Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein

Daouda A K Traore; Abdelnasser El Ghazouani; Lilian Jacquamet; Franck Borel; Jean -Luc Ferrer; David Lascoux; Jean -Luc Ravanat; Michel Jaquinod; Genevieve Blondin; Christelle Caux-Thang; Victor Duarte; Jean -Marc Latour

doi:10.1038/nchembio.133

Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein

Daouda A K Traore, Abdelnasser El Ghazouani, Lilian Jacquamet, Franck Borel, Jean -Luc Ferrer, David Lascoux, Jean -Luc Ravanat, Michel Jaquinod, Genevieve Blondin, Christelle Caux-Thang, Victor Duarte, Jean -Marc Latour

Research output: Contribution to journal › Article › Research › peer-review

78 Citations (Scopus)

Abstract

In Bacillus subtilis, PerR is a metal-dependent sensor of hydrogen peroxide. PerR is a dimeric zinc protein with a regulatory site that coordinates either Fe2+ (PerR-Zn-Fe) or Mn2+ (PerR-Zn-Mn). Though most of the peroxide sensors use cysteines to detect H2O2, it has been shown that reaction of PerR-Zn-Fe with H2O2 leads to the oxidation of one histidine residue. Oxidation of PerR leads to the incorporation of one oxygen atom into His37 or His91. This study presents the crystal structure of the oxidized PerR protein (PerR-Zn-ox), which clearly shows a 2-oxo-histidine residue in position 37. Formation of 2-oxo-histidine is demonstrated and quantified by HPLC-MS/MS. EPR experiments indicate that PerR-Zn-H37ox retains a significant affinity for the regulatory metal, whereas PerR-Zn-H91ox shows a considerably reduced affinity for the metal ion. In spite of these major differences in terms of metal binding affinity, oxidation of His37 and/or His91 in PerR prevents DNA binding.

Original language	English
Pages (from-to)	53 - 59
Number of pages	7
Journal	Nature Chemical Biology
Volume	5
Issue number	1
DOIs	https://doi.org/10.1038/nchembio.133
Publication status	Published - 2009
Externally published	Yes

Cite this

Traore, D. A. K., El Ghazouani, A., Jacquamet, L., Borel, F., Ferrer, J. -L., Lascoux, D., Ravanat, J. -L., Jaquinod, M., Blondin, G., Caux-Thang, C., Duarte, V., & Latour, J. -M. (2009). Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein. Nature Chemical Biology, 5(1), 53 - 59. https://doi.org/10.1038/nchembio.133

Traore, Daouda A K ; El Ghazouani, Abdelnasser ; Jacquamet, Lilian ; Borel, Franck ; Ferrer, Jean -Luc ; Lascoux, David ; Ravanat, Jean -Luc ; Jaquinod, Michel ; Blondin, Genevieve ; Caux-Thang, Christelle ; Duarte, Victor ; Latour, Jean -Marc. / Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein. In: Nature Chemical Biology. 2009 ; Vol. 5, No. 1. pp. 53 - 59.

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title = "Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein",

abstract = "In Bacillus subtilis, PerR is a metal-dependent sensor of hydrogen peroxide. PerR is a dimeric zinc protein with a regulatory site that coordinates either Fe2+ (PerR-Zn-Fe) or Mn2+ (PerR-Zn-Mn). Though most of the peroxide sensors use cysteines to detect H2O2, it has been shown that reaction of PerR-Zn-Fe with H2O2 leads to the oxidation of one histidine residue. Oxidation of PerR leads to the incorporation of one oxygen atom into His37 or His91. This study presents the crystal structure of the oxidized PerR protein (PerR-Zn-ox), which clearly shows a 2-oxo-histidine residue in position 37. Formation of 2-oxo-histidine is demonstrated and quantified by HPLC-MS/MS. EPR experiments indicate that PerR-Zn-H37ox retains a significant affinity for the regulatory metal, whereas PerR-Zn-H91ox shows a considerably reduced affinity for the metal ion. In spite of these major differences in terms of metal binding affinity, oxidation of His37 and/or His91 in PerR prevents DNA binding.",

