Burak, Y., Ariel, G. & Andelman, D. Onset of DNA aggregation in presence of monovalent and multivalent counterions. Biophys. J. 85, 2100–2110 (2003).
Google ScholarÂÂ
Post, C. B. & Zimm, B. H. Theory of DNA condensation: collapse versus aggregation. Biopolymers 21, 2123–2137 (1982).
Google ScholarÂÂ
Woodcock, C. L. F. Ultrastructure of inactive chromatin. J. Cell Biol. 59, A368 (1973).
Olins, A. L. & Olins, D. E. Spheroid chromatin units (v bodies). Science 183, 330–332 (1974).
Google ScholarÂÂ
Finch, J. T. & Klug, A. Solenoidal model for superstructure in chromatin. Proc. Natl Acad. Sci. USA 73, 1897 (1976).
Google ScholarÂÂ
Ou, H. D. et al. ChromEMT: visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science 357, eaag0025 (2017).
Google ScholarÂÂ
Maeshima, K. et al. Nucleosomal arrays self-assemble into supramolecular globular structures lacking 30-nm fibers. EMBO J. 35, 1115–1132 (2016).
Google ScholarÂÂ
Adhireksan, Z., Sharma, D., Lee, P. L. & Davey, C. A. Near-atomic resolution structures of interdigitated nucleosome fibres. Nat. Commun. 11, 4747 (2020).
Google ScholarÂÂ
Hsieh, T. H. S. et al. Mapping nucleosome resolution chromosome folding in yeast by Micro-C. Cell 162, 108 (2015).
Google ScholarÂÂ
Ricci, M. A., Manzo, C., GarcÃÂa-Parajo, M. F., Lakadamyali, M. & Cosma, M. P. Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160, 1145–1158 (2015).
Google ScholarÂÂ
Gibson, B. A. et al. Organization of chromatin by intrinsic and regulated phase separation. Cell 179, 470–484.e21 (2019).
Google ScholarÂÂ
Strickfaden, H. et al. Condensed chromatin behaves like a solid on the mesoscale in vitro and in living cells. Cell 183, 1772–1784.e13 (2020).
Google ScholarÂÂ
Zhang, Y., Narlikar, G. J. & Kutateladze, T. G. Enzymatic reactions inside biological condensates. J. Mol. Biol. 433, 166624 (2021).
Google ScholarÂÂ
Hihara, S. et al. Local nucleosome dynamics facilitate chromatin accessibility in living mammalian cells. Cell Rep. 2, 1645–1656 (2012).
Google ScholarÂÂ
Kornberg, R. D. & Lorch, Y. Primary role of the nucleosome. Mol. Cell 79, 371–375 (2020).
Google ScholarÂÂ
Kim, J. M. et al. Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin. eLife 10, e69387 (2021).
Google ScholarÂÂ
Corona, D. F. V. et al. ISWI is an ATP-dependent nucleosome remodeling factor. Mol. Cell 3, 239–245 (1999).
Google ScholarÂÂ
Hamiche, A., Sandaltzopoulos, R., Gdula, D. A. & Wu, C. ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell 97, 833–842 (1999).
Google ScholarÂÂ
Ludwigsen, J., Hepp, N., Klinker, H., Pfennig, S. & Mueller-Planitz, F. Remodeling and repositioning of nucleosomes in nucleosomal arrays. Methods Mol. Biol. 1805, 349–370 (2018).
Google ScholarÂÂ
Mueller-Planitz, F., Klinker, H., Ludwigsen, J. & Becker, P. B. The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat. Struct. Mol. Biol. 20, 82–89 (2013).
Google ScholarÂÂ
Schram, R. D., Klinker, H., Becker, P. B. & Schiessel, H. Computational study of remodeling in a nucleosomal array. Eur. Phys. J. E 38, 85 (2015).
Google ScholarÂÂ
Klinker, H. et al. ISWI remodelling of physiological chromatin fibres acetylated at lysine 16 of histone H4. PLoS ONE 9, e88411 (2014).
