche. J. Mol. Biol. 2009, 385, 1076–1086. [Google Scholar] [CrossRef]
- Lange, M.; Kaynak, B.; Forster, U.B.; Tönjes, M.; Fischer, J.J.; Grimm, C.; Schlesinger, J.; Just, S.; Dunkel, I.; Krueger, T.; et al. Regulation of Muscle Development by DPF3, a Novel Histone Acetylation and Methylation Reader of the BAF Chromatin Remodeling Complex. Genes Dev. 2008, 22, 2370–2384. [Google Scholar] [CrossRef] [Green Version]
- Smith, E.; Shilatifard, A. Enhancer Biology and Enhanceropathies. Nat. Struct. Mol. Biol. 2014, 21, 210–219. [Google Scholar] [CrossRef]
- Efremov, R.G.; Chugunov, A.O.; Pyrkov, T.V.; Priestle, J.P.; Arseniev, A.S.; Jacoby, E. Molecular Lipophilicity in Protein Modeling and Drug Design. Curr. Med. Chem. 2007, 14, 393–415. [Google Scholar] [CrossRef]
- Pyrkov, T.V.; Chugunov, A.O.; Krylov, N.A.; Nolde, D.E.; Efremov, R.G. PLATINUM: A Web Tool for Analysis of Hydrophobic/hydrophilic Organization of Biomolecular Complexes. Bioinformatics 2009, 25, 1201–1202. [Google Scholar] [CrossRef]
- Black, J.C.; Van Rechem, C.; Whetstine, J.R. Histone Lysine Methylation Dynamics: Establishment, Regulation, and Biological Impact. Mol. Cell 2012, 48, 491–507. [Google Scholar] [CrossRef] [Green Version]
- Karmodiya, K.; Krebs, A.R.; Oulad-Abdelghani, M.; Kimura, H.; Tora, L. H3K9 and H3K14 Acetylation Co-Occur at Many Gene Regulatory Elements, While H3K14ac Marks a Subset of Inactive Inducible Promoters in Mouse Embryonic Stem Cells. BMC Genomics 2012, 13, 424. [Google Scholar] [CrossRef] [Green Version]
- Regadas, I.; Dahlberg, O.; Vaid, R.; Ho, O.; Belikov, S.; Dixit, G.; Deindl, S.; Wen, J.; Mannervik, M. A Unique Histone 3 Lysine 14 Chromatin Signature Underlies Tissue-Specific Gene Regulation. Mol. Cell 2021, 81, 1766–1780. [Google Scholar] [CrossRef] [PubMed]
- Huang, X.; Gao, X.; Li, W.; Jiang, S.; Li, R.; Hong, H.; Zhao, C.; Zhou, P.; Chen, H.; Bo, X.; et al. Stable H3K4me3 Is Associated with Transcription Initiation during Early Embryo Development. Bioinformatics 2019, 35, 3931–3936. [Google Scholar] [CrossRef] [PubMed]
- Hughes, A.L.; Kelley, J.R.; Klose, R.J. Understanding the Interplay between CpG Island-Associated Gene Promoters and H3K4 Methylation. Biochim. Biophys. Acta (BBA)-Gene Regul. Mech. 2020, 1863, 194567. [Google Scholar] [CrossRef] [PubMed]
- Howe, F.S.; Fischl, H.; Murray, S.C.; Mellor, J. Is H3K4me3 Instructive for Transcription Activation? Bioessays 2017, 39, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.-J.; Ullah, M. MOZ and MORF, Two Large MYSTic HATs in Normal and Cancer Stem Cells. Oncogene 2007, 26, 5408–5419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burki, F. The Eukaryotic Tree of Life from a Global Phylogenomic Perspective. Cold Spring Harb. Perspect. Biol. 2014, 6, a016147. [Google Scholar] [CrossRef] [PubMed]
- Vogel, C.; Teichmann, S.A.; Pereira-Leal, J. The Relationship between Domain Duplication and Recombination. J. Mol. Biol. 2005, 346, 355–365. [Google Scholar] [CrossRef] [PubMed]
- Bagowski, C.P.; Bruins, W.; Te Velthuis, A.J.W. The Nature of Protein Domain Evolution: Shaping the Interaction Network. Curr. Genomics 2010, 11, 368–376. [Google Scholar] [CrossRef] [Green Version]
- Björklund, A.K.; Ekman, D.; Elofsson, A. Expansion of Protein Domain Repeats. PLoS Comput. Biol. 2006, 2, e114. [Google Scholar] [CrossRef] [Green Version]
Protein | Length | PDB | Peptide (Length) | References |
---|---|---|---|---|
DPF2 | 123 | 5VDC | - | [10] |
5B79 | - | [13] | ||
DPF3b | 115 | 5SZB | H3K14ac (18) | [11] |
5SZC | H3K4me1K14ac (16) | |||
5I3L | H3K14ac (21) | [37] | ||
114 | 2KWJ | H3K14ac | [12] | |
2KWO | H4S1ac (20) | |||
2KWN | H4K16ac (15) | |||
2KWK | H3 wt (20) | |||
MOZ | 131 | 5B75 | H3K14bu (25) | [13] |
5B76 | H3K14cr (26) | |||
5B77 | H3K14pr (25) | |||
5B78 | H3K14cr (25) | |||
136 | 4LJN | - | [14] | |
4LKA | H3K9ac (12) | |||
4LK9 | H3 wt (12) | |||
4LLB | H3K14ac (15) | |||
112 | 2LN0 | - | [38] | |
3V43 * | H3R2 with no modification | |||
MORF | 111 | 5U2J | H3K14bu (16) | [15] |
116 | 6OIE | H3K14cr | [15,16] |
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Chugunov, A.O.; Potapova, N.A.; Klimenko, N.S.; Tatarskiy, V.V.; Georgieva, S.G.; Soshnikova, N.V. Conserved Structure and Evolution of DPF Domain of PHF10—The Specific Subunit of PBAF Chromatin Remodeling Complex. Int. J. Mol. Sci. 2021, 22, 11134. https://doi.org/10.3390/ijms222011134
Chugunov AO, Potapova NA, Klimenko NS, Tatarskiy VV, Georgieva SG, Soshnikova NV. Conserved Structure and Evolution of DPF Domain of PHF10—The Specific Subunit of PBAF Chromatin Remodeling Complex. International Journal of Molecular Sciences. 2021; 22(20):11134. https://doi.org/10.3390/ijms222011134
Chicago/Turabian StyleChugunov, Anton O., Nadezhda A. Potapova, Natalia S. Klimenko, Victor V. Tatarskiy, Sofia G. Georgieva, and Nataliya V. Soshnikova. 2021. "Conserved Structure and Evolution of DPF Domain of PHF10—The Specific Subunit of PBAF Chromatin Remodeling Complex" International Journal of Molecular Sciences 22, no. 20: 11134. https://doi.org/10.3390/ijms222011134