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Sesamin Modulates Gene Expression Without Corresponding Effects on Fatty acids in Atlantic Salmon (Salmo salar L.)

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Lipids

Abstract

This study examined the effects of sesamin inclusion in vegetable oil-based diets fed to Atlantic salmon (Salmo salar L.). The diets used differed in n-6/n-3 fatty acid (FA) ratio (0.5 and 1) and sesamin content (high 5.8 g/kg, low 1.16 g/kg and no sesamin). The oils used in the feeds were a mixture of rapeseed, linseed and palm oil. Fish were fed for 4 months. Fatty acids and expression of hepatic genes involved in transcription, lipid uptake, desaturation, elongation and β-oxidation were measured. No major effects on the percentage of DHA in white muscle, liver triacylglycerol and phospholipid fraction were detected. Genes involved in β-oxidation, elongation and desaturation were affected by sesamin addition. Limited effects were seen on any of the transcription factors tested and no effect was seen on the expression of peroxisome proliferator-activated receptors (PPAR). Expression of both SREBP-1 and SREBP-2 increased with sesamin addition. It was concluded that supplementation of fish feed with a high level of sesamin had a negative effect on the growth rate and live weight and did not alter the proportions of DHA in tissues even though gene expression was affected. Thus, more studies are needed to formulate a diet that would increase the percentage of DHA in fish without negative effects on fish growth.

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Abbreviations

ARA:

Arachidonic acid (20:4n-6)

ACO:

Acyl-CoA oxidase

ALA:

Alpha-linolenic acid (18:3n-3)

CPT1:

Carnitine palmitoyl transferase I

Δ5 fad:

Delta 5 fatty acid desaturase

Δ6 fad:

Delta 6 fatty acid desaturase

DHA:

Docosahexaenoic acid (22:6n-3)

DTA:

Dodecylthioacetic acid

ELOVL:

Elongation of very long chain fatty acids gene

EPA:

Eicosapentaenoic acid (20:5n-3)

FAME:

Fatty acid methyl ester(s)

FA:

Fatty acid(s)

FCR:

Feed conversion ratio

FO:

Fish oil

K:

Condition factor

LNA:

Linoleic acid (18:2n-6)

LCPUFA:

Long chain polyunsaturated fatty acid(s)

LXRα:

Liver X receptor α

MUFA:

Monounsaturated fatty acid(s)

n-3:

Omega-3

n-6:

Omega-6

n-6/n-3:

n-6/n-3 PUFA

PUFA:

Polyunsaturated fatty acid(s)

PPAR:

Peroxisomal proliferator-activated receptor(s)

PGC-1α:

Peroxisome proliferator activated receptor γ coactivator-1α

PL:

Phospholipid(s)

SFA:

Saturated fatty acid(s)

SD:

Standard deviation

SGR:

Specific growth rate

SR-B1:

Scavenger receptor class BI

SREBP:

Sterol regulatory element binding protein

TAG:

Triacylglycerol

TTA:

Tetradecylthioacetic acid

VO:

Vegetable oil

References

  1. Gordon Bell J, James Henderson R, Tocher DR, McGhee F, Dick JR, Porter A, Smullen RP, Sargent JR (2002) Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects muscle fatty acid composition and hepatic fatty acid metabolism. J Nutr 132:222–230

    PubMed  Google Scholar 

  2. Torstensen BE, Bell JG, Rosenlund G, Henderson RJ, Graff IE, Tocher DR, Lie Ø, Sargent JR (2005) Tailoring of Atlantic salmon (Salmo salar L.) flesh lipid composition and sensory quality by replacing fish oil with a vegetable oil blend. J Agric Food Chem 53:10166–10178

    Article  PubMed  CAS  Google Scholar 

  3. Sargent J, McEvoy L, Estevez A, Bell G, Bell M, Henderson J, Tocher DR (1999) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 179:217–229

    Article  CAS  Google Scholar 

  4. Bell JG, McEvoy J, Tocher DR, McGhee F, Campbell PJ, Sargent JR (2001) Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J Nutr 131:1535–1543

    PubMed  CAS  Google Scholar 

  5. Bell JG, Henderson RJ, Tocher DR, Sargent JR (2004) Replacement of dietary fish oil with increasing levels of linseed oil: modification of flesh fatty acid compositions in Atlantic salmon (Salmo salar) using a fish oil finishing diet. Lipids 39:223–232

