1932

Abstract

The rapid development of aquaculture production throughout the world over the past few decades has led to the emergence of new scientific challenges to improve fish nutrition. The diet formulations used for farmed fish have been largely modified in the past few years. However, bottlenecks still exist in being able to suppress totally marine resources (fish meal and fish oil) in diets without negatively affecting growth performance and flesh quality. A better understanding of fish metabolism and its regulation by nutrients is thus mandatory. In this review, we discuss four fields of research that are highly important for improving fish nutrition in the future: () fish genome complexity and subsequent consequences for metabolism, () microRNAs (miRNAs) as new actors in regulation of fish metabolism, () the role of autophagy in regulation of fish metabolism, and () the nutritional programming of metabolism linked to the early life of fish.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-020518-115250
2019-02-15
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/animal/7/1/annurev-animal-020518-115250.html?itemId=/content/journals/10.1146/annurev-animal-020518-115250&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Klinger D, Naylor R 2012. Searching for solutions in aquaculture: charting a sustainable course. Annu. Rev. Environ. Resour. 37:247–76
    [Google Scholar]
  2. 2. Food Agric. Organ. 2016. The State of the World Fisheries and Aquaculture 2016: Contributing to Food Security and Nutrition for All Rome: Food Agric. Organ.
  3. 3.  Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M et al. 2009. Feeding aquaculture in an era of finite resources. PNAS 106:3615103–10
    [Google Scholar]
  4. 4.  Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylor TG et al. 2007. Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquacult. Res. 38:551–79
    [Google Scholar]
  5. 5.  Lazzarotto V, Medale F, Larroquet L, Corraze G 2018. Long-term dietary replacement of fishmeal and fish oil in diets for rainbow trout (Oncorhynchus mykiss): effects on growth, whole body fatty acids and intestinal and hepatic gene expression. PLOS ONE 13:e0190730
    [Google Scholar]
  6. 6.  Panserat S, Hortopan GA, Plagnes-Juan E, Kolditz C, Lansard M et al. 2009. Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 294:123–31
    [Google Scholar]
  7. 7.  Kamalam BJ, Medale F, Panserat S 2017. Utilisation of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies. Aquaculture 467:3–27
    [Google Scholar]
  8. 8.  Tocher DR 2015. Omega-3 long-chain polyunsaturated fatty acids and aquaculture in perspective. Aquaculture 449:94–107
    [Google Scholar]
  9. 9.  Yu WP, Yew K, Rajasegaran V, Venkatesh B 2007. Sequencing and comparative analysis of fugu protocadherin clusters reveal diversity of protocadherin genes among teleosts. BMC Evol. Biol. 7:49
    [Google Scholar]
  10. 10.  Chen S, Zhang G, Shao C, Huang Q, Liu G et al. 2014. Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat. Genet. 46:253–60
    [Google Scholar]
  11. 11.  Hu W, Chen J 2015. Whole-genome sequencing opens a new era for molecular breeding of grass carp (Ctenopharyngodon idellus). Sci. China Life Sci. 58:619–20
    [Google Scholar]
  12. 12.  Wang Y, Lu Y, Zhang Y, Ning Z, Li Y et al. 2015. The draft genome of the grass carp (Ctenopharyngodon idellus) provides insights into its evolution and vegetarian adaptation. Nat. Genet. 47:625–31
    [Google Scholar]
  13. 13.  Taylor JS, Van de Peer Y, Meyer A 2001. Genome duplication, divergent resolution and speciation. Trends Genet 17:299–301
    [Google Scholar]
  14. 14.  Conrad B, Antonarakis SE 2007. Gene duplication: a drive for phenotypic diversity and cause of human disease. Annu. Rev. Genom. Hum. Genet. 8:17–35
    [Google Scholar]
  15. 15.  Chen S, Krinsky BH, Long M 2013. New genes as drivers of phenotypic evolution. Nat. Rev. Genet. 14:645–60
    [Google Scholar]
  16. 16.  Volff JN 2005. Genome evolution and biodiversity in teleost fish. Heredity 94:280–94
    [Google Scholar]
  17. 17.  Hahn MW 2009. Distinguishing among evolutionary models for the maintenance of gene duplicates. J. Hered. 100:605–17
    [Google Scholar]
  18. 18.  Marandel L, Seiliez I, Veron V, Skiba-Cassy S, Panserat S 2015. New insights into the nutritional regulation of gluconeogenesis in carnivorous rainbow trout (Oncorhynchus mykiss): a gene duplication trail. Physiol. Genom. 47:253–63
