Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T13:15:09.042Z Has data issue: false hasContentIssue false

Selective transport of long-chain fatty acids by FAT/CD36 in skeletal muscle of broilers

Published online by Cambridge University Press:  16 August 2012

J. Guo
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
G. Shu
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
L. Zhou
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
X. Zhu
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
W. Liao
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
S. Wang
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
J. Yang
Affiliation:
Department of Human Nutrition, Food and Animal Science, University of Hawaii at Manoa, Honolulu, HI 97822, USA
G. Zhou
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
Q. Xi
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
P. Gao
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
Y. Zhang
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
S. Zhang
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
L. Yuan
Affiliation:
Key Laboratory of the Ministry of Education for Cell Biology and Tumor Cell Engineering, School of Life Sciences, Xiamen University, Xiamen 361005, P.R. China
Q. Jiang*
Affiliation:
College of Animal Science, South China Agricultural University, Guangzhou 510640, P.R. China
*
Get access

Abstract

Fatty acid translocase (FAT/CD36) is a membrane receptor that facilitates long-chain fatty acid uptake. To investigate its role in the regulation of long-chain fatty acid composition in muscle tissue, we studied and compared FAT/CD36 gene expression in muscle tissues of commercial broiler chickens and Chinese local Silky fowls. The results from gas chromatography–mass spectrometry analysis of muscle samples demonstrated that Chinese local Silky fowls had significantly higher (P < 0.05) proportions of linoleic acid (LA) and palmitic acid, lower proportions (P < 0.05) of arachidonic acid (AA) and oleic acid than the commercial broiler chickens. The mRNA expression levels of fatty acid (FA) transporters (FA transport protein-1, membrane FA-binding protein, FAT/CD36 and caveolin-1) in the m. ipsilateral pectoralis and biceps femoris were analyzed by Q-PCR, and FAT/CD36 expression levels showed significant differences between these types of chickens (P < 0.01). Interestingly, the levels of FAT/CD36 expression are positively correlated with LA content (r = 0.567, P < 0.01) but negatively correlated with palmitic acid content (r = −0.568, P < 0.01). Further experiments in the stably transfected Chinese hamster oocytes cells with chicken FAT/CD36 cDNA demonstrated that overexpression of FAT/CD36 improves total FA uptake with a significant increase in the proportion of LA and AA, and a decreased proportion of palmitic acid. These results suggest that chicken FAT/CD36 may selectively transport LA and AA, which may lead to the higher LA deposition in muscle tissue.

Type
Physiology and functional biology of systems
Copyright
Copyright © The Animal Consortium 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authours contributed equally to this work.

