Dietary threonine supplementation improves hepatic lipid metabolism of Pekin ducks
Y. Jiang A B , X. D. Liao A , M. Xie A , J. Tang A , S. Y. Qiao B , Z. G. Wen C and S. S. Hou A DA State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China.
B State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China.
C Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100193, China.
D Corresponding author. Email: houss@263.net
Animal Production Science 59(4) 673-680 https://doi.org/10.1071/AN17633
Submitted: 20 September 2017 Accepted: 3 March 2018 Published: 5 June 2018
Abstract
The present study was conducted to evaluate the regulatory role of threonine (Thr) on hepatic lipid metabolism by determining the effects of dietary Thr concentration on lipid deposition and on genes related to lipid expression in the liver of Pekin duck. In total, 240 1-day-old ducklings were randomly allocated according to the average bodyweight to one of five dietary treatments with six replicate cages of eight birds per cage for each treatment. Birds were fed diets with 0.52%, 0.59%, 0.66%, 0.73% and 0.80% Thr (as-fed basis) from 1 to 21 days of age respectively. The results showed that dietary Thr supplementation increased average daily gain (P < 0.0001), average daily feed intake (P < 0.0001) and abdominal fat percentage (P < 0.04), while it decreased feed to gain ratio (P < 0.0001), the hepatic contents of total lipid (P < 0.003) and triglycerides (P < 0.003) of Pekin ducks. However, dietary Thr supplementation had no influence (P > 0.05) on the concentration of hepatic cholesterol, and plasma amino acids and biochemical parameters of Pekin ducks. Moreover, Thr-unsupplemented control diet upregulated (P < 0.05) hepatic gene expression related to lipid uptake (fatty acid-binding protein, apolipoprotein A4, lipoprotein lipase), fatty acid synthesis (sterol regulatory element-binding protein 1c, malic enzyme), fatty acid β-oxidation (peroxisome proliferator-activated receptor α, fatty acyl– coenzyme A (CoA) oxidase), ketogenesis (hydroxymethylglutaryl–CoA synthase 1, and acetyl–CoA synthetase1), responsive genes to amino acid deficiency (general control non-derepressible 2 (GCN2), GCN1, eukaryotic initiation factor 2α, impact RWD domain protein (IMPACT)), and triglyceride transport (apolipoprotein B) of Pekin ducks. In addition, dietary Thr deficiency had no effect on the expression of stearoyl CoA desaturase, fatty acid synthase, and ATP–citrate lyase in the liver of Pekin ducks. It is suggested that dietary Thr supplementation improved hepatic lipid metabolism of Pekin ducks by regulating lipid synthesis, transport and oxidation.
Additional keywords: duck, lipid.
References
Brito CO, Dutra JLL, Dias TN, Barbosa LT, Nascimento CS, Pinto APG, Albino LFT, Fernandes RPM, Macario MS, Melo JS (2017) Effect of dietary lysine on performance and expression of electron transport chain genes in the pectoralis major muscle of broilers. Animal 11, 778–783.| Effect of dietary lysine on performance and expression of electron transport chain genes in the pectoralis major muscle of broilers.Crossref | GoogleScholarGoogle Scholar |
Cambiaghi TD, Pereira CM, Shanmugam R, Bolech M, Wek RC, Sattlegger E, Castilho BA (2014) Evolutionarily conserved IMPACT impairs various stress responses that require GCN1 for activating the eIF2 kinase GCN2. Biochemical and Biophysical Research Communications 443, 592–597.
| Evolutionarily conserved IMPACT impairs various stress responses that require GCN1 for activating the eIF2 kinase GCN2.Crossref | GoogleScholarGoogle Scholar |
Çiftci I, Ceylan N (2004) Effects of dietary threonine and crude protein on growth performance, carcase and meat composition of broiler chickens. British Poultry Science 45, 280–289.
| Effects of dietary threonine and crude protein on growth performance, carcase and meat composition of broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Feller DD, Feist E (1959) Metabolism of adipose tissue: incorporation of isoleucine carbon into lipids by slices of adipose tissue. Journal of Lipid Research 1, 90–96.