    [Google Scholar]
  19. 19.  Jin M, Monroig Ó, Navarro JC, Tocher DR, Zhou QC 2017. Molecular and functional characterisation of two elovl4 elongases involved in the biosynthesis of very long-chain (>C24) polyunsaturated fatty acids in black seabream Acanthopagrus schlegelii. Comp. Biochem. Physiol. B Biochem. Mol. Biol 212:41–50
    [Google Scholar]
  20. 20.  Castro LF, Monroig Ó, Leaver MJ, Wilson J, Cunha I, Tocher DR 2012. Functional desaturase Fads1 (Δ5) and Fads2 (Δ6) orthologues evolved before the origin of jawed vertebrates. PLOS ONE 7:e31950
    [Google Scholar]
  21. 21.  Bergot F 1979. Specific problems posed by carbohydrate utilization in the rainbow trout. Ann. Nutr. Aliment. 33:247–57
    [Google Scholar]
  22. 22.  Bergot F 1979. Effects of dietary carbohydrates and of their mode of distribution on glycemia in rainbow-trout (Salmo gairdneri Richardson). Comp. Biochem. Physiol. A 64:543–47
    [Google Scholar]
  23. 23.  Polakof S, Moon TW, Aguirre P, Skiba-Cassy S, Panserat S 2011. Glucose homeostasis in rainbow trout fed a high-carbohydrate diet: Metformin and insulin interact in a tissue-dependent manner. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300:R166–74
    [Google Scholar]
  24. 24.  Skiba-Cassy S, Panserat S, Larquier M, Dias K, Surget A et al. 2013. Apparent low ability of liver and muscle to adapt to variation of dietary carbohydrate:protein ratio in rainbow trout (Oncorhynchus mykiss). Br. J. Nutr. 109:1359–72
    [Google Scholar]
  25. 25.  Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M et al. 2014. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat. Commun. 5:3657
    [Google Scholar]
  26. 26.  Panserat S, Blin C, Médale F, Plagnes-Juan E, Brèque J et al. 2000. Molecular cloning, tissue distribution and sequence analysis of complete glucokinase cDNAs from gilthead seabream (Sparus aurata), rainbow trout (Oncorhynchus mykiss) and common carp (Cyprinus carpio). Biochim. Biophys. Acta 1474:61–69
    [Google Scholar]
  27. 27.  Marandel L, Panserat S, Plagnes-Juan E, Arbenoits E, Soengas JL, Bobe J 2017. Evolutionary history of glucose-6-phosphatase encoding genes in vertebrate lineages: towards a better understanding of the functions of multiple duplicates. BMC Genom 18:342
    [Google Scholar]
  28. 28.  Marandel L, Dai W, Panserat S, Skiba-Cassy S 2016. The five glucose-6-phosphatase paralogous genes are differentially regulated by insulin alone or combined with high level of amino acids and/or glucose in trout hepatocytes. Mol. Biol. Rep. 43:207–11
    [Google Scholar]
  29. 29.  Marandel L, Lepais O, Arbenoits E, Véron V, Dias K et al. 2016. Remodelling of the hepatic epigenetic landscape of glucose-intolerant rainbow trout (Oncorhynchus mykiss) by nutritional status and dietary carbohydrates. Sci. Rep. 6:32187
    [Google Scholar]
  30. 30.  Otero-Rodiño C, Rocha A, Álvarez-Otero R, Ceinos RM, López-Patiño MA et al. 2018. Glucosensing capacity of rainbow trout telencephalon. J. Neuroendocrinol. 30:3e12583
    [Google Scholar]
  31. 31.  Polakof S, Míguez JM, Soengas JL 2008. Dietary carbohydrates induce changes in glucosensing capacity and food intake of rainbow trout. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295:R478–89
    [Google Scholar]
  32. 32.  Tocher DR 2009. Issues surrounding fish as a source of omega-3 long-chain polyunsaturated fatty acids. Lipids Technol 21:13–16
    [Google Scholar]
  33. 33.  Castro LFC, Tocher DR, Monroig O 2016. Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Prog. Lipid Res. 62:25–40
    [Google Scholar]
  34. 34.  Fonseca-Madrigal J, Navarro JC, Hontoria F, Tocher DR, Martínez-Palacios CA, Monroig Ó 2014. Diversification of substrate specificities in Teleostei Fads2: characterization of Δ4 and Δ6Δ5 desaturases of Chirostoma estor. J. Lipid Res 55:1408–19
    [Google Scholar]
  35. 35.  Hastings N, Agaba M, Tocher DR, Leaver MJ, Dick JR et al. 2001. A vertebrate fatty acid desaturase with Δ5 and Δ6 activities. PNAS 98:14304–9
    [Google Scholar]
  36. 36.  Hastings N, Agaba MK, Tocher DR, Zheng X, Dickson CA et al. 2005. Molecular cloning and functional characterization of fatty acyl desaturase and elongase cDNAs involved in the production of eicosapentaenoic and docosahexaenoic acids from α-linolenic acid in Atlantic salmon (Salmo salar). Mar. Biotechnol. 6:463–74
    [Google Scholar]
