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Title: Structural basis for the modulation of plant cytosolic triosephosphate isomerase activity by mimicry of redox‐based modifications

Abstract

Summary Reactive oxidative species ( ROS ) and S‐ glutathionylation modulate the activity of plant cytosolic triosephosphate isomerases ( cTPI ). Arabidopsis thaliana cTPI (Atc TPI ) is subject of redox regulation at two reactive cysteines that function as thiol switches. Here we investigate the role of these residues, Atc TPI ‐Cys13 and At‐Cys218, by substituting them with aspartic acid that mimics the irreversible oxidation of cysteine to sulfinic acid and with amino acids that mimic thiol conjugation. Crystallographic studies show that mimicking Atc TPI ‐Cys13 oxidation promotes the formation of inactive monomers by reposition residue Phe75 of the neighboring subunit, into a conformation that destabilizes the dimer interface. Mutations in residue Atc TPI ‐Cys218 to Asp, Lys, or Tyr generate TPI variants with a decreased enzymatic activity by creating structural modifications in two loops (loop 7 and loop 6) whose integrity is necessary to assemble the active site. In contrast with mutations in residue Atc TPI ‐Cys13, mutations in Atc TPI ‐Cys218 do not alter the dimeric nature of Atc TPI . Therefore, modifications of residues Atc TPI ‐Cys13 and Atc TPI ‐Cys218 modulate Atc TPI activity by inducing the formation of inactive monomers and by altering the activemore » site of the dimeric enzyme, respectively. The identity of residue Atc TPI ‐Cys218 is conserved in the majority of plant cytosolic TPI s, this conservation and its solvent‐exposed localization make it the most probable target for TPI regulation upon oxidative damage by reactive oxygen species. Our data reveal the structural mechanisms by which S ‐glutathionylation protects Atc TPI from irreversible chemical modifications and re‐routes carbon metabolism to the pentose phosphate pathway to decrease oxidative stress.« less

Authors:
 [1];  [1];  [2];  [1];  [1];  [1];  [2];  [3]; ORCiD logo [1]
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  1. Laboratorio Nacional de Genómica para la Biodiversidad Centro de Investigación y de Estudios Avanzados del IPN Apartado Postal 629, Irapuato Guanajuato México CP 36821 México
  2. Departamento de Bioquímica Facultad de Medicina Universidad Nacional Autónoma de México Circuito Exterior s/n Ciudad Universitaria Apartado Postal 70‐243 Mexico City 04510 México
  3. Departamento de Bioquímica y Biología Estructural Instituto de Fisiología Celular Universidad Nacional Autónoma de México Circuito Exterior s/n Ciudad Universitaria Apartado Postal 70‐243 México City 04510 México
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1526080
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Name: The Plant Journal Journal Volume: 99 Journal Issue: 5; Journal ID: ISSN 0960-7412
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Castro‐Torres, Eduardo, Jiménez‐Sandoval, Pedro, Romero‐Romero, Sergio, Fuentes‐Pascacio, Alma, López‐Castillo, Laura M., Díaz‐Quezada, Corina, Fernández‐Velasco, D. Alejandro, Torres‐Larios, Alfredo, and Brieba, Luis G. Structural basis for the modulation of plant cytosolic triosephosphate isomerase activity by mimicry of redox‐based modifications. United Kingdom: N. p., 2019. Web. doi:10.1111/tpj.14375.
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Castro‐Torres, Eduardo, Jiménez‐Sandoval, Pedro, Romero‐Romero, Sergio, Fuentes‐Pascacio, Alma, López‐Castillo, Laura M., Díaz‐Quezada, Corina, Fernández‐Velasco, D. Alejandro, Torres‐Larios, Alfredo, & Brieba, Luis G. Structural basis for the modulation of plant cytosolic triosephosphate isomerase activity by mimicry of redox‐based modifications. United Kingdom. https://doi.org/10.1111/tpj.14375
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Castro‐Torres, Eduardo, Jiménez‐Sandoval, Pedro, Romero‐Romero, Sergio, Fuentes‐Pascacio, Alma, López‐Castillo, Laura M., Díaz‐Quezada, Corina, Fernández‐Velasco, D. Alejandro, Torres‐Larios, Alfredo, and Brieba, Luis G. Thu . "Structural basis for the modulation of plant cytosolic triosephosphate isomerase activity by mimicry of redox‐based modifications". United Kingdom. https://doi.org/10.1111/tpj.14375.
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@article{osti_1526080,
title = {Structural basis for the modulation of plant cytosolic triosephosphate isomerase activity by mimicry of redox‐based modifications},
author = {Castro‐Torres, Eduardo and Jiménez‐Sandoval, Pedro and Romero‐Romero, Sergio and Fuentes‐Pascacio, Alma and López‐Castillo, Laura M. and Díaz‐Quezada, Corina and Fernández‐Velasco, D. Alejandro and Torres‐Larios, Alfredo and Brieba, Luis G.},
abstractNote = {Summary Reactive oxidative species ( ROS ) and S‐ glutathionylation modulate the activity of plant cytosolic triosephosphate isomerases ( cTPI ). Arabidopsis thaliana cTPI (Atc TPI ) is subject of redox regulation at two reactive cysteines that function as thiol switches. Here we investigate the role of these residues, Atc TPI ‐Cys13 and At‐Cys218, by substituting them with aspartic acid that mimics the irreversible oxidation of cysteine to sulfinic acid and with amino acids that mimic thiol conjugation. Crystallographic studies show that mimicking Atc TPI ‐Cys13 oxidation promotes the formation of inactive monomers by reposition residue Phe75 of the neighboring subunit, into a conformation that destabilizes the dimer interface. Mutations in residue Atc TPI ‐Cys218 to Asp, Lys, or Tyr generate TPI variants with a decreased enzymatic activity by creating structural modifications in two loops (loop 7 and loop 6) whose integrity is necessary to assemble the active site. In contrast with mutations in residue Atc TPI ‐Cys13, mutations in Atc TPI ‐Cys218 do not alter the dimeric nature of Atc TPI . Therefore, modifications of residues Atc TPI ‐Cys13 and Atc TPI ‐Cys218 modulate Atc TPI activity by inducing the formation of inactive monomers and by altering the active site of the dimeric enzyme, respectively. The identity of residue Atc TPI ‐Cys218 is conserved in the majority of plant cytosolic TPI s, this conservation and its solvent‐exposed localization make it the most probable target for TPI regulation upon oxidative damage by reactive oxygen species. Our data reveal the structural mechanisms by which S ‐glutathionylation protects Atc TPI from irreversible chemical modifications and re‐routes carbon metabolism to the pentose phosphate pathway to decrease oxidative stress.},
doi = {10.1111/tpj.14375},
journal = {The Plant Journal},
number = 5,
volume = 99,
place = {United Kingdom},
year = {Thu Jun 13 00:00:00 EDT 2019},
month = {Thu Jun 13 00:00:00 EDT 2019}
}
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