Transcriptome and functional responses to absence of astaxanthin in Atlantic salmon fed low marine diets

Aas, 1997, Idoxanthin, a major carotenoid in the muscle of Arctic charr (Salvelinus alpinus) fed diets containing astaxanthin, Aquaculture, 150, 135, 10.1016/S0044-8486(96)01458-5 Aas, 2019, Utilization of feed resources in the production of Atlantic salmon (Salmo salar) in Norway: an update for 2016, Aquacult. Rep., 15, 100216 Ahmadi, 2006, Effects of dietary astaxanthin supplementation on reproductive characteristics of rainbow trout (Oncorhynchus mykiss), J. Appl. Ichthyol., 22, 388, 10.1111/j.1439-0426.2006.00770.x Alvarez, 2014, Antimicrobial activity of trout hepcidin, Fish Shellfish Immunol., 41, 93, 10.1016/j.fsi.2014.04.013 Amar, 2001, Influence of various dietary synthetic carotenoids on bio-defence mechanisms in rainbow trout, Oncorhynchus mykiss (Walbaum), Aquac. Res., 32, 162, 10.1046/j.1355-557x.2001.00051.x Amar, 2004, Enhancement of innate immunity in rainbow trout (Oncorhynchus mykiss Walbaum) associated with dietary intake of carotenoids from natural products, Fish Shellfish Immunol., 16, 527, 10.1016/j.fsi.2003.09.004 Amengual, 2011, A mitochondrial enzyme degrades carotenoids and protects against oxidative stress, FASEB J., 25, 948, 10.1096/fj.10-173906 Ando, 1987, Metabolic pathways of carotenoids in chum salmon Oncorhynchus keta during spawning migration, Comp. Biochem. Physiol., 87B, 411 Aoi, 2008, Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification, Biochem. Biophys. Res. Commun., 366, 892, 10.1016/j.bbrc.2007.12.019 Bazyar Lakeh, 2010, Growth performance, mortality and carotenoid pigmentation of fry offspring as affected by dietary supplementation of astaxanthin to female rainbow trout (Oncorhynchus mykiss) broodstock, J. Appl. Ichthyol., 26, 29, 10.1111/j.1439-0426.2009.01349.x Bell, 2000, Depletion of α-tocopherol and astaxanthin in Atlantic Salmon (Salmo salar) affects autoxidative defense and fatty acid metabolism, J. Nutr., 130, 1800, 10.1093/jn/130.7.1800 Bhuvaneswari, 2010, Astaxanthin restricts weight gain, promotes insulin sensitivity and curtails fatty liver disease in mice fed a obesity-promoting diet, Process Biochem., 45, 1406, 10.1016/j.procbio.2010.05.016 Bjerkeng, 1992, Pigmentation of rainbow trout from start feeding to sexual maturation, Aquaculture, 108, 333, 10.1016/0044-8486(92)90117-4 Bjerkeng, 1997, Bioavailability of all-E-astaxanthin and Z-isomers in rainbow trout (Oncorhynchus mykiss), Aquaculture, 157, 63, 10.1016/S0044-8486(97)00146-4 Bjerkeng, 1997, Quality parameters of the flesh of Atlantic salmon (Salmo salar) as affected by dietary fat content and full-fat soybean meal as a partial substitute for fish meal in the diet, Aquaculture, 157, 297, 10.1016/S0044-8486(97)00162-2 Bjerkeng, 1999, Influence of 11-ketotestosterone, 17β-estradiol, and 3,5,3′-triiodo-L-thyronine on distribution and metabolism of carotenoids in Arctic charr, Salvelinus alpinus L.