4,657
Views
50
CrossRef citations to date
0
Altmetric
Research Paper

Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon

ORCID Icon, ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon show all
Pages 1191-1207 | Received 06 Jul 2018, Accepted 26 Nov 2018, Published online: 13 Dec 2018

References

  • Chrousos GP. Stress and disorders of the stress system. Nat Rev Endocrinol. 2009;5(7):374–382.
  • Calcagni E, Elenkov I. Stress system activity, innate and T helper cytokines, and susceptibility to immune-related diseases. Ann N Y Acad Sci. 2006;1069:62–76.
  • Tort L. Stress and immune modulation in fish. Dev Comp Immunol. 2011;35(12):1366–1375.
  • Dhabhar FS. Effects of stress on immune function: the good, the bad, and the beautiful. Immunol Res. 2014;58(2):193–210.
  • Dhabhar FS. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. Neuroimmunomodulation. 2009;16(5):300–317.
  • Cao-Lei L, de Rooij SR, King S, et al. Prenatal stress and epigenetics. Neurosci Biobehav Rev. 2017. https://www.sciencedirect.com/science/article/pii/S0149763416307266
  • Silberman DM, Acosta GB, Zorrilla Zubilete MA. Long-term effects of early life stress exposure: role of epigenetic mechanisms. Pharmacol Res. 2016;109:64–73.
  • Vaiserman AM. Epigenetic programming by early-life stress: evidence from human populations. Dev Dyn. 2015;244(3):254–265.
  • Mattson MP, Calabrese EJ. Hormesis: a revolution in biology, toxicology and medicine. Berlin: Springer Science & Business Media; 2009.
  • Monaghan P, Haussmann MF. The positive and negative consequences of stressors during early life. Early Hum Dev. 2015;91(11):643–647.
  • Nasca C, Bigio B, Zelli D, et al. Mind the gap: glucocorticoids modulate hippocampal glutamate tone underlying individual differences in stress susceptibility. Mol Psychiatry. 2015;20(6):755–763.
  • Hunter RG, Gagnidze K, McEwen BS, et al. Stress and the dynamic genome: steroids, epigenetics, and the transposome. Proc Nat Acad Sci. 2015;112(22):6828–6833.
  • Nasca C, Zelli D, Bigio B, et al. Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Proc Nat Acad Sci. 2015;112(48):14960–14965.
  • Cruceanu C, Matosin N, Binder EB. Interactions of early-life stress with the genome and epigenome: from prenatal stress to psychiatric disorders. Curr Opin Behav Sci. 2017;14:167–171.
  • McGowan PO, Sasaki A, D’alessio AC, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12(3):342–348.
  • Papadopoulou A, Siamatras T, Delgado-Morales R, et al. Acute and chronic stress differentially regulate cyclin-dependent kinase 5 in mouse brain: implications to glucocorticoid actions and major depression. Transl Psychiatry. 2015;5:e578.
  • Vindas MA, Madaro A, Fraser TWK, et al. Coping with a changing environment: the effects of early life stress. R Soc Open Sci. 2016;3(10):160382.
  • Stentiford GD, Sritunyalucksana K, Flegel TW, et al. New paradigms to help solve the global aquaculture disease crisis. PLoS Pathog. 2017;13(2):e1006160.
  • Schreck CB, Tort L, Farrell AP, et al. Biology of stress in fish. Vol. 35. Cambridge: Academic Press; 2016.
  • Elliott J. The critical‐period concept for juvenile survival and its relevance for population regulation in young sea trout, Salmo trutta. J Fish Biol. 1989;35(sA):91–98.
  • Castro R, Jouneau L, Tacchi L, et al. Disparate developmental patterns of immune responses to bacterial and viral infections in fish. Sci Rep. 2015;5:15458.
  • Moghadam HK, Johnsen H, Robinson N, et al. Impacts of early life stress on the methylome and transcriptome of Atlantic salmon. Sci Rep. 2017;7(1):5023.
  • Khansari AR, Balasch JC, Reyes-López FE, et al. Stressing the inflammatory network: immuno-endocrine responses to allostatic load in fish. Mar Sci Res Technol. 2017;1(2):856–862.
  • Gomez D, Sunyer JO, Salinas I. The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immunol. 2013;35(6):1729–1739.
  • Parra D, Reyes-Lopez FE, Tort L. Mucosal immunity and B cells in teleosts: effect of vaccination and stress. Front Immunol. 2015;6(354):354.
  • Lien S, Koop BF, Sandve SR, et al. The Atlantic salmon genome provides insights into rediploidization. Nature. 2016;533:200–205.
  • Chatterjee A, Ozaki Y, Stockwell PA, et al. Mapping the zebrafish brain methylome using reduced representation bisulfite sequencing. Epigenetics. 2013;8(9):979–989.
