Skip to main content Accessibility help
×
Home

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

  • Marine Lansard (a1) (a2) (a3), Stéphane Panserat (a1) (a2) (a3), Iban Seiliez (a1) (a2) (a3), Sergio Polakof (a1) (a2) (a3) (a4), Elisabeth Plagnes-Juan (a1) (a2) (a3) (a4), Inge Geurden (a1) (a2) (a3), Françoise Médale (a1) (a2) (a3), Sadasivam Kaushik (a1) (a2) (a3), Geneviève Corraze (a1) (a2) (a3) and Sandrine Skiba-Cassy (a1) (a2) (a3)...

Abstract

The aim of the present study was to analyse the effects of partial or total replacement of fish meal (FM) and fish oil (FO) by a mixture of plant protein (PP) and a mixture of vegetable oils (VO) on the hepatic insulin–nutrient-signalling pathway and intermediary metabolism-related gene expression in rainbow trout (Oncorhynchus mykiss). Triplicate groups of fish were fed four practical diets containing graded levels of replacement of FM and FO by PP and VO for 12 weeks: diet 0/0 (100 % FM, 100 % FO); diet 50/50 (50 % FM and 50 % PP, 50 % FO and 50 % VO); diet 50/100 (50 % FM and 50 % PP, 100 % VO); diet 100/100 (100 % PP, 100 % VO). Samplings were performed on trout starved for 5 d then refed with their allocated diet. In contrast to partial substitution (diet 50/50), total substitution of FM and FO (diet 100/100) led to significantly lower growth compared with diet 0/0. The insulin–nutrient-signalling pathway (protein kinase B (Akt), target of rapamycin (TOR), S6 protein kinase 1 (S6K1) and S6) was characterised in trout liver and found to be activated by refeeding. However, changes in diet compositions did not differentially affect the Akt–TOR-signalling pathway. Moreover, expression of genes encoding fructose-1,6-biphosphatase, mitochondrial phosphoenolpyruvate carboxykinase, glucokinase, pyruvate kinase and carnitine palmitoyl transferase 1 were not affected by refeeding or by dietary changes. Refeeding down- and up-regulated the expression of gluconeogenic glucose-6-phosphatase isoform 1 and lipogenic fatty acid synthase genes, respectively. Expression of both genes was also increased with partial replacement of FM and total replacement of FO (diet 50/100). These findings indicate that plant-based diets barely affect glucose and lipid metabolism in trout.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      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
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      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
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      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
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Dr Sandrine Skiba-Cassy, fax +33 5 59 54 51 52, email skiba@st-pee.inra.fr