    Article  PubMed  CAS  Google Scholar 

  6. Trattner S, Kamal-Eldin A, Brännäs E, Moazzami AA, Žlábek V, Larsson P, Ruyter B, Gjøen T, Pickova J (2008) Sesamin supplementation increases white muscle docosahexaenoic acid (DHA) levels in rainbow trout (Oncorhynchus mykiss) fed high alpha-linolenic acid (ALA) containing vegetable oil: metabolic actions. Lipids 43:989–997

    Article  PubMed  CAS  Google Scholar 

  7. Trattner S, Pickova J, Park KH, Rinchard J, Dabrowski K (2007) Effects of alpha-lipoic and ascorbic acid on the muscle and brain fatty acids and antioxidant profile of the South American pacu Piaractus mesopotamicus. Aquaculture 273:158–164

    Article  CAS  Google Scholar 

  8. Trattner S, Ruyter B, Ostbye TK, Gjøen T, Zlabek V, Kamal-Eldin A, Pickova J (2008) Sesamin increases alpha-linolenic acid conversion to docosahexaenoic acid in Atlantic salmon (Salmo salar L.) hepatocytes: role of altered gene expression. Lipids 43:999–1008

    Article  PubMed  CAS  Google Scholar 

  9. Kennedy SR, Bickerdike R, Berge RK, Porter AR, Tocher DR (2007) Influence of dietary conjugated linoleic acid (CLA) and tetradecylthioacetic acid (TTA) on growth, lipid composition and key enzymes of fatty acid oxidation in liver and muscle of Atlantic cod (Gadus morhua L.). Aquaculture 264:372–382

    Article  CAS  Google Scholar 

  10. Vegusdal A, Gjøen T, Berge RK, Thomassen MS, Ruyter B (2005) Effect of 18:1n–9, 20:5n–3, and 22:6n–3 on lipid accumulation and secretion by Atlantic salmon hepatocytes. Lipids 40:477–486

    Article  PubMed  CAS  Google Scholar 

  11. Vegusdal A, Østbye T-K, Tran TN, Gjøen T, Ruyter B (2004) β-Oxidation, esterification, and secretion of radiolabeled fatty acids in cultivated Atlantic salmon skeletal muscle cells. Lipids 39:649–658

    Article  PubMed  CAS  Google Scholar 

  12. Buzzi M, Henderson RJ, Sargent JR (1996) The desaturation and elongation of linolenic acid and eicosapentaenoic acid by hepatocytes and liver microsomes from rainbow trout (Oncorhynchus mykiss) fed diets containing fish oil or olive oil. Biochim Biophys Acta Lipids Lipid Metab 1299:235–244

    Article  Google Scholar 

  13. Tocher DR, Dick JR (1990) Polyunsaturated fatty acid metabolism in cultured fish cells: incorporation and metabolism of (n-3) and (n-6) series acids by Atlantic salmon (Salmo salar) cells. Fish Physiol Biochem 8:311–319

    Article  CAS  Google Scholar 

  14. Buzzi M, Henderson RJ, Sargent JR (1997) Biosynthesis of docosahexaenoic acid in trout hepatocytes proceeds via 24-carbon intermediates. Comp Biochem Physiol B: Biochem Mol Biol 116:263–267

    Article  CAS  Google Scholar 

  15. Bell MV, Dick JR, Porter AEA (2001) Biosynthesis and tissue deposition of docosahexaenoic acid (22:6n–3) in rainbow trout (Oncorhynchus mykiss). Lipids 36:1153–1159

    Article  PubMed  CAS  Google Scholar 

  16. 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 11:627–639

    Article  PubMed  CAS  Google Scholar 

  17. Hastings N, Agaba MK, Tocher DR, Zheng X, Dickson CA, Dick JR, Teale AJ (2004) 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 6:463–474

    Article  PubMed  CAS  Google Scholar 

  18. Trattner S, Ruyter B, Ostbye TK, Kamal-Eldin A, Moazzami A, Pan J, Gjoen T, Brannas E, Zlabek V, Pickova J (2011) Influence of dietary sesamin, a bioactive compound on fatty acids and expression of some lipid regulating genes in Baltic Atlantic salmon (Salmo salar L.) juveniles. Physiol Res 60:125–137

    PubMed  CAS  Google Scholar 

  19. Ide T, Nakashima Y, Iida H, Yasumoto S, Katsuta M (2009) Lipid metabolism and nutrigenomics—Impact of sesame lignans on gene expression profiles and fatty acid oxidation in rat liver. Forum Nutr 61:10–24

