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      Tolerance and dose-response assessment of subchronic dietary ethoxyquin exposure in Atlantic salmon ( Salmo salar L.)

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          Abstract

          Ethoxyquin (EQ; 6-Ethoxy-2,2,4-trimethyl-1,2-dihydroquinoline) has been used as an antioxidant in feed components for pets, livestock and aquaculture. However, possible risks of EQ used in aquafeed for fish health have not yet been characterized. The present study investigated the toxicity and dose-response of subchronic dietary EQ exposure at doses ranging from 41 to 9666 mg EQ/kg feed in Atlantic salmon ( Salmo salar L.). Feed at concentrations higher than 1173 mg EQ/kg were rejected by the fish, resulting in reduced feed intake and growth performance. No mortality was observed in fish exposed to any of the doses. A multi-omic screening of metabolome and proteome in salmon liver indicated an effect of dietary EQ on bioenergetics pathways and hepatic redox homeostasis in fish fed concentrations above 119 mg EQ/kg feed. Increased energy expenditure associated with an upregulation of hepatic fatty acid β-oxidation and induction and carbohydrate catabolic pathways resulted in a dose-dependent depletion of intracytoplasmic lipid vacuoles in liver histological sections, decreasing whole body lipid levels and altered purine/pyrimidine metabolism. Increased GSH and TBARS in the liver indicated a state of oxidative stress, which was associated with activation of the NRF2-mediated oxidative stress response and glutathione-mediated detoxification processes. However, no oxidative DNA damage was observed. As manifestation of altered energy metabolism, the depletion of liver intracytoplasmic lipid vacuoles was considered the critical endpoint for benchmark dose assessment, and a BMDL 10 of 243 mg EQ/kg feed was derived as a safe upper limit of EQ exposure in Atlantic salmon.

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          Lipid peroxidation-DNA damage by malondialdehyde.

          Malondialdehyde is a naturally occurring product of lipid peroxidation and prostaglandin biosynthesis that is mutagenic and carcinogenic. It reacts with DNA to form adducts to deoxyguanosine and deoxyadenosine. The major adduct to DNA is a pyrimidopurinone called M1G. Site-specific mutagenesis experiments indicate that M1G is mutagenic in bacteria and is repaired by the nucleotide excision repair pathway. M1G has been detected in liver, white blood cells, pancreas, and breast from healthy human beings at levels ranging from 1-120 per 108 nucleotides. Several different assays for M1G have been described that are based on mass spectrometry, 32P-postlabeling, or immunochemical techniques. Each technique offers advantages and disadvantages based on a combination of sensitivity and specificity. Application of each of these techniques to the analysis of M1G is reviewed and future needs for improvements are identified. M1G appears to be a major endogenous DNA adduct in human beings that may contribute significantly to cancer linked to lifestyle and dietary factors. High throughput methods for its detection and quantitation will be extremely useful for screening large populations. Copyright 1999 Elsevier Science B.V.
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            Visualization of LC‐MS/MS proteomics data in MaxQuant

            Modern software platforms enable the analysis of shotgun proteomics data in an automated fashion resulting in high quality identification and quantification results. Additional understanding of the underlying data can be gained with the help of advanced visualization tools that allow for easy navigation through large LC‐MS/MS datasets potentially consisting of terabytes of raw data. The updated MaxQuant version has a map navigation component that steers the users through mass and retention time‐dependent mass spectrometric signals. It can be used to monitor a peptide feature used in label‐free quantification over many LC‐MS runs and visualize it with advanced 3D graphic models. An expert annotation system aids the interpretation of the MS/MS spectra used for the identification of these peptide features.
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              Normal ranges of some blood chemistry parameters in adult farmed Atlantic salmon, Salmo salar

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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                25 January 2019
                2019
                : 14
                : 1
                : e0211128
                Affiliations
                [1 ] Institute of Marine Research, Bergen, Norway
                [2 ] Institute of Aquaculture, Faculty of Natural Sciences, University of Stirling, Stirling, United Kingdom
                [3 ] Department of Morphology, Veterinary School, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain
                University of Illinois, UNITED STATES
                Author notes

                Competing Interests: This study was financed by the Marine Ingredients Organisation (IFFO), Marine Harvest ASA, EWOS AS/Cargill Aqua Nutrition, Biomar AS, Skretting AS and Europharma through the Norwegian Seafood Research Fund (FHF; project no. 901327). The financial contribution could reasonably be perceived as interfering with the full and objective presentation of this work. The funders had, however, no role in the study design, the collection, analysis or interpretation of data, or the preparation of the manuscript. Capsoquin S-5162 was a courtesy of Industrial Técnica Pecuaria, which had no commercial strings attached and did not in any way influence the results reported in the manuscript. The Norwegian Seafood Federation (SjømatNorge) is a trade organization for the fishery and aquaculture sector in Norway. The Norwegian Seafood Federation was part of the project group and had a coordinating role, and mediated contact with Industrial Técnica Pecuaria, but did not contribute with finances. Furthermore, the Norwegian Seafood Federation had no involvement in the study design, collection, analysis or interpretation of data, or in the writing of the manuscript. Outside of the submitted work, Robin Ørnsrud reports that he has been leading another project, which had a similar consortium as the current project and was financed by the Norwegian Seafood Research Fund (FHF), Marine Harvest ASA, EWOS AS/Cargill Aqua Nutrition, Biomar AS, Skretting AS and Europharma (FHF project no. 900871). These circumstances do not alter our adherence to PLOS ONE policies on sharing data and materials.

                Article
                PONE-D-18-24095
                10.1371/journal.pone.0211128
                6347454
                30682099
                65ece553-de11-459d-81b1-c436715b600d
                © 2019 Bernhard et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 August 2018
                : 8 January 2019
                Page count
                Figures: 9, Tables: 7, Pages: 36
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100010197, Fiskeri - og havbruksnæringens forskningsfond;
                Award ID: 901327
                This study was financed by the Norwegian Seafood Research Fund (FHF; https://www.fhf.no/), the Marine Ingredients Organisation (IFFO) Marine Harvest ASA, EWOS AS/Cargill Aqua Nutrition, Biomar AS, Skretting AS and Europharma (FHF project no. 901327). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Fish
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolic Pathways
                Biology and Life Sciences
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Protein Metabolism
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolites
                Biology and Life Sciences
                Cell Biology
                Oxidative Stress
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Blood
                Blood Plasma
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Blood
                Blood Plasma
                Biology and Life Sciences
                Physiology
                Body Fluids
                Blood
                Blood Plasma
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Blood
                Blood Plasma
                Research and Analysis Methods
                Mathematical and Statistical Techniques
                Statistical Methods
                Analysis of Variance
                Physical Sciences
                Mathematics
                Statistics
                Statistical Methods
                Analysis of Variance
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                All relevant data are within the paper and its Supporting Information files.

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