期刊论文详细信息
BMC Veterinary Research
Expression of genes controlling fat deposition in two genetically diverse beef cattle breeds fed high or low silage diets
José António Mestre Prates1  Carlos Mendes Godinho Andrade Fontes1  Virgínia Maria Rico Pires1  Ana Sofia Henriques da Costa1 
[1] Secção de Bioquímica, CIISA, Faculdade de Medicina Veterinária, Universidade Técnica de Lisboa, Av. da Universidade Técnica, Pólo Universitário do Alto da Ajuda, Lisboa 1300-477, Portugal
关键词: Fat deposition;    Gene expression;    Muscle;    Adipose tissue;    Beef cattle;   
Others  :  1119520
DOI  :  10.1186/1746-6148-9-118
 received in 2012-10-09, accepted in 2013-06-12,  发布年份 2013
PDF
【 摘 要 】

Background

Both genetic background and finishing system can alter fat deposition, thus indicating their influence on adipogenic and lipogenic factors. However, the molecular mechanisms underlying fat deposition and fatty acid composition in beef cattle are not fully understood. This study aimed to assess the effect of breed and dietary silage level on the expression patterns of key genes controlling lipid metabolism in subcutaneous adipose tissue (SAT) and longissimus lumborum (LL) muscle of cattle. To that purpose, forty bulls from two genetically diverse Portuguese bovine breeds with distinct maturity rates, Alentejana and Barrosã, were selected and fed either low (30% maize silage/70% concentrate) or high silage (70% maize silage/30% concentrate) diets.

Results

The results suggested that enhanced deposition of fatty acids in the SAT from Barrosã bulls, when compared to Alentejana, could be due to higher expression levels of lipogenesis (SCD and LPL) and β-oxidation (CRAT) related genes. Our results also indicated that SREBF1 expression in the SAT is increased by feeding the low silage diet. Together, these results point out to a higher lipid turnover in the SAT of Barrosã bulls when compared to Alentejana. In turn, lipid deposition in the LL muscle is related to the expression of adipogenic (PPARG and FABP4) and lipogenic (ACACA and SCD) genes. The positive correlation between ACACA expression levels and total lipids, as well trans fatty acids, points to ACACA as a major player in intramuscular deposition in ruminants. Moreover, results reinforce the role of FABP4 in intramuscular fat development and the SAT as the major site for lipid metabolism in ruminants.

Conclusions

Overall, the results showed that SAT and LL muscle fatty acid composition are mostly dependent on the genetic background. In addition, dietary silage level impacted on muscle lipid metabolism to a greater extent than on that of SAT, as evaluated by gene expression levels of adipogenic and lipogenic factors. Moreover, the response to diet composition evaluated through mRNA levels and fatty acid composition showed interesting differences between Alentejana and Barrosã bulls. These findings provide evidence that the genetic background should be taken into account while devising diet-based strategies to manipulate fatty acid composition of beef cattle tissues.

【 授权许可】

   
2013 da Costa et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150208074019458.pdf 544KB PDF download
Figure 3. 24KB Image download
Figure 2. 37KB Image download
Figure 1. 42KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】
  • [1]Hocquette JF, Chatellier V: Prospects for the European beef sector over the next 30 years. Anim Front 2011, 25:20-28.
  • [2]Scollan N, Hocquette JF, Nuernberg K, Dannenberger D, Richardson I, Moloney A: Innovations in beef production systems that enhance the nutritional and health value of beef lipids and their relationship with meat quality. Meat Sci 2006, 74:17-33.
  • [3]Pickworth CL, Loerch SC, Velleman SG, Pate JL, Poole DH, Fluharty FL: Adipogenic differentiation state-specific gene expression as related to bovine carcass adiposity. J Anim Sci 2011, 89:355-366.
  • [4]Hiller B, Hocquette JF, Cassar-Malek I, Nuernberg G, Nuernberg K: Dietary n-3 PUFA affect lipid metabolism and tissue function-related genes in bovine muscle. Br J Nutr 2012, 108:858-863.
  • [5]Roh S, Hishikawa D, Hong Y-H, Sasaki S: Control of adipogenesis in ruminants. Anim Sci J 2006, 77:472-477.
