Impact of uranium (U) on the cellular glutathione pool and resultant consequences for the redox status of U

Viehweger, Katrin; Geipel, Gerhard; Bernhard, Gert

doi:10.1007/s10534-011-9478-6

Cited by 22 publications

(18 citation statements)

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“…The fact that GSH and oxidized GSH (GSSG) levels are increased in uranyl-supplemented cultures of plant cells (26) or hepatocytes (27) is a strong indication that GSH is also involved in uranyl detoxification in higher organisms, in which uranyl toxicity has been related to oxidative stress (1). Although consistent with uranyl-induced GSH production, mechanisms other than ROS suppression by GSH-dependent detoxification need to be considered.…”

Section: Discussionmentioning

confidence: 99%

“…The toxicity of uranium has been linked to oxidative stress, as deduced from effects on intracellular GSH levels in plants (24,25). It has been shown that uranyl affects the levels of both GSH and its oxidized form, GSSG, in cultured plant cells (26) and animals (27). However, the effect of uranyl on GSH levels is not uniform among the tested model organisms and cell cultures, nor does the GSH level vary in proportion to the uranyl concentration within a given system.…”

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confidence: 99%

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Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis

Obeid

Oertel

Solioz

et al. 2016

Appl Environ Microbiol

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b ABSTRACTBoth prokaryotic and eukaryotic organisms possess mechanisms for the detoxification of heavy metals, and these mechanisms are found among distantly related species. We investigated the role of intracellular glutathione (GSH), which, in a large number of taxa, plays a role in protection against the toxicity of common heavy metals. Anaerobically grown Lactococcus lactis containing an inducible GSH synthesis pathway was used as a model organism. Its physiological condition allowed study of putative GSH-dependent uranyl detoxification mechanisms without interference from additional reactive oxygen species. By microcalorimetric measurements of metabolic heat during cultivation, it was shown that intracellular GSH attenuates the toxicity of uranium at a concentration in the range of 10 to 150 M. In this concentration range, no effect was observed with copper, which was used as a reference for redox metal toxicity. At higher copper concentrations, GSH aggravated metal toxicity. Isothermal titration calorimetry revealed the endothermic binding of U(VI) to the carboxyl group(s) of GSH rather than to the reducing thiol group involved in copper interactions. The data indicate that the primary detoxifying mechanism is the intracellular sequestration of carboxyl-coordinated U(VI) into an insoluble complex with GSH. The opposite effects on uranyl and on copper toxicity can be related to the difference in coordination chemistry of the respective metal-GSH complexes, which cause distinct growth phase-specific effects on enzyme-metal interactions. IMPORTANCEUnderstanding microbial metal resistance is of particular importance for bioremediation, where microorganisms are employed for the removal of heavy metals from the environment. This strategy is increasingly being considered for uranium. However, little is known about the molecular mechanisms of uranyl detoxification. Existing studies of different taxa show little systematics but hint at a role of glutathione (GSH). Previous work could not unequivocally demonstrate a GSH function in decreasing the presumed uranyl-induced oxidative stress, nor could a redox-independent detoxifying action of GSH be identified. Combining metabolic calorimetry with cell number-based assays and genetics analysis enables a novel and general approach to quantify toxicity and relate it to molecular mechanisms. The results show that GSH-expressing microorganisms appear advantageous for uranyl bioremediation.T he natural abundance of uranium and the increasing health risks that originate from its anthropogenic release to the environment have generated a high demand for understanding the molecular mechanisms of uranium toxicity. Its radiotoxicity is of minor ecological relevance compared to its toxicity due to chemical interference with metabolism (1, 2). The latter is caused mostly by the displacement of Ca 2ϩ and Mg 2ϩ from functionally important binding sites in enzymes (3). The water-soluble uranyl cation UO 2 2ϩ is the most commonly found contaminant, which contains uranium in its highest ...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis

