Molecular Genetics and Genomics

, Volume 290, Issue 5, pp 1673–1682 | Cite as

Transcriptomic analysis to elucidate the molecular mechanisms that underlie feed efficiency in meat-type chickens

  • Jeeyoung Lee
  • Arthur B. Karnuah
  • Romdhane Rekaya
  • Nicholas B. Anthony
  • Samuel E. Aggrey
Original Paper

Abstract

Feed efficiency phenotypes defined by genotypes or gene markers are unknown. To date, there are only limited studies on global gene expression profiling on feed efficiency. The objective of this study was to identify genes and pathways associated with residual feed intake (RFI) through transcriptional profiling of duodenum at two different ages in a chicken population divergently selected for low (LRFI) or high (HRFI) RFI. The global gene expression differences in LRFI and HRFI were assessed by the Affymetrix GeneChip® Chicken Genome Array and RT-PCR using duodenal tissue on days 35 and 42. The Ingenuity Pathway Analysis program was used to identify canonical and gene network pathways associated with RFI. A global view of gene expression differences between LRFI and HRFI suggest that RFI can be explained by differences in cell division, growth, proliferation and apoptosis, protein synthesis, lipid metabolism, and molecular transport of cellular molecules. Chickens selected for improved RFI achieve efficiency by reducing feed intake with a nominal or no change in weight gain by either up-regulating CD36, PPARα, HMGCS2, GCG or down-regulating PCSK2, CALB1, SAT1, and SGK1 genes within the lipid metabolism, small molecule biochemistry, molecular transport, cell death, and protein synthesis molecular and cellular functions. Chickens selected for reduced RFI via reduced feed intake with no change in weight gain achieve feed efficiency for growth by the up-regulation of genes that reduce appetite with increased cellular oxidative stress, prolonged cell cycle, DNA damage, and apoptosis in addition to increased oxidation of dietary fat and efficient fatty acids transported from the intestines.

