Skip to main content
Log in

Fatty Acid-Specific Alterations in Leptin, PPARα, and CPT-1 Gene Expression in the Rainbow Trout

  • Original Article
  • Published:
Lipids

Abstract

It is known that fatty acids (FA) regulate lipid metabolism by modulating the expression of numerous genes. In order to gain a better understanding of the effect of individual FA on lipid metabolism related genes in rainbow trout (Oncorhynchus mykiss), an in vitro time-course study was implemented where twelve individual FA (butyric 4:0; caprylic 8:0; palmitic (PAM) 16:0; stearic (STA) 18:0; palmitoleic16:1n-7; oleic 18:1n-9; 11-cis-eicosenoic 20:1n-9; linoleic (LNA) 18:2n-6; α-linolenic (ALA) 18:3n-3; eicosapentenoic (EPA) 20:5n-3; docosahexaenoic (DHA) 22:6n-3; arachidonic (ARA) 20:4n-6) were incubated in rainbow trout liver slices. The effect of FA administration over time was evaluated on the expression of leptin, PPARα and CPT-1 (lipid oxidative related genes). Leptin mRNA expression was down regulated by saturated fatty acids (SFA) and LNA, and was up regulated by monounsaturated fatty acids (MUFA) and long chain PUFA, whilst STA and ALA had no effect. PPARα and CPT-1mRNA expression were up regulated by SFA, MUFA, ALA, ARA and DHA; and down regulated by LNA and EPA. These results suggest that there are individual and specific FA induced modifications of leptin, PPARα and CPT-1 gene expression in rainbow trout, and it is envisaged that such results may provide highly valuable information for future practical applications in fish nutrition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ALA:

α-Linolenic acid

ARA:

Arachidonic acid

ATP:

Adenosine triphosphate

CPT:

Carnitine palmitoyl-transferase

DHA:

Docosahexaenoic acid

EPA:

Eicosapentenoic acid

FA:

Fatty acids

LNA:

Linoleic acid

MUFA:

Monounsaturated fatty acids

OLA:

Oleic acid

PPAR:

Peroxisome proliferator-activated receptors

PUFA:

Polyunsaturated fatty acids

SFA:

Saturated fatty acids

STA:

Stearic acid

References

  1. Tacon AGJ, Forster IP (2003) Aquafeeds and the environment: policy implications (Conference Paper). Aquaculture 226:181–189

    Article  Google Scholar 

  2. Turchini GM, Torstensen BE, Ng W-K (2009) Fish oil replacement in finfish nutrition. Rev Aquac 1(1):10–57

    Article  Google Scholar 

  3. Torstensen BE, Tocher DR (2011) The effects of fish oil replacement on lipid metabolism of fish. In: Turchini GM, Ng W-K, Tocher DR (eds) Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Taylor and Francis Group, USA, pp 405–437

    Google Scholar 

  4. Sargent JR, Henderson RJ and Tocher DR (2002) The lipids. In: Halver JE and Hardy RW (eds) Fish nutrition. Academic Press, Elsevier USA, pp 181–257

  5. Jordal A-EO, Torstensen BE, Tsoi S, Tocher DR, Lall SP, Douglas SE (2005) Dietary rapeseed oil affects the expression of genes involved in hepatic lipid metabolism in Atlantic salmon (Salmo salar L). J Nutr 135:2355–2361

    PubMed  CAS  Google Scholar 

  6. Kennedy SR, Bickerdike R, Berge RK, Dick JR, Tocher DR (2007) Influence of conjugated linoleic acid (CLA) or tetradecylthio acetic acid (TTA) on growth, lipid composition, fatty acid metabolism and lipid gene expression of rainbow trout (Oncorhynchus mykiss L). Aquaculture 272:489–501

    Article  CAS  Google Scholar 

  7. Kjær MA, Todorčević M, Torstensen BE, Vegusdal A, Ruyter B (2008) Dietary n-3 HUFA affects mitochondrial fatty acid β-oxidation capacity and susceptibility to oxidative stress in Atlantic salmon. J Lipids 43:813–827

    Article  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`) hepatocytes: role of altered gene expression. J Lipids 43:999–1008