    Article  PubMed  CAS  Google Scholar 

  20. Ashakumary L, Rouyer I, Takahashi Y, Ide T, Fukuda N, Aoyama T, Hashimoto T, Mizugaki M, Sugano M (1999) Sesamin, a sesame lignan, is a potent inducer of hepatic fatty acid oxidation in the rat. Metab Clin Exp 48:1303–1313

    Article  PubMed  CAS  Google Scholar 

  21. Lim JS, Adachi Y, Takahashi Y, Ide T (2007) Comparative analysis of sesame lignans (sesamin and sesamolin) in affecting hepatic fatty acid metabolism in rats. Br J Nutr 97:85–95

    Article  PubMed  CAS  Google Scholar 

  22. Kiso Y, Tsuruoka N, Kidokoro A, Matsumoto I, Abe K (2005) Sesamin ingestion regulates the transcription levels of hepatic metabolizing enzymes for alcohol and lipids in rats. Alcoholism Clin Exp Res 29:116S–120S

    Article  CAS  Google Scholar 

  23. Tsuruoka N, Kidokoro A, Matsumoto I, Abe K, Kiso Y (2005) Modulating effect of sesamin, a functional lignan in sesame seeds, on the transcription levels of lipid- and alcohol-metabolizing enzymes in rat liver: a DNA microarray study. Biosci Biotechnol Biochem 69:179–188

    Article  PubMed  CAS  Google Scholar 

  24. Kiso Y (2004) Antioxidative roles of sesamin, a functional lignan in sesame seed, and it’s effect on lipid- and alcohol-metabolism in the liver: a DNA microarray study. BioFactors 21:191–196

    Article  PubMed  CAS  Google Scholar 

  25. Kushiro M, Masaoka T, Hageshita S, Takahashi Y, Ide T, Sugano M (2002) Comparative effect of sesamin and episesamin on the activity and gene expression of enzymes in fatty acid oxidation and synthesis in rat liver. J Nutr Biochem 13:289–295

    Article  PubMed  CAS  Google Scholar 

  26. Fujiyamafujiwara Y, Umedasawada R, Kuzuyama M, Igarashi O (1995) Effects of sesamin on the fatty-acid composition of the liver of rats fed N-6 and N-3 fatty acid-rich diet. J Nutr Sci Vitam 41:217–225

    Article  CAS  Google Scholar 

  27. Arachchige PG, Takahashi Y, Ide T (2006) Dietary sesamin and docosahexaenoic and eicosapentaenoic acids synergistically increase the gene expression of enzymes involved in hepatic peroxisomal fatty acid oxidation in rats. Metabolism Clin Exp 55:381–390

    Article  CAS  Google Scholar 

  28. LeMoine CMR, Genge CE, Moyes CD (2008) Role of the PGC-1 family in the metabolic adaptation of goldfish to diet and temperature. J Exp Biol 211:1448–1455

    Article  PubMed  CAS  Google Scholar 

  29. McGarry JD, Brown NF (1997) The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem 244:1–14

    Article  PubMed  CAS  Google Scholar 

  30. Varanasi U, Chu R, Huang Q, Castellon R, Yeldandi AV, Reddy JK (1996) Identification of a peroxisome proliferator-responsive element upstream of the human peroxisomal fatty acyl coenzyme A oxidase gene. J Biol Chem 271:2147–2155

    Article  PubMed  CAS  Google Scholar 

  31. Boukouvala E, Leaver MJ, Favre-Krey L, Theodoridou M, Krey G (2010) Molecular characterization of a gilthead sea bream (Sparus aurata) muscle tissue cDNA for carnitine palmitoyltransferase 1B (CPT1B). Comp Biochem Physiol B: Biochem Mol Biol 157:189–197

    Article  Google Scholar 

  32. 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 9:299

    Article  PubMed  Google Scholar 

  33. Zhou J, Febbraio M, Wada T, Zhai Y, Kuruba R, He J, Lee JH, Khadem S, Ren S, Li S et al (2008) Hepatic fatty acid transporter Cd36 is a common target of LXR, PXR, and PPAR[gamma] in promoting steatosis. Gastroenterology 134(556–567):e551

    Google Scholar 

  34. Cruz-Garcia L, Minghetti M, Navarro I, Tocher DR (2009) Molecular cloning, tissue expression and regulation of liver X Receptor (LXR) transcription factors of Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B: Biochem Mol Biol 153:81–88

    Article  CAS  Google Scholar 

  35. Carmona-Antoñanzas G, Monroig Ó, Dick JR, Davie A, Tocher DR (2011) Biosynthesis of very long-chain fatty acids (C > 24) in Atlantic salmon: cloning, functional characterisation, and tissue distribution of an Elovl4 elongase. Comp Biochem Physiol B: Biochem Mol Biol 159:122–129

