Abstract
Epidemiological evidence and subsequent studies using mammalian models have established a strong correlation between suboptimal nutritional status during early life and predisposition to metabolic diseases later, such as permanent growth retardation and impairment of neural development and key metabolic pathways. This phenomenon, termed nutritional programming or metabolic programming, is beginning to be studied in fishes. Despite important differences in maternal nutrient delivery and developmental processes between mammals and fishes, early nutrition of fishes from both endogenous (maternally derived) and exogenous (larval feeding) sources, could induce similar programming effects on development and metabolism. Documented programming effects in fishes include: growth, survival, brain development, and nutrient metabolism. These programming effects could be mediated through altered metabolic pathways and/or epigenetic regulation of gene expression during a critical window when organisms exhibit high plasticity in development. As a result, nutritional programming could be employed as a strategy in aquaculture to promote sustainable feeding strategies. In addition, this critical window overlaps with high mortality during the early life stages. This means programming effects could potentially translate into measurable consequences for the dynamics of wild populations. Given the wide variety of metabolic consequences of programming and the diversity of fishes, many important questions remain unanswered. This report summarizes research from mammalian and fish models and identifies knowledge gaps and priority areas for research into nutritional programming in fishes.
Similar content being viewed by others
Notes
PEPCK is involved in gluconeogenesis. Glucokinase (GK) is a key enzyme in glycolysis.
3-hydroxyacyl-CoA dehydrogenase (hoad) is involved in lipid catabolism. Pyruvate kinase muscle isoform (pkm) is a glycolytic enzyme that catalyzes the last step in glycolysis. Glutamate dehydrogenase (gdh) is involved in amino acid catabolism.
Ubiquitinol cytochrome c reductase core protein 2 (qcr2) and cytochrome oxidase 4 (cox4) are involved in oxidative phosphorylation processes in mitochondria.
Proinflammatory cytokines interleukin 1 β (il1b), anti-inflammatory cytokine interleukin 10 (il10), matrix remodeling enzyme matrix metalloproteases 9 and 13 (mmp9 and mmp13) are all involved in inflammation in fish. Elevated trypsin levels are associated with intestinal inflammation in fishes.
Glucose-6-phosphatase (G6Pase) is involved in glucose production (gluconeogenesis and glycogenolysis).
Phosphofructokinase (pfkmbb, pfkmaa) is involved in glycolysis.
Glucose transporter (Glut) transports glucose across the plasma membrane.
Lpl, lipoprotein lipase, facilitates the tissue uptake of circulating fatty acids from lipoproteins. Elovl6, elongation of very long-chain fatty acids protein 6, is a key lipogenic enzyme that elongates saturated and monounsaturated fatty acids of 12, 14 and 16 carbon atoms and 18:0 is a terminal product of lipogenesis. Cpt1, carnitine palmitoyltransferase I, is responsible for the formation of fatty acyl-carnitine esters from fatty acid that allows for the transport into mitochondria for β-oxidation.
Fatty acid binding protein 2 gene (fabp) is related to fatty acid transport and uptake. Solute carrier family 15 oligopeptide transporter member 1b (slc15a1) is related dipeptide and tripeptide absorption and growth in fishes (Perera and Yúfera 2016a).
CPTI (carnitine palmitoyltransferase I) and UCP3 (uncoupling protein 3) regulates skeletal muscle fatty acid oxidation and their expression is positively associated with increased substrate flux for mitochondrial β-oxidation. HADH (trifunctional protein of β-oxidation, also referred to as TFE, MTPA) is an inner mitochondrial membrane protein and its function causes a decline in NAD + /NADH ratio in skeletal muscle mitochondria, which subsequently leads to a reduced Krebs cycle flux. HADHA is the HADH α subunit (Lane et al. 2001).
SCAD (short chain acyl-CoA dehydrogenase).
Δ5D mediates synthesis of ARA and EPA from their respective precursors, 20:3(n-6) and 20:4(n-3).
Dnmt 1 is responsible for methylation maintenance during cell replication. HDAC1-Dnmt1 complexes initiate the recruitment of methyl-CpG-binding domain proteins that mediate CpG island methylation.
ER-α, estrogen receptor α; ERR-α, estrogen-related receptor α; HNF-4α, hepatic nuclear factor 4α.
ppp2r2ba, encodes protein phosphatase 2, regulatory subunit B, β a.