    Article  CAS  Google Scholar 

  9. Torstensen BE, Nanton DA, Olsvik PA, Sundvold H, Stubhaug I (2009) Gene expression of fatty acid binging proteins, fatty acid transport proteins (cd36 and FATP) and b-oxidation-related genes in Atlantic salmon (Salmo salar L) fed fish oil or vegetable oil. Aquac Nutr 15:440–451

    Article  CAS  Google Scholar 

  10. Martins DA, Rocha F, Martínez-Rodríguez G, Bell G, Morais S, Castanheira F, Bandarra N, Coutinho J, Yúfera M, Conceição LEC (2012) Teleost fish larvae adapt to dietary arachidonic acid supply through modulation of the expression of lipid metabolism and stress response genes. Br J Nutr 108:864–874

    Article  Google Scholar 

  11. Figueiredo-Silva C, Kaushik A, Terrier S, Schrama F, Médale JW, Geurden FI (2012) Link between lipid metabolism and voluntary food intake in rainbow trout fed coconut oil rich in medium-chain TAG. Br J Nutr 107:1714–1725

    Article  PubMed  CAS  Google Scholar 

  12. Zuo R, Ai Q, Mai K, Xu W (2013) Effects of conjugated linoleic acid on growth, non-specific immunity, antioxidant capacity, lipid deposition and related gene expression in juvenile large yellow croaker (Larmichthyscrocea) fed soyabean oil-based diets. Br J Nutr 110:1220–1232

    Article  PubMed  CAS  Google Scholar 

  13. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425

    Article  PubMed  CAS  Google Scholar 

  14. Huising MO, Geven EJ, Kruiswijk CP, Nabuurs SB, Stolte EH, Spanings FA, Verburg-van Kemenade BM, Flik G (2006) Increased leptin expression in common carp (Cyprinus carpio) after food intake but not after fasting or feeding to satiation. Endocrinology 147:5786

    Article  PubMed  CAS  Google Scholar 

  15. Luckman S (2007) Endocrinology of feeding and nutrition. Gen Comp Endocrinol 152:223

    Article  PubMed  CAS  Google Scholar 

  16. Buono S, Putti R (2010) Leptin effects on energy metabolism in non-mammalian vertebrates. In: Paolucci M (ed) Leptin in non-mammalian vertebrates. Transworld Research Network, Trivandrum pp 125–150

  17. Paolucci M (2010) Leptin reproduction in non mammalian vertebrates. In: Paolucci M (ed) Leptin in non-mammalian vertebrates. Transworld Research Network, Trivandrum-695 023, Kerala, India pp 107–123

  18. Mariano G, Stilo R, Terrazzano G, Coccia E, Vito P, Varricchio E, Paolucci M (2013) Effects of recombinant trout leptin in superoxide production and NF-kB/MAPK phosphorylation in blood leukocytes. Pept 48:59–69

    Article  CAS  Google Scholar 

  19. Siegrist-Kaiser CA, Pauli V, Juge-Aubry CE, Boss O, Pernin A, Chin WW, Cusin I, Rohner-Jeanrenaud F, Burger AJ, Zapf J, Meier CA (1997) Direct effects of leptin on brown and white adipose tissue. J Clin Invest 100:2858–2864

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  20. Minokoshi Y, Kim Y-B, Peroni OD, Fryer LGD, Müller C, Carling D, Kahn BB (2002) Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415:339–343

    Article  PubMed  CAS  Google Scholar 

  21. Wang Y, Barton BA, Thim L, Nielsen PF, Conlon JM (1999) Purification and characterization of galanin and scyliorhinin I from the hybrid sturgeon, Scaphirhynchus platorynchus × Scaphirhynchus albus (Acipenseriformes). Gen Comp Endocrinol 113:38–45

    Article  PubMed  CAS  Google Scholar 

  22. Morash AJ, Kajimura M, McClelland GB (2008) Intertissue regulation of carnitine palmitoyl transferase I (CPTI): mitochondrial membrane properties and gene expression in rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta 1778:1382–1389

    Article  PubMed  CAS  Google Scholar 

  23. Morash AJ, Bureau DP, McClelland GB (2009) Effects of dietary fatty acid composition on the regulation of carnitine palmitoyl transferase (CPT) I in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B 152:85–93