References

Alexson, SEH, Cannon, B 1984. A direct comparison between peroxisomal and mitochondrial preferences for fatty-acyl [beta]-oxidation predicts channelling of medium-chain and very-long-chain unsaturated fatty acids to peroxisomes. Biochimica et Biophysica Acta – Lipids and Lipid Metabolism 796, 110.CrossRefGoogle ScholarPubMed
Belichenko, VM, Korostishevskaya, IM, Maximov, VF, Shoshenko, CA 2004. Mitochondria and blood supply of chicken skeletal muscle fibers in ontogenesis. Microvascular Research 68, 265272.Google Scholar
Belury, MA, Moya-Camarena, SY, Lu, M, Shi, LL, Leesnitzer, LM, Blanchard, SG 2002. Conjugated linoleic acid is an activator and ligand for peroxisome proliferator-activated receptor-gamma (PPAR gamma). Nutrition Research 22, 817824.Google Scholar
Berk, PD, Wada, H, Horio, Y, Potter, BJ, Sorrentino, D, Zhou, SL, Isola, LM, Stump, D, Kiang, CL, Thung, S 1990. Plasma-membrane fatty acid-binding protein and mitochondrial glutamic-oxaloacetic transaminase of rat-liver are related. Proceedings of the National Academy of Sciences of the United States of America 87, 34843488.Google Scholar
Bezaire, V, Bruce, CR, Heigenhauser, GJF, Tandon, NN, Glata, JFC, Luiken, JJJF, Bonen, A, Spriet, LL 2006. Identification of fatty acid translocase on human skeletal muscle mitochondrial membranes: essential role in fatty acid oxidation. American Journal of Physiology – Endocrinology and Metabolism 290, 509515.Google Scholar
Cameron, N, Enser, M, Nute, G, Whittington, F, Penman, J, Fisken, A, Perry, A, Wood, J 2000. Genotype with nutrition interaction on fatty acid composition of intramuscular fat and the relationship with flavour of pig meat. Meat Science 55, 187195.Google Scholar
Campbell, SE, Tandon, NN, Woldegiorgis, G, Luiken, JJFP, Glatz, JFC, Bonen, A 2004. A novel function for fatty acid translocase (FAT)/CD36. Journal of Biological Chemistry 279, 3623536241.Google Scholar
Chizzolini, R, Zanardi, E, Dorigoni, V, Ghidini, S 1999. Calorific value and cholesterol content of normal and low-fat meat and meat products. Trends in Food Science & Technology 10, 119128.Google Scholar
Cortinas, L, Villaverde, C, Galobart, J, Baucells, MD, Codony, R, Barroeta, AC 2004. Fatty acid content in chicken thigh and breast as affected by dietary polyunsaturation level. Poultry Science 83, 11551164.Google Scholar
De Luis, DA, Conde, R, Aller, R, Izaola, O, Sagrado, MG, Castrillon, JLP, Duenas, A, Romero, E 2009. Effect of omega-3 fatty acids on cardiovascular risk factors in patients with type 2 diabetes mellitus and hypertriglyceridemia: an open study. European Review for Medical and Pharmacological Sciences 13, 5155.Google Scholar
Dransfield, E 2008. The taste of fat. Meat Science 80, 3742.Google Scholar
Eyre, NS, Cleland, LG, Tandon, NN, Mayrhofer, G 2007. Importance of the carboxyl terminus of FAT/CD36 for plasma membrane localization and function in long-chain fatty acid uptake. Journal of Lipid Research 48, 528542.Google Scholar
Feng, JY, Song, YZ, Shu, G, Zhu, XT, Jiang, QY, Gao, P, Xu, PW, Wang, XQ, Feng, DY 2007. Molecular cloning and ontogenetic expression of fatty acid translocase cDNA in yellow-feathered broiler. Scientia Agricultura Sinica 40, 23362342.Google Scholar
Fiedler, I, Nurnberg, K, Hardge, T, Nurnberg, G, Ender, K 2003. Phenotypic variations of muscle fibre and intramuscular fat traits in Longissimus muscle of F-2 population Duroc×Berlin Miniature Pig and relationships to meat quality. Meat Science 63, 131139.CrossRefGoogle ScholarPubMed
Fukuwatari, T, Shibata, K, Iguchi, K, Saeki, T, Iwata, A, Tani, K, Sugimoto, E, Fushiki, T 2003. Role of gustation in the recognition of oleate and triolein in anosmic rats. Physiology & Behavior 78, 579583.Google Scholar
Gao, J, Serrero, G 1999. Adipose differentiation related protein (ADRP) expressed in transfected COS-7 cells selectively stimulates long chain fatty acid uptake. Journal of Biological Chemistry 274, 1682516830.Google Scholar
Griffin, HD, Guo, KD, Windsor, D, Butterwith, SC 1992. Adipose-tissue lipogenesis and fat deposition in leaner broiler-chickens. Journal of Nutrition 122, 363368.Google Scholar
Harmon, CM, Abumrad, NA 1993. Binding of sulfosuccinimidyl fatty-acids to adipocyte membrane-proteins – isolation and amino-terminal sequence of an 88-KD protein implicated in transport of long-chain fatty-acids. Journal of Membrane Biology 133, 4349.Google Scholar
Heinen, MM, Verhage, BAJ, Goldbohm, RA, van den Brandt, PA 2009. Meat and fat intake and pancreatic cancer risk in the Netherlands Cohort Study. International Journal of Cancer 125, 11181126.Google Scholar
Holloway, GP, Luiken, J, Glatz, JFC, Spriet, LL, Bonen, A 2008. Contribution of FAT/CD36 to the regulation of skeletal muscle fatty acid oxidation: an overview. Acta Physiologica 194, 293309.Google Scholar
