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DNA damage and transcriptional changes in the gills of mytilus galloprovincialis exposed to nanomolar doses of combined metal salts (Cd, Cu, Hg)
Aiming at an integrated and mechanistic view of the early biological effects of selected metals in the marine sentinel organism Mytilus galloprovincialis, we exposed mussels for 48 hours to 50, 100 and 200 nM solutions of equimolar Cd, Cu and Hg salts and measured cytological and molecular biomarker...
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Published in: | PloS one 2013-01, Vol.8 (1), p.e54602 |
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description | Aiming at an integrated and mechanistic view of the early biological effects of selected metals in the marine sentinel organism Mytilus galloprovincialis, we exposed mussels for 48 hours to 50, 100 and 200 nM solutions of equimolar Cd, Cu and Hg salts and measured cytological and molecular biomarkers in parallel. Focusing on the mussel gills, first target of toxic water contaminants and actively proliferating tissue, we detected significant dose-related increases of cells with micronuclei and other nuclear abnormalities in the treated mussels, with differences in the bioconcentration of the three metals determined in the mussel flesh by atomic absorption spectrometry. Gene expression profiles, determined in the same individual gills in parallel, revealed some transcriptional changes at the 50 nM dose, and substantial increases of differentially expressed genes at the 100 and 200 nM doses, with roughly similar amounts of up- and down-regulated genes. The functional annotation of gill transcripts with consistent expression trends and significantly altered at least in one dose point disclosed the complexity of the induced cell response. The most evident transcriptional changes concerned protein synthesis and turnover, ion homeostasis, cell cycle regulation and apoptosis, and intracellular trafficking (transcript sequences denoting heat shock proteins, metal binding thioneins, sequestosome 1 and proteasome subunits, and GADD45 exemplify up-regulated genes while transcript sequences denoting actin, tubulins and the apoptosis inhibitor 1 exemplify down-regulated genes). Overall, nanomolar doses of co-occurring free metal ions have induced significant structural and functional changes in the mussel gills: the intensity of response to the stimulus measured in laboratory supports the additional validation of molecular markers of metal exposure to be used in Mussel Watch programs. |
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Focusing on the mussel gills, first target of toxic water contaminants and actively proliferating tissue, we detected significant dose-related increases of cells with micronuclei and other nuclear abnormalities in the treated mussels, with differences in the bioconcentration of the three metals determined in the mussel flesh by atomic absorption spectrometry. Gene expression profiles, determined in the same individual gills in parallel, revealed some transcriptional changes at the 50 nM dose, and substantial increases of differentially expressed genes at the 100 and 200 nM doses, with roughly similar amounts of up- and down-regulated genes. The functional annotation of gill transcripts with consistent expression trends and significantly altered at least in one dose point disclosed the complexity of the induced cell response. The most evident transcriptional changes concerned protein synthesis and turnover, ion homeostasis, cell cycle regulation and apoptosis, and intracellular trafficking (transcript sequences denoting heat shock proteins, metal binding thioneins, sequestosome 1 and proteasome subunits, and GADD45 exemplify up-regulated genes while transcript sequences denoting actin, tubulins and the apoptosis inhibitor 1 exemplify down-regulated genes). Overall, nanomolar doses of co-occurring free metal ions have induced significant structural and functional changes in the mussel gills: the intensity of response to the stimulus measured in laboratory supports the additional validation of molecular markers of metal exposure to be used in Mussel Watch programs.