Skip to main content
×
Home
    • Aa
    • Aa

Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.)

  • Trond M. Kortner (a1), Jinni Gu (a1), Åshild Krogdahl (a1) and Anne Marie Bakke (a1)
Abstract

Inclusion of plant protein sources such as soyabean meal (SBM) in aquafeeds is associated with decreased lipid digestibility, reduced bile acid levels and hypocholesterolaemia. The mechanism for these metabolic abnormalities is unknown. The present study aimed at gaining further insight into how cholesterol and bile acid metabolism is modulated by SBM feeding by quantifying a number of mRNA species corresponding to key proteins involved in cholesterol and bile acid metabolism using quantitative real-time PCR. A 21 d feeding trial with sequential sampling at ten time points following initiation of 20 % SBM exposure was conducted on Atlantic salmon. A histological evaluation confirmed distal intestinal enteritis after 5 d of dietary exposure to the SBM, whereas diminished glycogen/lipid deposition was the only relevant finding observed in the liver. SBM inclusion resulted in reduced body pools of cholesterol and bile acids. Hepatic gene expression profiles revealed up-regulation of genes encoding rate-limiting enzymes in cholesterol (3-hydroxy-3-methyl-glutaryl-CoA reductase; HMGCR) and bile acid (cytochrome P4507A1 (CYP7A1)) biosynthesis, as well as up-regulation of their associated transcription factors (sterol regulatory element binding proteins 1 and 2, liver X receptor, farnesoid X receptor and PPAR isoforms). Hepatic gene expressions of cholesterol (ATP binding cassette G5 (ABCG5)) and bile acid (ATP binding cassette B11 (ABCB11)) transporters were, by and large, not influenced by the SBM, but distal intestinal expression patterns of ABCG5 and apical Na-dependent bile acid transporter indicated impaired cholesterol and bile acid reabsorption. In conclusion, hepatic gene expression profiles indicated that the capacity for cholesterol and bile acid synthesis was up-regulated, whereas the indicated impaired cholesterol and bile acid reabsorption probably occurred as a direct result of distal intestinal inflammation.

  • 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.

      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.

      Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.)
      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 Dropbox account. Find out more about sending content to Dropbox.

      Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.)
      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 Google Drive account. Find out more about sending content to Google Drive.

      Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.)
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Dr T. M. Kortner, fax +47 22 59 73 10, E-mail: trond.kortner@nvh.no
References
Hide All
1Gatlin DM, Barrows FT, Brown P, et al. (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38, 551579.
2van den Ingh TSGA, Krogdahl Å, Olli JJ, et al. (1991) Effects of soybean-containing diets on the proximal and distal intestine in Atlantic Salmon (Salmo salar): a morphological study. Aquaculture 94, 297305.
3Baeverfjord G & Krogdahl Å (1996) Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J Fish Dis 19, 375387.
4van den Ingh TSGA, Olli JJ & Krogdahl Å (1996) Alcohol-soluble components in soybeans cause morphological changes in the distal intestine of Atlantic salmon, Salmo salar L. J Fish Dis 19, 4753.
5Uran PA, Goncalves AA, Taverne-Thiele JJ, et al. (2008) Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 25, 751760.
6Olli JJ & Krogdahl Å (1994) Nutritive value of 4 soybean products as protein sources in diets for rainbow trout (Oncorhynchus mykiss, Walbaum) reared in fresh-water. Acta Agricult Scand A – Anim Sci 44, 185192.
7Kaushik 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.
8Krogdahl Å, Bakke-McKellep AM & Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquaculture Nutr 9, 361371.
9Romarheim OH, Skrede A, Gao YL, et al. (2006) Comparison of white flakes and toasted soybean meal partly replacing fish meal as protein source in extruded feed for rainbow trout (Oncorhynchus mykiss). Aquaculture 256, 354364.
10Yamamoto T, Suzuki N, Furuita H, et al. (2007) Supplemental effect of bile salts to soybean meal-based diet on growth and feed utilization of rainbow trout Oncorhynchus mykiss. Fish Sci 73, 123131.
11Romarheim OH, Skrede A, Penn M, et al. (2008) Lipid digestibility, bile drainage and development of morphological intestinal changes in rainbow trout (Oncorhynchus mykiss) fed diets containing defatted soybean meal. Aquaculture 274, 329338.
12Sørensen M, Penn M, El-Mowafi A, et al. (2011) Effect of stachyose, raffinose and soya-saponins supplementation on nutrient digestibility, digestive enzymes, gut morphology and growth performance in Atlantic salmon (Salmo salar, L). Aquaculture 314, 145152.
13Regost C, Arzel J & Kaushik SJ (1999) Partial or total replacement of fish meal by corn gluten meal in diet for turbot (Psetta maxima). Aquaculture 180, 99117.
14Gomez-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.
15Sitja-Bobadilla A, Pena-Llopis S, Gomez-Requeni P, et al. (2005) Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture 249, 387400.
16Hansen AC, Rosenlund G, Karlsen O, et al. (2007) Total replacement of fish meal with plant proteins in diets for Atlantic cod (Gadus morhua L.) I – effects on growth and protein retention. Aquaculture 272, 599611.
17Lim SJ & Lee KJ (2009) Partial replacement of fish meal by cottonseed meal and soybean meal with iron and phytase supplementation for parrot fish Oplegnathus fasciatus. Aquaculture 290, 283289.
18Yun BA, Mai KS, Zhang WB, et al. (2011) Effects of dietary cholesterol on growth performance, feed intake and cholesterol metabolism in juvenile turbot (Scophthalmus maximus L.) fed high plant protein diets. Aquaculture 319, 105110.
19Hofmann AF & Hagey LR (2008) Bile acids: chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell Mol Life Sci 65, 24612483.
20Dawson PA, Lan T & Rao A (2009) Bile acid transporters. J Lipid Res 50, 23402357.
21Hylemon PB, Zhou HP, Pandak WM, et al. (2009) Bile acids as regulatory molecules. J Lipid Res 50, 15091520.
22Fiorucci S, Cipriani S, Mencarelli A, et al. (2010) Counter-regulatory role of bile acid activated receptors in immunity and inflammation. Cur Mol Med 10, 579595.
23D'Aldebert E, Mve MJBB, Mergey M, et al. (2009) Bile salts control the antimicrobial peptide cathelicidin through nuclear receptors in the human biliary epithelium. Gastroenterol 136, 14351443.
24Bajor A, Gillberg PG & Abrahamsson H (2010) Bile acids: short and long term effects in the intestine. Scand J Gastroenterol 45, 645664.
25Schlottmann K, Wachs FP, Krieg RC, et al. (2000) Characterization of bile salt-induced apoptosis in colon cancer cell lines. Cancer Res 60, 42704276.
26Wachs FP, Krieg RC, Rodrigues CMP, et al. (2005) Bile salt-induced apoptosis in human colon cancer cell lines involves the mitochondrial transmembrane potential but not the CD95 (Fas/Apo-1) receptor. Int J Col Dis 20, 103113.
27Cronin J, Williams L, McAdam E, et al. (2010) The role of secondary bile acids in neoplastic development in the oesophagus. Biochem Soc Trans 38, 337342.
28Park JS, Yoo DH, Lee IJ, et al. (2010) Therapeutic effect of whole bear bile and its components against croton oil-induced rectal inflammation in rats. Biomol Therap 18, 8391.
29Claudel T, Zollner G, Wagner M, et al. (2011) Role of nuclear receptors for bile acid metabolism, bile secretion, cholestasis, and gallstone disease. Biochim Biophys Acta – Mol Bas Dis 1812, 867878.
30Kalaany NY & Mangelsdorf DJ (2006) LXRs and FXR: the yin and yang of cholesterol and fat metabolism. Ann Rev Physiol 68, 159191.
31Francis G, Makkar HPS & Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199, 197227.
32Krogdahl Å, Penn M, Thorsen J, et al. (2010) Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquac Res 41, 333344.
33Ricketts ML, Moore DD, Banz WJ, et al. (2005) Molecular mechanisms of action of the soy isoflavones includes activation of promiscuous nuclear receptors. A review. J Nutr Biochem 16, 321330.
34Mullen E, Brown RM, Osborne TF, et al. (2004) Soy isoflavones affect sterol regulatory element binding proteins (SREBPs) and SREBP-regulated genes in HepG2 cells. J Nutr 134, 29422947.
