Marine Biotechnology

, Volume 16, Issue 1, pp 88–102 | Cite as

Microarray Analysis of Hepatic Gene Expression in Juvenile Japanese Flounder Paralichthys olivaceus Fed Diets Supplemented with Fish or Vegetable Oils

  • Ubonrat Limtipsuntorn
  • Yutaka Haga
  • Hidehiro Kondo
  • Ikuo Hirono
  • Shuichi Satoh
Original Article
First Online:
Received:
Accepted:

Abstract

Gene expression profiling was performed in Japanese flounder Paralichthys olivaceus fed diets supplemented with fish oil (FO), linseed oil (LO), or olive oil (OO) for 6 weeks. The LO and OO groups showed significantly retarded growth, lower feed intake, lower protein efficiency ratio, and lower hepatosomatic index (P < 0.05). Liver fatty acid composition reflected the dietary fatty acid composition. Microarray analysis revealed that dietary n − 3 highly unsaturated fatty acid (HUFA) deficiency affected 169 transcripts. In the LO group, 57 genes were up-regulated and 38 genes were down-regulated, whereas in the OO group nine genes were up-regulated and 87 genes were down-regulated. Analysis of the functional annotations suggested that dietary n − 3 HUFA affected genes involved in signal transduction (23.2 %), cellular processes (21.1 %), metabolism (including glucose, lipid, and nucleobase; 15.5 %), transport (11.3 %), regulation of transcription (10.5 %), and immune response (4.2 %). Several genes encoding serine/threonine kinases such as protein kinase C and calmodulin-dependent kinase and nuclear hormone receptors such as vitamin D receptor, retinoic acid receptor, and receptors for cytokines (bone morphogenic protein and transforming growth factor β) were affected. Among 169 transcripts, 22 genes were affected in both LO and OO groups. The present study identified several genes involved in n − 3 HUFA deficiency-sensitive pathways, which will be useful for selective breeding of flounder strains able to adapt to n − 3 HUFA deficiency.

Keywords

Microarray Fatty acid Japanese flounder Protein kinase Transcription factor 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The expenses of this study were partially defrayed by a grant to Y.H. from JSPS-NRCT Asian Core University Program “Development of new bio-technology for aquaculture and risk management of aquaculture products”. U.L. is supported by a scholarship from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

References

  1. Aoki T, Wang HC, Unajak S, Santos MD, Kondo H, Hirono I (2011) Microarray analyses of shrimp immune responses. Mar Biotechnol 13:629–638CrossRefPubMedGoogle Scholar
  2. Araki K, Ozaki T, Okauchi M, Okamoto H, Hara M, Yamada T, Masaoka T, Matsuyama T, Sakai T, Yoshida K, Hattori K, Takeuchi H (2011) Current flounder breeding in Japan. Fish Genet Breed Sci 40:67–69Google Scholar
  3. Belke DD, Larsen TS, Lopaschuk GD, Severson DL (1999) Glucose and fatty acid metabolism in the isolated working mouse heart. Am J Physiol 277:1210–1217Google Scholar
  4. Bell JG (1998) Current aspects of lipid nutrition in fish farming. In: Black KD, Pickering AD (eds) Biology of farmed fish. Academic Press, SheffieldGoogle Scholar
  5. Breslow DK, Collins SR, Bodenmiller B, Aebersold R, Simons K, Shevchenko A, Ejsing CS, Weissman JS (2010) Orm family proteins mediate sphingolipid homeostasis. Nature 463:1048–1053PubMedCentralCrossRefPubMedGoogle Scholar