References
Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, McKnight R, Lane RH (2008) Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41:91–102. https://doi.org/10.1677/JME-08-0025
Adam A-C, Skjærven KH, Whatmore P, Moren M, Lie KK (2018) Parental high dietary arachidonic acid levels modulated the hepatic transcriptome of adult zebrafish (Danio rerio) progeny. PLoS ONE 13:e0201278. https://doi.org/10.1371/journal.pone.0201278
Adam A-C, Lie KK, Whatmore P, Jakt LM, Moren M, Skjærven KH (2019) Profiling DNA methylation patterns of zebrafish liver associated with parental high dietary arachidonic acid. PLoS ONE 14:e0220934. https://doi.org/10.1371/journal.pone.0220934
Alami-Durante H, Cluzeaud M, Duval C, Maunas P, Girod-David V, Médale F (2014) Early decrease in dietary protein:energy ratio by fat addition and ontogenetic changes in muscle growth mechanisms of rainbow trout: short- and long-term effects. Br J Nutr 112:674–687. https://doi.org/10.1017/S0007114514001391
Balasubramanian MN, Panserat S, Dupont-Nivet M, Quillet E, Montfort J, Cam AL, Medale F, Kaushik SJ, Geurden I (2016) Molecular pathways associated with the nutritional programming of plant-based diet acceptance in rainbow trout following an early feeding exposure. BMC Genomics 17:1–20. https://doi.org/10.1186/s12864-016-2804-1
Bieswal F, Ahn M-T, Reusens B, Holvoet P, Raes M, Rees WD, Remacle C (2006) The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity 14:1330–1343. https://doi.org/10.1038/oby.2006.151
Bonacic K, Campoverde C, Gómez-Arbonés J, Gisbert E, Estevez A, Morais S (2016) Dietary fatty acid composition affects food intake and gut–brain satiety signaling in Senegalese sole (Solea senegalensis, Kaup 1858) larvae and post-larvae. Gen Comp Endocrinol 228:79–94. https://doi.org/10.1016/j.ygcen.2016.02.002
Borengasser SJ, Lau F, Kang P, Blackburn ML, Ronis MJJ, Badger TM, Shankar K (2011) Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS ONE 6:e24068. https://doi.org/10.1371/journal.pone.0024068
Canada P, Engrola S, Mira S, Teodósio R, del Yust M, Sousa V, Pedroche J, Fernandes JMO, Conceição LEC, Valente LMP (2018) Larval dietary protein complexity affects the regulation of muscle growth and the expression of DNA methyltransferases in Senegalese sole. Aquaculture 491:28–38. https://doi.org/10.1016/j.aquaculture.2018.02.044
Chang G-Q, Gaysinskaya V, Karatayev O, Leibowitz SF (2008) Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 28:12107–12119. https://doi.org/10.1523/JNEUROSCI.2642-08.2008
Chango A, Pogribny I (2015) Considering maternal dietary modulators for epigenetic regulation and programming of the fetal epigenome. Nutrients 7:2748–2770. https://doi.org/10.3390/nu7042748
Choi S-W, Friso S (2010) Epigenetics: a new bridge between nutrition and health. Adv Nutr 1:8–16. https://doi.org/10.3945/an.110.1004
Clarkson M, Migaud H, Metochis C, Vera LM, Leeming D, Tocher DR, Taylor JF (2017) Early nutritional intervention can improve utilisation of vegetable-based diets in diploid and triploid Atlantic salmon Salmo salar. Br J Nutr 118:17–29. https://doi.org/10.1017/S0007114517001842
Coates PM, Brown SA, Sonawane BR, Koldovsky O (1983) Effect of early nutrition on serum cholesterol levels in adult rats challenged with high fat diet. J Nutr 113:1046–1050
Collins SA, Øverland M, Skrede A, Drew MD (2013) Effect of plant protein sources on growth rate in salmonids: meta-analysis of dietary inclusion of soybean, pea and canola/rapeseed meals and protein concentrates. Aquaculture 400:85–100. https://doi.org/10.1016/j.aquaculture.2013.03.006
Connor WE, Neuringer M, Lin DS (1990) Dietary effects on brain fatty acid composition: the reversibility of n-3 fatty acid deficiency and turnover of docosahexaenoic acid in the brain, erythrocytes, and plasma of rhesus monkeys. J Lipid Res 31:237–247
Connor WE, Neuringer M, Reisbick S (1992) Essential fatty acids: the importance of n-3 fatty acids in the retina and brain. Nutr Rev 50:21–29. https://doi.org/10.1111/j.1753-4887.1992.tb01286.x
Corapci F, Radan AE, Lozoff B (2006) Iron deficiency in infancy and mother-child interaction at 5 years. J Dev Behav Pediatr 27:371
D’Alessandro M, Eugenia Oliva M, Alejandra Fortino M, Chicco A (2014) Maternal sucrose-rich diet and fetal programming: changes in hepatic lipogenic and oxidative enzymes and glucose homeostasis in adult offspring. Food Funct 5:446–453. https://doi.org/10.1039/C3FO60436E
Desai M, Crowther NJ, Ozanne SE, Lucas A, Hales CN (1995) Adult glucose and lipid metabolism may be programmed during fetal life. Biochem Soc Trans 23:331–335
Desai M, Crowther NJ, Lucas A, Hales CN (1996) Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 76:591–603
Engelbregt MJT, Houdijk MECAM, Popp-Snijders C, Delemarre-van de Waal HA (2000) The effects of intra-uterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatr Res 48:803–807. https://doi.org/10.1203/00006450-200012000-00017
Engrola S, Aragão C, Valente LMP, Conceição LEC (2018) Nutritional modulation of marine fish larvae performance. In: Yúfera M (ed) Emerging issues in fish larvae research. Springer, Cham, pp 209–228
Eroldoğan TO, Yilmaz AH, Turchini GM, Arslan M, Sirkecioğlu NA, Engin K, Özşahinoğlu I, Mumoğullarında P (2013) Fatty acid metabolism in European sea bass (Dicentrarchus labrax): effects of n-6 PUFA and MUFA in fish oil replaced diets. Fish Physiol Biochem Dordr 39:941–955. https://doi.org/10.1007/s10695-012-9753-7
Fall CHD (2012) Fetal programming and the risk of noncommunicable disease. Indian J Pediatr 80:13–20. https://doi.org/10.1007/s12098-012-0834-5
Fang L, Liang X-F, Zhou Y, Guo X-Z, He Y, Yi T-L, Liu L-W, Yuan X-C, Tao Y-X (2014) Programming effects of high-carbohydrate feeding of larvae on adult glucose metabolism in zebrafish, Danio rerio. Br J Nutr 111:808–818. https://doi.org/10.1017/S0007114513003243
Faulk CK and Fuiman LA. Nutritional programming of n-3 highly unsaturated fatty acid metabolism in larvae of the marine fish Sciaenops ocellatus. Fish Physiol Biochem (Submitted).
Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13:97–109. https://doi.org/10.1038/nrg3142
Fernández-Palacios H, Norberg B, Izquierdo M, Hamre K (2011) Effects of broodstock diet on eggs and larvae. Larval Fish Nutrition. John Wiley and Sons Publisher, Oxford, UK, Wiley-Blackwell, pp 151–181
Fernandez-Twinn DS, Ozanne SE (2010) Early life nutrition and metabolic programming. Ann N Y Acad Sci 1212:78–96. https://doi.org/10.1111/j.1749-6632.2010.05798.x
Fontagné-Dicharry S, Alami-Durante H, Aragão C, Kaushik SJ, Geurden I (2017) Parental and early-feeding effects of dietary methionine in rainbow trout (Oncorhynchus mykiss). Aquaculture 469:16–27. https://doi.org/10.1016/j.aquaculture.2016.11.039
Fuiman LA (2018) Egg boon fatty acids reveal effects of a climatic event on a marine food web. Ecol Monogr 88:585–599. https://doi.org/10.1002/ecm.1324
Fuiman LA, Faulk CK (2013) Batch spawning facilitates transfer of an essential nutrient from diet to eggs in a marine fish. Biology Letters 9(5):20130593
Fuiman LA, Perez KO (2015) Metabolic programming mediated by an essential fatty acid alters body composition and survival skills of a marine fish. Proc R Soc B Biol Sci 282:20151414. https://doi.org/10.1098/rspb.2015.1414
Fuiman LA, Connelly TL, Lowerre-Barbieri SK, McClelland JW (2015) Egg boons: central components of marine fatty acid food webs. Ecology 96:362–372. https://doi.org/10.1890/14-0571.1
Geurden I, Aramendi M, Zambonino-Infante J, Panserat S (2007) Early feeding of carnivorous rainbow trout (Oncorhynchus mykiss) with a hyperglucidic diet during a short period: effect on dietary glucose utilization in juveniles. Am J Physiol Regul Integr Comp Physiol 292:R2275–R2283. https://doi.org/10.1152/ajpregu.00444.2006
Geurden I, Borchert P, Balasubramanian MN, Schrama JW, Dupont-Nivet M, Quillet E, Kaushik SJ, Panserat S, Médale F (2013) The positive impact of the early-feeding of a plant-based diet on its future acceptance and utilisation in rainbow trout. PLoS ONE 8:e83162. https://doi.org/10.1371/journal.pone.0083162
Geurden I, Mennigen J, Plagnes-Juan E, Veron V, Cerezo T, Mazurais D, Zambonino-Infante J, Gatesoupe J, Skiba-Cassy S, Panserat S (2014) High or low dietary carbohydrate:protein ratios during first-feeding affect glucose metabolism and intestinal microbiota in juvenile rainbow trout. J Exp Biol 217:3396–3406. https://doi.org/10.1242/jeb.106062
Gong G, Xue M, Wang J, Wu X, Zheng Y, Han F, Liang X, Su X (2015) The regulation of gluconeogenesis in the Siberian sturgeon (Acipenser baerii) affected later in life by a short-term high-glucose programming during early life. Aquaculture 436:127–136. https://doi.org/10.1016/j.aquaculture.2014.10.044
Govoni JJ, Boehlert GW, Watanabe Y (1986) The physiology of digestion in fish larvae. Environ Biol Fishes 16:59–77. https://doi.org/10.1007/BF00005160
Guilloteau P, Zabielski R, Hammon HM, Metges CC (2010) Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr Res Rev 23:4–22. https://doi.org/10.1017/S0954422410000077
Hahn P (1984) Effect of litter size on plasma cholesterol and insulin and some liver and adipose tissue enzymes in adult rodents. J Nutr 114:1231–1234
Hales CN, Barker DJP (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601. https://doi.org/10.1007/BF00400248
Hales CN, Desai M, Ozanne SE, Crowther NJ (1996) Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem Soc Trans 24:341–350
Hamre K, Yúfera M, Rønnestad I, Boglione C, Conceição LEC, Izquierdo M (2013) Fish larval nutrition and feed formulation: knowledge gaps and bottlenecks for advances in larval rearing. Rev Aquac 5:S26–S58. https://doi.org/10.1111/j.1753-5131.2012.01086.x
Hawkyard M, Stuart K, Langdon C, Drawbridge M (2016) The enrichment of rotifers (Brachionus plicatilis) and Artemia franciscana with taurine liposomes and their subsequent effects on the larval development of California yellowtail (Seriola lalandi). Aquac Nutr 22:911–922. https://doi.org/10.1111/anu.12317
Hemre G-I, Mommsen TP, Krogdahl Å (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194. https://doi.org/10.1046/j.1365-2095.2002.00200.x
Hoile SP, Irvine NA, Kelsall CJ, Sibbons C, Feunteun A, Collister A, Torrens C, Calder PC, Hanson MA, Lillycrop KA, Burdge GC (2013) Maternal fat intake in rats alters 20:4n-6 and 22:6n-3 status and the epigenetic regulation of Fads2 in offspring liver. J Nutr Biochem 24:1213–1220. https://doi.org/10.1016/j.jnutbio.2012.09.005
