Using muscle gene expression to estimate triacylglyceride deposition, and relative contributions of fatty acid synthesis and fatty acid import in intramuscular fat in cattle
B. P. Dalrymple A C , B. Guo A B , G. H. Zhou B and W. Zhang B
+ Author Affiliations
- Author Affiliations
A CSIRO Animal, Food and Health Sciences, 306 Carmody Road, St Lucia, Qld 4067, Australia.
B Key Laboratory of Meat Processing and Quality Control, Synergetic Innovation Center of Food Safety and Nutrition, College of Food Science and Technology, Nanjing Agriculture University, Nanjing 210095, P.R. China.
C Corresponding author. Email: brian.dalrymple@csiro.au
Animal Production Science 54(9) 1436-1442 https://doi.org/10.1071/AN14247
Submitted: 12 March 2014 Accepted: 8 June 2014 Published: 17 July 2014
Abstract
Intramuscular fat content (IMF%) in cattle influences the value of individual animals, especially for higher marbling markets. IMF is triacylglyceride (TAG) in lipid droplets in the intramuscular adipocytes. However, there are many different pathways from feed intake to the final common process of TAG synthesis and storage as IMF. To evaluate the relative importance of different pathways we compared changes in the expression of genes encoding proteins involved in the TAG and fatty acid (FA) synthesis pathways in the longissimus muscle of Piedmontese × Hereford (P×H) and Wagyu × Hereford (W×H) crosses. Based on these changes we have estimated the relative contributions of FA synthesised de novo in the intramuscular adipocyte and the uptake of circulating FA (both free and from TAG), from the diet or synthesised de novo in other tissues, to TAG deposition as IMF. We have analysed the impact of different developmental times and different diets on these processes. Increased de novo FA synthesis in intramuscular adipocytes appeared to contribute more than increased FA uptake from circulation to the additional TAG deposition in W×H compared with P×H cattle between 12 and 25 months (forage diet). Changing diet from forage to concentrate appeared to increase the importance of FA uptake from circulation relative to de novo FA synthesis for TAG synthesis in intramuscular adipocytes. These results are consistent with the literature based on analysis of lipid composition. Gene expression appears to provide a simple assay for identification of the source of FA for the deposition of IMF.
Additional keywords: Brahman, fatty acid binding protein 4, Piedmontese, stearoyl-CoA desaturase, Wagyu.
References
Aldai N, Murray BE, Olivan M, Martinez A, Troy DJ, Osoro K, Najera AI (2006) The influence of breed and mh-genotype on carcass conformation, meat physico-chemical characteristics, and the fatty acid profile of muscle from yearling bulls. Meat Science 72, 486–495.| The influence of breed and mh-genotype on carcass conformation, meat physico-chemical characteristics, and the fatty acid profile of muscle from yearling bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWktLrO&md5=4427c805a22aecb10b069259dfc5f486CAS | 22061732PubMed |
Aoki Y, Nakanishi N, Yamada T, Harashima N, Yamazaki T (2001) Subsequent performance and carcass characteristics of Japanese Black x Holstein crossbred steers reared on pasture from weaning at three months of age. Bulletin of the National Grassland Research Institute 60, 40–55.
De Jager N, Hudson NJ, Reverter A, Barnard R, Cafe LM, Greenwood PL, Dalrymple BP (2013) Gene expression phenotypes for lipid metabolism and intramuscular fat in skeletal muscle of cattle. Journal of Animal Science 91, 1112–1128.
| Gene expression phenotypes for lipid metabolism and intramuscular fat in skeletal muscle of cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmsFKntL8%3D&md5=42e5290454673192a1b8f961074a9464CAS | 23296809PubMed |
De Smet S, Webb EC, Claeys E, Uytterhaegen L, Demeyer DI (2000) Effect of dietary energy and protein levels on fatty acid composition of intramuscular fat in double-muscled Belgian Blue bulls. Meat Science 56, 73–79.