Holloway, GP, Bezaire, V, Heigenhauser, GJF, Tandon, NN, Glatz, JFC, Luiken, J, Bonen, A, Spriet, LL 2006. Mitochondrial long chain fatty acid oxidation, fatty acid translocase/CD36 content and carnitine palmitoyltransferase I activity in human skeletal muscle during aerobic exercise. Journal of Physiology – London 571, 201210.Google Scholar
Koonen, DPY, Glatz, JFC, Bonen, A, Luiken, JJFP 2005. Long-chain fatty acid uptake and FAT/CD36 translocation in heart and skeletal muscle. Biochimica et Biophysica Acta – Molecular and Cell Biology of Lipids 1736, 163180.Google Scholar
Laugerette, F, Passilly-Degrace, P, Patris, B, Niot, I, Febbraio, M, Montmayeur, JP, Besnard, P 2005. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. Journal of Clinical Investigation 115, 31773184.Google Scholar
Li, JJ, Wen, J, Chen, J, Zhao, GP, Zheng, MQ 2003. Species and age effect on the content of taste things and flavor precursors in chicken. Journal of Animal Husbandry and Veterinary 34, 548553.Google Scholar
Lobo, S, Wiczer, BM, Bernlohr, DA 2009. Functional analysis of long-chain acyl-CoA synthetase 1 in 3T3-L1 adipocytes. Journal of Biological Chemistry 284, 1834718356.Google Scholar
Lyon, C, Lyon, B, Savage, E 2003. Effect of postchill deboning time on the texture profile of broiler breeder hen breast meat. The Journal of Applied Poultry Research 12, 348355.Google Scholar
Marotta, M, Ferrer-Martinez, A, Parnau, J, Turini, M, Mace, K, Foix, AMG 2004. Fiber type- and fatty acid composition-dependent effects of high-fat diets on rat muscle triacylglyceride and fatty acid transporter protein-1 content. Metabolism – Clinical and Experimental 53, 10321036.Google Scholar
Monteiro, ACG, Santos-Silva, J, Bessa, RJB, Navas, DR, Lemos, JPC 2006. Fatty acid composition of intramuscular fat of bulls and steers. Livestock Science 99, 1319.Google Scholar
Morash, AJ, Bureau, DP, McClelland, GB 2009. Effects of dietary fatty acid composition on the regulation of carnitine palmitoyltransferase (CPT) I in rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology B – Biochemistry & Molecular Biology 152, 8593.Google Scholar
Morrison, WR, Smith, LM 1964. Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride–methanol. Journal of Lipid Research 5, 600608.Google Scholar
Mossab, A, Lessire, M, Guillaumin, S, Kouba, M, Mourot, J, Peiniau, P, Hermier, D 2002. Effect of dietary fats on hepatic lipid metabolism in the growing turkey. Comparative Biochemistry and Physiology B – Biochemistry & Molecular Biology 132, 473483.Google Scholar
Motohashi, K, Yamamoto, Y, Shioda, N, Kondo, H, Owada, Y, Fukunaga, K 2009. Role of heart-type fatty acid binding protein in the brain function. Yakugaku Zasshi – Journal of the Pharmaceutical Society of Japan 129, 191195.Google ScholarPubMed
Murphy, EJ, Owada, Y, Kitanaka, N, Kondo, H, Glatz, JFC 2005. Brain arachidonic acid incorporation is decreased in heart fatty acid binding protein gene-ablated mice. Biochemistry 44, 63506360.Google Scholar
Schaffer, JE, Lodish, HF 1994. Expression cloning and characterization of a novel adipocyte long-chain fatty-acid transport protein. Cell 79, 427436.Google Scholar
Scollan, ND, Dhanoa, MS, Choi, NJ, Maeng, WJ, Enser, M, Wood, JD 2001. Biohydrogenation and digestion of long chain fatty acids in steers fed on different sources of lipid. Journal of Agricultural Science 136, 345355.CrossRefGoogle Scholar
Shu, XF, Lin, SM, Wu, HH, Ouyang, KH 2001. Detection and analysis on the fatty acid composition of Jiangxi local chicken. Animal Science & Veterinary Medicine 18, 2224.Google Scholar
Teboul, L, Febbraio, M, Gaillard, D, Amri, EZ, Silverstein, R, Grimaldi, PA 2001. Structural and functional characterization of the mouse fatty acid translocase promoter: activation during adipose differentiation. Biochemical Journal 360, 305312.Google Scholar
Trigatti, BL, Mangroo, D, Gerber, GE 1991. Photoaffinity-labeling and fatty-acid permeation in 3T3-L1 adipocytes. Journal of Biological Chemistry 266, 2262122625.Google Scholar
Trindade, MA, Felício, PE, Castillo, CJC 2004. Mechanically separated meat of broiler breeder and white layer spent hens. Scientia Agricola 61, 234239.Google Scholar
Wang, AX, Liu, GJ, Li, TS 2004. The comparison of muscle fatty acid composition of different yellow-feathered breeds. Feed Exposition 3, 13.Google Scholar
Wong, BXW, Kyle, RA, Croft, KD, Quinn, CM, Jessup, W, Yeap, BB 2011. Modulation of macrophage fatty acid content and composition by exposure to dyslipidemic serum in vitro. Lipids 4, 371380.Google Scholar
Yun, JS, Seo, DS, Kim, WK, Ko, Y 2005. Expression and relationship of the insulin-like growth factor system with posthach growth in the Korean Native Ogol chicken. Poultry Science 84, 8390.Google Scholar