Houde ED (1997) Patterns and trends in larval-stage growth and mortality of teleost fish. J Fish Biol 51:52–83. https://doi.org/10.1111/j.1095-8649.1997.tb06093.x
Houde ED (2006) Subtleties and episodes in the early life of fishes. J Fish Biol 35:29–38. https://doi.org/10.1111/j.1095-8649.1989.tb03043.x
Hu H, Liu J, Plagnes-Juan E, Herman A, Leguen I, Goardon L, Geurden I, Panserat S, Marandel L (2018) Programming of the glucose metabolism in rainbow trout juveniles after chronic hypoxia at hatching stage combined with a high dietary carbohydrate: protein ratios intake at first-feeding. Aquaculture 488:1–8. https://doi.org/10.1016/j.aquaculture.2018.01.015
Imsland AK, Foss A, Koedijk R, Folkvord A, Stefansson SO, Jonassen TM (2006) Short- and long-term differences in growth, feed conversion efficiency and deformities in juvenile Atlantic cod (Gadus morhua) startfed on rotifers or zooplankton. Aquac Res 37:1015–1027. https://doi.org/10.1111/j.1365-2109.2006.01523.x
Izquierdo MS, Socorro J, Arantzamendi L, Hernández-Cruz CM (2000) Recent advances in lipid nutrition in fish larvae. Fish Physiol Biochem 22:97–107. https://doi.org/10.1023/A:1007810506259
Izquierdo MS, Turkmen S, Montero D, Zamorano MJ, Afonso JM, Karalazos V, Fernández-Palacios H (2015) Nutritional programming through broodstock diets to improve utilization of very low fishmeal and fish oil diets in gilthead sea bream. Aquaculture 449:18–26. https://doi.org/10.1016/j.aquaculture.2015.03.032
Jump DB (2004) Fatty acid regulation of gene transcription. Crit Rev Clin Lab Sci 41:41–78. https://doi.org/10.1080/10408360490278341
Kemski M, Wick M, Dabrowski K (2018) Nutritional programming effects on growth and reproduction of broodstock and embryonic development of progeny in yellow perch (Perca flavescens) fed soybean meal-based diets. Aquaculture 497:452–461. https://doi.org/10.1016/j.aquaculture.2018.07.001
Kersten AH (2011) Nutrigenomics of fatty acid sensing. In: Rodriguez RL, Bidlack WR (eds) Nutritional genomics: the impact of dietary regulation of gene function on human disease. CRC Press, Boca Raton, pp 173–184
Koedijk RM, Folkvord A, Foss A, Pittman K, Stefansson SO, Handeland S, Imsland AK (2010) The influence of first-feeding diet on the Atlantic cod Gadus morhua phenotype: survival, development and long-term consequences for growth. J Fish Biol 77:1–19. https://doi.org/10.1111/j.1095-8649.2010.02652.x
Kolkovski S (2001) Digestive enzymes in fish larvae and juveniles—implications and applications to formulated diets. Aquaculture 200:181–201. https://doi.org/10.1016/S0044-8486(01)00700-1
Lane RH, Kelley DE, Ritov VH, Tsirka AE, Gruetzmacher EM (2001) Altered expression and function of mitochondrial β-oxidation enzymes in juvenile intrauterine-growth-retarded rat skeletal muscle. Pediatr Res 50:83–90. https://doi.org/10.1203/00006450-200107000-00016
Langley-Evans SC (2009) Nutritional programming of disease: unravelling the mechanism. J Anat 215:36–51. https://doi.org/10.1111/j.1469-7580.2008.00977.x
Lazo JP, Darias MJ, Gisbert E (2011) Ontogeny of the digestive tract. In: Holt GJ (ed) Larval fish nutrition. John Wiley and Sons Publisher, Oxford, UK, Wiley-Blackwell, pp 5–46
Lazzarotto V, Corraze G, Larroquet L, Mazurais D, Médale F (2016) Does broodstock nutritional history affect the response of progeny to different first-feeding diets? A whole-body transcriptomic study of rainbow trout alevins. Br J Nutr 115:2079–2092. https://doi.org/10.1017/S0007114516001252
Lemonnier D, Suquet JP, Aubert R, Rosselin G (1973) Long term effect of mouse neonate food intake on adult body composition, insulin and glucose serum levels. Horm Metab Res 5:223–224. https://doi.org/10.1055/s-0028-1096731
Lewis DS, Bertrand HA, McMahan CA, McGill HC, Carey KD, Masoro EJ (1986) Preweaning food intake influences the adiposity of young adult baboons. J Clin Invest 78:899–905. https://doi.org/10.1172/JCI112678
Li D, Weisinger HS, Weisinger RS, Mathai M, Armitage JA, Vingrys AJ, Sinclair AJ (2006) Omega 6 to omega 3 fatty acid imbalance early in life leads to persistent reductions in DHA levels in glycerophospholipids in rat hypothalamus even after long-term omega 3 fatty acid repletion. Prostaglandins Leukot Essent Fatty Acids 74:391–399. https://doi.org/10.1016/j.plefa.2006.03.010
