Abstract
The aim of the study was to investigate the effect of n-3 PUFA enrichment in longissimus muscle on intramuscular fat (IMF) content and expression of related genes in growing-finishing barrows. Two isoenergetic, isonitrogenous and isolipidic diets were formulated: one was basal diet and the other contained 10% linseed. Twenty-four Landrace × NewDamLine barrows weighing 35 ± 3.7 kg were randomly assigned to four treatment groups with six pigs per group. During the whole experimental period of 90 days, all groups were first fed the basal diet and then the linseed diet for 0, 30, 60, and 90 days before slaughter, respectively. Meat quality, fatty acid composition, and expression of genes involved in adipogenesis in longissimus muscle were measured and analyzed. The IMF content increased linearly (P < 0.05) as the linseed diet feeding time prolonged. Meanwhile, n-3 PUFA content and expression of peroxisome proliferator-activated receptor δ (PPARδ), PPARγ, adipocyte fatty acid–binding protein (aP2) and lipoprotein lipase (LPL) increased linearly (P < 0.01) as well, while the expression of wingless related MMTV integration site 10b (Wnt10b) linearly decreased (P < 0.01). Furthermore, significant (P < 0.01) quadratic or linear relation was observed between n-3 PUFA enrichment and expression of these genes, while significant (P < 0.01) quadratic or linear relation was observed between the expression of PPARγ, aP2 or Wnt10b and IMF content. These data show that enhancing n-3 PUFA enrichment in muscle leads to significant increase in IMF content. A possible explanation is due to alterations in the expression of genes involved in adipogenesis, however this will need to be confirmed by protein and enzyme activity studies.
Similar content being viewed by others
Abbreviations
- ALA:
-
α-Linolenic acid
- aP2:
-
Adipocyte fatty acid–binding protein
- IMF:
-
Intramuscular fat
- LPL:
-
Lipoprotein lipase
- MyoD:
-
Myogenic differentiation 1
- n-3 PUFA:
-
n-3 Polyunsaturated fatty acids
- PPARδ:
-
Peroxisome proliferator-activated receptor δ
- PPARγ:
-
Peroxisome proliferator-activated receptor γ
- TNF-α:
-
Tumor necrosis factor-α
- Wnt10b:
-
Wingless related MMTV integration site 10b
References
Verbeke W, Van Oeckel MJ, Warnants N, Viaene J, Boucque CV (1999) Consumer perception, facts and possibilities to improve acceptability of health and sensory characteristics of pork. Meat Sci 53:77–99
Poulos SP, Hausman GJ (2005) Intramuscular adipocytes-potential to prevent lipotoxicity in skeletal muscle. Adipocytes 1:79–94
Young HE, Mancini ML, Wright RP, Smith JC, Black AC Jr, Reagan CR, Lucas PA (1995) Mesenchymal stem cells reside within the connective tissues of many organs. Dev Dyn 202:137–144
Shepherd PR, Gnudi L, Tozzo E, Yang H, Leach F, Kahn BB (1993) Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J Biol Chem 268:22243–22246
Gerbens F (2004) Genetic control of intramuscular fat accretion. In: MFW te Pas, Everts ME, Haagsman HP (ed) Muscle development of livestock animals: physiology, genetics and meat quality. CABI Publishing, London
Lee YB, Kauffman RG (1974) Cellular and enzymatic changes with animal growth in porcine intramuscular adipose tissue. J Anim Sci 38:532–537
Farmer SR (2006) Transcriptional control of adipocyte formation. Cell Metab 4:263–273
Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM (2000) Transcriptional regulation of adipogenesis. Genes Dev 14:1293–1307
Otto TC, Lane MD (2005) Adipose development: from stem cell to adipocyte. Crit Rev Biochem Mol Biol 40:229–242
Rosen ED, MacDougald OA (2006) Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7:885–896
Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA (2000) Inhibition of adipogenesis by Wnt signaling. Science 289:950–953
Prestwich TC, Macdougald OA (2007) Wnt/beta-catenin signaling in adipogenesis and metabolism. Curr Opin Cell Biol 19:612–617
Grimaldi PA (2001) The roles of PPARs in adipocyte differentiation. Prog Lipid Res 40:269–281
Matsusue K, Peters JM, Gonzalez FJ (2004) PPARbeta/delta potentiates PPARgamma -stimulated adipocyte differentiation. FASEB J 18:1477–1479
Grimaldi PA (2007) Peroxisome proliferator-activated receptors as sensors of fatty acids and derivatives. Cell Mol Life Sci 64:2459–2464
MacLaren LA, Guzeloglu A, Michel F, Thatcher WW (2006) Peroxisome proliferator-activated receptor (PPAR) expression in cultured bovine endometrial cells and response to omega-3 fatty acid, growth hormone and agonist stimulation in relation to series 2 prostaglandin production. Domest Anim Endocrinol 30:155–169