  • [6]Mannen H: Identification and utilization of genes associated with beef qualities. Anim Sci J 2011, 82:1-7.
  • [7]Taniguchi M, Guan LL, Zhang B, Dodson MV, Okine E, Moore SS: Gene expression patterns of bovine perimuscular preadipocytes during adipogenesis. Biochem Bioph Res Co 2008, 366:346-351.
  • [8]Fernyhough ME, Helterline DL, Vierck JL, Hausman GJ, Hill RA, Dodson MV: Dedifferentiation of mature adipocytes to form adipofibroblasts: more than just a possibility. Adipocytes 2005, 1:17-24.
  • [9]Wang YH, Byrne KA, Reverter A, Harper GS, Taniguchi M, McWilliam SM, Mannen H, Oyama K, Lehnert S: Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mamm Genome 2005, 16:201-210.
  • [10]Zhang Q, Lee HG, Han JA, Kim EB, Kang SK, Yin J, Baik M, Shen Y, Kim SH, Seo KS, Choi YJ: Differentially expressed proteins during fat accumulation in bovine skeletal muscle. Meat Sci 2010, 86:814-820.
  • [11]Lee SH, Gondro C, van der Werf J, Kim NK, Lim DJ, Park EW, Oh SJ, Gibson JP, Thompson JM: Use of a bovine genome array to identify new biological pathways for beef marbling in Hanwoo (Korean Cattle). BMC Genomics 2010, 11:623. BioMed Central Full Text
  • [12]Lehnert S, Reverter A, Byrne KA, Wang Y, Nattrass GS, Hudson NJ, PL G w: Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds. BMC Dev Biol 2007, 7:95. BioMed Central Full Text
  • [13]Aldai N, Najera AI, Dugan ME, Celaya R, Osoro K: Characterization of intramuscular, intermuscular and subcutaneous adipose tissues in yearling bulls of different genetic groups. Meat Sci 2007, 76:682-691.
  • [14]Wood JD, Enser M, Fisher AV, Nute GR, Sheard PR, Richardson RI, Hughes SI, Whittington FM: Fat deposition, fatty acid composition and meat quality: a review. Meat Sci 2008, 78:343-358.
  • [15]Widman P, Nuernberg K, Kuehn C, Weikard R: Association of an ACSL1 gene variant with polyunsaturated fatty acids in bovine skeletal muscle. BMC Genet 2011, 12:96.
  • [16]Pavan E, Duckett SK: Corn oil or corn grain supplementation to steers grazing endophyte-free tall fescue. I. Effects on in vivo digestibility, performance, and carcass quality. J Anim Sci 2008, 86:3215-3223.
  • [17]Hoashi S, Hinenoya T, Tanaka A, Ohsaki H, Sasaki S, Taniguchi M, Oyama K, Mukai F, Mannen H: Association between fatty acid compositions and genotypes of FABP4 and LXR-alpha in Japanese Black cattle. BMC Genet 2008, 9:84.
  • [18]Beja-Pereira A, Alexandrino P, Bessa I, Carretero Y, Dunner S, Ferrand N, Jordana J, Laloe D, Moazami-Goudarzi K, Sanchez A, Cañon J: Genetic characterization of Southwestern European bovine breeds: a historical and biogeographical reassessment with a set of 16 microsatellites. J Hered 2003, 94:243-250.
  • [19]Costa P, Lemos JP, Lopes PA, Alfaia CM, Costa ASH, Bessa RJB, Prates JAM: Effect of low- and high-forage diets on meat quality and fatty acid composition of Alentejana and Barrosã beef breeds. Animal 2012, 6:1187-1197.
  • [20]Wang YH, Bower NI, Reverter A, Tan SH, De Jager N, Wang R, Macwilliam SM, Cafe LM, Greenwood PL, Lenhert SA: Gene expression patterns during intramuscular fat development in cattle. J Anim Sci 2009, 87:119-130.
  • [21]Albrecht E, Gotoh T, Ebara F, Xu JX, Viergutz T, Nüernberg G, Maak S, Wegner J: Cellular conditions for intramuscular fat deposition in Japanese Black and Holstein steers. Meat Sci 2011, 89:13-20.