Li N, Ye M, Li Y, Yan Z, Butcher LM, Sun J, Han X, Chen Q, Zhang X, Wang J (2010) Whole genome DNA methylation analysis based on high throughput sequencing technology. Methods 52:203–212. https://doi.org/10.1016/j.ymeth.2010.04.009
Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135:1382–1386
Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97:1064–1073. https://doi.org/10.1017/S000711450769196X
Liu J, Dias K, Plagnes-Juan E, Veron V, Panserat S, Marandel L (2017) Long-term programming effect of embryonic hypoxia exposure and high-carbohydrate diet at first feeding on glucose metabolism in juvenile rainbow trout. J Exp Biol 220:3686–3694. https://doi.org/10.1242/jeb.161406
London RM, Snowdon CT, Smithana JM (1979) Early experience with sour and bitter solutions increases subsequent ingestion. Physiol Behav 22:1149–1155. https://doi.org/10.1016/0031-9384(79)90270-1
Lozoff B, Jimenez E, Wolf AW (1991) Long-term developmental outcome of infants with iron deficiency. N Engl J Med 325:687–694. https://doi.org/10.1056/NEJM199109053251004
Lucas A (1991) Programming by early nutrition in man. In: Bock GR, Whelan J (eds) The childhood environment and adult disease. CIBA Foundation Symposium 156. Wiley, Chichester, UK, pp 38–55
Lucas A (1998) Programming by early nutrition: an experimental approach. J Nutr 128:401S–406S
Lucas A, Baker BA, Desai M, Hales CN (1996) Nutrition in pregnant or lactating rats programs lipid metabolism in the offspring. Br J Nutr 76:605–612
Lund I, Skov PV, Hansen BW (2012) Dietary supplementation of essential fatty acids in larval pikeperch (Sander lucioperca); short and long term effects on stress tolerance and metabolic physiology. Comp Biochem Physiol A Mol Integr Physiol 162:340–348. https://doi.org/10.1016/j.cbpa.2012.04.004
Marandel L, Véron V, Surget A, Plagnes-Juan É, Panserat S (2016) Glucose metabolism ontogenesis in rainbow trout (Oncorhynchus mykiss) in the light of the recently sequenced genome: new tools for intermediary metabolism programming. J Exp Biol 219:734–743. https://doi.org/10.1242/jeb.134304
Mathers JC (2017) Nutrigenomics in the modern era. Proc Nutr Soc 76:265–275. https://doi.org/10.1017/S002966511600080X
McMullen S, Langley-Evans SC, Gambling L, Lang C, Swali A, McArdle HJ (2012) A common cause for a common phenotype: the gatekeeper hypothesis in fetal programming. Med Hypotheses 78:88–94. https://doi.org/10.1016/j.mehy.2011.09.047
Monroig Ó, Navarro JC, Tocher DR (2011) Long-chain polyunsaturated fatty acids in fish: recent advances on desaturases and elongases involved in their biosynthesis. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Nieto-López MG, Villarreal-Cavazos DA, Gamboa-Delgado J, Hernández-Hernández L (eds) Avances en Nutrición Acuícola XI—Memorias del Décimo Primer Simposio Internacional de Nutrición Acuícola, 23–25 de Noviembre, San Nicolás de los Garza, N. L., México. Universidad Autónoma de Nuevo León, Monterrey, México, pp 257–283
Morais S, Cahu C, Zambonino-Infante JL, Robin J, Rønnestad I, Dinis MT, Conceição LEC (2004) Dietary TAG source and level affect performance and lipase expression in larval sea bass (Dicentrarchus labrax). Lipids 39:449. https://doi.org/10.1007/s11745-004-1250-2
Morais S, Mendes AC, Castanheira MF, Coutinho J, Bandarra N, Dias J, Conceição LEC, Pousão-Ferreira P (2014) New formulated diets for Solea senegalensis broodstock: Effects of parental nutrition on biosynthesis of long-chain polyunsaturated fatty acids and performance of early larval stages and juvenile fish. Aquaculture 432:374–382. https://doi.org/10.1016/j.aquaculture.2014.04.033
Morisson M, Coustham V, Frésard L, Collin A, Zerjal T, Métayer-Coustard S, Bodin L, Minvielle F, Brun J-M, Pitel F (2017) Nutritional programming and effect of ancestor diet in birds. In: Patel V, Preedy V (eds) Handbook of nutrition, diet, and epigenetics. Springer International Publishing, Cham, pp 1–18
Müller M, Kersten S (2003) Nutrigenomics: goals and strategies. Nat Rev Genet 4:315–322. https://doi.org/10.1038/nrg1047
Øie G, Galloway T, Sørøy M, Holmvaag Hansen M, Norheim IA, Halseth CK, Almli M, Berg M, Gagnat MR, Wold P-A, Attramadal K, Hagemann A, Evjemo JO, Kjørsvik E (2015) Effect of cultivated copepods (Acartia tonsa) in first-feeding of Atlantic cod (Gadus morhua) and ballan wrasse (Labrus bergylta) larvae. Aquac Nutr. https://doi.org/10.1111/anu.12352
