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      Training the salmon’s genes: influence of aerobic exercise, swimming performance and selection on gene expression in Atlantic salmon

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          Abstract

          Background

          Farmed and wild Atlantic salmon are exposed to many infectious and non-infectious challenges that can cause mortality when they enter the sea. Exercise before transfer promotes growth, health and survival in the sea. Swimming performance in juveniles at the freshwater parr stage is positively associated with resistance to some diseases. Genetic variation is likely to affect response to exercise. In this study we map genetic differences associated with aerobic exercise, swimming performance and genetic origin.

          Eggs from the selectively bred Bolaks salmon and wild Lærdal River salmon strains were reared until parr in a common environment. Swimming performance was assessed by subjecting the fish to either continuous hard exercise or control conditions for 18 days. Heart was sampled for examination of gene expression using RNA-seq (~60 fish/treatment).

          Results

          Lower expression of genes affecting immune function was found in domesticated than wild parr. Among wild parr under control exercise the expression of a large number of genes involved in general metabolism, stress and immune response was lower in superior swimmers suggesting that minimisation of energy expenditure during periods of low activity makes parr better able to sustain bursts of swimming for predator avoidance. A similar set of genes were down-regulated with training among wild parr with inferior swimming performance. These parr react to training in a way that their cardiac expression patterns become like the superior performing wild parr under control exercise conditions. Diversifying selection caused by breeding of domesticated stock, and adaptive pressures in wild stock, has affected the expression and frequency of single nucleotide polymorphisms (SNPs) for multiple functional groups of genes affecting diverse processes. SNPs associated with swimming performance in wild parr map to genes involved in energetic processes, coding for contractile filaments in the muscle and controlling cell proliferation.

          Conclusions

          Domesticated parr have less phenotypic plasticity in response to training and lower expression of genes with functions affecting immune response. The genetic response to training is complex and depends on the background of parr and their swimming ability. Exercise should be tailored to the genetics and swimming performance of fish.

          Electronic supplementary material

          The online version of this article (doi: 10.1186/s12864-017-4361-7) contains supplementary material, which is available to authorized users.

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          Most cited references62

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          Control of apoptosis and mitotic spindle checkpoint by survivin.

          Progression of the cell cycle and control of apoptosis (programmed cell death) are thought to be intimately linked processes, acting to preserve homeostasis and developmental morphogenesis. Although proteins that regulate apoptosis have been implicated in restraining cell-cycle entry and controlling ploidy (chromosome number), the effector molecules at the interface between cell proliferation and cell survival have remained elusive. Here we show that a new inhibitor of apoptosis (IAP) protein, survivin, is expressed in the G2/M phase of the cell cycle in a cycle-regulated manner. At the beginning of mitosis, survivin associates with microtubules of the mitotic spindle in a specific and saturable reaction that is regulated by microtubule dynamics. Disruption of survivin-microtubule interactions results in loss of survivin's anti-apoptosis function and increased caspase-3 activity, a mechanism involved in cell death, during mitosis. These results indicate that survivin may counteract a default induction of apoptosis in G2/M phase. The overexpression of survivin in cancer may overcome this apoptotic checkpoint and favour aberrant progression of transformed cells through mitosis.
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            Connective tissue growth factor: a cysteine-rich mitogen secreted by human vascular endothelial cells is related to the SRC-induced immediate early gene product CEF-10

            Human umbilical vein endothelial (HUVE) cells have been previously reported to express the genes for the A and B chains of PDGF and to secrete PDGF-related factors into culture media. Antihuman PDGF IgG affinity chromatography was used to purify PDGF-related activity from HUVE cell-conditioned media. Immunoblot analysis of the affinity- purified proteins with anti-PDGF IgG and antibodies specific for the A or B chain peptides of PDGF combined with chemotactic and mitogenic assays revealed that the major PDGF immunorelated molecule secreted by HUVE cells is a monomer of approximately 36-38 kD and that less than 10% of the purified biologically active molecules are PDGF A or B chain peptides. Screening of an HUVE cell cDNA library in the expression vector lambda gtl 1 with the anti-PDGF antibody resulted in the cloning and sequencing of a cDNA with an open reading frame encoding a 38-kD cysteine-rich secreted protein which we show to be the major PDGF- related mitogen secreted by human vascular endothelial cells. The protein has a 45% overall homology to the translation product of the v- src-induced CEF-10 mRNA from chick embryo fibroblasts. We have termed this new mitogen connective tissue growth factor.
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              The HSP90 family of genes in the human genome: insights into their divergence and evolution.

              HSP90 proteins are important molecular chaperones. Transcriptome and genome analyses revealed that the human HSP90 family includes 17 genes that fall into four classes. A standardized nomenclature for each of these genes is presented here. Classes HSP90AA, HSP90AB, HSP90B, and TRAP contain 7, 6, 3, and 1 genes, respectively. HSP90AA genes mapped onto chromosomes 1, 3, 4, and 11; HSP90AB genes mapped onto 3, 4, 6, 13 and 15; HSP90B genes mapped onto 1, 12, and 15; and the TRAP1 gene mapped onto 16. Six genes, HSP90AA1, HSP90AA2, HSP90N, HSP90AB1, HSP90B1 and TRAP1, were recognized as functional, and the remaining 11 genes were considered putative pseudogenes. Amino acid polymorphic variants were detected for genes HSP90AA1, HSP90AA2, HSP90AB1, HSP90B1, and TRAP1. The structures of these genes and the functional motifs and polymorphic variants of their proteins were documented and the features and functions of their proteins were discussed. Phylogenetic analyses based on both nucleotide and protein data demonstrated that HSP90(AA+AB+B) formed a monophyletic clade, whereas TRAP is a relatively distant paralogue of this clade.
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                Author and article information

                Contributors
                +61 448984002 , nicholas.robinson@nofima.no
                gerrit.timmerhaus@nofima.no
                matthew.baranski@marineharvest.com
                oivind.andersen@nofima.no
                harald.takle@cermaq.com
                aleksei.krasnov@nofima.no
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                15 December 2017
                15 December 2017
                2017
                : 18
                : 971
                Affiliations
                [1 ]ISNI 0000 0004 0451 2652, GRID grid.22736.32, Nofima, ; Osloveien 1, 1430 Ås, Norway
                [2 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Sustainable Aquaculture Laboratory - Temperate and Tropical (SALTT), School of BioSciences, , The University of Melbourne, ; Parkville, Vic 3010 Australia
                [3 ]ISNI 0000 0004 0451 2652, GRID grid.22736.32, Nofima, ; PO Box 210, 1431 Ås, Norway
                Article
                4361
                10.1186/s12864-017-4361-7
                5731093
                672e927d-d31a-4b6d-9866-2c607918355c
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 25 August 2016
                : 1 December 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100005416, Norges Forskningsråd;
                Award ID: 225219
                Award Recipient :
                Funded by: Norwegian Seafood Research Fund
                Award ID: 900870
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Genetics
                salmo salar,exercise,swimming performance,gene expression,snp polymorphisms,immune function,natural selection,selective breeding

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