1,920
Views
15
CrossRef citations to date
0
Altmetric
Research Paper

Dietary inclusion of plant ingredients induces epigenetic changes in the intestine of zebrafish

ORCID Icon, , , , & ORCID Icon
Pages 1035-1051 | Received 14 Nov 2019, Accepted 19 Mar 2020, Published online: 05 Apr 2020

References

  • Bird A. Perceptions of epigenetics. Nature. 2007;447(7143):396–398.
  • Kadayifci FZ, Zheng S, Pan Y-X. Molecular mechanisms underlying the link between diet and DNA methylation. Int J Mol Sci. 2018;19(12):4055.
  • Zhang N. Epigenetic modulation of DNA methylation by nutrition and its mechanisms in animals. Anim Nutr. 2015 Sept 1;1(3):144–151.
  • Hardy RW. Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res. 2010;41:770–776.
  • Gatlin DM, Barrows FT, Brown P, et al. Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res. 2007;38:551–579.
  • Ytrestøyl T, Aas TS, Åsgård T. Utilisation of feed resources in production of Atlantic salmon (Salmo salar) in Norway. Aquaculture. 2015;448:365–374.
  • FAO. The state of world fisheries and aquaculture 2016: contributing to food security and nutrition for all. Rome; 2016. FAO.
  • Krogdahl Å, Penn M, Thorsen J, et al. Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquac Res. 2010;41(3):333–344.
  • Francis G, Makkar HPS, Becker K. Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture. 2001;199:197–227.
  • Shankar S, Kumar D, Srivastava RK. Epigenetic modifications by dietary phytochemicals: implications for personalized nutrition. Pharmacol Ther. 2013;138(1):1–17.
  • Rietjens IMCM, Sotoca AM, Vervoort J, et al. Mechanisms underlying the dualistic mode of action of major soy isoflavones in relation to cell proliferation and cancer risks. Mol Nutr Food Res. 2013;57(1):100–113.
  • Zhou Z, Ringø E, Olsen RE, et al. Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: a review. Aquac Nutr. 2018;24(1):644–665.
  • Drew MD, Borgeson TL, Thiessen DL. A review of processing of feed ingredients to enhance diet digestibility in finfish. Anim Feed Sci Technol. 2007 Oct 22;138(2):118–136.
  • Król E, Douglas A, Tocher DR, et al. Differential responses of the gut transcriptome to plant protein diets in farmed Atlantic salmon. BMC Genomics. 2016;17:156.
  • Penn MH, Bendiksen EÅ, Campbell P, et al. High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.). Aquaculture. 2011;310:267–273.
  • Howard TD, Ho S-M, Zhang L, et al. Epigenetic changes with dietary soy in cynomolgus monkeys. PLoS One. 2011;6(10):e26791.
  • Day JK, Bauer AM, desBordes C, et al. Genistein alters methylation patterns in mice. J Nutr. 2002;132(8):2419S–2423S.
  • Øverland M, Sørensen M, Storebakken T, et al. Pea protein concentrate substituting fish meal or soybean meal in diets for Atlantic salmon (Salmo salar)—Effect on growth performance, nutrient digestibility, carcass composition, gut health, and physical feed quality. Aquaculture. 2009 Mar 20;288(3):305–311.
  • Burel C, Boujard T, Tulli F, et al. Digestibility of extruded peas, extruded lupin, and rapeseed meal in rainbow trout (Oncorhynchus mykiss) and turbot (Psetta maxima). Aquaculture. 2000;188(3–4):285–298.
  • Zhang Y, Øverland M, Sørensen M, et al. Optimal inclusion of lupin and pea protein concentrates in extruded diets for rainbow trout (Oncorhynchus mykiss). Aquaculture. 2012;344–349:100–113.
  • Kortner TM, Skugor S, Penn MH, et al. Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar). BMC Vet Res. 2012 July 02;8(1):101.
  • Apper-Bossard E, Feneuil A, Wagner A, et al. Use of vital wheat gluten in aquaculture feeds. Aquat Biosyst. 2013;9:21.
  • Storebakken T, Shearer KD, Baeverfjord G, et al. Digestibility of macronutrients, energy and amino acids, absorption of elements and absence of intestinal enteritis in Atlantic salmon, Salmo salar, fed diets with wheat gluten. Aquaculture. 2000;184(1–2):115–132.
  • Carter CG, Hauler RC. Fish meal replacement by plant meals in extruded feeds for Atlantic salmon, Salmo salar L. Aquaculture. 2000;185(3–4):299–311.
  • McKay JA, Mathers JC. Diet induced epigenetic changes and their implications for health. Acta Physiol. 2011;202(2):103–118.
  • 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 Feb 14;8(1):3055.
  • Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38(1):23–38.
  • Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012 May 29 online;13:484.
  • 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 Mar 04 online;39:457.
  • Maunakea AK, Nagarajan RP, Bilenky M, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010 July 08 online;466:253.
  • 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.
  • Francis WR, Wörheide G. Similar ratios of introns to intergenic sequence across animal genomes. Genome Biol Evol. 2017;9(6):1582–1598.
  • Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007 Apr 01;8(4):272–285.
  • Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr. 2002;132(8):2393S–2400S.
  • Zhang C, Hoshida Y, Sadler KC. Comparative epigenomic profiling of the DNA methylome in mouse and zebrafish uncovers high interspecies divergence. Front Genet. 2016;7:110.
  • Kamstra JH, Sales LB, Aleström P, et al. Differential DNA methylation at conserved non-genic elements and evidence for transgenerational inheritance following developmental exposure to mono(2-ethylhexyl) phthalate and 5-azacytidine in zebrafish. Epigenetics Chromatin. 2017;10:20.
