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:
-
- 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
- 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
- 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:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1638899
- Alternate Identifier(s):
- OSTI ID: 1562718
- 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
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
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. doi: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}
}
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