  37. 37.  Zheng X, Tocher DR, Dickson CA, Bell JG, Teale AJ 2005. Highly unsaturated fatty acid synthesis in vertebrates: new insights with the cloning and characterization of a Δ6 desaturase of Atlantic salmon. Lipids 40:13–24
    [Google Scholar]
  38. 38.  Monroig Ó, Zheng X, Morais S, Leaver MJ, Taggart JB, Tocher DR 2010. Multiple genes for functional Δ6 fatty acyl desaturases (Fad) in Atlantic salmon (Salmo salar L.): gene and cDNA characterization, functional expression, tissue distribution and nutritional regulation. Biochim. Biophys. Acta 1801:1072–81
    [Google Scholar]
  39. 39.  Morais S, Mourente G, Martínez A, Gras N, Tocher DR 2015. Docosahexaenoic acid biosynthesis via fatty acyl elongase and Δ4-desaturase and its modulation by dietary lipid level and fatty acid composition in a marine vertebrate. Biochim. Biophys. Acta 1851:588–97
    [Google Scholar]
  40. 40.  Carmona-Antoñanzas G, Tocher DR, Taggart JB, Leaver MJ 2013. An evolutionary perspective on Elovl5 fatty acid elongase: comparison of Northern pike and duplicated paralogs from Atlantic salmon. BMC Evol. Biol. 13:85
    [Google Scholar]
  41. 41.  Morais S, Monroig O, Zheng XZ, Leaver MJ, Tocher DR 2009. Highly unsaturated fatty acid synthesis in Atlantic salmon: characterization of ELOVL5-and ELOVL2-like elongases. Mar. Biotechnol. 11:627–39
    [Google Scholar]
  42. 42.  Monroig Ó, Rotllant J, Cerdá-Reverter JM, Dick JR, Figueras A, Tocher DR 2010. Expression and role of Elovl4 elongases in biosynthesis of very long-chain fatty acids during zebrafish Danio rerio early embryonic development. Biochim. Biophys. Acta 1801:1145–54
    [Google Scholar]
  43. 43.  Xue X, Feng CY, Hixson SM, Johnstone K, Anderson DM et al. 2014. Characterization of the fatty acyl elongase (elovl) gene family, and hepatic elovl and delta-6 fatty acyl desaturase transcript expression and fatty acid responses to diets containing camelina oil in Atlantic cod (Gadus morhua). Comp. Biochem. Physiol. B 175:9–22
    [Google Scholar]
  44. 44.  Caruso MA, Kittilson JD, Raine J, Sheridan MA 2008. Rainbow trout (Oncorhynchus mykiss) possess two insulin-encoding mRNAs that are differentially expressed. Gen. Comp. Endocrinol. 155:695–704
    [Google Scholar]
  45. 45.  Caruso MA, Sheridan MA 2012. The expression of insulin and insulin receptor mRNAs is regulated by nutritional state and glucose in rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 175:321–28
    [Google Scholar]
  46. 46.  Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T 2001. Identification of novel genes coding for small expressed RNAs. Science 294:853–58
    [Google Scholar]
  47. 47.  Desvignes T, Batzel P, Berezikov E, Eilbeck K, Eppig JT et al. 2015. miRNA nomenclature: a view incorporating genetic origins, biosynthetic pathways, and sequence variants. Trends Genet 31:613–26
    [Google Scholar]
  48. 48.  Esau C, Davis S, Murray SF, Yu XX, Pandey SK et al. 2006. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 3:87–98
    [Google Scholar]
  49. 49.  Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T et al. 2005. Silencing of microRNAs in vivo with “antagomirs. .” Nature 438:685–89
    [Google Scholar]
  50. 50.  Juanchich A, Bardou P, Rue O, Gabillard JC, Gaspin C et al. 2016. Characterization of an extensive rainbow trout miRNA transcriptome by next generation sequencing. BMC Genom 17:164
    [Google Scholar]
  51. 51.  Salem M, Xiao C, Womack J, Rexroad CE 3rd, Yao J 2009. A microRNA repertoire for functional genome research in rainbow trout (Oncorhynchus mykiss). Mar. Biotechnol. 12:4410–29
    [Google Scholar]
  52. 52.  Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE et al. 2010. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328:1566–69
    [Google Scholar]
  53. 53.  Mennigen JA, Panserat S, Larquier M, Plagnes-Juan E, Medale F et al. 2012. Postprandial regulation of hepatic microRNAs predicted to target the insulin pathway in rainbow trout. PLOS ONE 7:e38604
    [Google Scholar]
  54. 54.  Mennigen JA, Martyniuk CJ, Seiliez I, Panserat S, Skiba-Cassy S 2014. Metabolic consequences of microRNA-122 inhibition in rainbow trout. Oncorhynchus mykiss. BMC Genom. 15:70
    [Google Scholar]
  55. 55.  Zhu T, Corraze G, Plagnes-Juan E, Quillet E, Dupont-Nivet M, Skiba-Cassy S 2018. Regulation of genes related to cholesterol metabolism in rainbow trout (Oncorhynchus mykiss) fed a plant-based diet. Am. J. Physiol. Regul. Integr. Comp. Physiol. 314:R58–R70
    [Google Scholar]