  • [22]Taniguchi M, Mannen H, Oyama K, Shimakura Y, Oka A, Watanabe H, Kojima T, Komatsu M, Harper GS, Tsuji S: Differences in stearoyl-CoA desaturase mRNA levels between Japanese Black and Holstein cattle. Livest Prod Sci 2004, 87:215-220.
  • [23]Medina-Gomez G, Gray SL, Yetukuri L, Shimomura K, Virtue S, Campbell M, Curtis RK, Jimenez-Linan M, Blount M, Yeo GSH, Lopez M, Seppänen-Laakso T, Ashcroft FM, Orešič M, Vidal-Puig A: PPAR gamma 2 prevents lipotoxicity by controlling adipose tissue expandability and peripheral lipid metabolism. PLoS Genet 2007, 3:e64.
  • [24]Gregoire FM, Smas CM, Sul HS: Understanding adipocyte differentiation. Physiol Rev 1998, 78:783-880.
  • [25]Harper GS, Pethick DW: How might marbling begin? Aust J Exp Agr 2004, 44:653-662.
  • [26]Briggs MR, Yokoyama C, Wang X, Brown MS, Goldstein JL: Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. I. Identification of the protein and delineation of its target nucleotide sequence. J Biol Chem 1993, 268:14490-14496.
  • [27]Brown MS, Goldstein JL: The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89:331-340.
  • [28]Worgall TS, Sturley SL, Seo T, Osborne TF, Deckelbaum RJ: Polyunsaturated fatty acids decrease expression of promoters with sterol regulatory element-binding protein. J Biol Chem 1998, 273:25537-25540.
  • [29]Graugnard DE, Berger LL, Faulkner DB, Loor JJ: High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle. Brit J Nutr 2010, 103:953-963.
  • [30]Kim JB, Wright HM, Wright M, Spiegelman BM: ADD1/SREBP1 activates PPARgamma through the production of endogenous ligand. Proc Natl Acad Sci USA 1998, 95:4333-4337.
  • [31]Costa ASH, Lopes PA, Estevão M, Martins SV, Alves SP, Pissarra H, Correia JJ, Pinho M, Fontes CMGA, Prates JAM: Contrasting cellularity and fatty acid composition in fat depots from Alentejana and Barrosã bovine breeds fed high and how forage diets. Int J Biol Sci 2012, 8:214-227.
  • [32]Sekiya M, Yahagi N, Matsuzaka T, Takeuchi Y, Nakagawa Y, Takahashi H, Okazaki H, Iizuka Y, Ohashi K, Gotoda T, Ishibashi S, Nagai R, Yamazaki T, Kadowaki T, Yamada N, Osuga J, Shimano H: SREBP-1-independent regulation of lipogenic gene expression in adipocytes. J Lipid Res 2007, 48:1581-1591.
  • [33]Yang R, Castriota G, Chen Y, Cleary MA, Ellsworth K, Shin MK, Tran J-L, Vogt TF, Wu M, Xu S, Yang X, Zhang BB, Berger JP, Quresh SA: RNAi-mediated germline knockdown of FABP4 increases body weight but does not improve the deranged nutrient metabolism of diet-induced obese mice. Int J Obesity 2011, 35:217-225.
  • [34]Shen WJ, Bernlohr K, Sridhar DA, Bernlohr DA, Kraemer FB: Interaction of rat hormone-sensitive lipase with adipocyte lipid-binding protein. P Natl Acad Sci USA 1999, 96:5528-5532.
  • [35]Damcott CM, Moffett SP, Feingold E, Barmada MM, Marshall JA, Hamman RF, Ferrell RE: Genetic variation in fatty acid-binding protein-4 and peroxisome proliferator-activated receptor gamma interactively influence insulin sensitivity and body composition in males. Metabolism 2004, 53:303-309.
  • [36]Cho S, Park TS, Yoon D, Cheong HS, Namgoong S, Park BL, Lee HW, Han CS, Kim EM, Cheong I-C, Kim H, Shin HD: Identification of genetic polymorphisms in FABP3 and FABP4 and putative association with back fat depth in Wagyu × Limousin F2 crosses. Anim Genet 2008, 37:29-34.