Google ScholarÂÂ
Boyer, L. A. et al. Functional delineation of three groups of the ATP-dependent family of chromatin remodeling enzymes. J. Biol. Chem. 275, 18864–18870 (2000).
Google ScholarÂÂ
Logie, C., Tse, C., Hansen, J. C. & Peterson, C. L. The core histone N-terminal domains are required for multiple rounds of catalytic chromatin remodeling by the SWI/SNF and RSC complexes. Biochemistry 38, 2514–2522 (1999).
Google ScholarÂÂ
Peeples, W. & Rosen, M. K. Mechanistic dissection of increased enzymatic rate in a phase-separated compartment. Nat. Chem. Biol. 17, 693–702 (2021).
Google ScholarÂÂ
Poirier, M. G., Bussiek, M., Langowski, J. & Widom, J. Spontaneous access to DNA target sites in folded chromatin fibers. J. Mol. Biol. 379, 772–786 (2008).
Google ScholarÂÂ
Poirier, M. G., Oh, E., Tims, H. S. & Widom, J. Dynamics and function of compact nucleosome arrays. Nat. Struct. Mol. Biol. 16, 938–944 (2009).
Google ScholarÂÂ
Hagerman, T. A. et al. Chromatin stability at low concentration depends on histone octamer saturation levels. Biophys. J. 96, 1944–1951 (2009).
Google ScholarÂÂ
Gibson, B. A. et al. In diverse conditions, intrinsic chromatin condensates have liquid-like material properties. Proc. Natl Acad. Sci. USA 120, e2218085120 (2023).
Google ScholarÂÂ
Goins, A. B., Sanabria, H. & Waxham, M. N. Macromolecular crowding and size effects on probe microviscosity. Biophys. J. 95, 5362–5373 (2008).
Google ScholarÂÂ
Yang, J. G. & Narlikar, G. J. FRET-based methods to study ATP-dependent changes in chromatin structure. Methods 41, 291–295 (2007).
Google ScholarÂÂ
Zhang, M. et al. Molecular organization of the early stages of nucleosome phase separation visualized by cryo-electron tomography. Mol. Cell 82, 3000 (2022).
Google ScholarÂÂ
Weidemann, T. et al. Counting nucleosomes in living cells with a combination of fluorescence correlation spectroscopy and confocal imaging. J. Mol. Biol. 334, 229–240 (2003).
Google ScholarÂÂ
Leonard, J. D. & Narlikar, G. J. A nucleotide-driven switch regulates flanking DNA length sensing by a dimeric chromatin remodeler. Mol. Cell 57, 850–859 (2015).
Google ScholarÂÂ
Larson, A. G. & Narlikar, G. J. The role of phase separation in heterochromatin formation, function, and regulation. Biochemistry 57, 2540–2548 (2018).
Google ScholarÂÂ
Grüne, T. et al. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 12, 449–460 (2003).
Google ScholarÂÂ
Bhardwaj, S. K. et al. Dinucleosome specificity and allosteric switch of the ISW1a ATP-dependent chromatin remodeler in transcription regulation. Nat. Commun. 11, 5913 (2020).
Google ScholarÂÂ
Yamada, K. et al. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472, 448–453 (2011).
Google ScholarÂÂ
Li, L. et al. Structure of the ISW1a complex bound to the dinucleosome. Nat. Struct. Mol. Biol. 31, 266–274 (2024). https://doi.org/10.1038/s41594-023-01174-6
Wang, J. et al. A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins. Cell 174, 688–699.e16 (2018).
Google ScholarÂÂ
Muzzopappa, F., Hertzog, M. & Erdel, F. DNA length tunes the fluidity of DNA-based condensates. Biophys. J. 120, 1288–1300 (2021).
Google ScholarÂÂ
Ludwigsen, J., Klinker, H. & Mueller-Planitz, F. No need for a power stroke in ISWI-mediated nucleosome sliding. EMBO Rep. 14, 1092–1097 (2013).
Google ScholarÂÂ
Harrer, N. et al. Structural architecture of the nucleosome remodeler ISWI determined from cross-linking, mass spectrometry, SAXS, and modeling. Structure 26, 282–294.e6 (2018).