    Article  PubMed  Google Scholar 

  24. Morash AJ, McClelland GB (2011) Regulation of carnitine palmitoyl transferase (CPT) I during fasting in rainbow trout (Oncorhynchus mykiss) promotes increased mitochondrial fatty acid oxidation. Physiol Biochem Zool 84:625–633

    Article  PubMed  CAS  Google Scholar 

  25. Cho HK, Kong HJ, Kim HY, Cheong J (2012) Characterization of Paralichthys olivaceus peroxisome proliferator-activated receptor-α gene as a master regulator of flounder lipid metabolism. Gen Comp Endocr 175:39–47

    Article  PubMed  CAS  Google Scholar 

  26. Taylor JS, Braash I, Frickey T, Meyer A, Van de Peer Y (2003) Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13:382–390

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  27. Morash AJ, LeMoine CMR, McClelland GB (2010) Genome duplication events have led to a diversification in the CPT1 gene family in fish. Am J Physiol Regul Integr Comp Physiol 229:R579–R589

    Article  Google Scholar 

  28. Leaver MJ, Boukouvala E, Antonopoulou E, Diez A, Favre-Krey L, Tariq Ezaz M, Bautista JM, Tocher DR, Krey G (2005) Three peroxisome proliferator-activated receptor isotypes from each of two species of marine fish. Endocrinology 146:3150–3162

    Article  PubMed  CAS  Google Scholar 

  29. Urbatzka R, Galante-Oliveira S, Rocha E, Castro LFC, Cunha I (2013) Tissue expression of PPAR-alpha isoforms in Scophthalmus maximus and transcriptional response of target genes in the heart after exposure to WY-14643. Fish Physiol Biochem 39:1043–1055

    Article  PubMed  CAS  Google Scholar 

  30. Batista-Pinto C, Rodrigues P, Rocha E, Lobo-da-Cunha A (2005) Identification and organ expression of peroxisome proliferator activated receptors in brown trout (Salmo trutta f. fario). Biochim Biophys Acta 1731:88–94

    Article  PubMed  CAS  Google Scholar 

  31. Panserat S, Ducasse-Cabanot S, Plagnes-Juan E, Srivastava PP, Koldiz C, Piumi F, Esquerre D, Kaushik S (2008) Dietary fat liver modifies the expression of hepatic genes in juvenile rainbow trout (Oncorhynchus mykiss) as revealed by microarray analysis. Aquaculture 275:235–241

    Article  CAS  Google Scholar 

  32. Kolditz C, Borthaire M, Richard N, Corraze G, Panserat S, Vachot C, Lefevre F, Medale F (2008) Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 294:R1154–R1164

    Article  PubMed  CAS  Google Scholar 

  33. Mennigen JA, Panserat S, Larquier M, Plagnes-Juan E, Seiliez I, Medale F, Skiba-Cassy S (2012) Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout. PLoS One 7(6):e38604. doi:10.1371/journal.pone.0038604

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  34. Vestergren ALS, Trattner S, Pan J, Johnsson P, Kamal-Eldin A, Brännäs E, Moazzami AA, Pickova J (2013) The effect of combining linseed oil and sesamin on the fatty acid composition in white muscle and on expression of lipid-related genes in white muscle and liver of rainbow trout (Oncorhynchus mykiss). Aquac Int 21:843–859

    Article  CAS  Google Scholar 

  35. Lansard M, Panserat S, Seiliez I, Polakof S, Plagnes-Juan E, Geurden I, Médale F, Kaushik S, Corraze G (2009) Hepatic protein kinase B (Akt)-target of rapamycin (TOR)-signalling pathways and intermediary metabolism in rainbow trout (Oncorhynchus mykiss) are not significantly affected by feeding plant-based diets. Br J Nutr 102:1564–1573

    Article  PubMed  CAS  Google Scholar 

  36. Morais S, Silva T, Cordeiro O, Rodrigues P, Guy DR, Bron JE, 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 (Salmo salar). BMC Genom 13:448

    Article  CAS  Google Scholar 

  37. Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR (2011) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genom 12:255