Lim K, Han C, Xu L, Isse K, Demetris AJ, Wu T (2008) Cyclooxygenase-2-derived prostaglandin E2 activates beta-catenin in human cholangiocarcinoma cells: evidence for inhibition of these signaling pathways by omega 3 polyunsaturated fatty acids. Cancer Res 68:553–560
Hsu JM, Wang PH, Liu BH, Ding ST (2004) The effect of dietary docosahexaenoic acid on the expression of porcine lipid metabolism-related genes. J Anim Sci 82:683–689
Wood JD, Richardson RI, Nute GR, Fisher AV, Campo MM, Kasapidou E, Sheard PR, Enser M (2004) Effects of fatty acids on meat quality: a review. Meat Sci 66:21–32
Wierbicki E, Deatherage FE (1958) Water content of meats, determination of water-holding capacity of fresh meats. J Agric Food Chem 6:387–392
Xiong YZ, Deng CY (1999) Principle and method of swine testing. Chinese Agriculture Press, Beijing
Bourke RS, Nelson KM, Naumann RA, Young OM (1970) Studies of the production and subsequent reduction swelling in primate: cerebral cortex under isosmotic conditions in vivo. Exp Brain Res 10:427–446
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Demirel G, Wachira AM, Sinclair LA, Wilkinson RG, Wood JD, Enser M (2004) Effects of dietary n-3 polyunsaturated fatty acids, breed and dietary vitamin E on the fatty acids of lamb muscle, liver and adipose tissue. Br J Nutr 91:551–565
Enser M, Hallett KG, Hewett B, Fursey GAJ, Wood JD, Harrington G (1998) The polyunsaturated fatty acid composition of beef and lamb liver. Meat Sci 49:321–327
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
Harper GS, Pethick DW (2004) How might marbling begin? Aust J Exp Agr 44:653–662
Zhan ZP, Huang FR, Luo J, Dai JJ, Yan XH, Peng J (2009) Duration of feeding linseed diet influences expression of inflammation-related genes and growth performance of growing-finishing barrows. J Anim Sci 87:603–611
Warnants N, Van Oeckel MJ, Boucqué CHV (1996) Incorporation of dietary polyunsaturated fatty acids in pork tissues and its implications for the quality of the end products. Meat Sci 44:125–144
Enser M, Richardson RI, Wood JD, Gill BP, Sheard PR (2000) Feeding linseed to increase the n-3 PUFA of pork: fatty acid composition of muscle, adipose tissue, liver and sausages. Meat Sci 55:201–212
Leskanich CO, Matthews KR, Warkup CC, Noble RC, Hazzledine M (1997) The effect of dietary oil containing (n-3) fatty acids on the fatty acid, physicochemical, and organoleptic characteristics of pig meat and fat. J Anim Sci 75:673–683
Riley PA, Enser M, Nute GR, Wood JD (2000) Effects of dietary linseed on nutritional value and other quality aspects of pig muscle and adipose tissue. Anim Sci 71:483–500
Van Oeckel MJ, Casteels M, Warnants N, Van Damme L, Boucqué ChV (1996) Omega-3 fatty acids in pig nutrition: Implications for the intrinsic and sensory quality of the meat. Meat Sci 44:55–63
Romans JR, Johnson RC, Wulf DM, Libal GW, Costello WJ (1995) Effects of ground flaxseed in swine diets on pig performance and on physical and sensory characteristics and omega-3 fatty acid content of pork: I. Dietary level of flaxseed. J Anim Sci 73:1982–1986
Kouba M, Enser M, Whittington FM, Nute GR, Wood JD (2003) Effect of a high-linolenic acid diet on lipogenic enzyme activities, fatty acid composition, and meat quality in the growing pig. J Anim Sci 81:1967–1979
Specht-Overholt S, Romans JR, Marchello MJ, Izard RS, Crews MG, Simon DM, Costello WJ, Evenson PD (1997) Fatty acid composition of commercially manufactured omega-3 enriched pork products, haddock, and mackerel. J Anim Sci 75:2335–2343
Högberg A, Pickova J, Andersson K, Lundström K (2003) Fatty acid composition and tocopherol content of muscle in pigs fed organic and conventional feed with different n6/n3 ratios, respectively. Food Chem 80:177–186
Cameron ND, Enser MB (1991) Fatty acid composition of lipid in Longissimus dorsi muscle of Duroc and British Landrace pigs and its relationship with eating quality. Meat Sci 29:295–307
Jump DB (2002) The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem 277:8755–8758
Sampath H, Ntambi JM (2005) Polyunsaturated fatty acid regulation of genes of lipid metabolism. Annu Rev Nutr 25:317–340
Lee C-H, Olson P, vans RM (2003) Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144:2201–2207
Escher P, Braissant O, Basu-Modak S, Michalik L, Wahli W, Desvergne B (2001) Rat PPARs: quantitative analysis in adult rat tissues and regulation in fasting and refeeding. Endocrinology 142:4195–4202
Tanaka T, Yamamoto J, Iwasaki S et al (2003) Activation of peroxisome proliferator-activated receptor delta induces fatty acid beta-oxidation in skeletal muscle and attenuates metabolic syndrome. Proc Natl Acad Sci USA 100:15924–15929
Fredenrich A, Grimaldi PA (2005) PPAR delta: an uncompletely known nuclear receptor. Diabetes Metab 31:23–27