  6. Burger K, Demel RA, Schmid SL, Kruijff BD (2000) Dynamin is membrane-active: lipid insertion is induced by phosphoinositides and phosphatidic acid. Biochemistry 39:12485–12493CrossRefPubMedGoogle Scholar
  7. Cantero-Recasens G, Fandos C, Rubio-Moscardo F, Valverde MA, Vicente R (2010) The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress. Human Mol Genet 19:111–121CrossRefGoogle Scholar
  8. Cerda J, Douglas S, Reith M (2010) Genomic resources for flatfish research and their applications. J Fish Biol 77:1045–1070CrossRefPubMedGoogle Scholar
  9. Coimbra MRM, Kobayashi K, Koretsugu K, Hasegawa S, Ohara E, Ozaki A, Sakamoto T, Naruse K, Okamoto N (2003) A genetic linkage map of the Japanese flounder, Paralichthys olivaceus. Aquaculture 220:203–218CrossRefGoogle Scholar
  10. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefPubMedGoogle Scholar
  11. Coutinho-Silva R, Parsons M, Robson T, Lincoln J, Burnstock G (2003) P2X and P2Y purinoceptor expression in pancreas from streptozotocin–diabetic rats. Mol Cell Endocrinol 204:141–154CrossRefPubMedGoogle Scholar
  12. Deng X, Cagen LM, Wilcox HG, Park EA, Raghow R, Elam MB (2002) Regulation of the rat SREBP-1c promoter in primary rat hepatocytes. Biochem Biophys Res Commun 290:256–262CrossRefPubMedGoogle Scholar
  13. Díaz-Rosales P, Romero A, Balseiro P, Dios S, Novoa B, Figueras A (2012) Microarray-based identification of differentially expressed genes in families of turbot (Scophthalmus maximus) after infection with viral haemorrhagic septicaemia virus (VHSV). Mar Biotechnol 14:515–529CrossRefPubMedGoogle Scholar
  14. Drivenes Ø, Taranger GL, Edvardsen RB (2012) Gene expression profiling of Atlantic cod (Gadus morhua) embryogenesis using microarray. Mar Biotechnol 14:167–176CrossRefPubMedGoogle Scholar
  15. Erck C, Peris L, Andrieux A, Meissirel C, Gruber AD, Vernet M, Schweitzer A, Saoudi Y, Pointu H, Bosc C, Salin PA, Job D, Wehland J (2005) A vital role of tubulin–tyrosine–ligase for neuronal organization. Proc Natl Acad Sci USA 102:7853–7858PubMedCentralCrossRefPubMedGoogle Scholar
  16. Espenshade PJ (2006) SREBPs: sterol-regulated transcription factors. J Cell Sci 119:973–976CrossRefPubMedGoogle Scholar
  17. Fletcher GL, Rise ML (2012) Aquaculture biotechnology. Wiley-Blackwell, ChichesterGoogle Scholar
  18. Fleury E, Huvet A (2012) Microarray analysis highlights immune response of pacific oysters as a determinant of resistance to summer mortality. Mar Biotechnol 14:203–217CrossRefPubMedGoogle Scholar
  19. Folch J, Lee M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J BiolChem 226:407–509Google Scholar
  20. Fountoulaki E, Vasilaki A, Hurtado R, Grigorakis K, Karacostas I, Nengas I, Rigos G, Kotzamanis Y, Venou B, Alexis MN (2009) Fish oil substitution by vegetable oils in commercial diets for gilthead sea bream (Sparus aurata L.); effects on growth performance, flesh quality and fillet fatty acid profile: recovery of fatty acid profiles by a fish oil finishing diet under fluctuating water temperatures. Aquaculture 289:317–326CrossRefGoogle Scholar