Oozeki Y, Bailey KM (1995) Ontogenetic development of digestive enzyme activities in larval walleye pollock, Theragra chalcogramma. Mar Biol 122:177–186. https://doi.org/10.1007/BF00348930
Ozanne SE, Martensz ND, Petry CJ, Loizou CL, Hales CN (1998) Maternal low protein diet in rats programmes fatty acid desaturase activities in the offspring. Diabetologia 41:1337–1342. https://doi.org/10.1007/s001250051074
Panserat S, Marandel L, Geurden I, Veron V, Dias K, Plagnes-Juan E, Pegourié G, Arbenoits E, Santigosa E, Weber G, Verlhac Trichet V (2017) Muscle catabolic capacities and global hepatic epigenome are modified in juvenile rainbow trout fed different vitamin levels at first feeding. Aquaculture 468:515–523. https://doi.org/10.1016/j.aquaculture.2016.11.021
Panserat S, Marandel L, Seiliez I, Skiba-Cassy S (2019) New insights on intermediary metabolism for a better understanding of nutrition in teleosts. Annu Rev Anim Biosci 7:195–220. https://doi.org/10.1146/annurev-animal-020518-115250
Patel MS, Srinivasan M, Laychock SG (2008) Metabolic programming: role of nutrition in the immediate postnatal life. J Inherit Metab Dis 32:218–228. https://doi.org/10.1007/s10545-008-1033-4
Perera E, Yúfera M (2016a) Soybean meal and soy protein concentrate in early diet elicit different nutritional programming effects on juvenile zebrafish. Zebrafish 13:61–69. https://doi.org/10.1089/zeb.2015.1131
Perera E, Yúfera M (2016b) Effects of soybean meal on digestive enzymes activity, expression of inflammation-related genes, and chromatin modifications in marine fish (Sparus aurata L.) larvae. Fish Physiol Biochem. https://doi.org/10.1007/s10695-016-0310-7
Petry CJ, Ozanne SE, Hales CN (2001) Programming of intermediary metabolism. Mol Cell Endocrinol 185:81–91. https://doi.org/10.1016/S0303-7207(01)00627-X
Pittman K, Yúfera M, Pavlidis M, Geffen AJ, Koven W, Ribeiro L, Zambonino-Infante JL, Tandler A (2013) Fantastically plastic: fish larvae equipped for a new world. Rev Aquac 5:S224–S267. https://doi.org/10.1111/raq.12034
Plagemann A, Harder T, Rake A, Melchior K, Rohde W, Dörner G (2000) Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 130:2582–2589. https://doi.org/10.1093/jn/130.10.2582
Pooya S, Blaise S, Moreno Garcia M, Giudicelli J, Alberto J-M, Guéant-Rodriguez R-M, Jeannesson E, Gueguen N, Bressenot A, Nicolas B, Malthiery Y, Daval J-L, Peyrin-Biroulet L, Bronowicki J-P, Guéant J-L (2012) Methyl donor deficiency impairs fatty acid oxidation through PGC-1α hypomethylation and decreased ER-α, ERR-α, and HNF-4α in the rat liver. J Hepatol 57:344–351. https://doi.org/10.1016/j.jhep.2012.03.028
Rao KR, Padmavathi IJN, Raghunath M (2012) Maternal micronutrient restriction programs the body adiposity, adipocyte function and lipid metabolism in offspring: a review. Rev Endocr Metab Disord 13:103–108. https://doi.org/10.1007/s11154-012-9211-y
Rocha F, Dias J, Engrola S, Gavaia P, Geurden I, Dinis MT, Panserat S (2014) Glucose overload in yolk has little effect on the long-term modulation of carbohydrate metabolic genes in zebrafish (Danio rerio). J Exp Biol 217:1139–1149. https://doi.org/10.1242/jeb.095463
Rocha F, Dias J, Engrola S, Gavaia P, Geurden I, Dinis MT, Panserat S (2015) Glucose metabolism and gene expression in juvenile zebrafish (Danio rerio) challenged with a high carbohydrate diet: effects of an acute glucose stimulus during late embryonic life. Br J Nutr 113:403–413. https://doi.org/10.1017/S0007114514003869
Rocha F, Dias J, Geurden I, Dinis MT, Panserat S, Engrola S (2016a) High-glucose feeding of gilthead seabream (Sparus aurata) larvae: effects on molecular and metabolic pathways. Aquaculture 451:241–253. https://doi.org/10.1016/j.aquaculture.2015.09.015
Rocha F, Dias J, Geurden I, Dinis MT, Panserat S, Engrola S (2016b) Dietary glucose stimulus at larval stage modifies the carbohydrate metabolic pathway in gilthead seabream (Sparus aurata) juveniles: an in vivo approach using 14C-starch. Comp Biochem Physiol A Mol Integr Physiol 201:189–199. https://doi.org/10.1016/j.cbpa.2016.07.016
Rønnestad I, Yúfera M, Ueberschär B, Ribeiro L, Sæle Ø, Boglione C (2013) Feeding behaviour and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Rev Aquac 5:S59–S98. https://doi.org/10.1111/raq.12010
Roseboom TJ, van der Meulen JHP, Ravelli ACJ, Osmond C, Barker DJP, Bleker OP (2001) Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Twin Res Hum Genet 4:293–298. https://doi.org/10.1375/twin.4.5.293
