Structure–function studies of histone H3/H4 tetramer maintenance during transcription by chaperone Spt2

Chen, Shoudeng; Rufiange, Anne; Huang, Hongda; Rajashankar, Kanagalaghatta R.; Nourani, Amine; Patel, Dinshaw J.

doi:10.1101/gad.261115.115

Title: Structure–function studies of histone H3/H4 tetramer maintenance during transcription by chaperone Spt2

Journal Article · Mon Jun 15 00:00:00 EDT 2015 · Genes & Development

DOI:https://doi.org/10.1101/gad.261115.115· OSTI ID:1344871

Chen, Shoudeng ^[1]; Rufiange, Anne ^[2]; Huang, Hongda ^[1]; Rajashankar, Kanagalaghatta R. ^[3]; Nourani, Amine ^[2]; Patel, Dinshaw J. ^[1]

Memorial Sloan-Kettering Cancer Center, New York, NY (United States). Structural Biology Program
Univ. of Laval, Quebec, QC (Canada)
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS) and Northeastern Collaborative Access Team (NE-CAT); cornell. Dept. of Chemistry and Chemical Biology

Cells use specific mechanisms such as histone chaperones to abrogate the inherent barrier that the nucleosome poses to transcribing polymerases. The current model postulates that nucleosomes can be transiently disrupted to accommodate passage of RNA polymerases and that histones H3 and H4 possess their own chaperones dedicated to the recovery of nucleosomes. Here, we determined the crystal structure of the conserved C terminus of human Suppressors of Ty insertions 2 (hSpt2C) chaperone bound to an H3/H4 tetramer. The structural studies demonstrate that hSpt2C is bound to the periphery of the H3/H4 tetramer, mimicking the trajectory of nucleosomal-bound DNA. These structural studies have been complemented with in vitro binding and in vivo functional studies on mutants that disrupt key intermolecular contacts involving two acidic patches and hydrophobic residues on Spt2C. We show that contacts between both human and yeast Spt2C with the H3/H4 tetramer are required for the suppression of H3/ H4 exchange as measured by H3K56ac and new H3 deposition. Furthermore, these interactions are also crucial for the inhibition of spurious transcription from within coding regions. In conclusion, together, our data indicate that Spt2 interacts with the periphery of the H3/H4 tetramer and promotes its recycling in the wake of RNA polymerase.

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Research Organization:: Cornell Univ., Ithaca, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357; LLS-SCOR 7132-08; I5-A554; S10 RR029205

OSTI ID:: 1344871

Journal Information:: Genes & Development, Vol. 29, Issue 12; ISSN 0890-9369

Publisher:: Cold Springs Harbor PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 26 works

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The Oligomerization Landscape of Histones Zhao, Haiqing; Winogradoff, David; Dalal, Yamini Biophysical Journal, Vol. 116, Issue 10 https://doi.org/10.1016/j.bpj.2019.03.021	journal	May 2019
Structural insights into the ability of nucleoplasmin to assemble and chaperone histone octamers for DNA deposition Franco, Aitor; Arranz, Rocío; Fernández-Rivero, Noelia Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-45726-7	journal	July 2019
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A Quantitative Characterization of Nucleoplasmin/Histone Complexes Reveals Chaperone Versatility Fernández-Rivero, Noelia; Franco, Aitor; Velázquez-Campoy, Adrian Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep32114	journal	August 2016
Casein kinase 2 mediated phosphorylation of Spt6 modulates histone dynamics and regulates spurious transcription Gouot, Emmanuelle; Bhat, Wajid; Rufiange, Anne Nucleic Acids Research, Vol. 46, Issue 15 https://doi.org/10.1093/nar/gky515	journal	June 2018
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59 BASIC BIOLOGICAL SCIENCES
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