| Effect of dietary energy and protein levels on fatty acid composition of intramuscular fat in double-muscled Belgian Blue bulls.Crossref | GoogleScholarGoogle Scholar |
De Smet S, Raes K, Demeyer D (2004) Meat fatty acid composition as affected by fatness and genetic factors: a review. Animal Research 53, 81–98.
| Meat fatty acid composition as affected by fatness and genetic factors: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFymtrs%3D&md5=a69d3edac70d09f8b9f9b55db599118cCAS |
Duckett SK, Wagner DG, Yates LD, Dolezal HG, May SG (1993) Effects of time on feed on beef nutrient composition. Journal of Animal Science 71, 2079–2088.
Goldberg IJ, Eckel RH, Abumrad NA (2009) Regulation of fatty acid uptake into tissues: lipoprotein lipase- and CD36-mediated pathways. Journal of Lipid Research 50, S86–S90.
| Regulation of fatty acid uptake into tissues: lipoprotein lipase- and CD36-mediated pathways.Crossref | GoogleScholarGoogle Scholar | 19033209PubMed |
Gotoh T, Albrecht E, Teuscher F, Kawabata K, Sakashita K, Iwamoto H, Wegner J (2009) Differences in muscle and fat accretion in Japanese Black and European cattle. Meat Science 82, 300–308.
| Differences in muscle and fat accretion in Japanese Black and European cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zisFGhsA%3D%3D&md5=74eec7f3cdd8e1bc3aeff7eca9f8f271CAS | 20416730PubMed |
Graugnard DE, Piantoni P, Bionaz M, Berger LL, Faulkner DB, Loor JJ (2009) Adipogenic and energy metabolism gene networks in longissimus lumborum during rapid post-weaning growth in Angus and Angus x Simmental cattle fed high-starch or low-starch diets. BMC Genomics 10, 142
| Adipogenic and energy metabolism gene networks in longissimus lumborum during rapid post-weaning growth in Angus and Angus x Simmental cattle fed high-starch or low-starch diets.Crossref | GoogleScholarGoogle Scholar | 19335898PubMed |
Graugnard DE, Berger LL, Faulkner DE, Loor JJ (2010) High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle. The British Journal of Nutrition 103, 953–963.
| High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlequ74%3D&md5=b373f44a47f28c24f13a1c9436299b13CAS | 20021700PubMed |
Greenwood PL, Cafe LM, Hearnshaw H, Hennessy DW, Thompson JM, Morris SG (2006) Long-term consequences of birth weight and growth to weaning on carcass, yield and beef quality characteristics of Piedmontese-and Wagyu-sired cattle. Animal Production Science 46, 257–269.
| Long-term consequences of birth weight and growth to weaning on carcass, yield and beef quality characteristics of Piedmontese-and Wagyu-sired cattle.Crossref | GoogleScholarGoogle Scholar |
Guo B, Kongsuwan K, Greenwood PL, Zhou G, Zhang W, Dalrymple BP (2014) A gene expression estimator of intramuscular fat percentage for use in both cattle and sheep. Journal of Animal Science and Biotechnology 5, 35
| A gene expression estimator of intramuscular fat percentage for use in both cattle and sheep.Crossref | GoogleScholarGoogle Scholar |
Hudson NJ, Reverter A, Dalrymple BP (2009) A differential wiring analysis of expression data correctly identifies the gene containing the causal mutation. PLoS Computational Biology 5, e1000382
| A differential wiring analysis of expression data correctly identifies the gene containing the causal mutation.Crossref | GoogleScholarGoogle Scholar | 19412532PubMed |
Im S-S, Kwon S-K, Kim T-H, Kim H-I, Ahn Y-H (2007) Regulation of glucose transporter type 4 isoform gene expression in muscle and adipocytes. IUBMB Life 59, 134–145.
