Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.

<h4>Background</h4>Members of the WhiB-like (Wbl) protein family possess iron-sulfur clusters and are implicated in the regulation of developmental processes in Actinomycetes. Mycobacterium tuberculosis possesses seven Wbl proteins. The [4Fe-4S] cluster of M. tuberculosis WhiB1 is relati...

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Main Authors: Laura J Smith, Melanie R Stapleton, Roger S Buxton, Jeffrey Green
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0040407&type=printable
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author Laura J Smith
Melanie R Stapleton
Roger S Buxton
Jeffrey Green
author_facet Laura J Smith
Melanie R Stapleton
Roger S Buxton
Jeffrey Green
author_sort Laura J Smith
collection DOAJ
description <h4>Background</h4>Members of the WhiB-like (Wbl) protein family possess iron-sulfur clusters and are implicated in the regulation of developmental processes in Actinomycetes. Mycobacterium tuberculosis possesses seven Wbl proteins. The [4Fe-4S] cluster of M. tuberculosis WhiB1 is relatively insensitive to O(2) but very sensitive to nitric oxide (NO). Nitric oxide nitrosylates the WhiB1 iron-sulfur cluster and promotes DNA-binding; the apo-forms of WhiB1 also bind DNA. However, the molecular requirements for iron-sulfur cluster acquisition and for DNA-binding by WhiB1 are poorly characterized.<h4>Methods and findings</h4>WhiB1 variants were created by site-directed mutagenesis and the abilities of the corresponding proteins to acquire an iron-sulfur cluster and/or bind to whiB1 promoter DNA were assessed. All four Cys residues (Cys9, 37, 40, and 46) in the N-terminal region of WhiB1 were required for incorporation of a [4Fe-4S] cluster, whereas a possible alternative cluster ligand Asp13 (by analogy with M. smegmatis WhiB2) was not. The C-terminal region of WhiB1 is predicted to house the DNA-binding domain of the protein consisting of a predicted β-turn ((58)GVWGG(62)) followed by two amino acid motifs ((72)KRRN(75) and (78)TKAR(81)) that are conserved in WhiB1 proteins. Gly residues (Gly58, 61 and 62) in the β-turn and positively-charged residues (Lys72, Arg73, Arg74, Lys79 and Arg81) in the downstream conserved regions were required for binding of WhiB1 DNA.<h4>Conclusions</h4>Site-directed mutagenesis of M. tuberculosis whiB1 and characterization of the corresponding proteins has been used to explore structure-function relationships of the NO-responsive transcription factor WhiB1. This showed that all four conserved Cys residues in the N-terminal region are required for incorporation of iron-sulfur clusters but not for DNA-binding. Analysis of variants with amino acid substitutions in the C-terminal region revealed the crucial roles played by a predicted β-turn and two conserved positively-charged motifs in facilitating DNA-binding, but not iron-sulfur cluster acquisition, by WhiB1.
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spelling doaj-art-10ece77a1e1a458089d5d5b6d7688b8f2025-08-20T02:30:51ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0177e4040710.1371/journal.pone.0040407Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.Laura J SmithMelanie R StapletonRoger S BuxtonJeffrey Green<h4>Background</h4>Members of the WhiB-like (Wbl) protein family possess iron-sulfur clusters and are implicated in the regulation of developmental processes in Actinomycetes. Mycobacterium tuberculosis possesses seven Wbl proteins. The [4Fe-4S] cluster of M. tuberculosis WhiB1 is relatively insensitive to O(2) but very sensitive to nitric oxide (NO). Nitric oxide nitrosylates the WhiB1 iron-sulfur cluster and promotes DNA-binding; the apo-forms of WhiB1 also bind DNA. However, the molecular requirements for iron-sulfur cluster acquisition and for DNA-binding by WhiB1 are poorly characterized.<h4>Methods and findings</h4>WhiB1 variants were created by site-directed mutagenesis and the abilities of the corresponding proteins to acquire an iron-sulfur cluster and/or bind to whiB1 promoter DNA were assessed. All four Cys residues (Cys9, 37, 40, and 46) in the N-terminal region of WhiB1 were required for incorporation of a [4Fe-4S] cluster, whereas a possible alternative cluster ligand Asp13 (by analogy with M. smegmatis WhiB2) was not. The C-terminal region of WhiB1 is predicted to house the DNA-binding domain of the protein consisting of a predicted β-turn ((58)GVWGG(62)) followed by two amino acid motifs ((72)KRRN(75) and (78)TKAR(81)) that are conserved in WhiB1 proteins. Gly residues (Gly58, 61 and 62) in the β-turn and positively-charged residues (Lys72, Arg73, Arg74, Lys79 and Arg81) in the downstream conserved regions were required for binding of WhiB1 DNA.<h4>Conclusions</h4>Site-directed mutagenesis of M. tuberculosis whiB1 and characterization of the corresponding proteins has been used to explore structure-function relationships of the NO-responsive transcription factor WhiB1. This showed that all four conserved Cys residues in the N-terminal region are required for incorporation of iron-sulfur clusters but not for DNA-binding. Analysis of variants with amino acid substitutions in the C-terminal region revealed the crucial roles played by a predicted β-turn and two conserved positively-charged motifs in facilitating DNA-binding, but not iron-sulfur cluster acquisition, by WhiB1.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0040407&type=printable
spellingShingle Laura J Smith
Melanie R Stapleton
Roger S Buxton
Jeffrey Green
Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.
PLoS ONE
title Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.
title_full Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.
title_fullStr Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.
title_full_unstemmed Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.
title_short Structure-function relationships of the Mycobacterium tuberculosis transcription factor WhiB1.
title_sort structure function relationships of the mycobacterium tuberculosis transcription factor whib1
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0040407&type=printable
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