Dynamic Changes in Histone Modifications Are Associated with Differential Chromatin Interactions
<p>Hi-C contact maps of mock- and IAV-treated MDMs and two DCIs on chromosome 11. The blue and green square represented a strengthened and weakened DCI, respectively.</p> "> Figure 2
<p>Genomic distances between DCI sites and patterns of CTCF and RAD21 binding within DCI sites after IAV infection. (<b>A</b>) Proportions of DCI sites with different distances after IAV and IFN-β treatment of MDMs. (<b>B</b>) Gains and losses of CTCF and RAD21 binding within DCI sites after IAV infection. (<b>C</b>) Changes in the patterns of CTCF and RAD21 binding within DCI sites after IAV infection. For two genomic regions where a DCI occurred, 0, 1, and 2 represent binding peaks of CTCF or RAD21 overlapped with neither, either, and both of the genomic regions, respectively.</p> "> Figure 3
<p>Changes in the binding of CTCF and RAD21 and histone modifications within DCI sites after IAV infection. (<b>A</b>) Changes within all DCI sites. (<b>B</b>) Changes within weakened and strengthened loops. (<b>C</b>,<b>D</b>) Gains and losses of CTCF and RAD21 binding and histone modifications within weakened and strengthened loops. Here, 0 and 1 represent a transcription factor or histone modification being absent or present within an interval, respectively. *, **, and *** represent a <span class="html-italic">p</span>-value of less than 0.05, 0.005, and 0.001, respectively.</p> "> Figure 4
<p>Changes in the binding of CTCF and RAD21 and histone modifications around DCI sites after IAV infection (<b>A</b>) and IFN-β treatment (<b>B</b>). * <span class="html-italic">p</span>-value of less than 0.05 produced by a Wilcoxon rank-sum test.</p> "> Figure 5
<p>Transcription factors most frequently bound within four types of intervals within DCI sites after IAV infection. Nodes represent transcription factors and four types of intervals. For each type of interval, W and S represent weakened and strengthened loops, respectively, while 0→1 and 1→0 represent gain and loss of a histone modification, respectively. The width of the lines between transcription factors and types of intervals is proportional to the occurrence number of transcription factors within the intervals.</p> "> Figure 6
<p>Colocalization of CTCF, RAD21, and five histone modifications in mock-, IAV-, and IFN-β-treated MDMs. The lower and upper triangular heat maps show pairwise similarities in mock and IAV (or IFN-β) conditions, respectively.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Data Source
2.2. Identification of DCIs
2.3. Binarization of ChIP-Seq Data for Transcription Factors and Histone Modifications
2.4. Statistical Significances of Changes in Transcription Factor Binding and Histone Modifications
2.5. Binding of Transcription Factors within DCI Sites
3. Results
3.1. Identification of DCIs
3.2. Binding of CTCF and RAD21 within DCI Sites
3.3. Dramatic Changes in Histone Modifications within and outside DCI Sites
3.4. Binding of Transcription Factors within DCI Sites
3.5. Colocalization of CTCF, RAD21, and Histone Modifications
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Oudelaar, A.M.; Higgs, D.R. The relationship between genome structure and function. Nat. Rev. Genet. 2021, 22, 154–168. [Google Scholar] [CrossRef] [PubMed]
- Mirny, L.A.; Imakaev, M.; Abdennur, N. Two major mechanisms of chromosome organization. Curr. Opin. Cell Biol. 2019, 58, 142–152. [Google Scholar] [CrossRef] [PubMed]