  56. 56.  Vickers KC, Landstreet SR, Levin MG, Shoucri BM, Toth CL et al. 2014. MicroRNA-223 coordinates cholesterol homeostasis. PNAS 111:14518–23
    [Google Scholar]
  57. 57.  Tao YF, Qiang J, Yin GJ, Xu P, Shi Q, Bao JW 2017. Identification and characterization of lipid metabolism-related microRNAs in the liver of genetically improved farmed tilapia (GIFT, Oreochromis niloticus) by deep sequencing. Fish Shellfish Immunol 69:227–35
    [Google Scholar]
  58. 58.  Tao YF, Qiang J, Bao JW, Li HX, Yin GJ et al. 2018. miR-205-5p negatively regulates hepatic acetyl-CoA carboxylase β mRNA in lipid metabolism of Oreochromis niloticus. . Gene 660:1–7
    [Google Scholar]
  59. 59.  Qiang J, Tao YF, He J, Sun YL, Xu P 2017. miR-29a modulates SCD expression and is regulated in response to a saturated fatty acid diet in juvenile genetically improved farmed tilapia (Oreochromis niloticus). J. Exp. Biol. 220:1481–89
    [Google Scholar]
  60. 60.  Miao LH, Lin Y, Pan WJ, Huang X, Ge XP et al. 2017. Identification of differentially expressed microRNAs associate with glucose metabolism in different organs of blunt snout bream (Megalobrama amblycephala). Int. J. Mol. Sci. 18:E1161
    [Google Scholar]
  61. 61.  Prabhu PAJ, Geurden I, Fontagné-Dicharry S, Veron V, Larroquet L et al. 2016. Responses in micro-mineral metabolism in rainbow trout to change in dietary ingredient composition and inclusion of a micro-mineral premix. PLOS ONE 11:e0149378
    [Google Scholar]
  62. 62.  Tang XL, Xu MJ, Li ZH, Pan Q, Fu JH 2013. Effects of vitamin E on expressions of eight microRNAs in the liver of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 34:1470–75
    [Google Scholar]
  63. 63.  Bizuayehu TT, Johansen SD, Puvanendran V, Toften H, Babiak I 2015. Temperature during early development has long-term effects on microRNA expression in Atlantic cod. BMC Genom 16:305
    [Google Scholar]
  64. 64.  Koturbash I, Melnyk S, James SJ, Beland FA, Pogribny IP 2013. Role of epigenetic and miR-22 and miR-29b alterations in the downregulation of Mat1a and Mthfr genes in early preneoplastic livers in rats induced by 2-acetylaminofluorene. Mol. Carcinog. 52:318–27
    [Google Scholar]
  65. 65.  Bao JW, Qiang J, Tao YF, Li HX, He J et al. 2018. Responses of blood biochemistry, fatty acid composition and expression of microRNAs to heat stress in genetically improved farmed tilapia (Oreochromis niloticus). J. Therm. Biol. 73:91–97
    [Google Scholar]
  66. 66.  Klionsky DJ 2005. The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118:7–18
    [Google Scholar]
  67. 67.  Komatsu M, Waguri S, Ueno T, Iwata J, Murata S et al. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169:425–34
    [Google Scholar]
  68. 68.  Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM et al. 2017. Molecular definitions of autophagy and related processes. EMBO J 36:1811–36
    [Google Scholar]
  69. 69.  Molino D, Nascimbeni AC, Giordano F, Codogno P, Morel E 2017. ER-driven membrane contact sites: Evolutionary conserved machineries for stress response and autophagy regulation?. Commun. Integr. Biol. 10:e1401699
    [Google Scholar]
  70. 70.  Stolz A, Ernst A, Dikic I 2014. Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 16:495–501
    [Google Scholar]
  71. 71.  Anding AL, Baehrecke EH 2017. Cleaning house: selective autophagy of organelles. Dev. Cell 41:10–22
    [Google Scholar]
  72. 72.  Delbridge LM, Mellor KM, Taylor DJ, Gottlieb RA 2015. Myocardial autophagic energy stress responses—macroautophagy, mitophagy, and glycophagy. Am. J. Physiol. Heart. Circ. Physiol. 308:H1194–204
    [Google Scholar]
  73. 73.  Liu K, Czaja MJ 2013. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ 20:3–11
    [Google Scholar]
  74. 74.  Nakatogawa H, Mochida K 2015. Reticulophagy and nucleophagy: new findings and unsolved issues. Autophagy 11:2377–78
    [Google Scholar]
  75. 75.  Mizushima N, Yoshimori T, Ohsumi Y 2011. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27:107–32
    [Google Scholar]
  76. 76.  Shen HM, Mizushima N 2014. At the end of the autophagic road: an emerging understanding of lysosomal functions in autophagy. Trends Biochem. Sci. 39:61–71
    [Google Scholar]
  77. 77.  Kaushik S, Cuervo AM 2012. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 22:407–17
    [Google Scholar]
  78. 78.  Chiang HL, Terlecky SR, Plant CP, Dice JF 1989. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246:382–85
    [Google Scholar]