Feller DD, Feist E (1962a) The conversion of leucine carbon into CO2, fatty acids and other products by adipose tissue. Biochimica et Biophysica Acta (BBA) – Bioenergetics 62, 40–44.
Feller DD, Feist E (1962b) Metabolism of alanine, serine and valine in adipose tissue. Metabolism: Clinical and Experimental 11, 448–455.
Feller DD, Feist E (1963) Conversion of methionine and threonine to fatty acids by adipose tissue. Biochemistry and Cell Biology 41, 269–273.
Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. The Journal of Biological Chemistry 226, 497–509.
Guo F, Cavener DR (2007) The GCN2 eIF2alpha kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell Metabolism 5, 103–114.
| The GCN2 eIF2alpha kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid.Crossref | GoogleScholarGoogle Scholar |
Horn NL, Donkin SS, Applegate TJ, Adeola O (2009) Intestinal mucin dynamics: response of broiler chicks and White Pekin ducklings to dietary threonine. Poultry Science 88, 1906–1914.
| Intestinal mucin dynamics: response of broiler chicks and White Pekin ducklings to dietary threonine.Crossref | GoogleScholarGoogle Scholar |
Horn N, Radcliffe J, Applegate T, Adeola O (2010) Gut morphology and nutrient retention responses of broiler chicks and White Pekin ducklings to dietary threonine deciency. Canadian Journal of Animal Science 90, 513–520.
| Gut morphology and nutrient retention responses of broiler chicks and White Pekin ducklings to dietary threonine deciency.Crossref | GoogleScholarGoogle Scholar |
Horton JD, Shimomura I (1999) Sterol regulatory element-binding proteins: activators of cholesterol and fatty acid biosynthesis. Current Opinion in Lipidology 10, 143–150.
| Sterol regulatory element-binding proteins: activators of cholesterol and fatty acid biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Horton JD, Goldstein JL, Brown MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. The Journal of Clinical Investigation 109, 1125–1131.
| SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver.Crossref | GoogleScholarGoogle Scholar |
Jiang Y, Uzma M, Tang J, Wen ZG, Hou SS, Huang W, Xie M (2016) Effects of dietary protein on threonine requirements of Pekin ducks from hatch to 21 days of age. Animal Feed Science and Technology 217, 95–99.
| Effects of dietary protein on threonine requirements of Pekin ducks from hatch to 21 days of age.Crossref | GoogleScholarGoogle Scholar |
Jiang Y, Tang J, Xie M, Wen ZG, Qiao SY, Hou SS (2017) Threonine supplementation reduces dietary protein and improves lipid metabolism in Pekin ducks. British Poultry Science 58, 687–693.
| Threonine supplementation reduces dietary protein and improves lipid metabolism in Pekin ducks.Crossref | GoogleScholarGoogle Scholar |
Kidd MT, Kerr BJ (1996) L-threonine for poultry: a review. Journal of Applied Poultry Research 5, 358–367.
| L-threonine for poultry: a review.Crossref | GoogleScholarGoogle Scholar |
Krishnamoorthy T, Pavitt GD, Zhang F, Dever TE, Hinnebusch AG (2001) Tight binding of the phosphorylated alpha subunit of initiation factor 2 (eIF2alpha) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Molecular and Cellular Biology 21, 5018–5030.
| Tight binding of the phosphorylated alpha subunit of initiation factor 2 (eIF2alpha) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method.Crossref | GoogleScholarGoogle Scholar |
National Research Council (1994) ‘Nutrient requirements of poultry.’ 9th edn. (National Academy Press: Washington, DC)
Pereira CM, Sattlegger E, Jiang HY, Longo BM, Jaqueta CB, Hinnebusch AG, Wek RC, Mello LE, Castilho BA (2005) IMPACT, a protein preferentially expressed in the mouse brain, binds GCN1 and inhibits GCN2 activation. The Journal of Biological Chemistry 280, 28316–28323.