  21. Frühbeck G, Gómez-Ambrosi J, Muruzábal FJ, Angela M (2001) The adipocyte: a model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am J Physiol Endocrinol Metab 280:E827–847PubMedGoogle Scholar
  22. Fuji K, Kobayashi K, Hasegawa O, Cimbra MRM, Sakamoto T, Okamoto N (2006) Identification of a single major locus controlling the resistance to lymphocystis disease in Japanese flounder (Paralichthys oliveceus). Aquaculture 254:203–210CrossRefGoogle Scholar
  23. Georgiadi A, Boekschoten MV, Müller M, Kersten S (2012) Detailed transcriptomics analysis of the effect of dietary fatty acids on gene expression in the heart. Physiol Genomics 44:352–361CrossRefPubMedGoogle Scholar
  24. Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res 41:770–776CrossRefGoogle Scholar
  25. Helmreich EJ (2003) Environmental influences on signal transduction through membranes: a retrospective mini-review. Biophys Chem 100:519–534CrossRefPubMedGoogle Scholar
  26. Hla T (2004) Physiological and pathological actions of sphingosine 1-phosphate. Semin Cell Dev Biol 15:513–520CrossRefPubMedGoogle Scholar
  27. Houtman SH, Rutteman M, De Zeeuw CI, French PJ (2007) Echinoderm microtubule-associated protein like protein 4, a member of the echinoderm microtubule-associated protein family, stabilizes microtubules. Neuroscience 144:1373–1382CrossRefPubMedGoogle Scholar
  28. Hu G, Wang X, Saunders DN, Henderson M, Russell AJ, Herring BP, Zhou J (2010) Modulation of myocardin function by the ubiquitin E3 ligase UBR5. J Biol Chem 285:11800–11809PubMedCentralCrossRefPubMedGoogle Scholar
  29. Inazuka F, Sugiyama N, Tomita M, Abe T, Shioi G, Esumi H (2012) Muscle-specific knock-out of NUAK family SNF1-like kinase 1 (NUAK1) prevents high fat diet-induced glucose intolerance. J Biol Chem 287:16379–16389PubMedCentralCrossRefPubMedGoogle Scholar
  30. Izumi M, Makimura Y, Dedola S, Seko A, Kanamori A, Sakono M, Ito Y, Kajihara Y (2012) Chemical synthesis of intentionally misfolded homogeneous glycoprotein: a unique approach for the study of glycoprotein quality control. J Am Chem Soc 134:7238–7241CrossRefPubMedGoogle Scholar
  31. Jordal A-EO, Torstensen BE, Tsoi S, Tocher DR, Lall SP, Douglas S (2005) Dietary rapeseed oil affects the expression of genes involved in hepatic lipid metabolism in Atlantic salmon (Salmo salar L.). J Nutr 35:2355–2361Google Scholar
  32. Juaneda P, Rocquelin G (1985) Rapid and convenient separation of phospholipids and nonphosphorus lipids from rat heart using silica cartridges. Lipids 20:40–41CrossRefPubMedGoogle Scholar
  33. Jump DB, BotolinD WY, Xu J, Christian B, Demeure O (2005) Fatty acid regulation of hepatic gene transcription. J Nutr 135:2503–2506PubMedGoogle Scholar
  34. Jump DB, Botolin D, Wang Y, Xu J, Demeure O, Christian B (2008) Docosahexaenoic acid (DHA) and hepatic gene transcription. Chem Phys Lipids 153:3–13PubMedCentralCrossRefPubMedGoogle Scholar
  35. Kato G, Kondo H, Aoki T, Hirono I (2010) BCG vaccine confers adaptive immunity against Mycobacterium sp. infection in fish. Dev Comp Immunol 34:133–140CrossRefPubMedGoogle Scholar
  36. Kikuchi K, Takeuchi T (2002) Japanese flounder, Paralichthys olivareas. In: Webster CD, Lim C (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, New YorkGoogle Scholar
  37. Knutson DM (2010) Iron-sensing proteins that regulate hepcidin and enteric iron absorption. Annu Rev Nutr 30:149–171CrossRefPubMedGoogle Scholar