  79. 79.  Cuervo AM, Dice JF 1996. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273:501–3
    [Google Scholar]
  80. 80.  Bandyopadhyay U, Kaushik S, Varticovski L, Cuervo AM 2008. The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol. Cell. Biol. 28:5747–63
    [Google Scholar]
  81. 81.  Bandyopadhyay U, Sridhar S, Kaushik S, Kiffin R, Cuervo AM 2010. Identification of regulators of chaperone-mediated autophagy. Mol. Cell 39:535–47
    [Google Scholar]
  82. 82.  Cuervo AM, Dice JF 2000. Unique properties of lamp2a compared to other lamp2 isoforms. J. Cell Sci. 113:244441–50
    [Google Scholar]
  83. 83.  Kiffin R, Christian C, Knecht E, Cuervo AM 2004. Activation of chaperone-mediated autophagy during oxidative stress. Mol. Biol. Cell 15:4829–40
    [Google Scholar]
  84. 84.  Ferreira JV, Fôfo H, Bejarano E, Bento CF, Ramalho JS et al. 2013. STUB1/CHIP is required for HIF1A degradation by chaperone-mediated autophagy. Autophagy 9:1349–66
    [Google Scholar]
  85. 85.  Hubbi ME, Hu H, Kshitiz, Ahmed I, Levchenko A, Semenza GL 2013. Chaperone-mediated autophagy targets hypoxia-inducible factor-1α (HIF-1α) for lysosomal degradation. J. Biol. Chem. 288:10703–14
    [Google Scholar]
  86. 86.  Cuervo AM, Knecht E, Terlecky SR, Dice JF 1995. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am. J. Physiol. 269:C1200–8
    [Google Scholar]
  87. 87.  Rodriguez-Navarro JA, Kaushik S, Koga H, Dall'Armi C, Shui G et al. 2012. Inhibitory effect of dietary lipids on chaperone-mediated autophagy. PNAS 109:E705–14
    [Google Scholar]
  88. 88.  Farre JC, Subramani S 2004. Peroxisome turnover by micropexophagy: an autophagy-related process. Trends Cell Biol 14:515–23
    [Google Scholar]
  89. 89.  Li WW, Li J, Bao JK 2012. Microautophagy: lesser-known self-eating. Cell. Mol. Life Sci. 69:1125–36
    [Google Scholar]
  90. 90.  Sahu R, Kaushik S, Clement CC, Cannizzo ES, Scharf B et al. 2011. Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 20:131–39
    [Google Scholar]
  91. 91.  Mukherjee A, Patel B, Koga H, Cuervo AM, Jenny A 2016. Selective endosomal microautophagy is starvation-inducible in Drosophila. . Autophagy 12:1984–99
    [Google Scholar]
  92. 92.  Madrigal-Matute J, Cuervo AM 2016. Regulation of liver metabolism by autophagy. Gastroenterology 150:328–39
    [Google Scholar]
  93. 93.  Eng CH, Yu K, Lucas J, White E, Abraham RT 2010. Ammonia derived from glutaminolysis is a diffusible regulator of autophagy. Sci. Signal. 3:ra31
    [Google Scholar]
  94. 94.  Lum JJ, Bauer DE, Kong M, Harris MH, Li C et al. 2005. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237–48
    [Google Scholar]
  95. 95.  Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H et al. 2007. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ. Res. 100:914–22
    [Google Scholar]
  96. 96.  Ezaki J, Matsumoto N, Takeda-Ezaki M, Komatsu M, Takahashi K et al. 2011. Liver autophagy contributes to the maintenance of blood glucose and amino acid levels. Autophagy 7:727–36
    [Google Scholar]
  97. 97.  Efeyan A, Zoncu R, Chang S, Gumper I, Snitkin H et al. 2013. Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature 493:679–83
    [Google Scholar]
  98. 98.  Singh R, Kaushik S, Wang Y, Xiang Y, Novak I et al. 2009. Autophagy regulates lipid metabolism. Nature 458:1131–35
    [Google Scholar]
  99. 99.  Ding WX, Li M, Chen X, Ni HM, Lin CW et al. 2010. Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice. Gastroenterology 139:1740–52
    [Google Scholar]
  100. 100.  Mei S, Ni HM, Manley S, Bockus A, Kassel KM et al. 2011. Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. J. Pharmacol. Exp. Ther. 339:487–98
    [Google Scholar]
  101. 101.  Jiang S, Heller B, Tagliabracci VS, Zhai L, Irimia JM et al. 2010. Starch binding domain-containing protein 1/genethonin 1 is a novel participant in glycogen metabolism. J. Biol. Chem. 285:34960–71
    [Google Scholar]
  102. 102.  Kotoulas OB, Kalamidas SA, Kondomerkos DJ 2006. Glycogen autophagy in glucose homeostasis. Pathol. Res. Pract. 202:631–38
    [Google Scholar]
  103. 103.  Schneider JL, Suh Y, Cuervo AM 2014. Deficient chaperone-mediated autophagy in liver leads to metabolic dysregulation. Cell Metab 20:417–32
    [Google Scholar]
  104. 104.  Kaushik S, Cuervo AM 2015. Degradation of lipid droplet-associated proteins by chaperone-mediated autophagy facilitates lipolysis. Nat. Cell Biol. 17:759–70
    [Google Scholar]
  105. 105.  Lemasters JJ 2005. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res 8:3–5