Samuelsson LM, Larsson DGJ (2008) Contributions from metabolomics to fish research. Mol Biosyst 4:974–979. https://doi.org/10.1039/B804196B
Sargent JR, Bell JG, Bell MV, Henderson RJ, Tocher DR (1995) Requirement criteria for essential fatty acids. J Appl Ichthyol 11:183–198. https://doi.org/10.1111/j.1439-0426.1995.tb00018.x
Seiliez I, Panserat S, Corraze G, Kaushik S, Bergot P (2003) Cloning and nutritional regulation of a Δ6-desaturase-like enzyme in the marine teleost gilthead seabream (Sparus aurata). Comp Biochem Physiol B Biochem Mol Biol 135:449–460. https://doi.org/10.1016/S1096-4959(03)00111-8
Seiliez I, Vélez EJ, Lutfi E, Dias K, Plagnes-Juan E, Marandel L, Panserat S, Geurden I, Skiba-Cassy S (2017) Eating for two: Consequences of parental methionine nutrition on offspring metabolism in rainbow trout (Oncorhynchus mykiss). Aquaculture 471:80–91. https://doi.org/10.1016/j.aquaculture.2017.01.010
Sinclair KD, Rutherford KMD, Wallace JM, Brameld JM, Stöger R, Alberio R, Sweetman D, Gardner DS, Perry VEA, Adam CL, Ashworth CJ, Robinson JE, Dwyer CM (2016) Epigenetics and developmental programming of welfare and production traits in farm animals. Reprod Fertil Dev 28:1443–1478. https://doi.org/10.1071/RD16102
Skjærven KH, Jakt LM, Dahl JA, Espe M, Aanes H, Hamre K, Fernandes JMO (2016) Parental vitamin deficiency affects the embryonic gene expression of immune-, lipid transport- and apolipoprotein genes. Sci Rep 6:34535. https://doi.org/10.1038/srep34535
Skjærven KH, Jakt LM, Fernandes JMO, Dahl JA, Adam A-C, Klughammer J, Bock C, Espe M (2018) Parental micronutrient deficiency distorts liver DNA methylation and expression of lipid genes associated with a fatty-liver-like phenotype in offspring. Sci Rep 8:1–16. https://doi.org/10.1038/s41598-018-21211-5
Smart JL (1986) Undernutrition, learning and memory: review of experimental studies. In: Taylor TG, Jenkins NK (eds) Proceedings of XIII International Congress of Nutrition. John Libbey, London, pp 74–78
Suzuki K, Simpson KA, Minnion JS, Shillito JC, Bloom SR (2010) The role of gut hormones and the hypothalamus in appetite regulation. Endocr J 57:359–372. https://doi.org/10.1507/endocrj.K10E-077
Symonds ME, Sebert SP, Hyatt MA, Budge H (2009) Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol 5:604–610. https://doi.org/10.1038/nrendo.2009.195
Thompson KL, Faulk CK, Fuiman LA (2019) Applying the ontogeny of digestive enzyme activity to guide early weaning of pigfish, Orthopristis chrysoptera (L.). Aquac Res 50:1404–1410. https://doi.org/10.1111/are.14015
Timofeeva NM, Egorova VV, Nikitina AA (2000) Metabolic/food programming of enzyme systems in digestive and nondigestive organs of rats. Dokl Biol Sci 375:587–589
Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184. https://doi.org/10.1080/713610925
Tocher DR, Zheng X, Schlechtriem C, Hastings N, Dick JR, Teale AJ (2006) Highly unsaturated fatty acid synthesis in marine fish: cloning, functional characterization, and nutritional regulation of fatty acyl Δ6 desaturase of Atlantic cod (Gadus morhua L.). Lipids 41:1003–1016. https://doi.org/10.1007/s11745-006-5051-4
Tonheim SK, Koven W, Rønnestad I (2000) Enrichment of Artemia with free methionine. Aquaculture 190:223–235. https://doi.org/10.1016/S0044-8486(00)00402-6
Trujillo E, Davis C, Milner J (2006) Nutrigenomics, proteomics, metabolomics, and the practice of dietetics. J Am Diet Assoc 106:403–413. https://doi.org/10.1016/j.jada.2005.12.002
Turchini GM, Francis DS (2009) Fatty acid metabolism (desaturation, elongation and β-oxidation) in rainbow trout fed fish oil- or linseed oil-based diets. Br J Nutr 102:69–81. https://doi.org/10.1017/S0007114508137874
Turkmen S, Zamorano MJ, Fernández-Palacios H, Hernández-Cruz CM, Montero D, Robaina L, Izquierdo M (2017) Parental nutritional programming and a reminder during juvenile stage affect growth, lipid metabolism and utilisation in later developmental stages of a marine teleost, the gilthead sea bream (Sparus aurata). Br J Nutr 118:500–512. https://doi.org/10.1017/S0007114517002434
Turkmen S, Hernández-Cruz CM, Zamorano MJ, Fernández-Palacios H, Montero D, Afonso JM, Izquierdo M (2019) Long-chain PUFA profiles in parental diets induce long-term effects on growth, fatty acid profiles, expression of fatty acid desaturase 2 and selected immune system-related genes in the offspring of gilthead seabream. Br J Nutr 122:25–38. https://doi.org/10.1017/S0007114519000977