Google ScholarÂÂ
Rudolph, J., Mahadevan, J., Dyer, P. & Luger, K. Poly(ADP-ribose) polymerase 1 searches DNA via a ‘monkey bar’ mechanism. Elife 7, e37818 (2018).
Google ScholarÂÂ
Deindl, S. et al. ISWI remodelers slide nucleosomes with coordinated multi-base-pair entry steps and single-base-pair exit steps. Cell 152, 442–452 (2013).
Google ScholarÂÂ
Gamarra, N., Johnson, S. L., Trnka, M. J., Burlingame, A. L. & Narlikar, G. J. The nucleosomal acidic patch relieves auto-inhibition by the ISWI remodeler SNF2h. eLife 7, e35322 (2018).
Google ScholarÂÂ
Dann, G. P. et al. ISWI chromatin remodellers sense nucleosome modifications to determine substrate preference. Nature 548, 607–611 (2017).
Google ScholarÂÂ
Clapier, C. R., Längst, G., Corona, D. F., Becker, P. B. & Nightingale, K. P. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 21, 875–883 (2001).
Google ScholarÂÂ
Schalch, T., Duda, S., Sargent, D. F. & Richmond, T. J. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436, 138–141 (2005).
Google ScholarÂÂ
Verschure, P. J. et al. Condensed chromatin domains in the mammalian nucleus are accessible to large macromolecules. EMBO Rep. 4, 861–866 (2003).
Google ScholarÂÂ
Beaudouin, J., Mora-Bermúdez, F., Klee, T., Daigle, N. & Ellenberg, J. Dissecting the contribution of diffusion and interactions to the mobility of nuclear proteins. Biophys. J. 90, 1878–1894 (2006).
Google ScholarÂÂ
Erdel, F., Baum, M. & Rippe, K. The viscoelastic properties of chromatin and the nucleoplasm revealed by scale-dependent protein mobility. J. Phys. Condens. Matter 27, 064115 (2015).
Google ScholarÂÂ
Maeshima, K. et al. A transient rise in free Mg2+ ions released from ATP-Mg hydrolysis contributes to mitotic chromosome condensation. Curr. Biol. 28, 444–451.e6 (2018).
Google ScholarÂÂ
Shimamoto, Y., Tamura, S., Masumoto, H. & Maeshima, K. Nucleosome–nucleosome interactions via histone tails and linker DNA regulate nuclear rigidity. Mol. Biol. Cell 28, 1580–1589 (2017).
Google ScholarÂÂ
Kroschwald, S. et al. Different material states of Pub1 condensates define distinct modes of stress adaptation and recovery. Cell Rep. 23, 3327–3339 (2018).
Google ScholarÂÂ
Munder, M. C. et al. A pH-driven transition of the cytoplasm from a fluid- to a solid-like state promotes entry into dormancy. eLife 5, e09347 (2016).
Google ScholarÂÂ
Erdel, F. & Rippe, K. Formation of chromatin subcompartments by phase separation. Biophys. J. 114, 2262–2270 (2018).
Google ScholarÂÂ
Schneider, M. W. G. et al. A mitotic chromatin phase transition prevents perforation by microtubules. Nature 609, 183 (2022).
Google ScholarÂÂ
Keizer, V. I. P. et al. Live-cell micromanipulation of a genomic locus reveals interphase chromatin mechanics. Science 377, 489–495 (2022).
Google ScholarÂÂ
Erdel, F. et al. Mouse heterochromatin adopts digital compaction states without showing hallmarks of HP1-driven liquid–liquid phase separation. Mol. Cell 78, 236–249.e7 (2020).
Google ScholarÂÂ
Irgen-Gioro, S., Yoshida, S., Walling, V. & Chong, S. Fixation can change the appearance of phase separation in living cells. Elife 11, e79903 (2022).
Google ScholarÂÂ
Hansen, J. C., Maeshima, K. & Hendzel, M. J. The solid and liquid states of chromatin. Epigenetics Chromatin 14, 50 (2021).