References

Hide All
1 Committee on Animal Nutrition, Board of Agriculture & National Research Council (1993) Nutrient Requirement of Fish. Washington, DC: National Academic Press.
2 Sargent, JR & Tacon, AG (1999) Development of farmed fish: a nutritionally necessary alternative to meat. Proc Nutr Soc 58, 377383.
3 Naylor, RL, Goldburg, RJ, Primavera, JH, et al. (2000) Effect of aquaculture on world fish supplies. Nature 405, 10171024.
4 New, MB & Wijkstroem, UN (2002) Use of Fishmeal and Fish Oil in Aquafeeds. Further Throughts on the Fishmeal Trap. Food and Agriculture Organization Fisheries Circular no. 975. Rome: FAO.
5 Gatlin, DM, Barrows, FT, Brown, P, et al. (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquaculture Res 38, 551579.
6 Francis, G, Makkar, HPS & Becker, K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199, 197227.
7 Bell, JG, Tocher, DR, Henderson, RJ, et al. (2003) Altered fatty acid compositions in Atlantic salmon (Salmo salar) fed diets containing linseed and rapeseed oils can be partially restored by a subsequent fish oil finishing diet. J Nutr 133, 27932801.
8 Glencross, BD, Hawkins, WE & Curnow, JG (2003) Restoration of the fatty acid composition of red seabream (Pagrus auratus) using a fish oil finishing diet after grow-out on plant oil based diets. Aquaculture Nutr 9, 409418.
9 Regost, C, Arzel, J, Cardinal, M, et al. (2003) Total replacement of fish oil by soybean or linseed oil with a return to fish oil in turbot (Psetta maxima) 2. Flesh quality properties. Aquaculture 220, 737747.
10 Bell, JG, Henderson, RJ, Tocher, DR, et al. (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, 222230.
11 Torstensen, BE, Lie, O & Froyland, 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, 653664.
12 Menoyo, D, Lopez-Bote, CJ, Obach, A, et al. (2005) Effect of dietary fish oil substitution with linseed oil on the performance, tissue fatty acid profile, metabolism, and oxidative stability of Atlantic salmon. J Anim Sci 83, 28532862.
13 Kaushik, SJ, Cravedi, JP, Lalles, JP, et al. (1995) Partial or total replacement of fish-meal by soybean protein on growth, protein-utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow-trout, Oncorhynchus-mykiss. Aquaculture 133, 257274.
14 Kaushik, SJ, Coves, D, Dutto, G, et al. (2004) Almost total replacement of fish meal by plant protein sources in the diet of a marine teleost, the European seabass, Dicentrarchus labrax. Aquaculture 230, 391404.
15 Gomez-Requeni, P, Mingarro, M, Calduch-Giner, JA, et al. (2004) Protein growth performance, amino acid utilisation and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 232, 493510.
16 Watanabe, T, Aoki, H, Shimamoto, K, et al. (1998) A trial to culture yellowtail with non-fishmeal diets. Fish Sci 64, 505512.
17 Watanabe, T, Verakunpiriya, V, Watanabe, K, et al. (1997) Feeding of rainbow trout with non-fish meal diets. Fish Sci 63, 258266.
18 Vilhelmsson, OT, Martin, SA, Medale, F, et al. (2004) Dietary plant-protein substitution affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss). Br J Nutr 92, 7180.
19 Panserat, S, Kolditz, C, Richard, N, et al. (2008) Hepatic gene expression profiles in juvenile rainbow trout (Oncorhynchus mykiss) fed fishmeal or fish oil-free diets. Br J Nutr 100, 953967.
20 Leaver, MJ, Villeneuve, LA, Obach, A, et al. (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.
21 Jordal, AE, Torstensen, BE, Tsoi, S, et al. (2005) Dietary rapeseed oil affects the expression of genes involved in hepatic lipid metabolism in Atlantic salmon (Salmo salar L.). J Nutr 135, 23552361.
22 Barrows, FT, Bellis, D, Krogdahl, ÃS, et al. (2008) Report of the Plant Products in Aquafeed Strategic Planning Workshop: an integrated, interdisciplinary research roadmap for increasing utilization of plant feedstuffs in diets for carnivorous fish. Rev Fish Sci 16, 449455.
23 Taniguchi, CM, Emanuelli, B & Kahn, CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7, 8596.
24 Barthel, A & Schmoll, D (2003) Novel concepts in insulin regulation of hepatic gluconeogenesis. Am J Physiol Endocrinol Metab 285, E685E692.
25 Sul, HS, Latasa, MJ, Moon, Y, et al. (2000) Regulation of the fatty acid synthase promoter by insulin. J Nutr 130, 315S320S.
26 Liao, J, Barthel, A, Nakatani, K, et al. (1998) Activation of protein kinase B/Akt is sufficient to repress the glucocorticoid and cAMP induction of phosphoenolpyruvate carboxykinase gene. J Biol Chem 273, 2732027324.
27 Schmoll, D (2000) Regulation of glucose-6-phosphatase gene expression by protein kinase Bα and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and -independent effects of insulin on promoter activity. Biol Chem 275, 3632436333.
28 Dentin, R, Denechaud, P-D, Benhamed, F, et al. (2006) Hepatic gene regulation by glucose and polyunsaturated fatty acids: a role for ChREBP. J Nutr 136, 11451149.
29 Tremblay, F, Lavigne, C, Jacques, H, et al. (2007) Role of dietary proteins and amino acids in the pathogenesis of insulin resistance. Annu Rev Nutr 27, 293310.
30 Wullschleger, S, Loewith, R & Hall, MN (2006) TOR signaling in growth and metabolism. Cell 124, 471484.
31 Porstmann, T, Santos, CR, Griffiths, B, et al. (2008) SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 8, 224236.
32 Plagnes-Juan, E, Lansard, M, Seiliez, I, et al. (2008) Insulin regulates the expression of several metabolism-related genes in the liver and primary hepatocytes of rainbow trout (Oncorhynchus mykiss). J Exp Biol 211, 25102518.
33 Towle, HC, Kaytor, EN & Shih, H (1997) Regulation of the expression of lipogenic enzyme genes by carbohydrate. Annu Rev Nutr 17, 405433.
34 Smith, S, Witkowski, A & Joshi, AK (2003) Structural and functional organization of the animal fatty acid synthase. Prog Lipid Res 42, 289317.
35 Pfaffl, MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, E45.
36 Seiliez, I, Gabillard, JC, Skiba-Cassy, S, 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, R329R335.
37 Torstensen, BE, Espe, M, Sanden, M, et al. (2008) Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 285, 193200.
38 Richard, N, Kaushik, S, Larroquet, L, et al. (2006) Replacing dietary fish oil by vegetable oils has little effect on lipogenesis, lipid transport and tissue lipid uptake in rainbow trout (Oncorhynchus mykiss). Br J Nutr 96, 299309.
39 Gutierrez, J, Carrillo, M, Zanuy, S, et al. (1984) Daily rhythms of insulin and glucose levels in the plasma of sea bass Dicentrarchus labrax after experimental feeding. Gen Comp Endocrinol 55, 393397.
40 Panserat, S, Medale, F, Breque, J, et al. (2000) Lack of significant long-term effect of dietary carbohydrates on hepatic glucose-6-phosphatase expression in rainbow trout (Oncorhynchus mykiss). J Nutr Biochem 11, 2229.
41 Panserat, S, Plagnes-Juan, E, Breque, J, et al. (2001) Hepatic phosphoenolpyruvate carboxykinase gene expression is not repressed by dietary carbohydrates in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204, 359365.
42 Panserat, S, Plagnes-Juan, E & Kaushik, S (2001) Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204, 23512360.
43 Panserat, S, Hortopan, GA, Plagnes-Juan, E, 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, 123131.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed