Identification and characterization of genes that control fat deposition in chickens

Journal of Animal Science and Biotechnology

Xiquan Zhang²  Liang Sun²  Rong Zhang²  Xinzheng Jia²  Xu Shen²  Wallace Paul¹  Hirwa Claire D’Andre² 

[1]Council for Scientific and Industrial Research (CSIR), Animal Research Institute, P. O. Box AH 20, Accra, Achimota, Ghana

[2]Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong 510642, China

关键词: Genes;    Fat deposition;    Chicken;   

Others  :  805001
DOI  :  10.1186/2049-1891-4-43

 received in 2013-03-26, accepted in 2013-10-30,  发布年份 2013

【 摘 要 】

Background

Fat deposits in chickens contribute significantly to meat quality attributes such as juiciness, flavor, taste and other organoleptic properties. The quantity of fat deposited increases faster and earlier in the fast-growing chickens than in slow-growing chickens. In this study, Affymetrix Genechip® Chicken Genome Arrays 32773 transcripts were used to compare gene expression profiles in liver and hypothalamus tissues of fast-growing and slow-growing chicken at 8 wk of age. Real-time RT-PCR was used to validate the differential expression of genes selected from the microarray analysis. The mRNA expression of the genes was further examined in fat tissues. The association of single nucleotide polymorphisms of four lipid-related genes with fat traits was examined in a F₂ resource population.

Results

Four hundred genes in the liver tissues and 220 genes hypothalamus tissues, respectively, were identified to be differentially expressed in fast-growing chickens and slow-growing chickens. Expression levels of genes for lipid metabolism (SULT1B1, ACSBG2, PNPLA3, LPL, AOAH) carbohydrate metabolism (MGAT4B, XYLB, GBE1, PGM1, HKDC1)cholesttrol biosynthesis (FDPS, LSS, HMGCR, NSDHL, DHCR24, IDI1, ME1) HSD17B7 and other reaction or processes (CYP1A4, CYP1A1, AKR1B1, CYP4V2, DDO) were higher in the fast-growing White Recessive Rock chickens than in the slow-growing Xinghua chickens. On the other hand, expression levels of genes associated with multicellular organism development, immune response, DNA integration, melanin biosynthetic process, muscle organ development and oxidation-reduction (FRZB, DMD, FUT8, CYP2C45, DHRSX, and CYP2C18) and with glycol-metabolism (GCNT2, ELOVL 6, and FASN), were higher in the XH chickens than in the fast-growing chickens. RT-PCR validated high expression levels of nine out of 12 genes in fat tissues. The G1257069A and T1247123C of the ACSBG2 gene were significantly associated with abdominal fat weight. The G4928024A of the FASN gene were significantly associated with fat bandwidth, and abdominal fat percentage. The C4930169T of the FASN gene was associated with abdominal fat weight while the A59539099G of the ELOVL 6 was significantly associated with subcutaneous fat. The A8378815G of the DDT was associated with fat band width.

Conclusion

The differences in fat deposition were reflected with differential gene expressions in fast and slow growing chickens.