Google ScholarÂÂ
Korber, P. & Becker, P. B. Nucleosome dynamics and epigenetic stability. Essays Biochem 48, 63–74 (2010).
Google ScholarÂÂ
Muzzopappa, F. et al. Detecting and quantifying liquid–liquid phase separation in living cells by model-free calibrated half-bleaching. Nat. Commun. 13, 1–15 (2022).
Google ScholarÂÂ
Whitehouse, I., Rando, O. J., Delrow, J. & Tsukiyama, T. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450, 1031–1035 (2007).
Google ScholarÂÂ
Gelbart, M. E., Bachman, N., Delrow, J., Boeke, J. D. & Tsukiyama, T. Genome-wide identification of Isw2 chromatin-remodeling targets by localization of a catalytically inactive mutant. Genes Dev. 19, 942 (2005).
Google ScholarÂÂ
Blosser, T. R., Yang, J. G., Stone, M. D., Narlikar, G. J. & Zhuang, X. Dynamics of nucleosome remodelling by individual ACF complexes. Nature 462, 1022–1027 (2009).
Google ScholarÂÂ
Tilly, B. C. et al. In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin. eLife 10, e69424 (2021).
Google ScholarÂÂ
Erdel, F., Schubert, T., Marth, C., Längst, G. & Rippe, K. Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc. Natl Acad. Sci. USA 107, 19873–19878 (2010).
Google ScholarÂÂ
Oppikofer, M. et al. Expansion of the ISWI chromatin remodeler family with new active complexes. EMBO Rep. 18, 1697–1706 (2017).
Google ScholarÂÂ
Clapier, C. R., Verma, N., Parnell, T. J. & Cairns, B. R. Cancer-associated gain-of-function mutations activate a SWI/SNF-family regulatory hub. Mol. Cell 80, 712–725.e5 (2020).
Google ScholarÂÂ
Hodges, H. C. et al. Dominant-negative SMARCA4 mutants alter the accessibility landscape of tissue-unrestricted enhancers. Nat. Struct. Mol. Biol. 25, 61–72 (2018).
Google ScholarÂÂ
Elfring, L. K. et al. Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2. Genetics 148, 251–265 (1998).
Google ScholarÂÂ
Li, W. et al. Biophysical properties of AKAP95 protein condensates regulate splicing and tumorigenesis. Nat. Cell Biol. 22, 960–972 (2020).
Google ScholarÂÂ
Shi, B. et al. UTX condensation underlies its tumour-suppressive activity. Nature 597, 726–731 (2021).
Google ScholarÂÂ
Pédelacq, J.-D., Cabantous, S., Tran, T., Terwilliger, T. C. & Waldo, G. S. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 24, 79–88 (2006).
Google ScholarÂÂ
Klinker, H., Haas, C., Harrer, N., Becker, P. B. & Mueller-Planitz, F. Rapid purification of recombinant histones. PLoS ONE 9, e104029 (2014).
Google ScholarÂÂ
Schuck, P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78, 1606–1619 (2000).
Google ScholarÂÂ
Demeler, B. & Gorbet, G. E. in Analytical Ultracentrifugation (eds Uchiyama, S. et al.) 119–143 (Springer, 2016).
Goins, A. B., Sanabria, H. & Waxham, M. N. Macromolecular crowding and size effects on probe microviscosity. Biophys J. 95, 5362–5373 (2008).
Google ScholarÂÂ
Digman, M. A., Caiolfa, V. R., Zamai, M. & Gratton, E. The phasor approach to fluorescence lifetime imaging analysis. Biophys. J. 94, 14–16 (2008).
Google ScholarÂÂ
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
Google ScholarÂÂ
MultiStackReg (BioImage Informatics Index, 2022); https://biii.eu/multistackreg
Koulouras, G. et al. EasyFRAP-web: a web-based tool for the analysis of fluorescence recovery after photobleaching data. Nucleic Acids Res. 46, 467–472 (2018).
Google ScholarÂÂ
R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing https://www.R-project.org/ (2022).
Vizjak_2023 (GitHub, 2023); https://github.com/StiglerLab/Vizjak_2023