Obeid

Oertel

Solioz

et al. 2016

Appl Environ Microbiol

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“…(Vandenhove et al 2006) found altered levels of the glutathione pool depending on the applied uranium concentrations in Phaseolus vulgaris after a week of exposure. Concerning the initial phase of metal contact (up to 24 hours), there was no significant change of GSH whereas the amount of GSSG increased upon exposure of moderate uranium concentrations (≤ 10 μM) in cell suspensions of canola ( Brassica napus ) (Viehweger et al 2011. This indicates clearly its function as redox couple (E pH7.4 ;Schafer and Buettner = −264 mV at 25°C, Schafer and Buettner Schafer and Buettner 2001) and underlines the consumption of cellular reducing capacity during heavy metal accumulation and causes oxidative stress.…”

Section: Heavy Metal Tolerance and Toxicity On Cellular Levelmentioning

confidence: 99%

How plants cope with heavy metals

2014

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Heavy metals are naturally occurring in the earth‘s crust but anthropogenic and industrial activities have led to drastic environmental pollutions in distinct areas. Plants are able to colonize such sites due to several mechanisms of heavy metal tolerance. Understanding of these pathways enables different fruitful approaches like phytoremediation and biofortification.Therefore, this review addresses mechanisms of heavy metal tolerance and toxicity in plants possessing a sophisticated network for maintenance of metal homeostasis. Key elements of this are chelation and sequestration which result either in removal of toxic metal from sensitive sites or conduct essential metal to their specific cellular destination. This implies shared pathways which can result in toxic symptoms especially in an excess of metal. These overlaps go on with signal transduction pathways induced by heavy metals which include common elements of other signal cascades. Nevertheless, there are specific reactions some of them will be discussed with special focus on the cellular level.Electronic supplementary materialThe online version of this article (doi:10.1186/1999-3110-55-35) contains supplementary material, which is available to authorized users.

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“…An increase in the antioxidative metabolites after heavy metal exposure has been observed before by Vanhoudt et al [ 15 ]. In addition, exposing a cell culture of Brassica napus to 50 µM U resulted in a significant increase in GSH concentration [ 45 ]. Finally, Aranjuelo et al [ 46 ] observed in glutathione deficient Arabidopsis mutants ( cad2.1 ) the highest MDA and least reduced ascorbate levels, which highlights the importance of GSH under U stress.…”

Section: Discussionmentioning

confidence: 99%

Induction of Oxidative Stress and Antioxidative Mechanisms in Arabidopsis thaliana after Uranium Exposure at pH 7.5

Saenen

Horemans

Vanhoudt

et al. 2015

IJMS

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To evaluate the environmental impact of uranium (U) contamination, it is important to investigate the effects of U at ecologically relevant conditions. Since U speciation, and hence its toxicity, strongly depends on environmental pH, the present study aimed to investigate dose-dependent effects of U at pH 7.5. Arabidopsis thaliana plants (Mouse-ear Cress) were exposed for three days to different U concentrations at pH 7.5. In the roots, the increased capacities of ascorbate peroxidase and glutathione reductase indicate an important role for the ascorbate-glutathione cycle during U-induced stress. However, a significant decrease in the ascorbate redox state was observed after exposure to 75 and 100 µM U, indicating that those roots are severely stressed. In accordance with the roots, the ascorbate-glutathione cycle plays an important role in the antioxidative defence systems in A. thaliana leaves exposed to U at pH 7.5 as the ascorbate and glutathione biosynthesis were upregulated. In addition, small inductions of enzymes of the antioxidative defence system were observed at lower U concentrations to counteract the U-induced stress. However, at higher U concentrations it seems that the antioxidative defence system of the leaves collapses as reductions in enzyme activities and gene expression levels were observed.

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Impact of uranium (U) on the cellular glutathione pool and resultant consequences for the redox status of U

Cited by 22 publications

References 29 publications

Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis

Mechanism of Attenuation of Uranyl Toxicity by Glutathione in Lactococcus lactis

How plants cope with heavy metals

Induction of Oxidative Stress and Antioxidative Mechanisms in Arabidopsis thaliana after Uranium Exposure at pH 7.5

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