Dual engagement of the nucleosomal acidic patches is essential for deposition of histone H2A.Z by SWR1C

Baier, Alexander S.; Gioacchini, Nathan; Eek, Priit; Leith, Erik M.; Tan, Song; Peterson, Craig L.

doi:10.7554/elife.94869

Dual engagement of the nucleosomal acidic patches is essential for deposition of histone H2A.Z by SWR1C

Journal Article · Wed May 29 00:00:00 EDT 2024 · eLife

DOI:https://doi.org/10.7554/elife.94869· OSTI ID:2471663

^[1]; Gioacchini, Nathan ^[1]; Eek, Priit ^[2]; Leith, Erik M. ^[3]; Tan, Song ^[3]; ^[1]

Univ. of Massachusetts, Worcester, MA (United States). Chan Medical School
Pennsylvania State Univ., University Park, PA (United States); Tallinn University of Technology (Estonia)
Pennsylvania State Univ., University Park, PA (United States)

The yeast SWR1C chromatin remodeling enzyme catalyzes the ATP-dependent exchange of nucleosomal histone H2A for the histone variant H2A.Z, a key variant involved in a multitude of nuclear functions. How the 14-subunit SWR1C engages the nucleosomal substrate remains largely unknown. Studies on the ISWI, CHD1, and SWI/SNF families of chromatin remodeling enzymes have demonstrated key roles for the nucleosomal acidic patch for remodeling activity, however a role for this nucleosomal epitope in nucleosome editing by SWR1C has not been tested. Here, we employ a variety of biochemical assays to demonstrate an essential role for the acidic patch in the H2A.Z exchange reaction. Utilizing asymmetrically assembled nucleosomes, we demonstrate that the acidic patches on each face of the nucleosome are required for SWR1C-mediated dimer exchange, suggesting SWR1C engages the nucleosome in a ‘pincer-like’ conformation, engaging both patches simultaneously. Loss of a single acidic patch results in loss of high affinity nucleosome binding and nucleosomal stimulation of ATPase activity. We identify a conserved arginine-rich motif within the Swc5 subunit that binds the acidic patch and is key for dimer exchange activity. In addition, our cryoEM structure of a Swc5–nucleosome complex suggests that promoter proximal, histone H2B ubiquitylation may regulate H2A.Z deposition. Together these findings provide new insights into how SWR1C engages its nucleosomal substrate to promote efficient H2A.Z deposition.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2471663

Journal Information:: eLife, Journal Name: eLife Vol. 13; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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