    [Google Scholar]
  106. 106.  Glick D, Zhang W, Beaton M, Marsboom G, Gruber M et al. 2012. BNip3 regulates mitochondrial function and lipid metabolism in the liver. Mol. Cell. Biol. 32:2570–84
    [Google Scholar]
  107. 107.  Narendra D, Tanaka A, Suen DF, Youle RJ 2008. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183:795–803
    [Google Scholar]
  108. 108.  Schweers RL, Zhang J, Randall MS, Loyd MR, Li W et al. 2007. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. PNAS 104:19500–5
    [Google Scholar]
  109. 109.  Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA et al. 2011. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331:456–61
    [Google Scholar]
  110. 110.  Shelburne JD, Arstila AU, Trump BF 1973. Studies on cellular autophagocytosis: the relationship of autophagocytosis to protein synthesis and to energy metabolism in rat liver and flounder kidney tubules in vitro. Am. J. Pathol. 73:641–70
    [Google Scholar]
  111. 111.  Bai R, You W, Chen J, Huang H, Ke C 2012. Molecular cloning and expression analysis of GABAA receptor-associated protein (GABARAP) from small abalone. Haliotis diversicolor. Fish Shellfish Immunol. 33:675–82
    [Google Scholar]
  112. 112.  Benato F, Skobo T, Gioacchini G, Moro I, Ciccosanti F et al. 2013. Ambra1 knockdown in zebrafish leads to incomplete development due to severe defects in organogenesis. Autophagy 9:476–95
    [Google Scholar]
  113. 113.  Bolliet V, Labonne J, Olazcuaga L, Panserat S, Seiliez I 2017. Modeling of autophagy-related gene expression dynamics during long term fasting in European eel (Anguillaanguilla). Sci. Rep. 7:17896
    [Google Scholar]
  114. 114.  He C, Bartholomew CR, Zhou W, Klionsky DJ 2009. Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy 5:520–26
    [Google Scholar]
  115. 115.  Hu Z, Zhang J, Zhang Q 2011. Expression pattern and functions of autophagy-related gene atg5 in zebrafish organogenesis. Autophagy 7:1514–27
    [Google Scholar]
  116. 116.  Kong HJ, Moon JY, Nam BH, Kim YO, Kim WJ et al. 2011. Molecular characterization of the autophagy-related gene Beclin-1 from the olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol 31:189–95
    [Google Scholar]
  117. 117.  Mathai BJ, Meijer AH, Simonsen A 2017. Studying autophagy in zebrafish. Cells 6:21
    [Google Scholar]
  118. 118.  Seiliez I, Gutierrez J, Salmerón C, Skiba-Cassy S, Chauvin C et al. 2010. An in vivo and in vitro assessment of autophagy-related gene expression in muscle of rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. B 157:258–66
    [Google Scholar]
  119. 119.  Wei CC, Luo Z, Song YF, Pan YX, Wu K, You WJ 2017. Identification of autophagy related genes LC3 and ATG4 from yellow catfish Pelteobagrus fulvidraco and their transcriptional responses to waterborne and dietborne zinc exposure. Chemosphere 175:228–38
    [Google Scholar]
  120. 120.  Seiliez I, Gabillard J-C, Skiba-Cassy S, Garcia-Serrana D, Gutiérrez J et al. 2008. An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am. J. Physiol. Regul. Integr. Comp. Physiol. 295:R329–35
    [Google Scholar]
  121. 121.  Seiliez I, Panserat S, Skiba-Cassy S, Polakof S 2011. Effect of acute and chronic insulin administrations on major factors involved in the control of muscle protein turnover in rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 172:363–70
    [Google Scholar]
  122. 122.  Seiliez I, Gabillard J-C, Riflade M, Sadoul B, Dias K et al. 2012. Amino acids downregulate the expression of several autophagy-related genes in rainbow trout myoblasts. Autophagy 8:364–75
    [Google Scholar]
  123. 123.  Hosseini R, Lamers GE, Hodzic Z, Meijer AH, Schaaf MJ, Spaink HP 2014. Correlative light and electron microscopy imaging of autophagy in a zebrafish infection model. Autophagy 10:1844–57
    [Google Scholar]
  124. 124.  Mostowy S, Boucontet L, Mazon Moya MJ, Sirianni A, Boudinot P et al. 2013. The zebrafish as a new model for the in vivo study of Shigella flexneri interaction with phagocytes and bacterial autophagy. PLOS Pathog 9:e1003588
    [Google Scholar]
  125. 125.  van der Vaart M, Korbee CJ, Lamers GE, Tengeler AC, Hosseini R et al. 2014. The DNA damage-regulated autophagy modulator DRAM1 links mycobacterial recognition via TLR-MYD88 to autophagic defense [corrected]. Cell Host Microbe 15:753–67
    [Google Scholar]