【 授权许可】

   
2013 Claire D’Andre et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Ricard FH, Rouvier R: Etude de la composition anatomique du poulet. 1. Variabilite de la repartition des differentes parties corporelle chez de coquelets “Bresse-Pile”. Anri Zoorerh 1967, 16:23.
• [2]Proudman W, Mellen J, Anderson DL: Utilization of feed in fast- and slow- growing lines of chickens. Poult Sci 1970, 49:961-972.
• [3]Leclercq B, Blum JC, Boyer JP: Selecting broilers for low or high abdominal fat: initial observations. Br Poult Sci 1980, 21:107-113.
• [4]Becker WA: Genotypic and phenotypic relations of abdominal fat in chickens. Kansas City, Missouri: Presented at the 27th Annual National Breeder’s roundtable; 1978.
• [5]Huan-Xian C, Ran-Ran L, Gui-Ping Z, Mai-Qing Z, Ji-Lan C, Jie W: Identification of differentially expressed genes and pathways for intramuscular fat deposition in pectoralis major tissues of fast-and slow-growing chickens. BMC Genomics 2012, 13:213. BioMed Central Full Text
• [6]Dunnington EA, Siegel PB: Long-term divergent selection for eight-week body weight in white Plymouth rock chickens. Poultry Sci 1996, 75:1168-1179.
• [7]Zhao SM, Ma HT, Zou SX, Chen WH: Effects of in ovo administration of DHEA on lipid metabolism and hepatic lipogenetic genes expression in broiler chickens during embryonic development. Lipids 2007, 42:749-757.
• [8]Zhao X, Mo DL, Li AN, Gong W, Xiao SQ, Zhang Y, Qin LM, Niu YN, Guo YX, Liu XH, Cong PQ, He ZY, Wang C, Li JQ, Chen YS: Comparative analyses by sequencing of transcriptomes during skeletal muscle development between pig breeds differing in muscle growth rate and fatness. PLoS One 2011, 6(5):e19774. 1–18
• [9]Havenstein GB, Ferket PR, Qureshi MA: Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult Sci 2003, 82:1509-1518.
• [10]Jakobsson A, Westerberg R, Jacobsson A: Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 2005, 45:237-249.
• [11]Li WJ, Li HB, Chen JL, Zhao GP, Zheng MQ, Wen J: Gene expression of heart and adipocyte-fatty acid-binding protein and correlation with intramuscular fat in Chinese chickens. Anim Biotechnol 2008, 19(3):189-193.
• [12]Carlborg O, Kerje S, Schütz K, Jacobsson L, Jensen P, Andersson L: A global search reveals epistatic interaction between QTL for early growth in the chicken. Genome Res 2003, 13(3):413-421.
• [13]Zhao SM, Ma HT, Zou SX, Chen WH, Zhao RQ: Hepatic lipogenesis gene expression in broiler chicken with different fat deposition during embryonic development. J Vet Med 2007, 54:1-6.
• [14]Cogburn LA, Wang X, Carre W, Rejto L, Aggrey SE, Duclos MJ, Simon J, Porter TE: Functional genomics in chickens: development of integrated systems microarrays for transcriptional profiling and discovery of regulatory pathways. Comp Funct Genomics 2004, 5:253-261.
• [15]Richards MP, Poch SM, Coon CN, Rosebrough RW, Ashwell CM, McMurtry JP: Feed restriction significantly alters lipogenic gene expression in broiler breeder chickens. J Nutr 2003, 133:707-715.
• [16]Goodridge AG, Ball EG: Lipogenesis in the pigeon: in vivo studies. Am J Physiol 1967, 213:245-249.
• [17]O’Hea EK, Leveille GA: Lipogenesis in isolated adipose tissue of the domestic chick (gallus domesticus). Comp Biochem Physiol 1968, 26:111-120.
• [18]Cai Y, Song Z, Zhang X, Wang X, Jiao H, Lin H: Increased de novo lipogenesis in liver contributes to the augmented fat deposition in dexamethasone exposed broiler chickens (Gallus gallus domesticus). Comp Biochem Physiol C Toxicol Pharmacol 2009, 150(2):164-169.
• [19]Wang HB, Li H, Wang QG, Zhang XY, Wang SZ, Wang YX, Wang XP: Profiling of chicken adipose tissue gene expression by genome array. BMC Genomics 2007, 27(8):193-207.