*, Fish Physiol. Biochem., 21, 353, 10.1023/A:1007802803008 Bonet, 2012, Lipid metabolism in mammalian tissues and its control by retinoic acid, Biochim. Biophys. Acta, Mol. Cell Biol. Lipids, 1821, 177, 10.1016/j.bbalip.2011.06.001 Bou, 2017, Requirements of n-3 very long-chain PUFA in Atlantic salmon (Salmo salar L): effects of different dietary levels of EPA and DHA on fish performance and tissue composition and integrity, Br. J. Nutr., 117, 30, 10.1017/S0007114516004396 Britton, 1995, UV/VIS spectroscopy, 13 Caballero-Solares, 2018, Changes in the liver transcriptome of farmed Atlantic salmon (Salmo salar) fed experimental diets based on terrestrial alternatives to fish meal and fish oil, BMC Genomics, 19, 796, 10.1186/s12864-018-5188-6 Chew, 2004, Carotenoid action on the immune response, J. Nutr., 134, 257, 10.1093/jn/134.1.257S Christiansen, 1996, Growth and survival of Atlantic salmon, Salmo salar L. fed different dietary levels of astaxanthin. Juveniles, Aquac. Nutr., 2, 55, 10.1111/j.1365-2095.1996.tb00008.x Christiansen, 1995, Growth and survival of Atlantic salmon, Salmo salar L., fed different dietary levels of astaxanthin. First-feeding fry, Aquac. Nutr., 1, 189, 10.1111/j.1365-2095.1995.tb00043.x Christiansen, 1995, Antioxidant status and immunity in Atlantic salmon, Salmo salar L., fed semi-purified diets with and without astaxanthin supplementation, J. Fish Dis., 18, 317, 10.1111/j.1365-2761.1995.tb00308.x Clarke, 2017, Impaired N-linked glycosylation of uptake and efflux transporters in human non-alcoholic fatty liver disease, Liver Int., 37, 1074, 10.1111/liv.13362 Datta, 2017, Survival of mature T cells in the periphery is intrinsically dependent on GIMAP1 in mice, Eur. J. Immunol., 47, 84, 10.1002/eji.201646599 Elvira-Torales, 2019, Nutritional importance of carotenoids and their effect on liver health: a review, Antioxidants, 8, 229, 10.3390/antiox8070229 Fakhri, 2018, Astaxanthin: a mechanistic review on its biological activities and health benefits, Pharmacol. Res., 136, 1, 10.1016/j.phrs.2018.08.012 Folch, 1957, A simple method for the isolation and purification of total lipids from animal tissues, J. Biol. Chem., 226, 497, 10.1016/S0021-9258(18)64849-5 Gammone, 2015, Carotenoids: potential allies of cardiovascular health?, Food Nutr. Res., 59, 26762, 10.3402/fnr.v59.26762 Geurts, 2015, Adipose tissue NAPE-PLD controls fat mass development by altering the browning process and gut microbiota, Nat. Commun., 6, 6495, 10.1038/ncomms7495 Gradelet, 1996, Effects of canthaxanthin, astaxanthin, lycopene and lutein on liver xenobiotic-metabolizing enzymes in the rat, Xenobiotica, 26, 49, 10.3109/00498259609046688 Grundy, 2004, Obesity, metabolic syndrome, and cardiovascular disease, J. Clin. Endocrinol. Metab., 89, 2595, 10.1210/jc.2004-0372 Guillou, 1989, Bioconversion pathway of astaxanthin into retinol-2 in mature rainbow-trout (Salmo-gairdneri Rich), Comp. Biochem. Physiol. B Biochem. Mol. Biol., 94, 481, 10.1016/0305-0491(89)90185-5 Hamre, 2010, Effects of dietary lipid, vitamins and minerals on total amounts and redox status of glutathione and ubiquinone in tissues of Atlantic salmon (Salmo salar): a multivariate approach, Br. J. Nutr., 104, 980, 10.1017/S0007114510001583 Helgeland, 2014, The evolution and functional divergence of the beta-carotene oxygenase gene family in teleost fish-exemplified by Atlantic salmon, Gene, 543, 268, 10.1016/j.gene.2014.02.042 Helgeland, 2019, Genomic and functional gene studies suggest a key role of beta-carotene oxygenase 