  126. 126.  Lee E, Koo Y, Ng A, Wei Y, Luby-Phelps K et al. 2014. Autophagy is essential for cardiac morphogenesis during vertebrate development. Autophagy 10:572–87
    [Google Scholar]
  127. 127.  Sasaki T, Lian S, Qi J, Bayliss PE, Carr CE et al. 2014. Aberrant autolysosomal regulation is linked to the induction of embryonic senescence: differential roles of Beclin 1 and p53 in vertebrate Spns1 deficiency. PLOS Genet 10:e1004409
    [Google Scholar]
  128. 128.  Lee E, Wei Y, Zou Z, Tucker K, Rakheja D et al. 2016. Genetic inhibition of autophagy promotes p53 loss-of-heterozygosity and tumorigenesis. Oncotarget 7:67919–33
    [Google Scholar]
  129. 129.  Saera-Vila A, Kish PE, Louie KW, Grzegorski SJ, Klionsky DJ, Kahana A 2016. Autophagy regulates cytoplasmic remodeling during cell reprogramming in a zebrafish model of muscle regeneration. Autophagy 12:1864–75
    [Google Scholar]
  130. 130.  Varga M, Sass M, Papp D, Takacs-Vellai K, Kobolak J et al. 2014. Autophagy is required for zebrafish caudal fin regeneration. Cell Death Differ 21:547–56
    [Google Scholar]
  131. 131.  Seiliez I, Belghit I, Gao Y, Skiba-Cassy S, Dias K et al. 2016. Looking at the metabolic consequences of the colchicine-based in vivo autophagic flux assay. Autophagy 12:343–56
    [Google Scholar]
  132. 132.  Tekirdag K, Cuervo AM 2018. Chaperone-mediated autophagy and endosomal microautophagy: jointed by a chaperone. J. Biol. Chem. 293:5414–24
    [Google Scholar]
  133. 133.  Lescat L, Herpin A, Mourot B, Véron V, Guiguen Y et al. 2018. CMA restricted to mammals and birds: Myth or reality?. Autophagy 14:1267–70
    [Google Scholar]
  134. 134.  Lucas A 1998. Programming by early nutrition: an experimental approach. J. Nutr. 128:2 Suppl.401S–6S
    [Google Scholar]
  135. 135.  Waterland RA, Jirtle RL 2003. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 23:155293–300
    [Google Scholar]
  136. 136.  Lillycrop KA, Burdge GC 2012. Epigenetic mechanisms linking early nutrition to long term health. Best Pract. Res. Clin. Endocrinol. Metab. 26:5667–76
    [Google Scholar]
  137. 137.  Marandel L, Veron V, Surget A, Plagnes-Juan E, Panserat S 2016. Glucose metabolism ontogenesis in rainbow trout (Oncorhynchusmykiss) in the light of the recently sequenced genome: new tools for intermediary metabolism programming in the light of the recently sequenced genome. J Exp. Biol. 219:734–43
    [Google Scholar]
  138. 138.  Mennigen J, Skiba-Cassy S, Panserat S 2013. Ontogenetic expression of metabolic genes and microRNAs in rainbow trout alevins during the transition from the endogenous to exogenous feeding period. J. Exp. Biol. 216:1597–608
    [Google Scholar]
  139. 139.  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:R2275–83
    [Google Scholar]
  140. 140.  Geurden I, Mennigen J, Plagnes-Juan E, Veron V, Cerezo T et al. 2014. High or low dietary carbohydrate: protein ratios during first-feeding affect glucose metabolism and intestinal microbiota in juvenile rainbow trout. J. Exp. Biol. 217:3396–406
    [Google Scholar]
  141. 141.  Rocha F, Dias J, Geurden I, Dinis MT, Panserat S, Engrola S 2016. 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 201:189–99
    [Google Scholar]
  142. 142.  Rocha F, Dias J, Geurden I, Dinis MT, Panserat S, Engrola S 2016. High glucose feeding of gilthead seabream (Sparus aurata) larvae: effects on molecular and metabolic pathways. Aquaculture 451:241–53
    [Google Scholar]
  143. 143.  Gong G, Xue M, Wang J, Wu X-f, Z Y-h et al. 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 436:127–36
    [Google Scholar]
  144. 144.  Liang X, Wang J, Gong G, Xue M, Dong Y et al. 2017. Gluconeogenesis during starvation and refeeding phase is affected by previous dietary carbohydrates levels and a glucose stimuli during early life in Siberian sturgeon (Acipenser baerii). Anim. Nutr. 3:284–94
    [Google Scholar]
  145. 145.  Castro LFC, Tocher DR, Monroig O 2016. Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Prog. Lipid Res. 62:25–40
    [Google Scholar]
  146. 146.  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. 101:101452–62
    [Google Scholar]
  147. 147.  Vagner M, Zambonino Infante U, Robin JH, Person-Le Ruyet JP 2007. Is it possible to influence European sea bass (Dicentrarchus labrax) juvenile metabolism by a nutritional conditioning during larval stage?. Aquaculture 267:165–74
    [Google Scholar]
  148. 148.  Geurden I, Borchert P, Balasubramanian M, Schrama JW, Dupont-Nivet M et al. 2013. The positive impact of the early-feeding of a plant-based diet on its future acceptance and utilisation in rainbow trout. PLOS ONE 8:12e83162