Keywords

Residual feed intake Microarray RT-PCR Gene network Chickens 

Supplementary material

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References

  1. Abumrad NA, el-Maghrabi MR, Amri EZ, Lopez E, Grimald PA (1993) Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J Biol Chem 268:17665–17668PubMedGoogle Scholar
  2. Aggrey SE, Sanglikar AP, Karnuah AB, McMurtry JP (2008) Molecular basis of feed efficiency in meat-type birds. In: Proceedings 23rd World Poultry Congress, CD Rom, Brisbane, p 8Google Scholar
  3. Aggrey SE, Karnuah AB, Sebastian B, Anthony NB (2010) Genetic properties of feed efficiency parameters in meat-type chickens. Genet Sel Evol 42:25PubMedCentralCrossRefPubMedGoogle Scholar
  4. Badouel C, Chartrain I, Blot J, Tassan J-P (2010) Maternal embryonic leucine zipper kinase is stabilized in mitosis by phosphorylation and is partially degraded upon mitotic exit. Exp Cell Res 316:2166–2173CrossRefPubMedGoogle Scholar
  5. Bottje W, Tang ZW, Iqbal M, Cauthon D, Okimoto R, Wing T, Cooper M (2002) Association of mitochondrial function with feed efficiency within a single genetic line of male broilers. Poult Sci 81:546–555CrossRefPubMedGoogle Scholar
  6. Casero RA Jr, Pegg AE (1993) Spermidine/spermine N1-acetyltransferase-the turning point in polyamine metabolism. FASEB J 7:653–661PubMedGoogle Scholar
  7. Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410:37–40CrossRefPubMedGoogle Scholar
  8. Chang H, Wang J, Tian Y, Xu J, Gou X, Cheng J (2012) The TPX2 gene is a promising diagnostic and therapeutic target for cervical cancer. Oncol Rep 27:1353–1359PubMedGoogle Scholar
  9. Chen Y, Gondro C, Quinn K, Herd RM, Parnell PF, Vanselow B (2011) Global gene expression profiling reveals genes expressed differentially in cattle with high and low residual feed intake. Anim Genet 42:475–490CrossRefPubMedGoogle Scholar
  10. Cogburn LA, Wang X, Carre W, Aggrey SE, Duclos MJ, Simon J, Porter TE (2004) Functional genomics in chickens: development of integrated-system microarrays for transcriptional profiling and discovery of regulatory pathways. Comp Funct Genomics 5:253–261PubMedCentralCrossRefPubMedGoogle Scholar
  11. Cummings DE, Overduin J (2007) Gastrointestinal regulation of food intake. J Clin Invest 117:13–23PubMedCentralCrossRefPubMedGoogle Scholar
  12. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239–252CrossRefPubMedGoogle Scholar
  13. De Koning DJ, Haley CS, Windsor D, Hocking PM, Griffin H, Morris A, Vincent J, Burt DW (2004) Segregation of QTL for production traits in commercial meat-type chickens. Genet Res Camb 83:211–220CrossRefGoogle Scholar
  14. Eulitz D, Mannherz HG (2007) Inhibition of deoxyribonuclease I by actin is to protect cells from premature cell death. Apoptosis 12:1511–1521CrossRefPubMedGoogle Scholar
  15. Fu J, Oveisi F, Gaetani S, Lin E, Piomelli D (2005) Oleoylethanolamide, an endogenous PPAR-α agonist, lowers body weight and hyperlipidemia in obese rats. Neuropharmacology 48:1147–1153CrossRefPubMedGoogle Scholar
  16. Gachon F, Leuenberger N, Claudel T, Gos P, Jouffe C, Olela FF, de Mollerat du Jeu X, Wahli W, Schibler U (2011) Proline- and acidic amino acid-rich basic leucine zipper proteins modulates peroxisome proliferator-activated receptor α (PPARα) activity. Proc Natl Acad Sci USA 108: 4794–4799Google Scholar
  17. Gagnon J, Mayne J, Chen A, Raymond A, Woulfe J, Mbikay M, Chretién M (2011) PCSK2-null mice exhibit delayed intestinal motility, reduced refeeding response and altered plasma levels of several regulatory peptides. Life Sci 88:212–217CrossRefPubMedGoogle Scholar
  18. Hadari YR, Arbel-Goren R, Levy Y, Amsterdam A, Alon R, Zakut R, Zick Y (2000) Galectin-8 binding to integrin inhibits cell adhesion and induces apoptosis. J Cell Sci 113(Pt 13):2385–2397PubMedGoogle Scholar
  19. Harmon CM, Abumrad NA (1993) Binding of sulfoccuinimidyl fatty acids to adipocyte membrane proteins: isolation and ammo-terminal sequenece of an 88-kD protein implicated in transport of long-chain fatty acids. J Membr Biol 133:43–49CrossRefPubMedGoogle Scholar
  20. He W, Liu W, Chew CS, Baker SS, Baker RD, Forte JG, Zhu L (2011) Acid secretion-associated translocated of KCNJ15 in gastric parietal cells. Am J Physiol Gastrointest Liver Physiol 301:G591–G600PubMedCentralCrossRefPubMedGoogle Scholar
  21. Hochberg Y, Benjamini Y (1990) More powerful procedure for multiple significance testing. Stats in Med 9:811–818CrossRefGoogle Scholar
