Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.

Selenium (Se) is an element that in trace quantities is both essential in mammals but also toxic to bacteria, yeast, plants and animals, including C. elegans. Our previous studies showed that selenite was four times as toxic as selenate to C. elegans, but that deletion of thioredoxin reductase did n...

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Main Authors: Christopher J Boehler, Anna M Raines, Roger A Sunde
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4074201?pdf=render
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author Christopher J Boehler
Anna M Raines
Roger A Sunde
author_facet Christopher J Boehler
Anna M Raines
Roger A Sunde
author_sort Christopher J Boehler
collection DOAJ
description Selenium (Se) is an element that in trace quantities is both essential in mammals but also toxic to bacteria, yeast, plants and animals, including C. elegans. Our previous studies showed that selenite was four times as toxic as selenate to C. elegans, but that deletion of thioredoxin reductase did not modulate Se toxicity. To characterize Se regulation of the full transcriptome, we conducted a microarray study in C. elegans cultured in axenic media supplemented with 0, 0.05, 0.1, 0.2, and 0.4 mM Se as selenite. C. elegans cultured in 0.2 and 0.4 mM Se displayed a significant delay in growth as compared to 0, 0.05, or 0.1 mM Se, indicating Se-induced toxicity, so worms were staged to mid-L4 larval stage for these studies. Relative to 0.1 mM Se treatment, culturing C. elegans at these Se concentrations resulted in 1.9, 9.7, 5.5, and 2.3%, respectively, of the transcriptome being altered by at least 2-fold. This toxicity altered the expression of 295 overlapping transcripts, which when filtered against gene sets for sulfur and cadmium toxicity, identified a dataset of 182 toxic-Se specific genes that were significantly enriched in functions related to oxidoreductase activity, and significantly depleted in genes related to structural components of collagen and the cuticle. Worms cultured in low Se (0 mM Se) exhibited no signs of deficiency, but low Se was accompanied by a transcriptional response of 59 genes changed ≥2-fold when compared to all other Se concentrations, perhaps due to decreases in Se-dependent TRXR-1 activity. Overall, these results suggest that Se toxicity in C. elegans causes an increase in ROS and stress responses, marked by increased expression of oxidoreductases and reduced expression of cuticle-associated genes, which together underlie the impaired growth observed in these studies.
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spelling doaj.art-6f25d567abe84a208352a3365eca46b12022-12-21T19:04:52ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0196e10140810.1371/journal.pone.0101408Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.Christopher J BoehlerAnna M RainesRoger A SundeSelenium (Se) is an element that in trace quantities is both essential in mammals but also toxic to bacteria, yeast, plants and animals, including C. elegans. Our previous studies showed that selenite was four times as toxic as selenate to C. elegans, but that deletion of thioredoxin reductase did not modulate Se toxicity. To characterize Se regulation of the full transcriptome, we conducted a microarray study in C. elegans cultured in axenic media supplemented with 0, 0.05, 0.1, 0.2, and 0.4 mM Se as selenite. C. elegans cultured in 0.2 and 0.4 mM Se displayed a significant delay in growth as compared to 0, 0.05, or 0.1 mM Se, indicating Se-induced toxicity, so worms were staged to mid-L4 larval stage for these studies. Relative to 0.1 mM Se treatment, culturing C. elegans at these Se concentrations resulted in 1.9, 9.7, 5.5, and 2.3%, respectively, of the transcriptome being altered by at least 2-fold. This toxicity altered the expression of 295 overlapping transcripts, which when filtered against gene sets for sulfur and cadmium toxicity, identified a dataset of 182 toxic-Se specific genes that were significantly enriched in functions related to oxidoreductase activity, and significantly depleted in genes related to structural components of collagen and the cuticle. Worms cultured in low Se (0 mM Se) exhibited no signs of deficiency, but low Se was accompanied by a transcriptional response of 59 genes changed ≥2-fold when compared to all other Se concentrations, perhaps due to decreases in Se-dependent TRXR-1 activity. Overall, these results suggest that Se toxicity in C. elegans causes an increase in ROS and stress responses, marked by increased expression of oxidoreductases and reduced expression of cuticle-associated genes, which together underlie the impaired growth observed in these studies.http://europepmc.org/articles/PMC4074201?pdf=render
spellingShingle Christopher J Boehler
Anna M Raines
Roger A Sunde
Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.
PLoS ONE
title Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.
title_full Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.
title_fullStr Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.
title_full_unstemmed Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.
title_short Toxic-selenium and low-selenium transcriptomes in Caenorhabditis elegans: toxic selenium up-regulates oxidoreductase and down-regulates cuticle-associated genes.
title_sort toxic selenium and low selenium transcriptomes in caenorhabditis elegans toxic selenium up regulates oxidoreductase and down regulates cuticle associated genes
url http://europepmc.org/articles/PMC4074201?pdf=render
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