  • [37]Jurie C, Cassar-Malek I, Bonnet M, Leroux C, Bauchart D, Boulesteix P, Pethick DW, Hocquette JF: Adipocyte fatty acid-binding protein and mitochondrial enzyme activities in muscles as relevant indicators of marbling in cattle. J Anim Sci 2007, 85:2660-2669.
  • [38]Michal JJ, Zhang ZW, Gaskins CT, Jiang Z: The bovine fatty acid binding protein 4 gene is significantly associated with marbling and subcutaneous fat depth in Wagyu × Limousin F2 crosses. Anim Genet 2006, 37:400-402.
  • [39]Laliotis GP, Bizelis I, Rogdakis E: Comparative approach of the de novo fatty acid synthesis (lipogenesis) between ruminant and non ruminant mammalian species: from biochemical level to the main regulatory lipogenic genes. Curr Genomics 2010, 11:168-183.
  • [40]McGarry JD, Woeltje KF, Kuwajima M, Foster DW: Regulation of ketogenesis and the renaissance of carnitine palmitoyltransferase. Diabetes Metab Rev 1989, 5:271-284.
  • [41]Joseph SJ, Robbins KR, Pavan E, Pratt SL, Duckett SK, Rekaya R: Effect of diet supplementation on the expression of bovine genes associated with fatty acid synthesis and metabolism. Bioinform Biol Insights 2010, 4:19-31.
  • [42]Chilliard Y, Gagliostro G, Fléchet J, Lefaivre J, Sebastian I: Duodenal rapeseed oil infusion in early and midlactation cows. 5. Milk fatty acids and adipose tissue lipogenic activities. J Dairy Sci 1991, 74:1844-1854.
  • [43]Underwood KR, Tong J, Zhu MJ, Shen QW, Means WJ, Ford SP, Paisley SI, Hess BW, Du M: Relationship between kinase phosphorylation, muscle fiber typing, and glycogen accumulation in longissimus muscle of beef cattle with high and low intramuscular fat. J Agr and Food Chem 2007, 55:9698-9703.
  • [44]Daniel CTR, Wynn RJ, Salter AM, Buttery PJ: Differing effects of forage and concentrate diets on the oleic acid and conjugated linoleic acid content of sheep tissues: The role of stearoyl-CoA desaturase. J Anim Sci 2004, 82:747-758.
  • [45]Ward RE, Woodward B, Otter N, Doran O: Relationship between the expression of key lipogenic enzymes, fatty acid composition, and intramuscular fat content of Limousin and Aberdeen Angus cattle. Livest Sci 2010, 127:22-29.
  • [46]Chung KY, Lunt DK, Kawachi H, Yano H, Smith SB: Lipogenesis and stearoyl-CoA desaturase gene expression and enzyme activity in adipose tissue of short- and long-fed Angus and Wagyu steers fed corn- or hay-based diets. J Anim Sci 2007, 85:380-387.
  • [47]Dance LJE, Matthews KR, Doran O: Effect of breed on fatty acid composition and stearoyl-CoA desaturase protein expression in the Semimembranosus muscle and subcutaneous adipose tissue of cattle. Livest Sci 2009, 125:291-297.
  • [48]Duckett SK, Pratt SL, Pavan E: Corn oil or corn grain supplementation to steers grazing endophyte-free tall fescue. II. Effects on subcutaneous fatty acid content and lipogenic gene expression. J Anim Sci 2009, 87:1120-1128.
  • [49]Bartoň L, Bureš D, Kott T, Řehák D: Effect of sex and age on bovine muscle and adipose fatty acid composition and stearoyl-CoA desaturase mRNA expression. Meat Sci 2011, 89:444-450.
  • [50]Nakamura MT, Nara TY: Essential fatty acid synthesis and its regulation in mammals. Prostag Leukotr Ess 2003, 68:145-150.
  • [51]Ntambi JM, Miyazaki M: Regulation of stearoyl-CoA desaturases and role in metabolism. Prog Lipid Res 2004, 43:91-104.
  • [52]Barbier O, Torra IP, Duguay Y, Blanquart C, Fruchart JC, Glineur C, Staels B: Pleiotropic actions of peroxisome proliferator-activated receptors in lipid metabolism and atherosclerosis. Arterioscler Thromb Vasc Biol 2002, 22:717-726.