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0054602</identifier><identifier>PMID: 23355883</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abnormalities ; Actin ; Alzheimer's disease ; Animals ; Annotations ; Apoptosis ; Atomic absorption analysis ; Bioaccumulation ; Bioindicators ; Biological effects ; Biological magnification ; Biology ; Biomarkers ; Bivalvia ; Cadmium ; Cell cycle ; Chemical bonds ; Chemical synthesis ; Contaminants ; Copper ; Deoxyribonucleic acid ; DNA ; DNA Damage ; DNA methylation ; Earth Sciences ; Exposure ; GADD45 protein ; Gene expression ; Gene Expression Regulation - drug effects ; Gene sequencing ; Genes ; Genetic aspects ; Gills ; Gills - metabolism ; Heat shock proteins ; Heavy Metal Poisoning ; Homeostasis ; Life sciences ; Ligands ; Medicine ; Mercury ; Metals ; Metals, Heavy - metabolism ; Metals, Heavy - pharmacology ; Micronuclei ; Mollusks ; Mussels ; Mytilus - metabolism ; Oxidative stress ; Permeability ; Poisoning - metabolism ; Proteasomes ; Protein binding ; Protein biosynthesis ; Protein synthesis ; Protein turnover ; Proteins ; Salts ; Spectral analysis ; Spectrometry ; Structure-function relationships ; Transcription ; Transcription (Genetics) ; Transcription, Genetic - drug effects ; Veterinary Science ; Water pollution</subject><ispartof>PloS one, 2013-01, Vol.8 (1), p.e54602</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Varotto et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Varotto et al 2013 Varotto et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-c1cad05af5887b9c9aa5c7aed9f950c3c72ac6e529c6aa5cf1d0206c5a5d06b73</citedby><cites>FETCH-LOGICAL-c692t-c1cad05af5887b9c9aa5c7aed9f950c3c72ac6e529c6aa5cf1d0206c5a5d06b73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1327868361/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1327868361?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,25783,27957,27958,37047,44625,53827,53829,75483</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23355883$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Balcazar, Jose Luis</contributor><creatorcontrib>Varotto, Laura</creatorcontrib><creatorcontrib>Domeneghetti, Stefania</creatorcontrib><creatorcontrib>Rosani, Umberto</creatorcontrib><creatorcontrib>Manfrin, Chiara</creatorcontrib><creatorcontrib>Cajaraville, Miren P</creatorcontrib><creatorcontrib>Raccanelli, Stefano</creatorcontrib><creatorcontrib>Pallavicini, Alberto</creatorcontrib><creatorcontrib>Venier, Paola</creatorcontrib><title>DNA damage and transcriptional changes in the gills of mytilus galloprovincialis exposed to nanomolar doses of combined metal salts (Cd, Cu, Hg)</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Aiming at an integrated and mechanistic view of the early biological effects of selected metals in the marine sentinel organism Mytilus galloprovincialis, we exposed mussels for 48 hours to 50, 100 and 200 nM solutions of equimolar Cd, Cu and Hg salts and measured cytological and molecular biomarkers in parallel. Focusing on the mussel gills, first target of toxic water contaminants and actively proliferating tissue, we detected significant dose-related increases of cells with micronuclei and other nuclear abnormalities in the treated mussels, with differences in the bioconcentration of the three metals determined in the mussel flesh by atomic absorption spectrometry. Gene expression profiles, determined in the same individual gills in parallel, revealed some transcriptional changes at the 50 nM dose, and substantial increases of differentially expressed genes at the 100 and 200 nM doses, with roughly similar amounts of up- and down-regulated genes. The functional annotation of gill transcripts with consistent expression trends and significantly altered at least in one dose point disclosed the complexity of the induced cell response. The most evident transcriptional changes concerned protein synthesis and turnover, ion homeostasis, cell cycle regulation and apoptosis, and intracellular trafficking (transcript sequences denoting heat shock proteins, metal binding thioneins, sequestosome 1 and proteasome subunits, and GADD45 exemplify up-regulated genes while transcript sequences denoting actin, tubulins and the apoptosis inhibitor 1 exemplify down-regulated genes). Overall, nanomolar doses of co-occurring free metal ions have induced significant structural and functional changes in the mussel gills: the intensity of response to the stimulus measured in laboratory supports the additional validation of molecular markers of metal exposure to be used in Mussel Watch programs.</description><subject>Abnormalities</subject><subject>Actin</subject><subject>Alzheimer's disease</subject><subject>Animals</subject><subject>Annotations</subject><subject>Apoptosis</subject><subject>Atomic absorption analysis</subject><subject>Bioaccumulation</subject><subject>Bioindicators</subject><subject>Biological effects</subject><subject>Biological magnification</subject><subject>Biology</subject><subject>Biomarkers</subject><subject>Bivalvia</subject><subject>Cadmium</subject><subject>Cell cycle</subject><subject>Chemical bonds</subject><subject>Chemical synthesis</subject><subject>Contaminants</subject><subject>Copper</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Damage</subject><subject>DNA methylation</subject><subject>Earth Sciences</subject><subject>Exposure</subject><subject>GADD45 protein</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Gills</subject><subject>Gills - metabolism</subject><subject>Heat shock proteins</subject><subject>Heavy Metal Poisoning</subject><subject>Homeostasis</subject><subject>Life sciences</subject><subject>Ligands</subject><subject>Medicine</subject><subject>Mercury</subject><subject>Metals</subject><subject>Metals, Heavy - metabolism</subject><subject>Metals, Heavy - pharmacology</subject><subject>Micronuclei</subject><subject>Mollusks</subject><subject>Mussels</subject><subject>Mytilus - metabolism</subject><subject>Oxidative stress</subject><subject>Permeability</subject><subject>Poisoning - metabolism</subject><subject>Proteasomes</subject><subject>Protein binding</subject><subject>Protein biosynthesis</subject><subject>Protein synthesis</subject><subject>Protein turnover</subject><subject>Proteins</subject><subject>Salts</subject><subject>Spectral analysis</subject><subject>Spectrometry</subject><subject>Structure-function relationships</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><subject>Transcription, Genetic - 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Performed the experiments: LV SD UR SR. Analyzed the data: LV SD UR MPC CM AP PV. Contributed reagents/materials/analysis tools: PV. Wrote the paper: PV.</notes><abstract>Aiming at an integrated and mechanistic view of the early biological effects of selected metals in the marine sentinel organism Mytilus galloprovincialis, we exposed mussels for 48 hours to 50, 100 and 200 nM solutions of equimolar Cd, Cu and Hg salts and measured cytological and molecular biomarkers in parallel. Focusing on the mussel gills, first target of toxic water contaminants and actively proliferating tissue, we detected significant dose-related increases of cells with micronuclei and other nuclear abnormalities in the treated mussels, with differences in the bioconcentration of the three metals determined in the mussel flesh by atomic absorption spectrometry. Gene expression profiles, determined in the same individual gills in parallel, revealed some transcriptional changes at the 50 nM dose, and substantial increases of differentially expressed genes at the 100 and 200 nM doses, with roughly similar amounts of up- and down-regulated genes. The functional annotation of gill transcripts with consistent expression trends and significantly altered at least in one dose point disclosed the complexity of the induced cell response. The most evident transcriptional changes concerned protein synthesis and turnover, ion homeostasis, cell cycle regulation and apoptosis, and intracellular trafficking (transcript sequences denoting heat shock proteins, metal binding thioneins, sequestosome 1 and proteasome subunits, and GADD45 exemplify up-regulated genes while transcript sequences denoting actin, tubulins and the apoptosis inhibitor 1 exemplify down-regulated genes). Overall, nanomolar doses of co-occurring free metal ions have induced significant structural and functional changes in the mussel gills: the intensity of response to the stimulus measured in laboratory supports the additional validation of molecular markers of metal exposure to be used in Mussel Watch programs.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23355883</pmid><doi>10.1371/journal.pone.0054602</doi><tpages>e54602</tpages><oa>free_for_read</oa></addata></record> |
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identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2013-01, Vol.8 (1), p.e54602 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1327868361 |
source | Open Access: PubMed Central; Publicly Available Content (ProQuest) |
subjects | Abnormalities Actin Alzheimer's disease Animals Annotations Apoptosis Atomic absorption analysis Bioaccumulation Bioindicators Biological effects Biological magnification Biology Biomarkers Bivalvia Cadmium Cell cycle Chemical bonds Chemical synthesis Contaminants Copper Deoxyribonucleic acid DNA DNA Damage DNA methylation Earth Sciences Exposure GADD45 protein Gene expression Gene Expression Regulation - drug effects Gene sequencing Genes Genetic aspects Gills Gills - metabolism Heat shock proteins Heavy Metal Poisoning Homeostasis Life sciences Ligands Medicine Mercury Metals Metals, Heavy - metabolism Metals, Heavy - pharmacology Micronuclei Mollusks Mussels Mytilus - metabolism Oxidative stress Permeability Poisoning - metabolism Proteasomes Protein binding Protein biosynthesis Protein synthesis Protein turnover Proteins Salts Spectral analysis Spectrometry Structure-function relationships Transcription Transcription (Genetics) Transcription, Genetic - drug effects Veterinary Science Water pollution |
title | DNA damage and transcriptional changes in the gills of mytilus galloprovincialis exposed to nanomolar doses of combined metal salts (Cd, Cu, Hg) |
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