  22. Huang ZH, Luque RM, Kineman RD, Mazzone T (2007) Nutritional regulation of adipose tissue apolipoprotein E expression. Am J Phyisol 293:E203–E209Google Scholar
  23. Inaba T, Roberts WM, Shapiro LH, Jolly KW, Raimondi SC, Smith SD, Look AT (1992) Fusion of the leucine zipper gene HLF to the E2A gene in human acute B-lineage leukemia. Science 257:531–534CrossRefPubMedGoogle Scholar
  24. Iqbal M, Pumford NR, Tang ZX, Lasiter K, Wing T, Cooper M, Bottje W (2004) Low feed efficiency broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity. Poult Sci 83:474–484CrossRefPubMedGoogle Scholar
  25. Iqbal M, Pumford N, Lassiter K, Tang ZX, Wing T, Cooper M, Bottje WG (2005) Compromised liver mitochondrial function and complex activity in low feed efficient broilers within a single line associated with higher oxidative stress and differential protein expression. Poult Sci 84:933–941CrossRefPubMedGoogle Scholar
  26. Jiang S, Katayama H, Wang J, Li SA, Hong Y, Radvanyi L, Li JJ, Sen S (2010) Estrogen-induced aurora kinase-A (AURKA) gene expression is activated by GATA-3 in estrogen receptor-positive breast cancer cells. Horm Cancer 1:11–20PubMedCentralCrossRefPubMedGoogle Scholar
  27. Kaufhold MA, Krabbenhoft A, Engelhardt R, Riederer B, Fahrmann M, Klocker N, Beil W, Manns M, Hagen SJ, Seidler U (2008) Localization, trafficking, and significance for acid secretion of parietal cell Kir4.1 and KCNQ1 K + channels. Gastroenterology 134:1058–1069CrossRefPubMedGoogle Scholar
  28. Kim JY, Chu K, Kim HJ, Seong HA, Park KC, Sanyal S, Takeda J, Ha H, Shong M, Tsai MJ, Choi HS (2004) Orphan nuclear receptor small heterodimer partner, a novel corepressor for basic helix-loop transcription factor BETA2/neuroD. Mol Endocrinol 18:776–790CrossRefPubMedGoogle Scholar
  29. Kolath WH, Kerley MS, Golden JW, Keisler DH (2006) The relationship between mitochondrial function and residual feed intake in Angus steers. J Anim Sci 84:861–865CrossRefPubMedGoogle Scholar
  30. Kong B-W, Song JJ, Lee JY, Hargis BM, Wing T, Lassiter K, Bottje W (2011) Gene expression in breast muscle associated with feed efficiency in a single broiler line using a chicken 44 K oligo microarray. I. Top differentially expressed genes. Poul Sci 90:2535–2547Google Scholar
  31. Kuribayashi K, Krigsfeld G, Wang W, Xu J, Mayes PA, Dicker DT, Wu GS, El-Deiry WS (2008) TNFS10 (TRAIL), a p53 target gene that mediates p53-dependent death. Cancer Biol Ther 7:2034–2038CrossRefPubMedGoogle Scholar
  32. Lemmens SG, Martens EA, Kester AD, Westerterp-Plantenga MS (2011) Changes in gut hormones and glucose concentration in relation to hunger and fullness. Am J Clin Nutr 94:717–725CrossRefPubMedGoogle Scholar
  33. Li F, MacFarlan T, Pittman RN, Chakravarti D (2002) Ataxin-3 is a histone-binding protein with two independent transcriptional corepressor activities. J Biol Chem 277:45004–45012CrossRefPubMedGoogle Scholar
  34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCt method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  35. Lkhagvadorj S, Qu L, Cai W, Couture OP, Barb R, Hausman GJ, Nettleton D, Anderson LL, Dekkers JCM, Tuggle CK (2010) Gene expression profiling of the short-term adaptive response to acute restriction in liver and adipose tissues of pigs differing in feed efficiency. Am J Physiol Regul Integr Comp Physiol 298:R494–R507CrossRefPubMedGoogle Scholar
  36. Madsen SL, Wong EA (2011) Expression of the chicken peptide transporter 1 and the peroxisome proliferator-activated receptor α following feed restriction and subsequent refeeding. Poult Sci 90:2295–2300CrossRefPubMedGoogle Scholar
  37. Maloney CA, Lilley C, Cruickshank M, McKinnon C, Hay SM, Rees WD (2005) The expression of growth-arrest genes in the liver and kidney of the protein-restricted rat fetus. Br J Nutrition 94:12–18CrossRefGoogle Scholar
  38. Márquez GC, Enns RM, Grosz MD, Alexander LJ, MacNiel MD (2009) Quantitative trait loci with effects on feed efficiency traits in Hereford X composite double backcross populations. Anim Genet 40:986–988CrossRefPubMedGoogle Scholar
  39. Millman SE, Pagano M (2011) MCL1 meets it end during mitotic arrest. EMBO Rep 12:384–385PubMedCentralCrossRefPubMedGoogle Scholar
  40. Mutch DM, Anderle P, Fiaux M, Mansourian R, Vidal K, Wahli W, Williamson G, Roberts MA (2004) Regional variations in ABC transporter expression along the mouse intestinal tract. Physiol Genomics 12:11–20CrossRefGoogle Scholar