    [Google Scholar]
  149. 149.  Balasubramanian MN, Panserat S, Dupont-Nivet M, Quillet E, Montfort J et al. 2016. Molecular pathways associated with the nutritional programming of plant-based diet acceptance in rainbow trout following an early feeding exposure. BMC Genom 17:449
    [Google Scholar]
  150. 150.  Michl S, Weis B, Hutchings JA, Schulz C 2017. Plastic responses by wild brow trout (Salmo trutta) to plant-based diets. Aquaculture 476:19–28
    [Google Scholar]
  151. 151.  Clarkson M, Migaud H, Metochis C, Vera LM, Leeming D et al. 2017. Early nutritional intervention can improve utilisation of vegetable-based diets in diploid and triploid Atlantic salmon (Salmo salar L.). Br. J. Nutr. 118:117–29
    [Google Scholar]
  152. 152.  Vera LM, Metochis C, Taylor JF, Clarkson M, Skjærven KH et al. 2017. Early nutritional programming affects liver transcriptome in diploid and triploid Atlantic salmon. Salmo salar. BMC Genom 18:1886
    [Google Scholar]
  153. 153.  Turkmen S, Castro PL, Caballero MJ, Hernández-Cruz CM, Saleh R et al. 2017. Nutritional stimuli of gilthead seabream (Sparus aurata) larvae by dietary fatty acids: effects on larval performance, gene expression and neurogenesis. Aquacult. Res. 48:202–13
    [Google Scholar]
  154. 154.  Rocha F, Dias J, 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: effect of an early glucose stimulus. Br. J. Nutr. 113:403–13
    [Google Scholar]
  155. 155.  Jiang L, Zhang J, Wang JJ, Wang L, Zhang L et al. 2013. Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 153:773–84
    [Google Scholar]
  156. 156.  Seiliez I, Vélez E, Lutfi E, Dias K, Plagnes-Juan E et al. 2017. Eating for two: consequences of parental methionine nutrition on offspring metabolism in rainbow trout (Oncorhynchus mykiss). Aquaculture 471:80–91
    [Google Scholar]
  157. 157.  Izquierdo MS, Turkmen S, Montero D, Zamorano MJ, Afonso JM et al. 2015. Nutritional programming through broodstock diets to improve utilization of very low fishmeal and fish oil diets in gilthead sea bream. Aquaculture 449:1826
    [Google Scholar]
  158. 158.  Turkmen S, Zamorano MJ, Fernández-Palacios H, Hernández-Cruz CM, Montero D et al. 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. 8:7500–12
    [Google Scholar]
  159. 159.  Lazzarotto V, Corraze G, Leprevost A, Quillet E, Dupont-Nivet M, Médale F 2015. Three-year breeding cycle of rainbow trout (Oncorhynchus mykiss) fed a plant-based diet, totally free of marine resources: consequences for reproduction, fatty acid composition and progeny survival. PLOS ONE 10:2e0117609
    [Google Scholar]
  160. 160.  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. 115:122079–92
    [Google Scholar]
  161. 161.  Panserat S, Marandel I, Geurden I, Veron V, Dias K et al. 2017. Muscle catabolic capacities and global hepatic epigenome are modified in juvenile rainbow trout fed different vitamin levels at first feeding. Aquaculture 468:515–23
    [Google Scholar]
  162. 162.  Skjærven KH, Jakt LM, Dahl JA, Espe M, Aanes H et al. 2016. Parental vitamin deficiency affects the embryonic gene expression of immune-, lipid transport- and apolipoprotein genes. Sci. Rep. 6:34535
    [Google Scholar]
  163. 163.  Skjærven KH, Jakt LM, Fernandes JMO, Dahl JA, Adam AC et al. 2018. Parental micronutrient deficiency distorts liver DNA methylation and expression of lipid genes associated with a fatty-liver-like phenotype in offspring. Sci. Rep. 8:13055
    [Google Scholar]
  164. 164.  Liu J, Dias K, Plagnes-Juan E, Veron V, Panserat S, Marandel L 2017. Long-term programming effect of early hypoxia and high carbohydrate diet at first feeding on glucose metabolism in rainbow trout juveniles. J. Exp. Biol. 220:3686–94
    [Google Scholar]
  165. 165.  Liu J, Plagnes-Juan E, Geurden I, Panserat S, Marandel L 2017. Exposure to an acute hypoxic stimulus during early life affects the expression of glucose metabolism-related genes at first-feeding in trout. Sci. Rep. 7:363
    [Google Scholar]
  166. 166.  Pasquier J, Cabau C, Nguyen T, Jouanno E, Severac D et al. 2016. Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database. BMC Genom 17:368
    [Google Scholar]
/content/journals/10.1146/annurev-animal-020518-115250
Loading
/content/journals/10.1146/annurev-animal-020518-115250
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error