  • Baerwald MR, Meek MH, Stephens MR, et al. Migration-related phenotypic divergence is associated with epigenetic modifications in rainbow trout. Mol Ecol. 2016;25(8):1785–1800.
  • Donaldson M, Cooke S, Patterson D, et al. Cold shock and fish. J Fish Biol. 2008;73(7):1491–1530.
  • Ankley GT, Villeneuve DL. Temporal changes in biological responses and uncertainty in assessing risks of endocrine-disrupting chemicals: insights from intensive time-course studies with fish. Toxicol Sci. 2015;144(2):259–275.
  • Uren Webster TM, Santos EM. Global transcriptomic profiling demonstrates induction of oxidative stress and of compensatory cellular stress responses in brown trout exposed to glyphosate and roundup. BMC Genomics. 2015;16:32–38.
  • Patel J, McLeod LE, Vries RG, et al. Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur J Biochem. 2002;269(12):3076–3085.
  • Sundin L, Turesson J, Taylor EW. Evidence for glutamatergic mechanisms in the vagal sensory pathway initiating cardiorespiratory reflexes in the shorthorn sculpin Myoxocephalus scorpius. J Exp Biol. 2003;206(5):867–876.
  • Zhang Z, Zhang R. Epigenetics in autoimmune diseases: pathogenesis and prospects for therapy. Autoimmun Rev. 2015;14(10):854–863.
  • Frost RA, Nystrom GJ, Lang CH. Lipopolysaccharide regulates proinflammatory cytokine expression in mouse myoblasts and skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2002;283(3):R698–R709.
  • Sepulcre MP, Alcaraz-Pérez F, López-Muñoz A, et al. Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-κB activation. J Immunol. 2009;182(4):1836–1845.
  • Linden SK, Sutton P, Karlsson NG, et al. Mucins in the mucosal barrier to infection. Mucosal Immunol. 2008;1:183–190.
  • Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell. 2010;141(7):1117–1134.
  • Sorokin L. The impact of the extracellular matrix on inflammation. Nat Rev Immunol. 2010;10(10):712–723.
  • Bonnans C, Chou J, Werb Z. Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol. 2014;15(12):786–801.
  • Naba A, Clauser KR, Ding H, et al. The extracellular matrix: tools and insights for the “omics” era. Matrix Biol. 2016;49(Supplement C):10–24.
  • Ragkousi K, Gibson MC. Cell division and the maintenance of epithelial order. J Cell Biol. 2014;207(2):181–188.
  • Kan A, Hodgkin PD. Mechanisms of cell division as regulators of acute immune response. Syst Synth Biol. 2014;8(3):215–221.
  • Köberlin Marielle S, Snijder B, Heinz Leonhard X, et al. A conserved circular network of coregulated lipids modulates innate immune responses. Cell. 2015;162(1):170–183.
  • Smith BL, Schmeltzer SN, Packard BA, et al. Divergent effects of repeated restraint versus chronic variable stress on prefrontal cortical immune status after LPS injection. Brain Behav Immun. 2016;57:263–270.
  • Glaser R, Kiecolt-Glaser JK. Stress-induced immune dysfunction: implications for health. Nat Rev Immunol. 2005;5(3):243–251.
  • Turecki G, Meaney MJ. Effects of the social environment and stress on glucocorticoid receptor gene methylation: a systematic review. Biol Psychiatry. 2016;79(2):87–96.
  • Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13(7):484–492.
  • Hu Y, Huang K, An Q, et al. Simultaneous profiling of transcriptome and DNA methylome from a single cell. Genome Biol. 2016;17(1):88–94.
  • Wang H, Wang J, Ning C, et al. Genome-wide DNA methylation and transcriptome analyses reveal genes involved in immune responses of pig peripheral blood mononuclear cells to poly I:C. Sci Rep. 2017;7(1):9709–9715.
  • Zhong Z, Du K, Yu Q, et al. Divergent DNA methylation provides insights into the evolution of duplicate genes in zebrafish. G3: Genes | Genomes | Genetics. 2016;6(11):3581–3591.
  • Huang Y-Z, Sun -J-J, Zhang L-Z, et al. Genome-wide DNA methylation profiles and their relationships with mRNA and the microRNA transcriptome in bovine muscle tissue (Bos taurine). Sci Rep. 2014;4:6546–6552.
  • Lim YC, Li J, Ni Y, et al. A complex association between DNA methylation and gene expression in human placenta at first and third trimesters. PloS One. 2017;12(7):e0181155.
  • Jjingo D, Conley AB, Yi SV, et al. On the presence and role of human gene-body DNA methylation. Oncotarget. 2012;3(4):462–474.
  • Wang H, Beyene G, Zhai J, et al. CG gene body DNA methylation changes and evolution of duplicated genes in cassava. Proc Nat Acad Sci. 2015;112(44):13729–13734.
