A competitive regulatory mechanism of the Chd1 remodeler is integral to distorting nucleosomal DNA

Eustermann, S., Patel, A. B., Hopfner, K., He, Y. & Korber, P. Energy-driven genome regulation by ATP-dependent chromatin remodellers. Nat. Rev. Mol. Cell Biol. https://doi.org/10.1038/s41580-023-00683-y (2023).

Article  PubMed  Google Scholar 

Winger, J., Nodelman, I. M., Levendosky, R. F. & Bowman, G. D. A twist defect mechanism for ATP-dependent translocation of nucleosomal DNA. eLife 7, e34100 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Nodelman, I. M. et al. Nucleosome recognition and DNA distortion by the Chd1 remodeler in a nucleotide-free state. Nat. Struct. Mol. Biol. 29, 121–129 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Nodelman, I. M. & Bowman, G. D. Biophysics of chromatin remodeling. Annu. Rev. Biophys. 50, 73–93 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Yan, L. & Chen, Z. A unifying mechanism of DNA translocation underlying chromatin remodeling. Trends Biochem. Sci. 45, 217–227 (2020).

Article  CAS  PubMed  Google Scholar 

Li, M. et al. Mechanism of DNA translocation underlying chromatin remodelling by Snf2. Nature 567, 409–413 (2019).

Article  CAS  PubMed  Google Scholar 

Bowman, G. D. & Deindl, S. Remodeling the genome with DNA twists. Science 366, 35–36 (2019).

Article  CAS  PubMed  Google Scholar 

Sabantsev, A., Levendosky, R. F., Zhuang, X., Bowman, G. D. & Deindl, S. Direct observation of coordinated DNA movements on the nucleosome during chromatin remodelling. Nat. Commun. 10, 1720 (2019).

Article  PubMed  PubMed Central  Google Scholar 

Tsukiyama, T., Palmer, J., Landel, C. C., Shiloach, J. & Wu, C. Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev. 13, 686–697 (1999).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lusser, A., Urwin, D. L. & Kadonaga, J. T. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat. Struct. Mol. Biol. 12, 160–166 (2005).

Article  CAS  PubMed  Google Scholar 

Ito, T., Bulger, M., Pazin, M. J., Kobayashi, R. & Kadonaga, J. T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90, 145–155 (1997).

Article  CAS  PubMed  Google Scholar 

Gkikopoulos, T. et al. A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333, 1758–1760 (2011).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Smolle, M. et al. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19, 884–892 (2012).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Engeholm, M. et al. Resolution of transcription-induced hexasome-nucleosome complexes by Chd1 and FACT. Mol. Cell 84, 3423–3437.e8 (2024).

Article  CAS  PubMed  Google Scholar 

Yang, J. G., Madrid, T. S., Sevastopoulos, E. & Narlikar, G. J. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nat. Struct. Mol. Biol. 13, 1078–1083 (2006).

Article  CAS  PubMed  Google Scholar 

Stockdale, C., Flaus, A., Ferreira, H. & Owen-Hughes, T. Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J. Biol. Chem. 281, 16279–16288 (2006).

Article  CAS  PubMed  Google Scholar 

Gangaraju, V. K. & Bartholomew, B. Dependency of ISW1a chromatin remodeling on extranucleosomal DNA. Mol. Cell. Biol. 27, 3217–3225 (2007).

Article  CAS  PubMed  PubMed Central  Google Scholar 

McKnight, J. N., Jenkins, K. R., Nodelman, I. M., Escobar, T. & Bowman, G. D. Extranucleosomal DNA binding directs nucleosome sliding by Chd1. Mol. Cell. Biol. 31, 4746–4759 (2011).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Nodelman, I. M. et al. Interdomain communication of the Chd1 chromatin remodeler across the DNA gyres of the nucleosome. Mol. Cell 65, 447–459 (2017).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Farnung, L., Vos, S. M., Wigge, C. & Cramer, P. Nucleosome-Chd1 structure and implications for chromatin remodelling. Nature 550, 539–542 (2017).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Sundaramoorthy, R. et al. Structure of the chromatin remodelling enzyme Chd1 bound to a ubiquitinylated nucleosome. eLife 7, e35720 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Li, L. et al. Structure of the ISW1a complex bound to the dinucleosome. Nat. Struct. Mol. Biol. 31, 266–274 (2024).

Article  CAS  PubMed  Google Scholar 

Yamada, K. et al. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472, 448–453 (2011).

Article  CAS  PubMed  Google Scholar 

Nodelman, I. M., Shen, Z., Levendosky, R. F. & Bowman, G. D. Autoinhibitory elements of the Chd1 remodeler block initiation of twist defects by destabilizing the ATPase motor on the nucleosome. Proc. Natl Acad. Sci. USA 118, e2014498118 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Hauk, G., McKnight, J. N., Nodelman, I. M. & Bowman, G. D. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol. Cell 39, 711–723 (2010).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Clapier, C. R. & Cairns, B. R. Regulation of ISWI involves inhibitory modules antagonized by nucleosomal epitopes. Nature 492, 280–284 (2012).

Article  CAS  PubMed  PubMed Central  Google Scholar 

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).

Article  CAS  PubMed  PubMed Central  Google Scholar 

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).

Article  PubMed  PubMed Central  Google Scholar 

Dao, H. T., Dul, B. E., Dann, G. P., Liszczak, G. P. & Muir, T. W. A basic motif anchoring ISWI to nucleosome acidic patch regulates nucleosome spacing. Nat. Chem. Biol. 16, 134–142 (2020).

Article  CAS  PubMed  Google Scholar 

Levendosky, R. F. & Bowman, G. D. Asymmetry between the two acidic patches dictates the direction of nucleosome sliding by the ISWI chromatin remodeler. eLife 8, e45472 (2019).

Article  PubMed 

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