| Regulation of glucose transporter type 4 isoform gene expression in muscle and adipocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtFGmu7w%3D&md5=efffded0b13f97552c2a48e5a3f4a8a7CAS | 17487684PubMed |
Lehnert SA, Reverter A, Byrne KA, Wang YH, Nattrass GS, Hudson NJ, Greenwood PL (2007) Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds. BMC Developmental Biology 7, 95
| Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds.Crossref | GoogleScholarGoogle Scholar | 17697390PubMed |
May SG, Sturdivant CA, Lunt DK, Miller RK, Smith SB (1993) Comparison of sensory characteristics and fatty acid composition between Wagyu crossbred and Angus steers. Meat Science 35, 289–298.
| Comparison of sensory characteristics and fatty acid composition between Wagyu crossbred and Angus steers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtlamu7Y%3D&md5=fa59b8d7631d0b861e97ab09b69a93f8CAS | 22061222PubMed |
Moisa SJ, Shike DW, Faulkner DB, Meteer WT, Keisler D, Loor JJ (2014) Central role of the PPARγ gene network in coordinating beef cattle intramuscular adipogenesis in response to weaning age and nutrition. Gene Regulation and Systems Biology 8, 17–32.
Pethick DW, Harper GS, Oddy VH (2004) Growth, development and nutritional manipulation of marbling in cattle: a review. Animal Production Science 44, 705–715.
| Growth, development and nutritional manipulation of marbling in cattle: a review.Crossref | GoogleScholarGoogle Scholar |
Smith SB, Kawachi H, Choi CB, Choi CW, Wu G, Sawyer JE (2009) Cellular regulation of bovine intramuscular adipose tissue development and composition. Journal of Animal Science 87, E72–E82.
| Cellular regulation of bovine intramuscular adipose tissue development and composition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3mtVWhuw%3D%3D&md5=d7caaa78ce7337657ca741776eab8180CAS | 18997081PubMed |
Sturdivant CA, Lunt DK, Smith GC, Smith SB (1992) Fatty acid composition of subcutaneous and intramuscular adipose tissues and M. longissimus dorsi of Wagyu cattle. Meat Science 32, 449–458.
| Fatty acid composition of subcutaneous and intramuscular adipose tissues and M. longissimus dorsi of Wagyu cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xls12kur8%3D&md5=8ac97a42d6fd3f449f557885ef0e61efCAS | 22059895PubMed |
Tanaka S (1985) Chemical studies on the adipose tissues and muscle lipids of fattening beef cattle IV. Fatty acid composition and their interrelationships of subcutaneous, intermuscular and abdominal adipose tissues from three beef breeds. Japanese Journal of Dairy and Food Science 34, A61
Wang YH, Reverter A, Mannen H, Taniguchi M, Harper GS, Oyama K, Byrne KA, Oka A, Tsuji S, Lehnert SA (2005) Transcriptional profiling of muscle tissue in growing Japanese Black cattle to identify genes involved with the development of intramuscular fat. Animal Production Science 45, 809–820.
| Transcriptional profiling of muscle tissue in growing Japanese Black cattle to identify genes involved with the development of intramuscular fat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpt1entLs%3D&md5=8d193ae8784829f93339ef875e9ee464CAS |
Wang YH, Bower N, Reverter A, Tan S, De Jager N, Wang R, McWilliam S, Cafe LM, Greenwood PL, Lehnert SA (2009) Gene expression patterns during intramuscular fat development in cattle. Journal of Animal Science 87, 119–130.
| Gene expression patterns during intramuscular fat development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptFOmtg%3D%3D&md5=fa27630644bf985596e674d645cadc9bCAS | 18820161PubMed |
Wood JD, Enser M, Fisher AV, Nute GR, Sheard PR, Richardson RI, Hughes SI, Whittington FM (2008) Fat deposition, fatty acid composition and meat quality: a review. Meat Science 78, 343–358.
| Fat deposition, fatty acid composition and meat quality: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCls7s%3D&md5=888ca6c1a34f7dd1dd0eca5d3e83e849CAS | 22062452PubMed |