- Davidson, I.F.; Barth, R.; Zaczek, M.; van der Torre, J.; Tang, W.; Nagasaka, K.; Janissen, R.; Kerssemakers, J.; Wutz, G.; Dekker, C.; et al. CTCF is a DNA-tension-dependent barrier to cohesin-mediated loop extrusion. Nature 2023, 616, 822–827. [Google Scholar] [CrossRef]
- Wei, C.; Jia, L.M.; Huang, X.N.; Tan, J.; Wang, M.L.; Niu, J.; Hou, Y.P.; Sun, J.; Zeng, P.G.H.; Wang, J.; et al. CTCF organizes inter-A compartment interactions through RYBP-dependent phase separation. Cell Res. 2022, 32, 744–760. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Q.; Yu, M.; Tirado-Magallanes, R.; Li, B.; Kong, L.; Guo, M.R.; Tan, Z.H.; Lee, S.; Chai, L.; Numata, A.; et al. ZNF143 mediates CTCF-bound promoter–enhancer loops required for murine hematopoietic stem and progenitor cell function. Nat. Commun. 2021, 12, 43. [Google Scholar] [CrossRef] [PubMed]
- Wei, Z.; Wang, S.; Xu, Y.N.; Wang, W.Z.; Soares, F.; Ahmed, M.; Su, P.; Wang, T.T.; Orouji, E.; Xu, X.; et al. MYC reshapes CTCF-mediated chromatin architecture in prostate cancer. Nat. Commun. 2023, 14, 1787. [Google Scholar] [CrossRef] [PubMed]
- Weintraub, A.S.; Li, C.H.; Zamudio, A.V.; Sigova, A.A.; Hannett, N.M.; Day, D.S.; Abraham, B.J.; Cohen, M.A.; Nabet, B.; Buckley, D.L.; et al. YY1 Is a Structural Regulator of Enhancer-Promoter Loops. Cell 2017, 171, 1573–1588.e28. [Google Scholar] [CrossRef] [PubMed]
- Heinz, S.; Texari, L.; Hayes, M.G.B.; Urbanowski, M.; Chang, M.W.; Givarkes, N.; Rialdi, A.; White, K.M.; Albrecht, R.A.; Pache, L.; et al. Transcription Elongation Can Affect Genome 3D Structure. Cell 2018, 174, 1522–1536.e22. [Google Scholar] [CrossRef] [PubMed]
- Hsieh, T.H.S.; Cattoglio, C.; Slobodyanyuk, E.; Hansen, A.S.; Darzacq, X.; Tjian, R. Enhancer-promoter interactions and transcription are largely maintained upon acute loss of CTCF, cohesin, WAPL or YY1. Nat. Genet. 2022, 54, 1919–1932. [Google Scholar] [CrossRef]
- Kang, H.; Shokhirev, M.N.; Xu, Z.; Chandran, S.; Dixon, J.R.; Hetzer, M.W. Dynamic regulation of histone modifications and long-range chromosomal interactions during postmitotic transcriptional reactivation. Genes Dev. 2020, 34, 913–930. [Google Scholar] [CrossRef]
- Brejc, K.; Bian, Q.; Uzawa, S.; Wheeler, B.S.; Anderson, E.C.; King, D.S.; Kranzusch, P.J.; Preston, C.G.; Meyer, B.J. Dynamic Control of X Chromosome Conformation and Repression by a Histone H4K20 Demethylase. Cell 2017, 171, 85–102.e23. [Google Scholar] [CrossRef]
- Wang, L.; Gao, Y.F.; Zheng, X.D.; Liu, C.F.; Dong, S.S.; Li, R.; Zhang, G.W.; Wei, Y.X.; Qu, H.Y.; Li, Y.H.; et al. Histone Modifications Regulate Chromatin Compartmentalization by Contributing to a Phase Separation Mechanism. Mol. Cell 2019, 76, 646–659.e6. [Google Scholar] [CrossRef]
- Bian, Q.; Anderson, E.C.; Yang, Q.; Meyer, B.J. Histone H3K9 methylation promotes formation of genome compartments in Caenorhabditis elegans via chromosome compaction and perinuclear anchoring. Proc. Natl. Acad. Sci. USA 2020, 117, 11459–11470. [Google Scholar] [CrossRef]
- Langmead, B.; Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9, 357–359. [Google Scholar] [CrossRef]
- Durand, N.C.; Robinson, J.T.; Shamim, M.S.; Machol, I.; Mesirov, J.P.; Lander, E.S.; Aiden, E.L. Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom. Cell Syst. 2016, 3, 99–101. [Google Scholar] [CrossRef]
- Stansfield, J.C.; Cresswell, K.G.; Dozmorov, M.G. multiHiCcompare: Joint normalization and comparative analysis of complex Hi-C experiments. Bioinformatics 2019, 35, 2916–2923. [Google Scholar] [CrossRef]
- Rao, S.S.P.; Huntley, M.H.; Durand, N.C.; Stamenova, E.K.; Bochkov, I.D.; Robinson, J.T.; Sanborn, A.L.; Machol, I.; Omer, A.D.; Lander, E.S.; et al. A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping. Cell 2014, 159, 1665–1680. [Google Scholar] [CrossRef]