  38. Kuwano R, Miyashita A, Arai H, Asada T, Imagawa M, Shoji M, Urakami K, Kakita A, Takahashi H, Tsukie T, Toyabe S, Akazawa K, Kanazawa I, Ihara Y (2006) Dynamin-binding protein gene on chromosome 10q is associated with late-onset Alzheimer's disease. Hum Mol Genet 15:2170–2182CrossRefPubMedGoogle Scholar
  39. Leaver MJ, Villeneuve LAN, Obach A, Jensen L, Bron JE, Tocher DR, Taggart JB (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 9:299PubMedCentralCrossRefPubMedGoogle Scholar
  40. Leaver M, Taggart JB, Villeneuve L, Bron JE, Guy DR, Bishop SC, Houston RD, Matika O, Tocher DR (2011) Heritability and mechanisms of n − 3 long chain polyunsaturated fatty acid deposition in the flesh of Atlantic salmon. Comp Biochem Physiol Part D Genomics Proteomics 6:62–69CrossRefPubMedGoogle Scholar
  41. Lee JE, Silhavy JL, Zaki MS, Schroth J, Bielas SL, Marsh SE, Olvera J, Brancati F, Iannicelli M, Ikegami K, Schlossman AM, Merriman B, Attié-Bitach T, Logan CV, Glass IA, Cluckey A, Louie CM, Lee JH, Raynes HR, Rapin I, Castroviejo IP, Setou M, Barbot C, Boltshauser E, Nelson SF, Hildebrandt F, Johnson CA, Doherty DA, Valente EM, Gleeson JG (2012) CEP41 is mutated in Joubert syndrome and is required for tubulin glutamylation at the cilium. Nat Genet 44:193–199PubMedCentralCrossRefPubMedGoogle Scholar
  42. Leonard TA, Hurley JH (2011) Regulation of protein kinases by lipids. Curr Opin Struc Biol 21:785–791CrossRefGoogle Scholar
  43. Massaugue J, Seoane J, Wotton D (2005) Smad transcription factors. Genes Dev 19:2783–2810CrossRefGoogle Scholar
  44. Matsuzaka T, ShimanoH YN, Amemiya-KudoM YT, Hasty AH, Tamura Y, Osuga J, Okazaki H, IizukaY TA, Sone H, Gotoda T, Ishibashi S, Yamada N (2002) Dual regulation of mouse Δ5- and Δ6-desaturase gene expression by SREBP-1 and PPARα. J Lipid Res 43:107–114PubMedGoogle Scholar
  45. McKenzie DJ (2001) Effects of dietary fatty acids on the respiratory and cardiovascular physiology of fish. Comp Biochem Physiol 128A:607–621Google Scholar
  46. Millán A, Gómez-Tato A, Pardo BG, Fernández C, Bouza C, Vera M, Alvarez-Dios JA, Cabaleiro S, Lamas J, Lemos ML, Martínez P (2011) Gene expression profiles of the spleen, liver, and head kidney in turbot (Scophthalmus maximus) along the infection process with Aeromonas salmonicida using an immune-enriched oligo-microarray. Mar Biotechnol 13:1099–1114CrossRefPubMedGoogle Scholar
  47. Minárik P, Tomásková N, Kollárová M, Antalík M (2001) Malate dehydrogenases—structure and function. Gen Physiol Biophys 21:257–265Google Scholar
  48. Mindnich R, Deluca D, Adamski J (2004) Identification and characterization of 17β-hydroxysteroid dehydrogenases in the zebrafish, Danio rerio. Mol Cell Endocrinol 215:19–30CrossRefPubMedGoogle Scholar
  49. Mishina Y, Starbuck MW, Gentile MA, Fukuda T, Kasparcova V, Seedor JG, Hanks MC, Amling M, Pinero GJ, Harada S, Behringer RR (2004) Bone morphogenetic protein type IA receptor signaling regulates postnatal osteoblast function and bone remodeling. J Biol Chem 279:27560–27566CrossRefPubMedGoogle Scholar
  50. Moeller G, Adamski J (2006) Multifunctionality of human 17β-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 248:47–55CrossRefPubMedGoogle Scholar