• [20]NRC: Nutrient requirements of poultry. 9th edition. Washington, DC: National Academy Press; 1994.
• [21]Lei MM, Nie QH, Peng X, Zhang DX, Zhang XQ: Single nucleotide polymorphisms of the chicken insulin-like factor binding protein 2 gene associated with chicken growth and carcass traits. Poult Sci 2005, 84(8):1191-1198.
• [22]Dodson MV, Hausman GJ, Guan L, Du M, Rasmussen TP, Poulos SP, Mir P, Bergen WG, Fernyhough ME, McFarland DC, Rhoads RP, Soret B, Reecy JM, Velleman SG, Jiang Z: Lipid metabolism, adipocyte depot physiology and utilization of meat animals as experimental models for metabolic research. Int J Biol Sci 2010, 6:691-699.
• [23]Duclos MJ, Wang X, Carre W, Rejto L, Simon J, Cogburn LA: Nutritional regulation of global gene expression in chicken liver during fasting and re-feeding. San Diego, CA: Plant Animal Genom XII Conf; 2004.
• [24]Bourneuf E, Herault F, Chicault C, Carre W, Assaf S, Monnier A, Mottier S, Lagarrigue S, Douaire M, Mosser J, et al.: Microarray analysis of differential gene expression in the liver of lean and fat chickens. Gene 2006, 372:162-170.
• [25]Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, Julie A, Gary R: Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 2003, 421:268-272.
• [26]Collin A, Swennen Q, Skiba-Cassy S, Buyse J, Chartrin P, Le Bihan-Duval E, Crochet S, Duclos MJ, Joubert R, Decuypere E, Tesseraud S: Regulation of fatty acid oxidation in chicken (Gallus gallus): Interactions between genotype and diet composition. Comp Biochem Physiol 2009, Part B 153:171-177.
• [27]Jump DB, Botolin D, Wang Y, Xu J, Christian B, Demeure O: Fatty acid regulation of hepatic gene transcription. J Nutr 2005, 135(11):2503-2506.
• [28]Sato K, Akiba Y, Chida Y, Takahashi K: Lipoprotein hydrolysis and fat accumulation in Chicken adipose tissues are reduced by chronic administration of lipoprotein lipase monoclonal antibodies. Poult Sci 1999, 78:1286-1291.
• [29]Sato K, Sook SH, Kamada T: Tissue distribution of lipase genes related to triglyceride metabolism in laying hens (Gallus gallus). Comp Biochem Physiol 2010, 155(1):62-66.
• [30]Fried SK, Russell CD, Grauso NL, Brolin RE: Lipoprotein lipase regulation by insulin and glucocorticoid in subcutaneous and omental adipose tissues of obese women and men. J Clin Invest 1993, 92:2191-2198.
• [31]Leveille GA: In vitro hepatic lipogenesis in the hen and chick. Comp Biochem Physiol 1969, 28:431-435.
• [32]Benistant C, Duchamps C, Cohen-Adad F, Rouanet JL, Barre H: Increased in vitro fatty acid supply and cellular transport capacities in cold-acclimated ducklings (Cairina moschata). Am J Physiol 1998, 275:R683-R690.
• [33]Saez G, Davail S, Gentès G, Hocquette JF, Jourdan T, Degrace P, Baéza E: Gene expression and protein content in relation to intramuscular fat content in Muscovy and Peki ducks. Poult Sci 2009, 88:2382-2391.
• [34]Back DW, Goldman MJ, Fisch JE, Ochs RS, Goodridge AG: The fatty acid synthase gene in avian liver. Two mRNAs are expressed and regulated in parallel by feeding, primarily at the level of transcription. J Biol Chem 1986, 261:4190-4197.
• [35]Goodridge AG, Ball EG: The Effect of Prolactin on Lipogenesis in the Pigeon. In Vitro Studies. Biochemistry 1967, 6(8):2335-2343.
• [36]Leveille GA, O’Hea EK, Chakrabarty K: In vivo lipogenesis in the domestic chicken. Proc Soc Exp Biol Med 1968, 128:398-401.
• [37]Leveille GA, Romsos DR, Yeh YY, O’Hea EK: Lipid biosynthesis in the chick. A consideration of site of synthesis, influence of diet and possible regulating mechanisms. Poult Sci 1975, 54:1075-1093.