Amri EZ, Bonino F, Ailhaud G, Abumrad NA, Grimaldi PA (1995) Cloning of a protein that mediates transcriptional effects of fatty acids in preadipocytes: homology to peroxisome proliferator-activated receptors. J Biol Chem 270:2367–2371
Forman BM, Chen J, Evans RM (1997) Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc Natl Acad Sci USA 94:4312–4317
Kliewer SA, Forman BM, Blumberg B, Ong ES, Borgmeyer U, Mangelsdorf DJ, Umesono K, Evans RM (1994) Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc Natl Acad Sci USA 91:7355–7359
Tontonoz P, Nagy L, Alvarez JG, Thomazy VA, Evans RM (1998) PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93:241–252
Kronberg SL, Barcelo-Coblijn G, Shin J, Lee K, Murphy EJ (2006) Bovine muscle n-3 fatty acid content is increased with flaxseed feeding. Lipids 41:1059–1068
Valet P, Tavernier G, Castan-Laurell I, Saulnier-Blache JS, Langin D (2002) Understanding adipose tissue development from transgenic animal models. J Lipid Res 43:835–860
Ding ST, Schinckel AP, Weber TE, Mersmann HJ (2000) Expression of porcine transcription factors and genes related to fatty acid metabolism in different tissues and genetic populations. J Anim Sci 78:2127–2134
Haunerland NH, Spener F (2004) Fatty acid-binding proteins–insights from genetic manipulations. Prog Lipid Res 43:328–349
Goldberg IJ (1996) Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res 37:693–707
Wang YH, Byrne KA, Reverter A, Harper GS, Taniguchi M, McWilliam SM, Mannen H, Oyama K, Lehnert SA (2005) Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mamm Genome 16:201–210
Moldes M, Zuo Y, Morrison RF, Silva D, Park BH, Liu J, Farmer SR (2003) Peroxisome-proliferator-activated receptor gamma suppresses Wnt/beta-catenin signalling during adipogenesis. Biochem J 376:607–613
Argiles JM, Lopez-Soriano J, Almendro V, Busquets S, Lopez-Soriano FJ (2005) Cross-talk between skeletal muscle and adipose tissue: a link with obesity? Med Res Rev 25:49–65
Katoh M, Katoh M (2007) AP1- and NF-kappaB-binding sites conserved among mammalian WNT10B orthologs elucidate the TNFalpha-WNT10B signaling loop implicated in carcinogenesis and adipogenesis. Int J Mol Med 19:699–703
Korver DR, Klasing KC (1997) Dietary fish oil alters specific and inflammatory immune responses in chicks. J Nutr 127:2039–2046
Xi S, Cohen D, Barve S, Chen LH (2001) Fish oil suppressed cytokines and nuclear factor-kappaB induced by murine AIDS virus infection. Nutr Res 21:865–878
Gaines AM, Carroll JA, Yi GF, Allee GL, Zannelli ME (2003) Effect of menhaden fish oil supplementation and lipopolysaccharide exposure on nursery pigs. II: effects on the immune axis when fed simple or complex diets containing no spray-dried plasma. Domest Anim Endocrinol 24:353–365
Dias P, Dilling M, Houghton P (1994) The molecular basis of skeletal muscle differentiation. Semin Diagn Pathol 11:3–14
Lee SH, Park EW, Cho YM, Kim SK, Lee JH, Jeon JT, Lee CS, Im SK, Oh SJ, Thompson JM, Yoon D (2007) Identification of differentially expressed genes related to intramuscular fat development in the early and late fattening stages of hanwoo steers. J Biochem Mol Biol 40:757–764
Teboul L, Gaillard D, Staccini L, Inadera H, Amri E-Z, Grimaldi PA (1995) Thiazolidinediones and fatty acids convert myogenic cells into adipose-like cells. J Biol Chem 270:28183–28187
Grimaldi PA, Teboul L, Inadera H, Gaillard D, Amri EZ (1997) Trans-differentiation of myoblasts to adipoblasts: triggering effects of fatty acids and thiazolidinediones. Prostagland Leuk Essent Fatty 57:71–75
Yeow K, Phillips B, Dani C, Cabane C, Amri EZ, Derijard B (2001) Inhibition of myogenesis enables adipogenic trans-differentiation in the C2C12 myogenic cell line. FEBS Lett 506:157–162
Acknowledgments
This research was supported by the National High Technology R & D Program of China (No. 2006AA10Z140), National Natural Science Foundation of China (No. 30871779) and Major Science & Technology Industrialization Projects in Wuhan City of China (No. 200720112026). All authors contributed to the preparation of the paper and agreed with the submitted manuscript content.
Conflict of interest statement
None.
Author information
Authors and Affiliations
Corresponding authors
Additional information
S. Jiang and J. Peng contributed equally.
About this article
Cite this article
Luo, HF., Wei, HK., Huang, FR. et al. The Effect of Linseed on Intramuscular Fat Content and Adipogenesis Related Genes in Skeletal Muscle of Pigs. Lipids 44, 999–1010 (2009). https://doi.org/10.1007/s11745-009-3346-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11745-009-3346-y