  • [53]Guillou H, Martin P, Jan S, D’Andrea S, Roulet A, Catheline D, Rioux V, Pineau T, Legrand P: Comparative Effect of Fenofibrate on Hepatic Desaturases in Wild-Type and Peroxisome Proliferator-Activated Receptor α-Deficient Mice. Lipids 2002, 37:981-989.
  • [54]Jogl G, Hsiao YS, Tong L: Structure and function of carnitine acyltransferases. Ann NY Acad Sci 2006, 1033:17-29.
  • [55]Calabrese V, Stella AMG, Calvani M, Butterfield DA: Acetylcarnitine and cellular stress response: roles in nutritional redox homeostasis and regulation of longevity genes. J Nutr Biochem 2006, 17:73-88.
  • [56]Smith SB, Crouse JD: Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. J Nutr 1984, 114:792-800.
  • [57]Schoonmaker JP, Fluharty FL, Loerch SC: Effect of source and amount of energy and rate of growth in the growing phase on adipocyte cellularity and lipogenic enzyme activity in the intramuscular and subcutaneous fat depots of Holstein steers. J Anim Sci 2004, 82:137-148.
  • [58]Dodson MV, Hausman GJ, Guan LL, Min D, 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 an- imals as experimental models for metabolic research. Int J Bio Sci 2010, 6:691-699.
  • [59]Eguinoa P, Brocklehurst S, Arana A, Mendizabal JA, Vernon RG, Purroy A: Lipogenic enzyme activities in different adipose depots of Pirenaican and Holstein bulls and heifers taking into account adipocyte size. J Anim Sci 2003, 81:432-440.
  • [60]Martins AP, Lopes PA, Costa ASH, Martins SV, Santos NC, Prates JAM, Moura TF, Soveral G: Differential mesenteric fat deposition in bovines fed on silage or concentrate is independent of glycerol membrane permeability. Animal 2011, 5:1949-1956.
  • [61]Costa ASH, Costa P, Bessa RJB, Lemos JPC, Simões JA, Santos-Silva J, Fontes CMGA, Prates JA: Carcass fat partitioning and meat quality of Alentejana and Barrosã young bulls fed high or low maize silage diets. Meat Sci 2013, 93:405-412.
  • [62]Folch J, Lees M, Stanley GHS: A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957, 226:497-509.
  • [63]Carlson LA: Extraction of lipids from human whole serum and lipoproteins and from rat liver tissue with methylene chloride-methanol: A comparison with extraction with chloroform-methanol. Clin Chim Acta 1985, 149:89-93.
  • [64]Raes K, Smet SD, Demeyer D: Effect of double-muscling in Belgian Blue young bulls on the intramuscular fatty acid composition with emphasis on conjugated linoleic acid and polyunsaturated fatty acids. Anim Sci 2001, 73:253-260.
  • [65]Bessa RJB, Alves SP, Jerónimo E, Alfaia CM, Prates JAM, Santos-Silva J: Effect of lipid supplements on ruminal biohydrogenation intermediates and muscle fatty acids in lambs. Eur J Lipid Sci Technol 2007, 109:868-878.
  • [66]Rego O, Rosa H, Regalo S, Alves S, Alfaia C, Prates J, Vouzela C, Bessa R: Seasonal changes of CLA isomers and other fatty acids of milk fat from grazing dairy herds in the Azores. J Agr Food Chem 2008, 88:1855-1859.
  • [67]Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:7.
  • [68]Andersen CL, Jensen JL, Orntoft TF: Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004, 64:5245-5250.
  • [69]Costa ASH, Silva MP, Alfaia CPM, Pires VMR, Fontes CMGA, Bessa RJB, Prates JAM: Genetic Background and Diet Impact Beef Fatty Acid Composition and Stearoyl-CoA Desaturase mRNA Expression. Lipids 2013, 48:369-381.
  • [70]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta C(T)) Method. Methods 2001, 25:402-408.
  • [71]Milliken GA, Johnson DE: Analysis of Messy Data, Volume III: Analysis of Covariance. London: Chapman and Hall/CRC; 2002.
  文献评价指标  
  下载次数:7次 浏览次数:6次