1 like (bco1l) gene in salmon flesh color, Sci. Rep., 9, 20061, 10.1038/s41598-019-56438-3 Helland, 1996, A simple method for the measurement of daily feed intake of groups of fish in tanks, Aquaculture, 139, 157, 10.1016/0044-8486(95)01145-5 Hoover, 1998, Plasma proteins of rainbow trout (Oncorhynchus mykiss) isolated by binding to lipopolysaccharide from Aeromonas salmonicida, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 120, 559, 10.1016/S0305-0491(98)10042-1 Hussein, 2006, Astaxanthin, a carotenoid with potential in human health and nutrition, J. Nat. Prod., 69, 443, 10.1021/np050354+ Ikeuchi, 2006, Effects of astaxanthin supplementation on exercise-induced fatigue in mice, Biol. Pharm. Bull., 29, 2106, 10.1248/bpb.29.2106 Ikeuchi, 2007, Effects of Astaxanthin in obese mice fed a high-fat diet, Biosci. Biotechnol. Biochem., 71, 893, 10.1271/bbb.60521 Immenschuh, 2010, Heme oxygenase-1 and iron in liver inflammation: a complex alliance, Curr. Drug Targets, 11, 1541, 10.2174/1389450111009011541 Johansen, 2015, Comparison of transcriptomic responses to pancreas disease (PD) and heart and skeletal muscle inflammation (HSMI) in heart of Atlantic salmon (Salmo salar L), Fish Shellfish Immunol., 46, 612, 10.1016/j.fsi.2015.07.023 Johnson, 2013, The regulatory power of glycans and their binding partners in immunity, Trends Immunol., 34, 10.1016/j.it.2013.01.006 Jordal, 2007, Complete replacement of dietary fish oil with a vegetable oil blend affect liver lipid and plasma lipoprotein levels in Atlantic salmon (Salmo salar L), Aquac. Nutr., 13, 114, 10.1111/j.1365-2095.2007.00455.x Karlsen, 2018, Atlantic salmon skin barrier functions gradually enhance after seawater transfer, Sci. Rep., 8, 9510, 10.1038/s41598-018-27818-y Kistler, 2002, Metabolism and CYP-inducer properties of astaxanthin in man and primary human hepatocytes, Arch. Toxicol., 75, 665, 10.1007/s00204-001-0287-5 Kortner, 2012, Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.), Br. J Nutr., 109, 593, 10.1017/S0007114512002024 Krasnov, 2011, Genomic survey of early responses to viruses in Atlantic salmon, Salmo salar L, Mol. Immunol., 49, 163, 10.1016/j.molimm.2011.08.007 Krasnov, 2013, Induced erythropoiesis during acute anemia in Atlantic salmon: a transcriptomic survey, Gen. Comp. Endocrinol., 192, 181, 10.1016/j.ygcen.2013.04.026 Krasnov, 2016, Gene expression profiling in melanised sites of Atlantic salmon fillets, Fish Shellfish Immunol., 55, 56, 10.1016/j.fsi.2016.05.012 Leaver, 2008, Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar), BMC Genomics, 9, 299, 10.1186/1471-2164-9-299 Lehnert, 2018, Significant differences in maternal carotenoid provisioning and effects on offspring fitness in Chinook salmon colour morphs, J. Evol. Biol., 31, 1876, 10.1111/jeb.13383 Liu, 2014, The astaxanthin-induced improvement in lipid metabolism during exercise is mediated by a PGC-1 alpha increase in skeletal muscle, J. Clin. Biochem. Nutr., 54, 86, 10.3164/jcbn.13-110 Liu, 2019, Effects of astaxanthin and emodin on the growth, stress resistance and disease resistance of yellow catfish (Pelteobagrus fulvidraco), Fish Shellfish Immunol., 51, 125, 10.1016/j.fsi.2016.02.020 Lobo, 2010, β,β-Carotene decreases peroxisome proliferator