    Article  CAS  Google Scholar 

  38. Shilling AD, Williams DE (2000) The non-aromatizable androgen, dihydrotestosterone, induces antiestrogenic responses in the rainbow trout. J Steroid Biochem Mol Biol 74:187–194

    Article  PubMed  CAS  Google Scholar 

  39. Leger C, Fremont L, Marion D, Nassour I, Desfarges M-F (1981) Essential fatty acids in trout serum lipoproteins, vitellogenin and egg lipid. J Lipids 16:593–598

    Article  CAS  Google Scholar 

  40. Murashita K, Uji S, Yamamoto T, Rønnestad I, Kurokawa T (2008) Production of recombinant leptin and its effects on food intake in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B: Biochem Mol Biol 150:377–384

    Article  Google Scholar 

  41. Francis DS, Thanuthong T, Senadheera SPSD, Paolucci M, Coccia E, De Silva SS, Turchini GM (2014) n-3 LC-PUFA deposition efficiency and appetite regulating hormones are modulated by the dietary lipid source during rainbow trout grow-out and finishing periods. Fish Physiol Biochem 40:577–593

    Article  PubMed  CAS  Google Scholar 

  42. Varricchio E, Russo F, Coccia E, Turchini G, Francis D, De Girolamo P, Paolucci M (2012) Immunohistochemical and immunological detection of ghrelin and leptin in rainbow trout (Oncorhynchus Mykiss) and Murray cod (Maccullochella peelii peelii) as affected by different dietary fatty acids. Microsc Res Tech 75:771–780

    Article  Google Scholar 

  43. Cammisotto PG, Gelinas Y, Deshaies Y, Bukowiecki LJ (2003) Regulation of leptin secretion from white adipocytes by free fatty acids. Am J Physiol Endocrinol Metab 285:E521–E526

    PubMed  CAS  Google Scholar 

  44. Shintani M, Nishimura H, Yonemitsu S, Masuzaki H, Ogawa Y, Hosoda K, Inoue G, Yoshimasa T, Nakao K (2000) Down regulation of leptin by free fatty acids in rat adipocytes: effects of triacsin C, palmitate, and 2-bromopalmitate. Metab Clin Exp 49:326–330

    Article  PubMed  CAS  Google Scholar 

  45. Reseland JE, Haugen F, Hollung K, Solvoll K, Halvorsen B, Brude IR, Nenseter MS, Christiansen EN, Drevon CA (2001) Reduction of leptin gene expression by dietary polyunsaturated fatty acids. J Lipid Res 42:743–750

    PubMed  CAS  Google Scholar 

  46. Li G-G, Liang X-F, Xie Q, Li G, Yu Y, Lai K (2010) Gene structure, recombinant expression and functional characterization of grass carp leptin. Gen Comp Endocrinol 166:117–127

    Article  PubMed  CAS  Google Scholar 

  47. Emery JA, Smullen RP, Turchini GM (2014) Tallow in Atlantic salmon feed. Aquaculture 422–423:98–108

    Article  Google Scholar 

  48. Libran-Perez M, Figueired-Silva C, Panserat S, Geurden I, Minguez JM, Polakof S, Soengas J (2013) Response of hepatic lipid and glucose metabolism to a mixture or single fatty acids: possible presence of fatty acid-sensing mechanisms. Comp Biochem Physiol A 164:241–248

    Article  CAS  Google Scholar 

  49. Sampath H, Ntambi JM (2005) Polyunsaturated fatty acid regulation of genes of lipid metabolism. Annu Rev Nutr 25:317–340

    Article  PubMed  CAS  Google Scholar 

  50. Muhlhausler BS, Cook-Johnson R, James M, Miljkovic D, Duthoit E, Gibson R (2010) Opposing effects of omega-3 and omega-6 long chain polyunsaturated fatty acids on the expression of lipogenic genes in omental and retroperitoneal adipose depots in the rat. J Nutr Metab 927836:14

    Google Scholar 

  51. Alvarez MJ, Díez M, López-Bote C, Gallego M, Bautista JM (2000) Short-term modulation of lipogenesis by macronutrients in rainbow trout (Oncorhynchus mykiss) hepatocytes. Br J Nutr 84:619–628