35Francis G, Kerem Z, Makkar HPS, et al. (2002) The biological action of saponins in animal systems: a review. Br J Nutr 88, 587605.
36Messina MJ (1999) Legumes and soybeans: overview of their nutritional profiles and health effects. Am J Clin Nut 70, 439S450S.
37Kortner TM, Valen EC, Kortner H, et al. (2011) Candidate reference genes for quantitative real-time PCR (qPCR) assays during development of a diet-related enteropathy in Atlantic salmon (Salmo salar L.) and the potential pitfalls of uncritical use of normalization software tools. Aquaculture 318, 355363.
38Minghetti 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 1811, 194202.
39Zaja R, Munic V, Klobucar RS, et al. (2008) Cloning and molecular characterization of apical efflux transporters (ABCB1, ABCB11 and ABCC2) in rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 90, 322332.
40Muller PY, Janovjak H, Miserez AR, et al. (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32, 1372–1374, 1376, 1378, 1379.
41Jordal AEO, 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.
42Leaver MJ, Villeneuve LAN, 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 Genom 9, 299.
43Panserat 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.
44Geay F, Ferraresso S, Zambonino-Infante JL, et al. (2011) Effects of the total replacement of fish-based diet with plant-based diet on the hepatic transcriptome of two European sea bass (Dicentrarchus labrax) half-sibfamilies showing different growth rates with the plant-based diet. BMC Genom 12, 522.
45Vilhelmsson OT, Martin SAM, Medale F, et al. (2004) Dietary plant-protein substitution affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss). Br J Nutr 92, 7180.
46Nordrum S, Bakke-McKellep AM, Krogdahl Å, et al. (2000) Effects of soybean meal and salinity on intestinal transport of nutrients in Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 125, 317335.
47Uran PA, Aydin R, Schrama JW, et al. (2008) Soybean meal-induced uptake block in Atlantic salmon Salmo salar distal enterocytes. J Fish Biol 73, 25712579.
48Potter SM (1995) Overview of proposed mechanisms for the hypocholesterolemic effect of soy. J Nutr 125, S606S611.
49Torres N, Torre-Villalvazo I & Tovar AR (2006) Regulation of lipid metabolism by diseases mediated soy protein and its implication in by lipid disorders. J Nutr Biochem 17, 365373.
50Brown MS & Goldstein JL (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89, 331340.
51Goldstein JL, DeBose-Boyd RA & Brown MS (2006) Protein sensors for membrane sterols. Cell 124, 3546.
52Sato R (2010) Sterol metabolism and SREBP activation. Arch Biochem Biophys 501, 177181.
53Maxwell KN, Soccio RE, Duncan EM, et al. (2003) Novel putative SREBP and LXR target genes identified by microarray analysis in liver of cholesterol-fed mice. J Lipid Res 44, 21092119.
54Maita M, Maekawa J, Satoh K, et al. (2006) Disease resistance and hypocholesterolemia in yellowtail Seriola quinqueradiata fed a non-fishmeal diet. Fish Sci 72, 513519.
55Li TG & Chiang JYL (2009) Regulation of bile acid and cholesterol metabolism by PPARs. Ppar Res 501739.
56Gadaleta RM, van Mil SWC, Oldenburg B, et al. (2010) Bile acids and their nuclear receptor FXR: relevance for hepatobiliary and gastrointestinal disease. Biochim Biophys Acta Mol Cell Biol Lipids 1801, 683692.
57Ruyter B, Andersen O, Dehli A, et al. (1997) Peroxisome proliferator activated receptors in Atlantic salmon (Salmo salar): effects on PPAR transcription and acyl-CoA oxidase activity in hepatocytes by peroxisome proliferators and fatty acids. Biochim Biophys Acta – Lipids Lipid Metabol 1348, 331338.
58Leaver MJ, Ezaz MT, Fontagne S, et al. (2007) Multiple peroxisome proliferator-activated receptor beta subtypes from Atlantic salmon (Salmo salar). J Mol Endocrinol 38, 391400.
59Leaver MJ, Bautista JM, Bjornsson BT, et al. (2008) Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev Fish Sci 16, 7394.
60Chawla A, Repa JJ, Evans RM, et al. (2001) Nuclear receptors and lipid physiology: opening the X-files. Science 294, 18661870.
61Hunt MC, Yang YZ, Eggertsen G, et al. (2000) The peroxisome proliferator-activated receptor alpha (PPAR alpha) regulates bile acid biosynthesis. J Biol Chem 275, 2894728953.
62Morais S, Pratoomyot J, Taggart JB, et al. (2011) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 12, 255.
63von Bergmann K, Sudhop T & Lutjohann D (2005) Cholesterol and plant sterol absorption: recent insights. Am J Cardiol 96, 10D14D.
64Sanden M, Berntssen MHG, Krogdahl Å, et al. (2005) An examination of the intestinal tract of Atlantic salmon, Salmo salar L., parr fed different varieties of soy and maize. J Fish Dis 28, 317330.
65Knudsen D, Jutfelt F, Sundh H, et al. (2008) Dietary soya saponins increase gut permeability and play a key role in the onset of soyabean-induced enteritis in Atlantic salmon (Salmo salar L.). Br J Nutr 100, 120129.
66Hagenbuch B & Dawson P (2004) The sodium bile salt cotransport family SLC10. Pflugers Arch Eur J Physiol 447, 566570.
67Gadaleta RM, van Erpecum KJ, Oldenburg B, et al. (2011) Farnesoid X receptor activation inhibits inflammation and preserves the intestinal barrier in inflammatory bowel disease. Gut 60, 463472.
68Bakke-McKellep AM, Penn MH, Salas PM, et al. (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 97, 699713.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 12
Total number of PDF views: 150 *
Loading metrics...

Abstract views

Total abstract views: 289 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 23rd October 2017. This data will be updated every 24 hours.