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Nutritional programming in fishes: insights from mammalian studies

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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.

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Notes

  1. PEPCK is involved in gluconeogenesis. Glucokinase (GK) is a key enzyme in glycolysis.

  2. 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.

  3. Ubiquitinol cytochrome c reductase core protein 2 (qcr2) and cytochrome oxidase 4 (cox4) are involved in oxidative phosphorylation processes in mitochondria.

  4. 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.

  5. Highly unsaturated fatty acid (HUFA) usually refers to 22 carbon atoms and at least 3 ethylenic bonds (Tocher 2003) or at least 20 carbon atoms and at least 4 ethylenic bonds (Morais et al. 2004).

  6. Glucose-6-phosphatase (G6Pase) is involved in glucose production (gluconeogenesis and glycogenolysis).

  7. Phosphofructokinase (pfkmbb, pfkmaa) is involved in glycolysis.

  8. Glucose transporter (Glut) transports glucose across the plasma membrane.

  9. 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.

  10. 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).

  11. 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).

  12. SCAD (short chain acyl-CoA dehydrogenase).

  13. Δ5D mediates synthesis of ARA and EPA from their respective precursors, 20:3(n-6) and 20:4(n-3).

  14. 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.

  15. ER-α, estrogen receptor α; ERR-α, estrogen-related receptor α; HNF-4α, hepatic nuclear factor 4α.

  16. ppp2r2ba, encodes protein phosphatase 2, regulatory subunit B, β a.

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Acknowledgement

The authors would like to thank Cynthia Faulk for her critical reading and insightful comments on the manuscript.

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Correspondence to Zhenxin Hou.

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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

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