• [38]Demeure O, Duby C, Desert C, Assaf S, Hazard D, Guillou H, Lagarrigue S: Liver X receptor regulates fatty acid synthase expression in chicken. Poult Sci 2009, 88:2628-2635.
• [39]Shimba S, Ishii N, Ohta Y, Ohno T, Watabe Y, Hayashi M, et al.: Brain and muscle arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci U S A 2005, 102:12071-12076.
• [40]Gómez-Santos C, Gómez-Abellán P, Madrid JA, Hernández-Morante JJ, Lujan JA, Ordovas JM, Garaulet M: Circadian rhythm of clock genes in human adipose explants. Obesity 2009, 17(8):1481-5.30.
• [41]Wu X, Zvonic S, Floyd ZE, Kilroy G, Goh BC, Hernandez TL, et al.: Induction of circadian gene expression in human subcutaneous adipose-derived stem cells. Obesity 2009, 15(11):2560-2570.
• [42]Baulande S, Lasnier F, Lucas M, Pairault J: Adiponutrin, a transmembrane protein corresponding to a novel dietary and obesity-linked mRNA specifically expressed in the adipose lineage. J Biol Chem 2001, 276:33336-33344.
• [43]Dooley TP, Haldeman-Cahill R, Joiner J, Wilborn TW: Expression profiling of human sulfotransferase and sulfatase gene superfamilies in epithelial tissues and cultured cells. Biochem Biophys Res Commun 2000, 277:236-245.
• [44]Yazdi M, Ahnmark A, William-Olsson L, Snaith M, Turner N, Osla F, Wedin M, Asztély AK, Elmgren A, Bohlooly-Y M, Schreyer S, Lindén D: The role of mitochondrial glycerol-3 phosphate acyltransferase-1 in regulating lipid and glucose homeostasis in high-fat diet fed mice. Biochem Biophys Res Commun 2008, 369:1065-1070.
• [45]Palou M, Priego T, Sánchez J, Villegas E, Rodríguez AM, Palou A, Picó C: Sequential changes in the expression of genes involved in lipid metabolism in adipose tissue and liver in response to fasting. Pflugers Arch 2008, 456(5):825-836.
• [46]Marsit CJ, Houseman EA, Christensen BC, Gagne L, Wrensch MR, et al.: Identification of methylated genes associated with aggressive bladder cancer. PLoS One 2010, 5(8):e12334.
• [47]Kan S, Abe H, Kono T, Yamazaki M, Nakashima K, Kamada T, Akiba Y: Changes in peroxisome proliferator-activated receptor gamma gene expression of chicken abdominal adipose tissue with different age, sex and genotype. Anim Sci J 2009, 80:322-327.
• [48]Hoenig M, McGoldrick JB, De Beer M, Demacker PNM, Ferguson DC: Activity and tissue-specific expression of lipases and tumor-necrosis factor a in lean and obese cats. Domest Anim Endocrinol 2006, 30:333-344.
• [49]Albalat A, Saera-Vila A, Capilla E, Gutierrez J, Perez-Sanchez J, Navarro I: Insulin regulation of lipoprotein lipase (LPL) activity and expression in gilthead Sea bream (sparus aurata). Comp Biochem Physiol B 2007, 148:151-159.
• [50]Sato K, Akiba Y: Lipoprotein lipase mRNA expression in abdominal adipose tissue is little modified by age and nutritional state in broiler chickens. Poultry Sci 2002, 81:846-885.
• [51]Nie Q, Fang M, Xie L, Shi J, Zhang X: cDNA cloning, characterization, and variation analysis of chicken adipose triglyceride lipase (ATGL) gene. Mol Cell Biochem 2009, 320:67-74.
• [52]D’André Hirwa C, Yan W, Wallace P, Nie Q, Luo C, Li H, Shen X, Sun L, Tang J, Li W, Zhu X, Yang G, Zhang X: Effects of the thyroid hormone responsive spot 14{alpha} gene on chicken growth and fat traits. Poult Sc. 2010, 89(9):1981-1991.
• [53]Griffin HD, Hermier D: Plasma lipoprotein metabolism and fattening on poultry. In Leanness in domestic birds. Edited by Leclercq B, Whitehead CC. London: Butterworths; 1988:175-201.
• [54]Griffin HD, Guo K, Windsor D, Butterwith SC: Adipose tissue lipogenesis and fat deposition in leaner broiler chickens. J Nutr 1996, 122:363-368.