receptor γ activity and reduces lipid storage capacity of adipocytes in a β,β-carotene-oxygenase 1-dependent manner, J. Biol. Chem., 36, 27891, 10.1074/jbc.M110.132571 Lobo, 2012, Mammalian carotenoid oxygenases: key players for carotenoid function and homeostasis, Biochim. Biophys. Acta, 1821, 78, 10.1016/j.bbalip.2011.04.010 Marques da Cunha, 2018, Consumption of carotenoids not increased by bacterial infection in brown trout embryos (Salmo trutta), PLoS One, 13, 10.1371/journal.pone.0198834 Miki, 1991, Biological functions and activities of animal carotenoids, Pure Appl. Chem., 63, 141, 10.1351/pac199163010141 Moren, 2002, Conversion of beta-carotene, canthaxanthin and astaxanthin to vitamin A in Atlantic halibut (Hippoglossus hippoglossus L.) juveniles, Fish Physiol. Biochem., 27, 71, 10.1023/B:FISH.0000021819.46235.12 Mørkøre, 2020, Dietary inclusion of Antarctic krill meal during the finishing feed period improves health and fillet quality of Atlantic salmon (Salmo salar L.), Br. J. Nutr., 124, 418, 10.1017/S0007114520001282 Naguib, 2000, Antioxidant activities of astaxanthin and related carotenoids, J. Agric. Food Chem., 48, 1150, 10.1021/jf991106k Origassa, 2013, Cytoprotective role of heme oxygenase-1 and heme degradation derived end products in liver injury, World J. Hepatol., 5, 541, 10.4254/wjh.v5.i10.541 Page, 2002, Astaxanthin and canthaxanthin do not induce liver or kidney xenobiotic-metabolizing enzymes in rainbow trout (Oncorhynchus mykiss Walbaum), Comp. Biochem. Physiol. Toxicol. Pharmacol., 133, 443, 10.1016/S1532-0456(02)00168-0 Page, 2005, Dietary carotenoid pigment supplementation influences hepatic lipid and mucopolysaccharide levels in rainbow trout (Oncorhynchus mykiss), Comp. Biochem. Physiol. B, 142, 398, 10.1016/j.cbpb.2005.09.001 Palozza, 1992, Astaxanthin and canthaxanthin are potent antioxidants in a membrane model, Arch. Biochem. Biophys., 297, 291, 10.1016/0003-9861(92)90675-M Reid, 2011, Rainbow trout Oncorhynchus mykiss ladderlectin, but not intelectin, binds viral hemorrhagic septicemia virus IVb, Dis. Aquat. Org., 95, 137, 10.3354/dao02358 Russell, 2009, Immunohistochemical localization of rainbow trout ladderlectin and intelectin in healthy and infected rainbow trout (Oncorhynchus mykiss), Fish Shellfish Immunol., 26, 154, 10.1016/j.fsi.2008.03.001 Ruyter, 2019, Omega-3 canola oil effectively replaces fish oil as a new safe dietary source of docosahexaenoic acid (DHA) in feed for juvenile Atlantic salmon, Br. J. Nutr., 122, 1329, 10.1017/S0007114519002356 Sahin, 2014, Lycopene improves activation of antioxidant systems and Nrf2/HO-1 pathway of muscle i rainbow trout (Oncorhyncus mykiss) with different stocking densities, Aquaculture, 430, 133, 10.1016/j.aquaculture.2014.04.007 Sahin, 2014, The effect of lycopene on antioxidant status in rainbow trout (Oncorhynchus mykiss) reared under high stocking density, Aquaculture, 418-419, 132, 10.1016/j.aquaculture.2013.10.009 Sangeetha, 2010, Retinol-deficient rats can convert a pharmacological dose of astaxanthin to retinol: antioxidant potential of astaxanthin, lutein, and β-carotene, Can. J. Physiol. Pharmacol., 88, 977, 10.1139/Y10-074 Saunders, 2010, Putative GTPase GIMAP1 is critical for the development of mature B