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Research Article

Epigenetic changes in pyloric caeca of Atlantic salmon fed diets containing increasing levels of lipids and choline

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Article: 2305079 | Received 28 Sep 2023, Accepted 09 Jan 2024, Published online: 28 Jan 2024

References

  • Bjørgen H, Li Y, Kortner TM, et al. Anatomy, immunology, digestive physiology and microbiota of the salmonid intestine: knowns and unknowns under the impact of an expanding industrialized production. Fish Shellfish Immunol. 2020;107:172–12. doi: 10.1016/j.fsi.2020.09.032
  • Hardy RW. Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquacult Res. 2010;41(5):770–776. doi: 10.1111/j.1365-2109.2009.02349.x
  • Krogdahl Å, Penn M, Thorsen J, et al. Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquacult Res. 2010;41(3):333–344. doi: 10.1111/j.1365-2109.2009.02426.x
  • Krogdahl Å, Midtlyng P, Berge G, et al. GutMatters – Defining and improving intestinal health in farmed salmon. Norway: FHF - Norwegian Seafood Research Fund; 2022. ( Final Report- FHF Project 901435). https://www.fhf.no/prosjekter/prosjektbasen/901435/.
  • Penn M. Lipid malabsorption in Atlantic Salmon–the recurring problem of floating feces. Fiskehelse Tekna Fiskehelseforeningen. 2011;Oslo:6–11.
  • Hansen AKG, Kortner TM, Denstadli V, et al. Dose–response relationship between dietary choline and lipid accumulation in pyloric enterocytes of Atlantic salmon (salmo salar L.) in seawater. Br J Nutr. 2020;123(10):1081–1093. doi: 10.1017/S0007114520000434
  • Hansen AKG, Kortner TM, Krasnov A, et al. Choline supplementation prevents diet induced gut mucosa lipid accumulation in post-smolt Atlantic salmon (Salmo salar L.). BMC Vet Res. 2020;16(1):32. doi: 10.1186/s12917-020-2252-7
  • Krogdahl Å, Hansen AKG, Kortner TM, et al. Choline and phosphatidylcholine, but not methionine, cysteine, taurine and taurocholate, eliminate excessive gut mucosal lipid accumulation in Atlantic salmon (Salmo salar L). Aquaculture. 2020;528:735552. doi: 10.1016/j.aquaculture.2020.735552
  • Siciliani D, Kortner TM, Berge GM, et al. Effects of dietary lipid level and environmental temperature on lipid metabolism in the intestine and liver, and choline requirement in Atlantic salmon (Salmo salar L) parr. J Nutr Sci. 2023;12:e61. doi: 10.1017/jns.2023.45
  • Korsmo HW, Jiang X, Caudill MA. Choline: exploring the growing science on its benefits for moms and babies. Nutrients. 2019;11(8):1823. doi: 10.3390/nu11081823
  • Ueland PM. Choline and betaine in health and disease. J Inherit Metabol Disease. 2011;34(1):3–15. doi: 10.1007/s10545-010-9088-4
  • Gibellini F, Smith TK. The Kennedy pathway—De novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life. 2010;62(6):414–428. doi: 10.1002/iub.337
  • van der Veen JN, Kennelly JP, Wan S, et al. The critical role of phosphatidylcholine and phosphatidylethanolamine metabolism in health and disease. Biochim Biophys Acta - Biomembr. 2017;1859(9, Part B):1558–1572. doi: 10.1016/j.bbamem.2017.04.006
  • Ridgway ND. Chapter 7 - phospholipid synthesis in Mammalian Cells. In: Ridgway ND McLeod RS, editors. Biochemistry of lipids, lipoproteins and membranes. Sixth Edition ed. Boston: Elsevier; 2016. pp. 209–236.