    PubMed  CAS  Google Scholar 

  52. Sprecher H (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta 1486:219–231

    Article  PubMed  CAS  Google Scholar 

  53. Hihi AK, Michalik L, Wahli W (2002) PPARs: transcriptional effectors of fatty acids and their derivatives. Cell Mol Life Sci 59:790–798

    Article  PubMed  CAS  Google Scholar 

  54. Pawar A, Jump DB (2003) Unsaturated fatty acid regulation of peroxisome proliferator activated receptor alpha activity in primary rat hepatocytes. J Biol Chem 278:35931–35939

    Article  PubMed  CAS  Google Scholar 

  55. Lee JY, Hwang DH (2002) Docosahexaenoic acid suppresses the activity of peroxisome proliferator-activated receptors in a colon tumor cell line. Biochem Biophys Res Commun 298:667–674

    Article  PubMed  CAS  Google Scholar 

  56. Deckelbaum RJ, Worgall TS, Seo T (2006) n-3 Fatty acids and gene expression1–4. Am J Clin Nutr 83:1520S–1525S

    PubMed  CAS  Google Scholar 

  57. Berge RK, Madsen L, Vaagenes H, Tronstad KJ, Gottlicher M, Rustan AC (1999) In contrast with docosahexaenoic acid, eicosapentaenoic acid and hypolipidemic derivatives decrease hepatic synthesis and secretion of triacylglycerol by decreased Diacylglycerol acyltransferase activity and stimulation of fatty acid oxidation. Biochem J 343:191–197

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  58. Turchini GM, Francis DS (2009) Fatty acid metabolism (desaturation, elongation and β-oxidation) in rainbow trout fed fish oil- or linseed oil-based diets. Br J Nutr 102:69–81

    Article  PubMed  CAS  Google Scholar 

  59. Codabaccus BM, Carterc CG, Bridlea AR, Nichols PD (2012) “The n-3 LC-PUFA sparing effect” of modified dietary n-3 LC-PUFA content and DHA to EPA ratio in Atlantic salmon smolt. Aquaculture 356–357:135–140

    Article  Google Scholar 

  60. Trushenski J, Schwarz M, Bergmana A, Rombenso A, Delbos B (2012) DHA is essential, EPA appears largely expendable, in meeting the n-3 long-chain polyunsaturated fatty acid requirements of juvenile cobia Rachycentron canadum. Aquaculture 326–329:81–89

    Article  Google Scholar 

  61. Glencross BD, Tocher DR, Matthew C, Bell JG (2014) Interactions between dietary docosahexaenoic acid and other long-chain polyunsaturated fatty acids on performance and fatty acid retention in post-smolt Atlantic salmon (Salmo salar). Fish Physiol Biochem 40(4):1213–1227

    PubMed  CAS  Google Scholar 

  62. Turchini GM, Nichols PD, Barrow C, Sinclair AJ (2012) Jumping on the omega-3 bandwagon: distinguishing the role of long-chain and short-chain omega-3 fatty acids. Crit Rev Food Sci Nutr 52:795–803

    Article  PubMed  CAS  Google Scholar 

  63. Henderson RJ, Sargent JR (1985) Fatty acid metabolism in fish. In: Cowey CB, Mackie AM, Bell JG (eds) Nutrition and feeding in fish. Acad Press, London, pp 349–364

    Google Scholar 

  64. Menoyo D, Lopez-Bote CJ, Bautista JM, Obach A (2003) Growth, digestibility and fatty acids utilization in large Atlantic salmon (Salmo salar) fed varying levels of n-3 and saturated fatty acids. Aquaculture 225:295–307

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by research funds (FRA) from the MIUR and University of Sannio. Elena Coccia was a recipient of a postdoctoral fellowship from the University of Sannio.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marina Paolucci.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coccia, E., Varricchio, E., Vito, P. et al. Fatty Acid-Specific Alterations in Leptin, PPARα, and CPT-1 Gene Expression in the Rainbow Trout. Lipids 49, 1033–1046 (2014). https://doi.org/10.1007/s11745-014-3939-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-014-3939-y

Keywords

Navigation