and T lymphocytes, Blood, 115, 3249, 10.1182/blood-2009-08-237586 Schiedt, 1985, Absorption, retention and metabolic transformations of carotenoids in rainbow-trout, salmon and chicken, Pure Appl. Chem., 57, 685, 10.1351/pac198557050685 Schiedt, 1986, Astaxanthin and its metabolites in wild rainbow trout (Salmo gairdneri R.), Comp. Biochem. Physiol., 83B, 9 Schiedt, 1989, Metabolism of carotenoids in salmonids I. Idoxanthin, a metabolite of astaxanthin in the flesh of Atlantic salmon (Salmo salar, L.) under varying external conditions, Comp. Biochem. Physiol., 92B, 277 Schierle, 1994, Revised supplement: Determination of stabilized astaxanthin in Carophyll Pink, premixes and fish feeds Schüep, 1995, Example 9, astaxanthin, 273 Shi, 2006, Hepcidins in amphibians and fishes: antimicrobial peptides or iron-regulatory hormones?, Dev. Comp. Immunol., 30, 746, 10.1016/j.dci.2005.10.009 Sobhkhez, 2017, Transcriptome analysis of plasmid-induced genes sheds light on the role of type I IFN as adjuvant in DNA vaccine against infectious salmon anemia virus, PLoS One, 12, 10.1371/journal.pone.0188456 Sveen, 2018, High fish density delays wound healing in Atlantic salmon (Salmo salar), Sci. Rep., 8, 16907, 10.1038/s41598-018-35002-5 Todorčević, 2009, N-3 HUFAs affect fat deposition, susceptibility to oxidative stress, and apoptosis in Atlantic salmon visceral adipose tissue, Comp. Biochem. Physiol. B, 152, 135, 10.1016/j.cbpb.2008.10.009 Torstensen, 2011, Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.), Br. J. Nutr., 106, 633, 10.1017/S0007114511000729 Webb, 2016, GIMAP1 is essential for the survival of naive and activated B cells in vivo, J. Immunol., 196, 207, 10.4049/jimmunol.1501582 White, 2003 Wilkins, 2017, Maternal allocation of carotenoids increases tolerance to bacterial infection in brown trout, Oecologia, 185, 351, 10.1007/s00442-017-3952-y Wolff, 2010, Astaxanthin protects mitochondrial redox state and functional integrity against oxidative stress, J. Nutr. Biochem., 21, 381, 10.1016/j.jnutbio.2009.01.011 Yang, 2014, Astaxanthin lowers plasma TAG concentrations and increases hepatic antioxidant gene expression in diet-induced obesity mice, Br. J. Nutr., 112, 1797, 10.1017/S0007114514002554 Yoshida, 2010, Administration of natural astaxanthin increases serum HDL-cholesterol and adiponectin in subjects with mild hyperlipidemia, Atherosclerosis, 209, 520, 10.1016/j.atherosclerosis.2009.10.012 Young, 2007, Bacterial-binding activity and plasma concentration of ladderlectin in rainbow trout (Oncorhynchus mykiss), Fish Shellfish Immunol., 23, 305, 10.1016/j.fsi.2006.10.014 Ytrestøyl, 2004, Carotenoid and lipid content in muscle of Atlantic salmon, Salmo salar, transferred to seawater as 0+ or 1+ smolts, Comp. Biochem. Physiol., 138, 29, 10.1016/j.cbpc.2004.01.011 Ytrestøyl, 2008, Utilisation of astaxanthin in Atlantic salmon from seawater transfer to slaughter Ytrestøyl, 2015, Utilisation of feed resources in production of Atlantic salmon (Salmo salar) in Norway, Aquaculture, 448, 365, 10.1016/j.aquaculture.2015.06.023 Zhang, 2013, Effects of dietary astaxanthin on growth, antioxidant capacity and gene expression in Pacific white shrimp Litopenaeus vannamei, Aquac. Nutr., 19, 917, 10.1111/anu.12037