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Title: Cooperative DNA binding by proteins through DNA shape complementarity

Abstract

Abstract Localized arrays of proteins cooperatively assemble onto chromosomes to control DNA activity in many contexts. Binding cooperativity is often mediated by specific protein–protein interactions, but cooperativity through DNA structure is becoming increasingly recognized as an additional mechanism. During the site-specific DNA recombination reaction that excises phage λ from the chromosome, the bacterial DNA architectural protein Fis recruits multiple λ-encoded Xis proteins to the attR recombination site. Here, we report X-ray crystal structures of DNA complexes containing Fis + Xis, which show little, if any, contacts between the two proteins. Comparisons with structures of DNA complexes containing only Fis or Xis, together with mutant protein and DNA binding studies, support a mechanism for cooperative protein binding solely by DNA allostery. Fis binding both molds the minor groove to potentiate insertion of the Xis β-hairpin wing motif and bends the DNA to facilitate Xis-DNA contacts within the major groove. The Fis-structured minor groove shape that is optimized for Xis binding requires a precisely positioned pyrimidine-purine base-pair step, whose location has been shown to modulate minor groove widths in Fis-bound complexes to different DNA targets.

Authors:
 [1];  [2];  [3]
  1. Department of Biological Chemistry, David Geffen School of Medicine at the University of California at Los Angeles, Los Angeles, CA 90095-1737, USA, Department of Chemistry, Towson University, 8000 York Rd., Towson, MD 21252, USA
  2. University of California at Los Angeles-Department of Energy Institute of Genomics and Proteomics, University of California at Los Angeles, Los Angeles, CA 90095-1570, USA
  3. Department of Biological Chemistry, David Geffen School of Medicine at the University of California at Los Angeles, Los Angeles, CA 90095-1737, USA, Molecular Biology Institute, University of California at Los Angeles, Los Angeles, CA 90095, USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1638899
Grant/Contract Number:  
FC02-02ER63421; AC02-06CH11357
Resource Type:
Published Article
Journal Name:
Nucleic Acids Research
Additional Journal Information:
Journal Name: Nucleic Acids Research Journal Volume: 47 Journal Issue: 16; Journal ID: ISSN 0305-1048
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Hancock, Stephen P., Cascio, Duilio, and Johnson, Reid C.. Cooperative DNA binding by proteins through DNA shape complementarity. United Kingdom: N. p., 2019. Web. https://doi.org/10.1093/nar/gkz642.
Hancock, Stephen P., Cascio, Duilio, & Johnson, Reid C.. Cooperative DNA binding by proteins through DNA shape complementarity. United Kingdom. https://doi.org/10.1093/nar/gkz642
Hancock, Stephen P., Cascio, Duilio, and Johnson, Reid C.. Thu . "Cooperative DNA binding by proteins through DNA shape complementarity". United Kingdom. https://doi.org/10.1093/nar/gkz642.
@article{osti_1638899,
title = {Cooperative DNA binding by proteins through DNA shape complementarity},
author = {Hancock, Stephen P. and Cascio, Duilio and Johnson, Reid C.},
abstractNote = {Abstract Localized arrays of proteins cooperatively assemble onto chromosomes to control DNA activity in many contexts. Binding cooperativity is often mediated by specific protein–protein interactions, but cooperativity through DNA structure is becoming increasingly recognized as an additional mechanism. During the site-specific DNA recombination reaction that excises phage λ from the chromosome, the bacterial DNA architectural protein Fis recruits multiple λ-encoded Xis proteins to the attR recombination site. Here, we report X-ray crystal structures of DNA complexes containing Fis + Xis, which show little, if any, contacts between the two proteins. Comparisons with structures of DNA complexes containing only Fis or Xis, together with mutant protein and DNA binding studies, support a mechanism for cooperative protein binding solely by DNA allostery. Fis binding both molds the minor groove to potentiate insertion of the Xis β-hairpin wing motif and bends the DNA to facilitate Xis-DNA contacts within the major groove. The Fis-structured minor groove shape that is optimized for Xis binding requires a precisely positioned pyrimidine-purine base-pair step, whose location has been shown to modulate minor groove widths in Fis-bound complexes to different DNA targets.},
doi = {10.1093/nar/gkz642},
journal = {Nucleic Acids Research},
number = 16,
volume = 47,
place = {United Kingdom},
year = {2019},
month = {7}
}

Journal Article:
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https://doi.org/10.1093/nar/gkz642

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