| IMPACT, a protein preferentially expressed in the mouse brain, binds GCN1 and inhibits GCN2 activation.Crossref | GoogleScholarGoogle Scholar |
Ross-Inta CM, Zhang Y-F, Almendares A, Giulivi C (2009) Threonine-deficient diets induced changes in hepatic bioenergetics. American Journal of Physiology. Gastrointestinal and Liver Physiology 296, G1130–G1139.
| Threonine-deficient diets induced changes in hepatic bioenergetics.Crossref | GoogleScholarGoogle Scholar |
SAS Institute Inc. (2003) ‘SAS user’s guide: statistics, version 9.1.’ (SAS Institute Inc.: Cary, NC)
Sattlegger E, Hinnebusch AG (2005) Polyribosome binding by GCN1 is required for full activation of eukaryotic translation initiation factor 2{alpha} kinase GCN2 during amino acid starvation. The Journal of Biological Chemistry 280, 16514–16521.
| Polyribosome binding by GCN1 is required for full activation of eukaryotic translation initiation factor 2{alpha} kinase GCN2 during amino acid starvation.Crossref | GoogleScholarGoogle Scholar |
Shimano H, Horton JD, Shimomura I, Hammer RE, Brown MS, Goldstein JL (1997) Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells. The Journal of Clinical Investigation 99, 846–854.
| Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells.Crossref | GoogleScholarGoogle Scholar |
Thiex NJ, Manson H, Anderson S, Persson J-Å (2002) Determination of crude protein in animal feed, forage, grain, and oilseeds by using block digestion with a copper catalyst and steam distillation into boric acid: collaborative study. Journal of AOAC International 85, 309–317.
Tordjman K, Bernal-Mizrachi C, Zemany L, Weng S, Feng C, Zhang F, Leone TC, Coleman T, Kelly DP, Semenkovich CF (2001) PPARalpha deficiency reduces insulin resistance and atherosclerosis in apoE-null mice. The Journal of Clinical Investigation 107, 1025–1034.
| PPARalpha deficiency reduces insulin resistance and atherosclerosis in apoE-null mice.Crossref | GoogleScholarGoogle Scholar |
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034.1–0034.11.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |
Xie M, Zhang L, Wen Z, Tang J, Huang W, Hou S (2014) Threonine requirement of White Pekin ducks from hatch to 21 days of age. British Poultry Science 55, 553–557.
| Threonine requirement of White Pekin ducks from hatch to 21 days of age.Crossref | GoogleScholarGoogle Scholar |
Yoshida A, Ashida K, Harper AE (1961) Prevention of fatty liver due to threonine deficiency by moderate caloric restriction. Nature 189, 917–918.
| Prevention of fatty liver due to threonine deficiency by moderate caloric restriction.Crossref | GoogleScholarGoogle Scholar |
Zaborske JM, Narasimhan J, Jiang L, Wek SA, Dittmar KA, Freimoser F, Pan T, Wek RC (2009) Genome-wide analysis of tRNA charging and activation of the eIF2 kinase Gcn2p. The Journal of Biological Chemistry 284, 25254–25267.
| Genome-wide analysis of tRNA charging and activation of the eIF2 kinase Gcn2p.Crossref | GoogleScholarGoogle Scholar |
Zhang Q, Xu L, Doster A, Murdoch R, Cotter P, Gardner A, Applegate TJ (2014) Dietary threonine requirement of Pekin ducks from 15 to 35 days of age based on performance, yield, serum natural antibodies, and intestinal mucin secretion. Poultry Science 93, 1972–1980.
| Dietary threonine requirement of Pekin ducks from 15 to 35 days of age based on performance, yield, serum natural antibodies, and intestinal mucin secretion.Crossref | GoogleScholarGoogle Scholar |
Zhang Q, Zeng QF, Cotter P, Applegate TJ (2016) Dietary threonine response of Pekin ducks from hatch to 14 days of age based on performance, serology, and intestinal mucin secretion. Poultry Science 95, 1348–1355.
| Dietary threonine response of Pekin ducks from hatch to 14 days of age based on performance, serology, and intestinal mucin secretion.Crossref | GoogleScholarGoogle Scholar |