  • Zeisel S. Choline, Other Methyl-Donors and Epigenetics. Nutrients. 2017;9(5):445. doi: 10.3390/nu9050445
  • Metzger DCH, Schulte PM. Epigenomics in marine fishes. Mar Genomics. 2016;30:43–54. doi: 10.1016/j.margen.2016.01.004
  • Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38(1):23–38. doi: 10.1038/npp.2012.112
  • Bird A. Perceptions of epigenetics. Nature. 2007;447(7143):396–398. doi: 10.1038/nature05913
  • Amenyah SD, Hughes CF, Ward M, et al. Influence of nutrients involved in one-carbon metabolism on DNA methylation in adults—a systematic review and meta-analysis. Nutr Rev. 2020;78(8):647–666. doi: 10.1093/nutrit/nuz094
  • Dhanasiri A, Chen X, Dahle D, et al. Dietary inclusion of plant ingredients induces epigenetic changes in the intestine of zebrafish. Epigenetics. 2020;15(10):1035–1051. doi: 10.1080/15592294.2020.1747777
  • Anderson OS, Sant KE, Dolinoy DC. Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem. 2012;23(8):853–859. doi: 10.1016/j.jnutbio.2012.03.003
  • Dhar GA, Saha S, Mitra P, et al. DNA methylation and regulation of gene expression: guardian of our health. Nucleus. 2021;64(3):259–270. doi: 10.1007/s13237-021-00367-y
  • Jones AC, Irvin MR, Claas SA, et al. Lipid phenotypes and DNA methylation: a review of the literature. Curr Atheroscler Rep. 2021;23(11):71. doi: 10.1007/s11883-021-00965-w
  • Saito T, Whatmore P, Taylor JF, et al. Micronutrient supplementation affects transcriptional and epigenetic regulation of lipid metabolism in a dose-dependent manner. Epigenetics. 2021;16(11):1217–1234. doi: 10.1080/15592294.2020.1859867
  • Bai ZY, Zheng H, Luo Z, et al. Dietary choline mitigates high-fat diet-impaired chylomicrons assembly via UPRer modulated by perk DNA methylation. Cells. 2022;11(23):3848. doi: 10.3390/cells11233848
  • Jiang X, Greenwald E, Jack-Roberts C. Effects of choline on DNA methylation and macronutrient metabolic gene expression in in vitro models of hyperglycemia. Nutr Metab Insights. 2016;9:11–7. doi: 10.4137/NMI.S29465
  • Podgorniak T, Dhanasiri A, Chen X, et al. Early fish domestication affects methylation of key genes involved in the rapid onset of the farmed phenotype. Epigenetics. 2022;17(10):1281–1298. doi: 10.1080/15592294.2021.2017554
  • Rodgers LS, Beam MT, Anderson JM, et al. Epithelial barrier assembly requires coordinated activity of multiple domains of the tight junction protein ZO-1. J Cell Sci. 2013;126(7):1565–1575. doi: 10.1242/jcs.113399
  • Zihni C, Mills C, Matter K, et al. Tight junctions: from simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol. 2016;17(9):564–580. doi: 10.1038/nrm.2016.80
  • Shi X, Xiang S, Cao J, et al. Kelch-like proteins: physiological functions and relationships with diseases. Pharmacol Res. 2019;148:104404. doi: 10.1016/j.phrs.2019.104404
  • Hanin G, Yayon N, Tzur Y, et al. miRNA-132 induces hepatic steatosis and hyperlipidaemia by synergistic multitarget suppression. Gut. 2018;67(6):1124–1134. doi: 10.1136/gutjnl-2016-312869
  • Bachmann M, Li W, Edwards MJ, et al. Voltage-Gated Potassium Channels as Regulators of Cell Death. Front Cell Dev Biol. 2020;8. doi: 10.3389/fcell.2020.611853
  • Massa López D, Thelen M, Stahl F, et al. The lysosomal transporter MFSD1 is essential for liver homeostasis and critically depends on its accessory subunit GLMP. Elife. 2019;8. doi: 10.7554/eLife.50025
  • He H, Huang J, Wu S, et al. The roles of GTPase-activating proteins in regulated cell death and tumor immunity. J Hematol Oncol. 2021;14(1):171. doi: 10.1186/s13045-021-01184-1
  • Honda A, Nogami M, Yokozeki T, et al. Phosphatidylinositol 4-phosphate 5-kinase α is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell. 1999;99(5):521–532. doi: 10.1016/S0092-8674(00)81540-8
  • Miura Y, Hongu T, Yamauchi Y, et al. ACAP3 regulates neurite outgrowth through its GAP activity specific to Arf6 in mouse hippocampal neurons. Biochem J. 2016;473(17):2591–2602. doi: 10.1042/BCJ20160183
