High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes

Benjamin Lang; Nicolas Blot; Emeline Bouffartigues; Malcolm Buckle; Marcel Geertz; Claudio O. Gualerzi; Ramesh Mavathur; Georgi Muskhelishvili; Cynthia L. Pon; Sylvie Rimsky; Stefano Stella; M. Madan Babu; Andrew Travers

doi:10.1093/nar/gkm712

High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes

Benjamin Lang, Nicolas Blot, Emeline Bouffartigues, Malcolm Buckle, Marcel Geertz, Claudio O. Gualerzi, Ramesh Mavathur, Georgi Muskhelishvili, Cynthia L. Pon, Sylvie Rimsky, Stefano Stella, M. Madan Babu^*, Andrew Travers

^*Corresponding author for this work

Protein Structure and Function Program

183 Citations (Scopus)

Abstract

The global transcriptional regulator H-NS selectively silences bacterial genes associated with pathogenicity and responses to environmental insults. Although there is ample evidence that H-NS binds preferentially to DNA containing curved regions, we show here that a major basis for this selectivity is the presence of a conserved sequence motif in H-NS target transcriptons. We further show that there is a strong tendency for the H-NS binding sites to be clustered, both within operons and in genes contained in the pathogenicity-associated islands. In accordance with previously published findings, we show that these motifs occur in AT-rich regions of DNA. On the basis of these observations, we propose that H-NS silences extensive regions of the bacterial chromosome by binding first to nucleating high-affinity sites and then spreading along AT-rich DNA. This spreading would be reinforced by the frequent occurrence of the motif in such regions. Our findings suggest that such an organization enables the silencing of extensive regions of the genetic material, thereby providing a coherent framework that unifies studies on the H-NS protein and a concrete molecular basis for the genetic control of H-NS transcriptional silencing.

Original language	English
Journal	Nucleic Acids Research
Volume	35
Issue number	18
Pages (from-to)	6330-6337
Number of pages	8
ISSN	0305-1048
DOIs	https://doi.org/10.1093/nar/gkm712
Publication status	Published - 1 Sept 2007

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Lang, B., Blot, N., Bouffartigues, E., Buckle, M., Geertz, M., Gualerzi, C. O., Mavathur, R., Muskhelishvili, G., Pon, C. L., Rimsky, S., Stella, S., Babu, M. M., & Travers, A. (2007). High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Research, 35(18), 6330-6337. https://doi.org/10.1093/nar/gkm712

Lang, B, Blot, N, Bouffartigues, E, Buckle, M, Geertz, M, Gualerzi, CO, Mavathur, R, Muskhelishvili, G, Pon, CL, Rimsky, S, Stella, S, Babu, MM & Travers, A 2007, 'High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes', Nucleic Acids Research, vol. 35, no. 18, pp. 6330-6337. https://doi.org/10.1093/nar/gkm712

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title = "High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes",

abstract = "The global transcriptional regulator H-NS selectively silences bacterial genes associated with pathogenicity and responses to environmental insults. Although there is ample evidence that H-NS binds preferentially to DNA containing curved regions, we show here that a major basis for this selectivity is the presence of a conserved sequence motif in H-NS target transcriptons. We further show that there is a strong tendency for the H-NS binding sites to be clustered, both within operons and in genes contained in the pathogenicity-associated islands. In accordance with previously published findings, we show that these motifs occur in AT-rich regions of DNA. On the basis of these observations, we propose that H-NS silences extensive regions of the bacterial chromosome by binding first to nucleating high-affinity sites and then spreading along AT-rich DNA. This spreading would be reinforced by the frequent occurrence of the motif in such regions. Our findings suggest that such an organization enables the silencing of extensive regions of the genetic material, thereby providing a coherent framework that unifies studies on the H-NS protein and a concrete molecular basis for the genetic control of H-NS transcriptional silencing.",

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T1 - High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes

AU - Lang, Benjamin

AU - Blot, Nicolas

AU - Bouffartigues, Emeline

AU - Buckle, Malcolm

AU - Geertz, Marcel

AU - Gualerzi, Claudio O.

AU - Mavathur, Ramesh

AU - Muskhelishvili, Georgi

AU - Pon, Cynthia L.

AU - Rimsky, Sylvie

AU - Stella, Stefano

AU - Babu, M. Madan

AU - Travers, Andrew

PY - 2007/9/1

Y1 - 2007/9/1

N2 - The global transcriptional regulator H-NS selectively silences bacterial genes associated with pathogenicity and responses to environmental insults. Although there is ample evidence that H-NS binds preferentially to DNA containing curved regions, we show here that a major basis for this selectivity is the presence of a conserved sequence motif in H-NS target transcriptons. We further show that there is a strong tendency for the H-NS binding sites to be clustered, both within operons and in genes contained in the pathogenicity-associated islands. In accordance with previously published findings, we show that these motifs occur in AT-rich regions of DNA. On the basis of these observations, we propose that H-NS silences extensive regions of the bacterial chromosome by binding first to nucleating high-affinity sites and then spreading along AT-rich DNA. This spreading would be reinforced by the frequent occurrence of the motif in such regions. Our findings suggest that such an organization enables the silencing of extensive regions of the genetic material, thereby providing a coherent framework that unifies studies on the H-NS protein and a concrete molecular basis for the genetic control of H-NS transcriptional silencing.

AB - The global transcriptional regulator H-NS selectively silences bacterial genes associated with pathogenicity and responses to environmental insults. Although there is ample evidence that H-NS binds preferentially to DNA containing curved regions, we show here that a major basis for this selectivity is the presence of a conserved sequence motif in H-NS target transcriptons. We further show that there is a strong tendency for the H-NS binding sites to be clustered, both within operons and in genes contained in the pathogenicity-associated islands. In accordance with previously published findings, we show that these motifs occur in AT-rich regions of DNA. On the basis of these observations, we propose that H-NS silences extensive regions of the bacterial chromosome by binding first to nucleating high-affinity sites and then spreading along AT-rich DNA. This spreading would be reinforced by the frequent occurrence of the motif in such regions. Our findings suggest that such an organization enables the silencing of extensive regions of the genetic material, thereby providing a coherent framework that unifies studies on the H-NS protein and a concrete molecular basis for the genetic control of H-NS transcriptional silencing.

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EP - 6337

JO - Nucleic Acids Research

JF - Nucleic Acids Research

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High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes

Abstract

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