    Article  Google Scholar 

  36. Kleveland EJ, Syvertsen BL, Ruyter B, Vegusdal A, Jørgensen SM, Gjøen T (2006) Characterization of scavenger receptor class B, type I in Atlantic salmon (Salmo salar L.). Lipids 71:1017–1027

    Article  Google Scholar 

  37. Zhou J, Stubhaug I, Torstensen BE (2010) Trans-membrane uptake and intracellular metabolism of fatty acids in Atlantic salmon (Salmo salar L.) hepatocytes. Lipids 45:301–311

    Article  PubMed  CAS  Google Scholar 

  38. Brannas E, Chaix T, Nilsson J, Eriksson LO (2005) Has a 4-generation selection programme affected the social behaviour and growth pattern of Arctic charr (Salvelinus alpinus)? Appl Anim Behav Sci 94:165–178

    Article  Google Scholar 

  39. Busacker GP, Adelman IR, Goolish EM (1990) Growth. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 363–388

  40. Pickova J, Dutta PC, Larsson PO, Kiessling A (1997) Early embryonic cleavage pattern, hatching success, and egg-lipid fatty acid composition: comparison between two cod (Gadus morhua) stocks. Can J Fish Aquat Sci 54:2410–2416

    CAS  Google Scholar 

  41. Appelqvist L-Å (1968) Rapid methods of lipid extraction and fatty acid methyl ester preparation for seed and leaf tissue with special remarks on preventing the accumulation of lipid contaminants. Arkiv För Kemi 28:551–570

    CAS  Google Scholar 

  42. Eriksson SF, Pickova J (2007) Fatty acids and tocopherol levels in M-Longissimus dorsi of beef cattle in Sweden—A comparison between seasonal diets. Meat Sci 76:746–754

    Article  Google Scholar 

  43. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  44. Nelder JA, Wedderburn RWM (1972) Generalized Linear Models. J R Stat Soc Ser A (General) 135:370–384

    Article  Google Scholar 

  45. Torstensen BE, Øyvind L, Frøyland L (2000) Lipid metabolism and tissue composition in Atlantic salmon (Salmo salar L.)—Effects of capelin oil, palm oil, and oleic acid-enriched sunflower oil as dietary lipid sources. Lipids 35:653–664

    Article  PubMed  CAS  Google Scholar 

  46. Trattner S, Ruyter B, Østbye TK, Kamal-Eldin A, Moazzami A, Pan J, Gjøen T, Brännäs E, Zlabek V, Pickova J (2011) Influence of dietary sesamin, a bioactive compound on fatty acids and expression of some lipid regulating genes in Baltic Atlantic salmon (Salmo salar L.) juveniles. Physiol Res 60:125–137

    PubMed  CAS  Google Scholar 

  47. Mraz J, Schlechtriem C, Olohan LA, Fang YX, Cossins AR, Zlabek V, Samuelsen T, Pickova J (2010) Sesamin as a potential modulator of fatty acid composition in common carp (Cyprinus carpio). Aquac Res 41:e851–e861

    Article  CAS  Google Scholar 

  48. Kleveland EJ, Ruyter B, Vegusdal A, Sundvold H, Berge RK, Gjøen T (2006) Effects of 3-thia fatty acids on expression of some lipid related genes in Atlantic salmon (Salmo salar L.). Comp Biochem Physiol B: Biochem Mol Biol 145:239–248

    Article  Google Scholar 

  49. Moya-Falcón C, Hvattum E, Dyrøy E, Skorve J, Stefansson SO, Thomassen MS, Jakobsen JV, Berge RK, Ruyter B (2004) Effects of 3-thia fatty acids on feed intake, growth, tissue fatty acid composition, β-oxidation and Na+, K+ -ATPase activity in Atlantic salmon. Comp Biochem Physiol B: Biochem Mol Biol 139:657–668

    Article  Google Scholar 

  50. Zheng X, Seiliez I, Hastings N, Tocher DR, Panserat S, Dickson CA, Bergot P, Teale A (2004) Characterization and comparison of fatty acyl Delta 6 desaturase cDNAs from freshwater and marine teleost fish species. Comp Biochem Physiol B-Biochem Mol Biol 139:269–279

    Article  PubMed  CAS  Google Scholar 

  51. Sargent JR, Tacon AGJ (1999) Development of farmed fish: a nutritionally necessary alternative to meat. Proc Nutr Soc 58:377–383