  41. Nadal A, Marrero PF, Haro D (2002) Down-regulation of the mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase gene by insulin: the role of the forkhead transcription factor FKHRL1. Biochem J 366(Pt 1):289–297PubMedCentralCrossRefPubMedGoogle Scholar
  42. Naville D, Duchampt A, Vigier M, Oursel D, Lessire R, Poirier H, Niot I, Begeot M, Besnard P, Mithieux G (2012) Link between intestinal CD36 ligand binding and satiety induced by high protein diet in mice. PLoS ONE 7(1):e30686PubMedCentralCrossRefPubMedGoogle Scholar
  43. Nemere I, Leathers VL, Thompson BS, Luben RA, Norman AW (1991) Redistribution of calbindin-D28 k in chick intestine in response to calcium transport. Endocrinology 129:2972–2984CrossRefPubMedGoogle Scholar
  44. Ojano-Dirain CP, Pumford NR, Toyomizu M, Bottje WG (2007) Association of mitochondrial function and feed efficiency. Jpn Poult Sci 44:221–237CrossRefGoogle Scholar
  45. Ortlund EA, Lee Y, Solomon IH, Harger JM, Safi R, Choi Y, Guan Z, Tripathy A, Raetz CR, McDonnel DP, Moore DD, Redinbo MR (2005) Modulation of human nuclear LRH-1 activity by phospholipids and SHP. Nat Struct Mol Biol 12:357–363CrossRefPubMedGoogle Scholar
  46. Pegg AE (2008) Spermidine/spermine-N(1)-acetyltransferase: a key metabolic regulator. Am J Physiol Endocrionol Metab 294:E995–E1010CrossRefGoogle Scholar
  47. Ramirez de Molina A, Gallego-Ortega D, Sarmentero-Estrada J, Lagares D, Gomez Del Pulgar T, Bandres E, Garcia-Foncillas J, Lacal JC (2008) Choline kinase as a link connecting phospholipid metabolism and cell cycle regulation: implications in cancer therapy. Int J Biochem Cell Biol 40:1753–1763CrossRefPubMedGoogle Scholar
  48. Rothschild MF, Hu Z, Jiang Z (2007) Advances in QTL mapping in pigs. Int J Biol Sci 3:192–197PubMedCentralCrossRefPubMedGoogle Scholar
  49. SAS Institute (2000) “SAS/STAT User’s Guide,” Version 8 edn. SAS Inst. Inc., Cary, NCGoogle Scholar
  50. Schwartz GJ, Fu J, Astarita G, Li X, Gaetani S, Campolongo P, Cuomo V, Piomelli D (2008) The lipid messenger OEA links dietary fat intake to satiety. Cell Metab 8:281–288PubMedCentralCrossRefPubMedGoogle Scholar
  51. Seidah NG, Chretien M (1999) Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res 848:45–62CrossRefPubMedGoogle Scholar
  52. Sherman EL, Nkrumah JD, Li C, Bartusiak R, Murdoch B, Moore SS (2009) Fine mapping quantitative trait loci for feed intake and feed efficiency in beef cattle. J Anim Sci 87:37–42CrossRefPubMedGoogle Scholar
  53. Silverstein RL, Asch AS, Nachman RL (1989) Glycoprotein IV mediates thrombospondin-dependent platelet-monocyte and platelet–monocyte adhesion. J Clin Invest 79:867–874CrossRefGoogle Scholar
  54. Song G, Park K, Wang L (2009) Gene expression profiling reveals a diverse array of pathways inhibited by nuclear receptor SHP during adipogenesis. Int J Clin Exp Pathol 2(3):275–285PubMedCentralPubMedGoogle Scholar
  55. van Kaam JBCHM, Groenen MAM, Bovenhius H, Veenendaal A, Vereijken ALJ, van Arendonk JAM (1999) Whole genome scan in chickens for quantitative trait loci affecting growth and feed efficiency. Poult Sci 78:15–23CrossRefPubMedGoogle Scholar
  56. van Raalte DH, Li M, Pritchard PH, Wasan KM (2004) Peroxisome proliferator-activated receptor (PPAR)-alpha: a pharmacological target with promising future. Pharm Res 21:1531–1538CrossRefPubMedGoogle Scholar
  57. Wang T, Xia D, Li N, Wang C, Wan T, Chen G, Cao X (2005) Bone marrow stromal cell-derived growth inhibitor inhibits growth and migration of breast cancer cells via inducation of cell cycle arrest and apoptosis. J Biol Chem 280:4374–4382CrossRefPubMedGoogle Scholar
  58. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediates cell death. Nat Rev Mol Cell Biol 9:48–59CrossRefGoogle Scholar
  59. Zhang W, Aggrey SE (2003) Genetic variation in feed utilization efficiency of meat-type chickens. World’s Poult Sci J 59:328–339CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jeeyoung Lee
    • 1
  • Arthur B. Karnuah
    • 1
  • Romdhane Rekaya
    • 2
  • Nicholas B. Anthony
    • 3
  • Samuel E. Aggrey
    • 1
  1. 1.NutriGenomics Laboratory, Department of Poultry ScienceUniversity of GeorgiaAthensUSA
  2. 2.Department of Animal and Dairy ScienceUniversity of GeorgiaAthensUSA
  3. 3.Department of Poultry ScienceUniversity of ArkansasFayettevilleUSA

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