Cargando…

Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae

Elemental uptake and export of the cell are tightly regulated thereby maintaining the ionomic homeostasis. This equilibrium can be disrupted upon exposure to exogenous reactive oxygen species (ROS), leading to reduction or elevation of the intracellular metal ions. In this study, the ionomic composi...

Descripción completa

Detalles Bibliográficos
Autores principales: Wu, Ming J., O’Doherty, Patrick J., Murphy, Patricia A., Lyons, Victoria, Christophersen, Melinda, Rogers, Peter J., Bailey, Trevor D., Higgins, Vincent J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Molecular Diversity Preservation International (MDPI) 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3233460/
https://www.ncbi.nlm.nih.gov/pubmed/22174654
http://dx.doi.org/10.3390/ijms12118119
_version_ 1782218414313439232
author Wu, Ming J.
O’Doherty, Patrick J.
Murphy, Patricia A.
Lyons, Victoria
Christophersen, Melinda
Rogers, Peter J.
Bailey, Trevor D.
Higgins, Vincent J.
author_facet Wu, Ming J.
O’Doherty, Patrick J.
Murphy, Patricia A.
Lyons, Victoria
Christophersen, Melinda
Rogers, Peter J.
Bailey, Trevor D.
Higgins, Vincent J.
author_sort Wu, Ming J.
collection PubMed
description Elemental uptake and export of the cell are tightly regulated thereby maintaining the ionomic homeostasis. This equilibrium can be disrupted upon exposure to exogenous reactive oxygen species (ROS), leading to reduction or elevation of the intracellular metal ions. In this study, the ionomic composition in the eukaryotic model organism Saccharomyces cerevisiae was profiled using the inductively-coupled plasma optical emission spectrometer (ICP-OES) following the treatment with individual ROS, including hydrogen peroxide, cumen hydroperoxide, linoleic acid hydroperoxide (LAH), the superoxide-generating agent menadione, the thiol-oxidising agent diamide [diazine-dicarboxylic acid-bis(dimethylamide)], dimedone and peroxynitrite. The findings demonstrated that different ROS resulted in distinct changes in cellular metal ions. Aluminium (Al(3+)) level rose up to 50-fold after the diamide treatment. Cellular potassium (K(+)) in LAH-treated cells was 26-fold less compared to the non-treated controls. The diamide-induced Al(3+) accumulation was further validated by the enhanced Al(3+) uptake along the time course and diamide doses. Pre-incubation of yeast with individual elements including iron, copper, manganese and magnesium failed to block diamide-induced Al(3+) uptake, suggesting Al(3+)-specific transporters could be involved in Al(3+) uptake. Furthermore, LAH-induced potassium depletion was validated by a rescue experiment in which addition of potassium increased yeast growth in LAH-containing media by 26% compared to LAH alone. Taken together, the data, for the first time, demonstrated the linkage between ionomic profiles and individual oxidative conditions.
format Online
Article
Text
id pubmed-3233460
institution National Center for Biotechnology Information
language English
publishDate 2011
publisher Molecular Diversity Preservation International (MDPI)
record_format MEDLINE/PubMed
spelling pubmed-32334602011-12-15 Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae Wu, Ming J. O’Doherty, Patrick J. Murphy, Patricia A. Lyons, Victoria Christophersen, Melinda Rogers, Peter J. Bailey, Trevor D. Higgins, Vincent J. Int J Mol Sci Article Elemental uptake and export of the cell are tightly regulated thereby maintaining the ionomic homeostasis. This equilibrium can be disrupted upon exposure to exogenous reactive oxygen species (ROS), leading to reduction or elevation of the intracellular metal ions. In this study, the ionomic composition in the eukaryotic model organism Saccharomyces cerevisiae was profiled using the inductively-coupled plasma optical emission spectrometer (ICP-OES) following the treatment with individual ROS, including hydrogen peroxide, cumen hydroperoxide, linoleic acid hydroperoxide (LAH), the superoxide-generating agent menadione, the thiol-oxidising agent diamide [diazine-dicarboxylic acid-bis(dimethylamide)], dimedone and peroxynitrite. The findings demonstrated that different ROS resulted in distinct changes in cellular metal ions. Aluminium (Al(3+)) level rose up to 50-fold after the diamide treatment. Cellular potassium (K(+)) in LAH-treated cells was 26-fold less compared to the non-treated controls. The diamide-induced Al(3+) accumulation was further validated by the enhanced Al(3+) uptake along the time course and diamide doses. Pre-incubation of yeast with individual elements including iron, copper, manganese and magnesium failed to block diamide-induced Al(3+) uptake, suggesting Al(3+)-specific transporters could be involved in Al(3+) uptake. Furthermore, LAH-induced potassium depletion was validated by a rescue experiment in which addition of potassium increased yeast growth in LAH-containing media by 26% compared to LAH alone. Taken together, the data, for the first time, demonstrated the linkage between ionomic profiles and individual oxidative conditions. Molecular Diversity Preservation International (MDPI) 2011-11-18 /pmc/articles/PMC3233460/ /pubmed/22174654 http://dx.doi.org/10.3390/ijms12118119 Text en © 2011 by the authors; licensee MDPI, Basel, Switzerland. http://creativecommons.org/licenses/by/3.0 This article is an open-access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
spellingShingle Article
Wu, Ming J.
O’Doherty, Patrick J.
Murphy, Patricia A.
Lyons, Victoria
Christophersen, Melinda
Rogers, Peter J.
Bailey, Trevor D.
Higgins, Vincent J.
Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae
title Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae
title_full Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae
title_fullStr Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae
title_full_unstemmed Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae
title_short Different Reactive Oxygen Species Lead to Distinct Changes of Cellular Metal Ions in the Eukaryotic Model Organism Saccharomyces cerevisiae
title_sort different reactive oxygen species lead to distinct changes of cellular metal ions in the eukaryotic model organism saccharomyces cerevisiae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3233460/
https://www.ncbi.nlm.nih.gov/pubmed/22174654
http://dx.doi.org/10.3390/ijms12118119
work_keys_str_mv AT wumingj differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae
AT odohertypatrickj differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae
AT murphypatriciaa differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae
AT lyonsvictoria differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae
AT christophersenmelinda differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae
AT rogerspeterj differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae
AT baileytrevord differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae
AT higginsvincentj differentreactiveoxygenspeciesleadtodistinctchangesofcellularmetalionsintheeukaryoticmodelorganismsaccharomycescerevisiae