author = "Traore, {Daouda A K} and {El Ghazouani}, Abdelnasser and Lilian Jacquamet and Franck Borel and Ferrer, {Jean -Luc} and David Lascoux and Ravanat, {Jean -Luc} and Michel Jaquinod and Genevieve Blondin and Christelle Caux-Thang and Victor Duarte and Latour, {Jean -Marc}",

year = "2009",

doi = "10.1038/nchembio.133",

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pages = "53 -- 59",

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Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein. / Traore, Daouda A K; El Ghazouani, Abdelnasser; Jacquamet, Lilian; Borel, Franck; Ferrer, Jean -Luc; Lascoux, David; Ravanat, Jean -Luc; Jaquinod, Michel; Blondin, Genevieve; Caux-Thang, Christelle; Duarte, Victor; Latour, Jean -Marc.

In: Nature Chemical Biology, Vol. 5, No. 1, 2009, p. 53 - 59.

Research output: Contribution to journal › Article › Research › peer-review

TY - JOUR

T1 - Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein

AU - Traore, Daouda A K

AU - El Ghazouani, Abdelnasser

AU - Jacquamet, Lilian

AU - Borel, Franck

AU - Ferrer, Jean -Luc

AU - Lascoux, David

AU - Ravanat, Jean -Luc

AU - Jaquinod, Michel

AU - Blondin, Genevieve

AU - Caux-Thang, Christelle

AU - Duarte, Victor

AU - Latour, Jean -Marc

PY - 2009

Y1 - 2009

N2 - In Bacillus subtilis, PerR is a metal-dependent sensor of hydrogen peroxide. PerR is a dimeric zinc protein with a regulatory site that coordinates either Fe2+ (PerR-Zn-Fe) or Mn2+ (PerR-Zn-Mn). Though most of the peroxide sensors use cysteines to detect H2O2, it has been shown that reaction of PerR-Zn-Fe with H2O2 leads to the oxidation of one histidine residue. Oxidation of PerR leads to the incorporation of one oxygen atom into His37 or His91. This study presents the crystal structure of the oxidized PerR protein (PerR-Zn-ox), which clearly shows a 2-oxo-histidine residue in position 37. Formation of 2-oxo-histidine is demonstrated and quantified by HPLC-MS/MS. EPR experiments indicate that PerR-Zn-H37ox retains a significant affinity for the regulatory metal, whereas PerR-Zn-H91ox shows a considerably reduced affinity for the metal ion. In spite of these major differences in terms of metal binding affinity, oxidation of His37 and/or His91 in PerR prevents DNA binding.

AB - In Bacillus subtilis, PerR is a metal-dependent sensor of hydrogen peroxide. PerR is a dimeric zinc protein with a regulatory site that coordinates either Fe2+ (PerR-Zn-Fe) or Mn2+ (PerR-Zn-Mn). Though most of the peroxide sensors use cysteines to detect H2O2, it has been shown that reaction of PerR-Zn-Fe with H2O2 leads to the oxidation of one histidine residue. Oxidation of PerR leads to the incorporation of one oxygen atom into His37 or His91. This study presents the crystal structure of the oxidized PerR protein (PerR-Zn-ox), which clearly shows a 2-oxo-histidine residue in position 37. Formation of 2-oxo-histidine is demonstrated and quantified by HPLC-MS/MS. EPR experiments indicate that PerR-Zn-H37ox retains a significant affinity for the regulatory metal, whereas PerR-Zn-H91ox shows a considerably reduced affinity for the metal ion. In spite of these major differences in terms of metal binding affinity, oxidation of His37 and/or His91 in PerR prevents DNA binding.

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U2 - 10.1038/nchembio.133

DO - 10.1038/nchembio.133

M3 - Article

VL - 5

SP - 53

EP - 59

JO - Nature Chemical Biology

JF - Nature Chemical Biology

SN - 1552-4450

IS - 1

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