  51. Monroig O, Li Y, Tocher DR (2011) Delta-8 desaturation activity varies among fatty acyl desaturases of teleost fish: high activity in delta-6 desaturases of marine species. Comp Biochem Phys B 159:206–213CrossRefGoogle Scholar
  52. Montero D, Grasso V, Izquierdo MS, Ganga R, Real R, Tort L, Caballero MJ, Acosta F (2008) Total substitution of fish oil by vegetable oils in gilthead sea bream (Sparus aurata) diets: effects on hepatic Mx expression and some immune parameters. Fish Shellfish Immunol 24:147–155CrossRefPubMedGoogle Scholar
  53. Montero D, Robaina L, Caballero MJ, Ginés R, Izquierdo MS (2005) Growth, feed utilization and flesh quality of European sea bass (Dicentrarchus labrax) fed diets containing vegetable oils: a time-course study on the effect of re-feeding period with a 100% fish oil diet. Aquaculture 248:121–134CrossRefGoogle Scholar
  54. Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR (2011a) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 12:255PubMedCentralCrossRefPubMedGoogle Scholar
  55. Morais S, Pratoomyot J, Torstensen BE, Taggart JB, Guy DR, Bell JG, Tocher DR (2011b) Diet × genotype interactions in hepatic cholesterol and lipoprotein metabolism in Atlantic salmon (Salmo salar) in response to replacement of dietary fish oil with vegetable oil. Br J Nutr 106:1457–1469CrossRefPubMedGoogle Scholar
  56. Morais S, Silva T, Cordeiro O, Rodrigues P, Guy DR, Bron TE, Taggart JB, Bell JG, Tocher DR (2012) Effects of genotype and dietary fish oil replacement with vegetable oil on the intestinal transcriptome and proteome of Atlantic salmon. BMC Genomics 13:448PubMedCentralCrossRefPubMedGoogle Scholar
  57. Mourente G, Good JE, Bell JG (2005) Partial substitution of fish oil with rapeseed, linseed and olive oils in diets for European sea bass (Dicentrarchus labrax L.) effects on flesh fatty acid composition, plasma prostaglandins E2; and F2a, immune function and effectiveness of a fish oil finishing diet. Aquac Nutr 11:25–40CrossRefGoogle Scholar
  58. Murray HM, Lall SP, Rajaselvam R, Boutilier LA, Blanchard B, Flight RM, Colombo S, Mohindra V, Douglas SE (2009) A nutrigenomic analysis of intestinal response to partial soybean meal replacement in diets for juvenile Atlantic halibut, Hippoglossus hippoglossus, L. Aquaculture 298:282–293CrossRefGoogle Scholar
  59. [NRC] National Research Council (1993) Nutrient requirements of fish. National Academies, Washington DCGoogle Scholar
  60. Pacaud P, Feolde E, Frelin C, Loirand G (1996) Characterization of the P2Y-purinoceptor involved in the ATP-induced rise in cytosolic Ca2+concentration in rat ileal myocytes. Br J Pharmacol 118:2213–2219PubMedCentralCrossRefPubMedGoogle Scholar
  61. Paige JA, Liao RL, Hajjar RJ (1996) Effect of a high omega-3 fatty acid diet on cardiac contractile performance in Oncorhynchus mykiss. Cardiovasc Res 31:249–262CrossRefPubMedGoogle Scholar
  62. Panserat S, Kolditz C, Richard N, Plagnes-Juan E, Piumi F, Esquerre D, Geurden I, Médale F, Corraze G, Kaushik S (2008) Hepatic gene expression profiles in rainbow trout (Oncorhynchus mykiss) fed fish meal or fish oil-free diets. Br J Nutr 100:953–967CrossRefPubMedGoogle Scholar
