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Research article

Molecular basis for the integration of environmental signals by FurB from Anabaena sp. PCC 7120

Violeta C. Sein-Echaluce, María Carmen Pallarés, Anabel Lostao, Inmaculada Yruela, Adrián Velázquez-Campoy, M. Luisa Peleato, María F. Fillat
Biochemical Journal Jan 05, 2018, 475 (1) 151-168; DOI: 10.1042/BCJ20170692
Violeta C. Sein-Echaluce
Departamento de Bioquímica y Biología Molecular y Celular, Universidad de Zaragoza, 50009 Zaragoza, SpainInstituto de Biocomputación y Física de Sistemas Complejos (BIFI), Joint Unit IQFR-CSIC-BIFI, Universidad de Zaragoza, 50018 Zaragoza, Spain
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María Carmen Pallarés
Laboratorio de Microscopías Avanzadas, Instituto de Nanociencia de Aragón (INA), Universidad de Zaragoza, 50018 Zaragoza, Spain
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Anabel Lostao
Laboratorio de Microscopías Avanzadas, Instituto de Nanociencia de Aragón (INA), Universidad de Zaragoza, 50018 Zaragoza, SpainFundación ARAID, 50018 Zaragoza, SpainFundación INA, 50018 Zaragoza, Spain
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Inmaculada Yruela
Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas (EEAD-CSIC), 50059 Zaragoza, SpainGBsC (BIFI, UNIZAR), Unidad Asociada al CSIC, Zaragoza, Spain
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Adrián Velázquez-Campoy
Departamento de Bioquímica y Biología Molecular y Celular, Universidad de Zaragoza, 50009 Zaragoza, SpainInstituto de Biocomputación y Física de Sistemas Complejos (BIFI), Joint Unit IQFR-CSIC-BIFI, Universidad de Zaragoza, 50018 Zaragoza, SpainFundación ARAID, 50018 Zaragoza, SpainGBsC (BIFI, UNIZAR), Unidad Asociada al CSIC, Zaragoza, SpainInstituto de Investigación Sanitaria Aragón (IIS Aragon), 50009 Zaragoza, Spain
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M. Luisa Peleato
Departamento de Bioquímica y Biología Molecular y Celular, Universidad de Zaragoza, 50009 Zaragoza, SpainInstituto de Biocomputación y Física de Sistemas Complejos (BIFI), Joint Unit IQFR-CSIC-BIFI, Universidad de Zaragoza, 50018 Zaragoza, SpainGBsC (BIFI, UNIZAR), Unidad Asociada al CSIC, Zaragoza, Spain
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María F. Fillat
Departamento de Bioquímica y Biología Molecular y Celular, Universidad de Zaragoza, 50009 Zaragoza, SpainInstituto de Biocomputación y Física de Sistemas Complejos (BIFI), Joint Unit IQFR-CSIC-BIFI, Universidad de Zaragoza, 50018 Zaragoza, SpainGBsC (BIFI, UNIZAR), Unidad Asociada al CSIC, Zaragoza, Spain
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  • For correspondence: fillat@unizar.es
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Abstract

FUR (Ferric uptake regulator) proteins are among the most important families of transcriptional regulators in prokaryotes, often behaving as global regulators. In the cyanobacterium Anabaena PCC 7120, FurB (Zur, Zinc uptake regulator) controls zinc and redox homeostasis through the repression of target genes in a zinc-dependent manner. In vitro, non-specific binding of FurB to DNA elicits protection against oxidative damage and avoids cleavage by deoxyribonuclease I. The present study provides, for the first time, evidence of the influence of redox environment in the interaction of FurB with regulatory zinc and its consequences in FurB–DNA-binding affinity. Calorimetry studies showed that, in addition to one structural Zn(II), FurB is able to bind two additional Zn(II) per monomer and demonstrated the implication of cysteine C93 in regulatory Zn(II) coordination. The interaction of FurB with the second regulatory zinc occurred only under reducing conditions. While non-specific FurB–DNA interaction is Zn(II)-independent, the optimal binding of FurB to target promoters required loading of two regulatory zinc ions. Those results combined with site-directed mutagenesis and gel-shift assays evidenced that the redox state of cysteine C93 conditions the binding of the second regulatory Zn(II) and, in turn, modulates the affinity for a specific DNA target. Furthermore, differential spectroscopy studies showed that cysteine C93 could also be involved in heme coordination by FurB, either as a direct ligand or being located near the binding site. The results indicate that besides controlling zinc homeostasis, FurB could work as a redox-sensing protein probably modifying its zinc and DNA-binding abilities depending upon environmental conditions.

  • cyanobacteria
  • FurB/Zur
  • heme binding
  • redox signalling
  • zinc loading
  • Abbreviations

    AFM,
    atomic force microscopy;
    CPV,
    cysteine-proline-valine motif;
    DNase I,
    deoxyribonuclease I;
    DTT,
    dithiothreitol;
    EMSA,
    electrophoretic mobility shift assay;
    FUR,
    ferric uptake regulator;
    GdnHCl,
    guanidine hydrochloride;
    ICP-MS,
    inductively coupled plasma mass spectrometry;
    IPTG,
    isopropyl β-d-1-thiogalactopyranoside;
    ITC,
    isothermal titration calorimetry;
    Mur,
    manganese uptake regulator;
    Nur,
    nickel uptake regulator;
    Pall425,
    promoter region of the all4725 gene;
    PAR,
    4-(2-pyridylazo)-resorcinol;
    PDB,
    Protein Data Bank;
    PerR,
    peroxide-stress response;
    PfurA,
    promoter region of the furA gene;
    PMSF,
    phenylmethylsulfonyl fluoride;
    PnifJ,
    promoter region of the nifJ gene;
    Zur,
    zinc uptake regulator
    • © 2018 The Author(s). Published by Portland Press Limited on behalf of the Biochemical Society
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    January 2018

    Volume: 475 Issue: 1

    Biochemical Journal: 475 (1)
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    Molecular basis for the integration of environmental signals by FurB from Anabaena sp. PCC 7120
    Violeta C. Sein-Echaluce, María Carmen Pallarés, Anabel Lostao, Inmaculada Yruela, Adrián Velázquez-Campoy, M. Luisa Peleato, María F. Fillat
    Biochemical Journal Jan 2018, 475 (1) 151-168; DOI: 10.1042/BCJ20170692
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    Molecular basis for the integration of environmental signals by FurB from Anabaena sp. PCC 7120
    Violeta C. Sein-Echaluce, María Carmen Pallarés, Anabel Lostao, Inmaculada Yruela, Adrián Velázquez-Campoy, M. Luisa Peleato, María F. Fillat
    Biochemical Journal Jan 2018, 475 (1) 151-168; DOI: 10.1042/BCJ20170692

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    Keywords

    cyanobacteria
    FurB/Zur
    heme binding
    redox signalling
    zinc loading

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