- Nix, D.A.; Courdy, S.J.; Boucher, K.M. Empirical methods for controlling false positives and estimating confidence in ChIP-Seq peaks. BMC Bioinform. 2008, 9, 523. [Google Scholar] [CrossRef]
- Grant, C.E.; Bailey, T.L.; Noble, W.S. FIMO: Scanning for occurrences of a given motif. Bioinformatics 2011, 27, 1017–1018. [Google Scholar] [CrossRef] [PubMed]
- Castro-Mondragon, J.A.; Riudavets-Puig, R.; Rauluseviciute, I.; Lemma, R.B.; Turchi, L.; Blanc-Mathieu, R.; Lucas, J.; Boddie, P.; Khan, A.; Pérez, N.M.; et al. JASPAR 2022: The 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 2022, 50, D165–D173. [Google Scholar] [CrossRef] [PubMed]
- Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of Biomolecular Interaction Networks. Genome Res. 2003, 13, 2498–2504. [Google Scholar] [CrossRef] [PubMed]
- Rao, S.S.P.; Huang, S.-C.; St Hilaire, B.G.; Engreitz, J.M.; Perez, E.M.; Kieffer-Kwon, K.-R.; Sanborn, A.L.; Johnstone, S.E.; Bascom, G.D.; Bochkov, I.D.; et al. Cohesin Loss Eliminates All Loop Domains. Cell 2017, 171, 305–320.e24. [Google Scholar] [CrossRef] [PubMed]
- Amoutzias, G.D.; Robertson, D.L.; Van de Peer, Y.; Oliver, S.G. Choose your partners: Dimerization in eukaryotic transcription factors. Trends Biochem. Sci. 2008, 33, 220–229. [Google Scholar] [CrossRef] [PubMed]
- Eram, M.S.; Bustos, S.P.; Lima-Fernandes, E.; Siarheyeva, A.; Senisterra, G.; Hajian, T.; Chau, I.; Duan, S.; Wu, H.; Dombrovski, L.; et al. Trimethylation of Histone H3 Lysine 36 by Human Methyltransferase PRDM9 Protein. J. Biol. Chem. 2014, 289, 12177–12188. [Google Scholar] [CrossRef]
- Sinha, K.K.; Bilokapic, S.; Du, Y.; Malik, D.; Halic, M. Histone modifications regulate pioneer transcription factor cooperativity. Nature 2023, 619, 378–384. [Google Scholar] [CrossRef] [PubMed]
- Cai, Y.; Zhang, Y.; Loh, Y.P.; Tng, J.Q.; Lim, M.C.; Cao, Z.; Raju, A.; Lieberman Aiden, E.L.; Li, S.; Manikandan, L.; et al. H3K27me3-rich genomic regions can function as silencers to repress gene expression via chromatin interactions. Nat. Commun. 2021, 12, 719. [Google Scholar] [CrossRef] [PubMed]
- Szalaj, P.; Plewczynski, D. Three-dimensional organization and dynamics of the genome. Cell Biol. Toxicol. 2018, 34, 381–404. [Google Scholar] [CrossRef] [PubMed]
- Falk, M.; Feodorova, Y.; Naumova, N.; Imakaev, M.; Lajoie, B.R.; Leonhardt, H.; Joffe, B.; Dekker, J.; Fudenberg, G.; Solovei, I.; et al. Heterochromatin drives compartmentalization of inverted and conventional nuclei. Nature 2019, 570, 395–399. [Google Scholar] [CrossRef] [PubMed]
- Allen, B.L.; Taatjes, D.J. The Mediator complex: A central integrator of transcription. Nat. Rev. Mol. Cell Biol. 2015, 16, 155–166. [Google Scholar] [CrossRef]
- Kim, S.; Shendure, J. Mechanisms of Interplay between Transcription Factors and the 3D Genome. Mol. Cell 2019, 76, 306–319. [Google Scholar] [CrossRef]
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Nie, Y.; Wang, M. Dynamic Changes in Histone Modifications Are Associated with Differential Chromatin Interactions. Genes 2024, 15, 988. https://doi.org/10.3390/genes15080988
Nie Y, Wang M. Dynamic Changes in Histone Modifications Are Associated with Differential Chromatin Interactions. Genes. 2024; 15(8):988. https://doi.org/10.3390/genes15080988
Chicago/Turabian StyleNie, Yumin, and Mengjie Wang. 2024. "Dynamic Changes in Histone Modifications Are Associated with Differential Chromatin Interactions" Genes 15, no. 8: 988. https://doi.org/10.3390/genes15080988