  63. Panserat S, Hortopan GA, Plagnes-Juan E, Kolditz C, Lansard M, Skiba-Cassy S, Esquerre D, Geurden I, Médale F, Kaushik S, Corraze G (2009) Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 294:123–131CrossRefGoogle Scholar
  64. Pike IH, Jackson A (2010) Fish oil: production and use now and in the future. Lipid Tech 22:59–61CrossRefGoogle Scholar
  65. Pollmann M, Parwaresch R, Adam-Klages S, Kruse ML, Buck F, Heidebrecht HJ (2006) Human EML4, a novel member of the EMAP family, is essential for microtubule formation. Exp Cell Res 312:3241–3251CrossRefPubMedGoogle Scholar
  66. Qin Y, Dalen KT, Gustafsson J-A, Nebb HI (2009) Regulation of hepatic fatty acid elongase 5 by LXR alpha-SREBP-1c. Biochimica Biophysica Acta 179:140–147CrossRefGoogle Scholar
  67. Rebl A, Verleih M, Köbis JM, Kühn C, Wimmers K, Köllner B, Goldammer T (2013) Transcriptome profiling of gill tissue in regionally bred and globally farmed rainbow trout strains reveals different strategies for coping with thermal stress. Mar Biotechnol 15:445–460Google Scholar
  68. Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758PubMedGoogle Scholar
  69. Ross S, Hill CS (2008) How the Smads regulate transcription. Int J Biochem Cell Biol 40:383–408CrossRefPubMedGoogle Scholar
  70. Sargent JR, Bell MV, Henderson RJ, Tocher DR (1995) Requirement criteria for essential fatty acids. J Appl Ichthyol 11:183–198CrossRefGoogle Scholar
  71. Sarker MA, Yamamoto Y, Haga Y, Saker SA, Miwa M, Yoshizaki G, Satoh S (2011) Influences of low salinity and dietary fatty acids on fatty acid composition and fatty acid desaturase and elongase expression in red sea bream Pagrus major. Fish Sci 77:385–396CrossRefGoogle Scholar
  72. Schmidt DR, Mangelsdorf DJ (2008) Nuclear receptors of the enteric tract: guarding the frontier. Nutr Rev 66S2:S88–S97CrossRefGoogle Scholar
  73. Senadheera SD, Turchini GM, Thanuthong T, Francis DS (2012) Effects of dietary iron supplementation on growth performance, fatty acid composition and fatty acid metabolism in rainbow trout (Oncorhynchus mykiss) fed vegetable oil based diets. Aquaculture 342–343:80–88CrossRefGoogle Scholar
  74. Sethi JK, Hotamisligil GS (1999) The role of TNFα in adipocyte metabolism. Semin Cell Dev Biol 10:19–29CrossRefPubMedGoogle Scholar
  75. Shi J, Camus AC (2006) Hepcidins in amphibians and fishes: antimicrobial peptides or iron-regulatory hormones? Dev Comp Immunol 30:746–755CrossRefPubMedGoogle Scholar
  76. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11:688–699CrossRefPubMedGoogle Scholar
  77. Sijben JW, Calder PC (2007) Differential immunomodulation with long chain n − 3 PUFA in health and chronic disease. Proc Nutr Soc 66:237–259CrossRefPubMedGoogle Scholar
  78. Sutherland E, Dixon BS, Leffeart HL, Skally S, Zaccaro L, Simon FR (1988) Biochemical localization of hepatic surface-membrane Na+, K + -ATPase activity depends on membrane lipid fluidity. Proc Natl Acad Sci U S A 85:8673–8677PubMedCentralCrossRefPubMedGoogle Scholar
  79. Swanson KS (2008) Using genomic biology to study liver metabolism. J Anim Physiol Anim Nutr 92:246–252CrossRefGoogle Scholar
  80. Tacchi L, Secombes CJ, Bickerdike R, Adler MA, Venegas C, Tackle H, Martin SA (2012) Transcriptomic and physiological responses to fish meal substitution with plant proteins in formulated feed in farmed Atlantic salmon (Salmo salar). BMC Genomics 13:363PubMedCentralCrossRefPubMedGoogle Scholar