  • Falisse E, Ducos B, Stockwell PA, et al. DNA methylation and gene expression alterations in zebrafish early-life stages exposed to the antibacterial agent triclosan. Environ Pollut. 2018 Dec 01;243:1867–1877.
  • Lappalainen T, Greally JM. Associating cellular epigenetic models with human phenotypes. Nat Rev Genet. 2017 July;18(7):441–451.
  • Olsson C. Autonomic innervation of the fish gut. Acta Histochem. 2009 May 01;111(3):185–195.
  • Furness JB. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol. 2012 May 01;9(5):286–294.
  • Neunlist M, Schemann M. Nutrient-induced changes in the phenotype and function of the enteric nervous system. J Physiol. 2014;592(14):2959–2965.
  • Briguglio M, Dell’Osso B, Panzica G, et al. Dietary neurotransmitters: a narrative review on current knowledge. Nutrients. 2018;10(5):591.
  • Maître J-L, Heisenberg C-P. Three functions of cadherins in cell adhesion. Curr Biol. 2013;23(14):R626–R633.
  • Klezovitch O, Vasioukhin V. Cadherin signaling: keeping cells in touch. F1000Res. 2015;4:550.
  • Knudsen D, Jutfelt F, Sundh H, et al. Dietary soya saponins increase gut permeability and play a key role in the onset of soyabean-induced enteritis in Atlantic salmon (Salmo salar L.). Br J Nutr. 2008;100(1):120–129.
  • Martin SAM, Dehler CE, Król E. Transcriptomic responses in the fish intestine. Dev Comp Immunol. 2016 Nov 01;64:103–117.
  • Zou J, Secombes CJ. The function of fish cytokines. Biology (Basel). 2016;5(2):23.
  • Fuentes-Appelgren P, Opazo R, Barros L, et al. Effect of the dietary inclusion of soybean components on the innate immune system in zebrafish [Article]. Zebrafish. 2014;11(1):41–49.
  • Stevens CB, Halloran MC. Developmental expression of sema3G, a novel zebrafish semaphorin. Gene Expr Patterns. 2005 June 1;5(5):647–653.
  • Roy S, Bag AK, Singh RK, et al. Multifaceted role of neuropilins in the immune system: potential targets for immunotherapy. Front Immunol. 2017 Oct 10;8:1228.
  • Karin M, Delhase M. The IκB kinase (IKK) and NF-κB: key elements of proinflammatory signalling. Semin Immunol. 2000 Feb 1;12(1):85–98.
  • Pomerantz JL, Baltimore D. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. Embo J. 1999;18(23):6694–6704.
  • Kim E, Yoon JY, Lee J, et al. TANK-binding kinase 1 and Janus kinase 2 play important roles in the regulation of mitogen-activated protein kinase phosphatase-1 expression after toll-like receptor 4 activation. J Cell Physiol. 2018;233(11):8790–8801.
  • Cuenda A. Mitogen-activated protein kinase kinase 4 (MKK4). Int J Biochem Cell Biol. 2000 June 01;32(6):581–587.
  • Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67(1):425–479.
  • Ben-Neriah Y. Regulatory functions of ubiquitination in the immune system. Nat Immunol. 2002 Jan 01 online;3:20.
  • Cron KR, Zhu K, Kushwaha DS, et al. Proteasome inhibitors block DNA repair and radiosensitize non-small cell lung cancer. PLoS One. 2013;8(9):e73710.
  • Ho MS, Tsai P-I, Chien C-T. F-box proteins: the key to protein degradation. J Biomed Sci. 2006 March 01;13(2):181–191.
  • Kobayashi A, Kang M-I, Okawa H, et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol. 2004;24(16):7130–7139.
  • Villeneuve NF, Lau A, Zhang DD. Regulation of the Nrf2-Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid Redox Signal. 2010;13(11):1699–1712.
  • Newsholme P, Lima MMR, Procopio J, et al. Glutamine and glutamate as vital metabolites. Braz J Med Biol Res. 2003;36:153–163.
  • Arnér ESJ, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem. 2000;267(20):6102–6109.
  • Kipp AP, Müller MF, Göken EM, et al. The selenoproteins GPx2, TrxR2 and TrxR3 are regulated by Wnt signalling in the intestinal epithelium. Biochim Biophys Acta Gen Subj. 2012 Oct 01;1820(10):1588–1596.
  • Ding C, Fan X, Peroxiredoxin WG. 1 - an antioxidant enzyme in cancer. J Cell Mol Med. 2017;21(1):193–202.
  • Mullen L, Hanschmann E-M, Lillig CH, et al. Cysteine oxidation targets peroxiredoxins 1 and 2 for exosomal release through a novel mechanism of redox-dependent secretion. Mol Med. 2015 January 01;21(1):98–108.
  • Johny A, Fæste CK, Bogevik AS, et al. Development and validation of a liquid chromatography high-resolution mass spectrometry method for the simultaneous determination of mycotoxins and phytoestrogens in plant-based fish feed and exposed fish. Toxins (Basel). 2019;11(4):222.
  • Geurden I, Borchert P, Balasubramanian MN, et al. The positive impact of the early-feeding of a plant-based diet on its future acceptance and utilisation in rainbow trout. PLoS One. 2013;8(12):e83162.
  • Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6–21.
  • Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–1572.
  • 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–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):576–589.
  • Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2008 Dec 18 online;4:44.
  • Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2008;37(1):1–13.
  • Supek F, Bošnjak M, Škunca N, et al. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6(7):e21800.
  • Berger MF, Levin JZ, Vijayendran K, et al. Integrative analysis of the melanoma transcriptome. Genome Res. 2010;20:413–427.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.