  • Miura Y, Kanaho Y. ACAP3, the GTPase-activating protein specific to the small GTPase Arf6, regulates neuronal migration in the developing cerebral cortex. Biochem Biophys Res Commun. 2017;493(2):1089–1094. doi: 10.1016/j.bbrc.2017.09.076
  • Oku Y, Huganir RL. AGAP3 and Arf6 regulate trafficking of AMPA receptors and synaptic plasticity. J Neurosci. 2013;33(31):12586–98. doi: 10.1523/JNEUROSCI.0341-13.2013
  • Fan X, Jin WY, Wang YT. The NMDA receptor complex: a multifunctional machine at the glutamatergic synapse. Front Cell Neurosci. 2014;8:160. doi: 10.3389/fncel.2014.00160
  • Skjærven KH, Jakt LM, Fernandes JMO, et al. Parental micronutrient deficiency distorts liver DNA methylation and expression of lipid genes associated with a fatty-liver-like phenotype in offspring. Sci Rep. 2018;8(1):3055. doi: 10.1038/s41598-018-21211-5
  • Santos RR, Ooosterveer-van der Doelen MAM, Tersteeg-Zijderveld MHG, et al. Induction of gut leakage in young broiler chickens fed a diet with low rye inclusion. Heliyon. 2021;7(12):e08547. doi: 10.1016/j.heliyon.2021.e08547
  • Slawinska A, Dunislawska A, Plowiec A, et al. Modulation of microbial communities and mucosal gene expression in chicken intestines after galactooligosaccharides delivery in ovo. PloS One. 2019;14(2):e0212318. doi: 10.1371/journal.pone.0212318
  • Jjingo D, Conley AB, Yi SV, et al. On the presence and role of human gene-body DNA methylation. Oncotarget. 2012;3(4):462–74. doi: 10.18632/oncotarget.497
  • Maunakea AK, Nagarajan RP, Bilenky M, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010;466(7303):253–257. doi: 10.1038/nature09165
  • Burek M, König A, Lang M, et al. Hypoxia-induced MicroRNA-212/132 alter blood-brain barrier integrity through inhibition of tight junction-associated proteins in human and mouse brain microvascular endothelial cells. Transl Stroke Res. 2019;10(6):672–683. doi: 10.1007/s12975-018-0683-2
  • Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13(7):484–492. doi: 10.1038/nrg3230
  • Weber M, Hellmann I, Stadler MB, et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet. 2007;39(4):457–66. doi: 10.1038/ng1990
  • Yee SW, Buitrago D, Stecula A, et al. Deorphaning a solute carrier 22 family member, SLC22A15, through functional genomic studies. FASEB J. 2020;34(12):15734–15752. doi: 10.1096/fj.202001497R
  • Longo N, Frigeni M, Pasquali M. Carnitine transport and fatty acid oxidation. Biochim Biophys Acta, Mol Cell Res. 2016;1863(10):2422–2435. doi: 10.1016/j.bbamcr.2016.01.023
  • Paton CM, Ntambi JM. Biochemical and physiological function of stearoyl-CoA desaturase. Am J Physiol Endocrinol Metab. 2009;297(1):E28–E37. doi: 10.1152/ajpendo.90897.2008
  • Nam S, Lim J-S. Essential role of interferon regulatory factor 4 (IRF4) in immune cell development. Arch Pharm Res. 2016;39(11):1548–1555. doi: 10.1007/s12272-016-0854-1
  • Eguchi J, Wang X, Yu S, et al. Transcriptional control of adipose lipid handling by IRF4. Cell Metab. 2011;13(3):249–259. doi: 10.1016/j.cmet.2011.02.005
  • Patel YC. Somatostatin and its receptor family. Front Neuroendocrinol. 1999;20(3):157–198. doi: 10.1006/frne.1999.0183
  • Elliott DE, Li J, Blum AM, et al. SSTR2A is the dominant somatostatin receptor subtype expressed by inflammatory cells, is widely expressed and directly regulates T cell IFN-γ release. Eur J Immunol. 1999;29(8):2454–2463. doi: 10.1002/(SICI)1521-4141(199908)29:08<2454:AID-IMMU2454>3.0.CO;2-H
  • Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for bisulfite-seq applications. Bioinformatics. 2011;27(11):1571–2. doi: 10.1093/bioinformatics/btr167
  • Akalin A, Kormaksson M, Li S, et al. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 2012;13(10):R87. doi: 10.1186/gb-2012-13-10-r87
  • Heinz S, Benner C, Spann N, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576–89. doi: 10.1016/j.molcel.2010.05.004
  • Raudvere U, Kolberg L, Kuzmin I, et al. G: profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 2019;47(W1):W191–W198. doi: 10.1093/nar/gkz369
  • Supek F, Bošnjak M, Škunca N, et al. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6(7):e21800. doi: 10.1371/journal.pone.0021800