  81. Tacon AGJ, Hasan MR,Subasinghe RP (2006) Use of fishery resources as feed inputs to aquaculture development: trends and policy implications. FAO Fisheries Circular No. 1018. Rome, ItalyGoogle Scholar
  82. Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compoundedaquafeeds: Trends and future prospects. Aquaculture 285:146–158CrossRefGoogle Scholar
  83. Taira K, Bujo H, Hirayama S, Yamazaki H, Kanaki T, Takahashi K, Ishii I, Miida T, Schneider WJ, Saito Y (2001) LR11, a mosaic LDL receptor family member, mediates the uptake of ApoE-rich lipoproteins in vitro. Arterioscler Thromb Vasc Biol 21:1501–1506CrossRefPubMedGoogle Scholar
  84. Taub R (2004) Liver regeneration: from myth to mechanism. Mol Cell Biol 5:836–847Google Scholar
  85. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184CrossRefGoogle Scholar
  86. Ushio H, Ohishima T, Koizumi C, Visuthi V, Kiron V, Watanabe T (1997) Effect of dietary fatty acids on Ca2+-ATPase activity of the sarcoplasmic reticulum of rainbow trout skeletal muscle. Comp Biochem Physiol 118B:681–691CrossRefGoogle Scholar
  87. Wenger M, Krasnov A, Skugor S, Goldschmidt-Clermont E, Sattler U, Afanasyev S, Segner H (2012) Estrogen modulates hepatic gene expression and survival of rainbow trout infected with pathogenic bacteria Yersinia ruckeri. Mar Biotechnol 14:530–543CrossRefPubMedGoogle Scholar
  88. Xu P, McIntyre LM, Scardina J, Wheeler PA, Thorgaard GH, Nichols KM (2011) Transcriptome profiling of embryonic development rate in rainbow trout advanced backcross introgression lines. Mar Biotechnol 13:215–231CrossRefPubMedGoogle Scholar
  89. Yanagisawa J, Yanagi Y, Masuhiro Y, Suzawa M, Watanabe M, Kashiwagi K, Toriyabe T, Kawabata M, Miyazono K, Kato S (1999) Convergence of transforming growth factor-βand vitamin D signaling pathways on SMAD transcriptional coactivators. Science 283:1317–1321CrossRefPubMedGoogle Scholar
  90. Yildiz M, Sener E (2004) The effect of dietary oils of vegetable origin on the performance, body composition and fatty acid profiles of sea bass (Dicentrarchuslabrax L., 1758) juveniles. Turk J Vet Anim Sci 28:553–556Google Scholar
  91. Yoshizawa T, Handa Y, Uematsu Y, Takeda S, Sekine K, Yoshihara Y, Kawakami T, Arioka K, Sato H, Uchiyama Y, Masushige S, Fukamizu A, Matsumoto T, Kato S (1997) Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat Genet 16:391–396CrossRefPubMedGoogle Scholar
  92. Yu YH, Ginsberg HN (2005) Adipocyte signaling and lipid homeostasis: Sequelae of insulin-resistant adipocyte tissue. Am Heart Assoc 96: 1042–1052Google Scholar
  93. Zhu J, Mounzih K, Chehab EF, Mitro N, Saez E, Chehab FF (2010) Effects of FoxO4 overexpression on cholesterol biosynthesis, triacylglycerol accumulation, and glucose uptake. J Lipid Res 51:1312–1324PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Ubonrat Limtipsuntorn
    • 1
  • Yutaka Haga
    • 1
  • Hidehiro Kondo
    • 1
  • Ikuo Hirono
    • 1
  • Shuichi Satoh
    • 1
  1. 1.Department of Marine Bioscience, Graduate School of Marine Science and TechnologyTokyo University of Marine Science and TechnologyTokyoJapan

Personalised recommendations