    Article  PubMed  CAS  Google Scholar 

  52. Sales J (2010) Quantification of the differences in flesh fatty acid components between farmed and wild fish. J Aquat Food Prod Technol 19:298–309

    Article  CAS  Google Scholar 

  53. Andersen Ø, Eijsink VGH, Thomassen M (2000) Multiple variants of the peroxisome proliferator-activated receptor (PPAR) [gamma] are expressed in the liver of Atlantic salmon (Salmo salar). Gene 255:411–418

    Article  PubMed  CAS  Google Scholar 

  54. Burri L, Thoresen GH, Berge RK (2010) The role of PPARα activation in liver and muscle. PPAR Res 2010, article ID 542359

  55. Motojima K, Passilly P, Peters JM, Gonzalez FJ, Latruffe N (1998) Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor α and γ activators in a tissue- and inducer-specific manner. J Biol Chem 273:16710–16714

    Article  PubMed  CAS  Google Scholar 

  56. Poirier H, Niot I, Monnot MC, Braissant O, Meunier-Durmort C, Costet P, Pineau T, Wahli W, Willson TM, Besnard P (2001) Differential involvement of peroxisome-proliferator-activated receptors α and δ in fibrate and fatty-acid-mediated inductions of the gene encoding liver fatty-acid-binding protein in the liver and the small intestine. Biochem J 355:481–488

    Article  PubMed  CAS  Google Scholar 

  57. Qin YF, Dalen KT, Gustafsson J-Å, Nebb HI (2009) Regulation of hepatic fatty acid elongase 5 by LXRα-SREBP-1c. Biochim Biophys Acta Mol Cell Biol Lipids 1791:140–147

    Article  CAS  Google Scholar 

  58. Matsuzaka T, Shimano H, Yahagi N, Amemiya-Kudo M, Yoshikawa T, Hasty AH, Tamura Y, Osuga JI, Okazaki H, Iizuka Y et al (2002) Dual regulation of mouse Δ5- and Δ6-desaturase gene expression by SREBP-1 and PPARα. J Lipid Res 43:107–114

    PubMed  CAS  Google Scholar 

  59. Jeng KCG, Hou RCW (2005) Sesamin and sesamolin: nature’s Therapeutic Lignans. Curr Enzyme Inhib 1:11–20

    Article  CAS  Google Scholar 

  60. 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

    Article  PubMed  Google Scholar 

  61. Tocher DR, Bell JG, MacGlaughlin P, McGhee F, Dick JR (2001) Hepatocyte fatty acid desaturation and polyunsaturated fatty acid composition of liver in salmonids: effects of dietary vegetable oil. Comp Biochem Physiol B-Biochem Mol Biol 130:257–270

    Article  PubMed  CAS  Google Scholar 

  62. Jorgensen SM, Kleveland EJ, Grimholt U, Gjoen T (2006) Validation of reference genes for real-time polymerase chain reaction studies in Atlantic salmon. Mar Biotechnol 8:398–408

    Article  PubMed  CAS  Google Scholar 

  63. Bahuaud D, Mørkøre T, Østbye TK, Veiseth-Kent E, Thomassen MS, Ofstad R (2010) Muscle structure responses and lysosomal cathepsins B and L in farmed Atlantic salmon (Salmo salar L.) pre- and post-rigor fillets exposed to short and long-term crowding stress. Food Chem 118:602–615

    Article  CAS  Google Scholar 

  64. Castro V, Grisdale-Helland B, Helland SJ, Kristensen T, Jørgensen SM, Helgerud J, Claireaux G, Farrell AP, Krasnov A, Takle H (2011) Aerobic training stimulates growth and promotes disease resistance in Atlantic salmon (Salmo salar). Comp Biochem Physiol Mol Integr Physiol 160:278–290

    Article  CAS  Google Scholar 

  65. Minghetti M, Leaver MJ, Tocher DR (2011) Transcriptional control mechanisms of genes of lipid and fatty acid metabolism in the Atlantic salmon (Salmo salar L.) established cell line, SHK-1. Biochim Biophys Acta Mol Cell Biol Lipids 1811:194–202

    Article  CAS  Google Scholar 

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Correspondence to L. Wagner.

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A. Schiller Vestergren and L. Wagner contributed equally.

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Schiller Vestergren, A., Wagner, L., Pickova, J. et al. Sesamin Modulates Gene Expression Without Corresponding Effects on Fatty acids in Atlantic Salmon (Salmo salar L.). Lipids 47, 897–911 (2012). https://doi.org/10.1007/s11745-012-3697-7

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