Vagner M, Zambonino Infante JL, Robin JH, Person-Le Ruyet J (2007) Is it possible to influence European sea bass (Dicentrarchus labrax) juvenile metabolism by a nutritional conditioning during larval stage? Aquaculture 267:165–174. https://doi.org/10.1016/j.aquaculture.2007.01.031
Vagner M, Robin JH, Zambonino-Infante JL, Tocher DR, Person-Le Ruyet J (2009) Ontogenic effects of early feeding of sea bass (Dicentrarchus labrax) larvae with a range of dietary n-3 highly unsaturated fatty acid levels on the functioning of polyunsaturated fatty acid desaturation pathways. Br J Nutr 101:1452–1462. https://doi.org/10.1017/S0007114508088053
Valsamakis G, Kanaka-Gantenbein C, Malamitsi-Puchner A, Mastorakos G (2006) Causes of intrauterine growth restriction and the postnatal development of the metabolic syndrome. Ann N Y Acad Sci 1092:138–147. https://doi.org/10.1196/annals.1365.012
Vera LM, Metochis C, Taylor JF, Clarkson M, Skjærven KH, Migaud H, Tocher DR (2017) Early nutritional programming affects liver transcriptome in diploid and triploid Atlantic salmon Salmo salar. BMC Genomics. https://doi.org/10.1186/s12864-017-4264-7
Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD (2000) Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol-Endocrinol Metab 279:E83–E87. https://doi.org/10.1152/ajpendo.2000.279.1.E83
Villeneuve L, Natarajan R (2011) Role of epigenetics in the complications associated with diabetes and related metabolic disorders. Nutritional genomics: the impact of dietary regulation of gene function on human disease. CRC Press, Boca Raton, pp 41–60
Volkoff H (2016) The neuroendocrine regulation of food intake in fish: a review of current knowledge. Front Neurosci. https://doi.org/10.3389/fnins.2016.00540
Warensjö E, Öhrvall M, Vessby B (2006) Fatty acid composition and estimated desaturase activities are associated with obesity and lifestyle variables in men and women. Nutr Metab Cardiovasc Dis 16:128–136. https://doi.org/10.1016/j.numecd.2005.06.001
Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S (2008) Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes 32:1373–1379. https://doi.org/10.1038/ijo.2008.100
West-Eberhard MJ (2019) Nutrition, the visceral immune system, and the evolutionary origins of pathogenic obesity. Proc Natl Acad Sci 116:723–731. https://doi.org/10.1073/pnas.1809046116
Winick M, Noble A (1966) Cellular response in rats during malnutrition at various ages. J Nutr 89:300–306
Yehuda S, Youdim MEH, Mostofsky DI (1986) Brain iron-deficiency causes reduced learning capacity in rats. Pharmacol Biochem Behav 25:141–144. https://doi.org/10.1016/0091-3057(86)90244-3
Young JI, Züchner S, Wang G (2015) Regulation of the epigenome by vitamin C. Annu Rev Nutr 35:545–564. https://doi.org/10.1146/annurev-nutr-071714-034228
Youngentob SL, Glendinning JI (2009) Fetal ethanol exposure increases ethanol intake by making it smell and taste better. Proc Natl Acad Sci 106:5359–5364. https://doi.org/10.1073/pnas.0809804106
Zambonino-Infante JL, Panserat S, Servili A, Mouchel O, Madec L, Mazurais D (2019) Nutritional programming by dietary carbohydrates in European sea bass larvae: not always what expected at juvenile stage. Aquaculture 501:441–447. https://doi.org/10.1016/j.aquaculture.2018.11.056
Zheng X, Seiliez I, Hastings N, Tocher DR, Panserat S, Dickson CA, Bergot P, Teale AJ (2004) Characterization and comparison of fatty acyl Δ6 desaturase cDNAs from freshwater and marine teleost fish species. Comp Biochem Physiol B Biochem Mol Biol 139:269–279. https://doi.org/10.1016/j.cbpc.2004.08.003
Zheng X, Ding Z, Xu Y, Monroig O, Morais S, Tocher DR (2009) Physiological roles of fatty acyl desaturases and elongases in marine fish: characterisation of cDNAs of fatty acyl Δ6 desaturase and elovl5 elongase of cobia (Rachycentron canadum). Aquaculture 290:122–131. https://doi.org/10.1016/j.aquaculture.2009.02.010
Acknowledgement
The authors would like to thank Cynthia Faulk for her critical reading and insightful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hou, Z., Fuiman, L.A. Nutritional programming in fishes: insights from mammalian studies. Rev Fish Biol Fisheries 30, 67–92 (2020). https://doi.org/10.1007/s11160-019-09590-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-019-09590-y