  • Zemach A, Kim MY, Silva P, et al. Local DNA hypomethylation activates genes in rice endosperm. Proc Nat Acad Sci. 2010;107(43):18729–18734.
  • Zhao Y, Sun H, Wang H. Long noncoding RNAs in DNA methylation: new players stepping into the old game. Cell Biosci. 2016;6:45.
  • Richards CL, Alonso C, Becker C, et al. Ecological plant epigenetics: evidence from model and non‐model species, and the way forward. Ecol Lett. 2017;20(12):1576–1590.
  • Cheung WA, Shao X, Morin A, et al. Functional variation in allelic methylomes underscores a strong genetic contribution and reveals novel epigenetic alterations in the human epigenome. Genome Biol. 2017;18(1):50.
  • Uribe C, Folch H, Enriquez R, et al. Innate and adaptive immunity in teleost fish: a review. Vet Med. 2011;56(10):486–503.
  • Schreck CB, Tort L. 1 - The concept of stress in fish. In: Schreck CB, Tort L, Farrell AP, et al., editors. Fish physiology. Vol. 35.Cambridge: Academic Press; 2016. p. 1–34.
  • Barry TP, Malison JA, Held JA, et al. Ontogeny of the cortisol stress response in larval rainbow trout. Gen Comp Endocrinol. 1995;97(1):57–65.
  • Bates L, Boucher M, Shrimpton J. Effect of temperature and substrate on whole body cortisol and size of larval white sturgeon (Acipenser transmontanus Richardson, 1836). J Appl Ichthyol. 2014;30(6):1259–1263.
  • Hansen T. Artificial hatching substrate: effect on yolk absorption, mortality and growth during first feeding of sea trout (Salmo trutta). Aquaculture. 1985;46(4):275–285.
  • Froese R. Cube law, condition factor and weight–length relationships: history, meta‐analysis and recommendations. J Appl Ichthyol. 2006;22(4):241–253.
  • Thorarensen H, Kubiriza GK, Imsland AK. Experimental design and statistical analyses of fish growth studies. Aquaculture. 2015;448:483–490.
  • nlme. Linear and nonlinear mixed effects models. Available from: https://CRAN.R-project.org/package=nlme.
  • R_Core_Team. R: A language and environment for statistical computing. Vienna, Austria.: R Foundation for Statistical Computing; 2014.
  • Sundaram AY, Consuegra S, Kiron V, et al. Positive selection pressure within teleost Toll-like receptors tlr21 and tlr22 subfamilies and their response to temperature stress and microbial components in zebrafish. Mol Biol Rep. 2012;39(9):8965–8975.
  • Osuna-Jimenez I, Williams TD, Prieto-Alamo MJ, et al. Immune- and stress-related transcriptomic responses of solea senegalensis stimulated with lipopolysaccharide and copper sulphate using heterologous cDNA microarrays. Fish Shellfish Immunol. 2009;26(5):699–706.
  • Seppola M, Mikkelsen H, Johansen A, et al. Ultrapure LPS induces inflammatory and antibacterial responses attenuated in vitro by exogenous sera in Atlantic cod and Atlantic salmon. Fish Shellfish Immunol. 2015;44(1):66–78.
  • Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics. 2014;30(15):2114–2120.
  • Davidson WS, Koop BF, Jones SJ, et al. Sequencing the genome of the Atlantic salmon (Salmo salar). Genome Biol. 2010;11(9):403–410.
  • Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–360.
  • Pertea M, Pertea GM, Antonescu CM, et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33(3):290–295.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550–555.
  • Kolde R. Pretty heatmaps. 2015. (R package version 31–131).
  • Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2008;4(1):44–57.
  • Kreger F. TrimGalore. A wrapper around cutadapt and FastQC to consistently apply adapter and quality trimming to FastQ files, with extra functionality for RRBS data. Available from: https://wwwbioinformaticsbabrahamacuk/projects/trim_galore/2016.
  • Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–1572.
  • Andrews S. SeqMonk: A tool to visualise and analyse high throughput mapped sequence data. Available from: https://wwwbioinformaticsbabrahamacuk/projects/seqmonk/2007.
  • Tao M, Xie P, Chen J, et al. Use of a generalized additive model to investigate key abiotic factors affecting microcystin cellular quotas in heavy bloom areas of lake taihu. PLOS ONE. 2012;7(2):e32020.
  • Muurinen M, Hannula-Jouppi K, Reinius LE, et al. Hypomethylation of HOXA4 promoter is common in Silver-Russell syndrome and growth restriction and associates with stature in healthy children. Sci Rep. 2017;7(1):15693–15699.
  • Lussier AA, Morin AM, MacIsaac JL, et al. DNA methylation as a predictor of fetal alcohol spectrum disorder. Clin Epigenetics. 2018;10(1):5–10.