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Dietary n-3 Fatty Acids Significantly Suppress Lipogenesis in Bovine Muscle and Adipose Tissue: A Functional Genomics Approach

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Lipids

Abstract

Changes in fatty acid composition of longissimus muscle and subcutaneous adipose tissue of German Holstein bulls induced by a grass-silage/n-3 fatty acid based intervention diet versus a maize-silage/n-6 fatty acid based control diet were analyzed and related to shifts in lipogenic gene expression, protein expression, and enzyme activity patterns. Significantly higher amounts of n-3 fatty acids and by mean factors of 2.2–2.5 decreased n-6/n-3 fatty acid ratios in both tissues were obtained upon n-3 fatty acid intervention. In longissimus muscle, these changes of fatty acid profiles were associated with reduced SREBP1c (p = 0.02), ACC (p = 0.00), FAS (p = 0.10) and SCD (p = 0.03) gene expression, Δ6D (p = 0.03) and SCD (p = 0.03) protein expression as well as SCD enzyme activity (p = 0.03). In subcutaneous adipose tissue, significantly reduced ACC (p = 0.00) and FAS (p = 0.01) gene expression, SCD protein expression (p = 0.02) and SCD enzyme activity (p = 0.03) were detected upon n-3 fatty acid intervention, although lower degrees of correlation between gene and corresponding gene products were obtained in relation to longissimus muscle. The study elucidates tissue-specific functional genomic responses to dietary fatty acid manipulation in regard to fatty acid profile tailoring of animal tissues.

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Abbreviations

ACC:

Acetyl-CoA carboxylase α

ACTB:

β-actin

B2M:

Β2-microglobulin

CG:

Control group

Δ5D:

Δ5 Desaturase

Δ6D:

Δ6 Desaturase

EEF1A2:

Eukaryotic translation elongation factor 1α2

FAME:

Fatty acid methyl ester(s)

FAS:

Fatty acid synthase

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

IG:

Intervention group

MUFA:

Monounsaturated fatty acids

PUFA:

Polyunsaturated fatty acids

RPS18:

Ribosomal protein S18

SCD:

Stearoyl-CoA desaturase

SFA:

Saturated fatty acids

SF3A1:

Splicing factor 3a, subunit 1

SREBP1c:

Sterol regulatory element binding protein 1c

References

  1. Givens DI, Kliem KE, Gibbs RA (2006) The role of meat as a source of n-3 polyunsaturated fatty acids in the human diet. Meat Sci 74:209–218

    Article  CAS  Google Scholar 

  2. Carpentier YA, Portois L, Malaisse WY (2006) n-3 Fatty acids and the metabolic syndrome. Am J Clin Nutr 83:1499S–1504S

    PubMed  CAS  Google Scholar 

  3. van Dijk SJ, Feskens EJM, Bos MB, Hoelen DWM, Heijligenberg R, Bromhaar MG, de Groot LCPGM, de Vries JHM, Müller M, Afman LA (2009) A saturated fatty acid-rich diet induces an obesity-linked proinflammatory gene expression profile in adipose tissue of subjects at risk of metabolic syndrome. Am J Clin Nutr 90:1656–1664

    Article  PubMed  Google Scholar 

  4. Gebauer SK, Psota TL, Harris WS, Kris-Etherton PM (2006) n-3 Fatty acid dietary recommendations and food sources to achieve essentiality and cardiovascular benefits. Am J Clin Nutr 83:1526S–1535S

    PubMed  CAS  Google Scholar 

  5. Howe P, Meyer B, Record S, Baghurst K (2006) Dietary intake of long-chain n-3 polyunsaturated fatty acids: contribution of meat sources. Nutr 22:47–53

    Article  CAS  Google Scholar 

  6. Woods VB, Fearon AM (2009) Dietary sources of unsaturated fatty acids for animals and their transfer into meat, milk and eggs: a review. Livestock Sci 126:1–20

    Article  Google Scholar 

  7. Scollan N, Hocquette J-F, Nuernberg K, Dannenberger D, Richardson I, Moloney A (2006) Innovations in beef production systems that enhance the nutritional and health value of beef lipids and their relationship with meat quality. Meat Sci 74:17–33

    Article  CAS  Google Scholar 

  8. Wood JD, Richardson RI, Nute GR, Fisher AV, Campo MM, Kasapidou E, Sheard PR, Enser M (2003) Effects of fatty acids on meat quality: a review. Meat Sci 66:21–32

    Article  Google Scholar 

  9. 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 Sci 78:343–358

    Article  CAS  Google Scholar 

  10. Raes K, De Smet S, Demeyer D (2004) Effect of dietary fatty acids on incorporation of long chain polyunsaturated fatty acids and conjugated linoleic acid in lamb, beef and pork meat: a review. Anim Feed Sci Technol 113:199–221

    Article  CAS  Google Scholar 

  11. Nuernberg K, Fischer A, Nuernberg G, Ender K, Dannenberger D (2008) Meat quality and fatty acid composition of lipids in muscle and fatty tissue of Skudde lambs fed grass versus concentrate. Small Ruminant Res 74:279–283

    Article  Google Scholar 

  12. Lee MRF, Evans PR, Nute GR, Richardson RI, Scollan ND (2009) A comparison between red clover silage and grass silage feeding on fatty acid composition, meat stability and sensory quality of the M. longissimus muscle of dairy cull cows. Meat Sci 81:738–744

    Article  CAS  Google Scholar 

  13. Machecha L, Dannenberger D, Nuernberg K, Nuernberg G, Hagemann E, Martin J (2010) Relationship between lipid peroxidation and antioxidant status in the muscle of German Holstein bulls fed n-3 and n-6 PUFA-enriched diets. J Agric Food Chem 58:8407–8413

    Article  Google Scholar 

  14. Zhang S, Knight TJ, Reecy JM, Beitz DC (2008) DNA polymorphisms in bovine fatty acid synthase are associated with beef fatty acid composition. Anim Genet 39:62–70

    Article  PubMed  Google Scholar 

  15. Zhang S, Knight TJ, Reecy JM, Wheeler TL, Shackelford SD, Cundiff LV, Beitz DC (2010) Associations of polymorphisms in the promoter I of bovine acetyl-CoA carboxylase-alpha gene with beef fatty acid composition. Anim Genet 41:417–420

    Article  PubMed  CAS  Google Scholar 

  16. Orrù L, Cifuni GF, Piasentier E, Corazzin M, Bovolenta S, Moioli B (2011) Association analyses of single nucleotide polymorphisms in the LEP and SCD1 genes on the fatty acid profile of muscle fat in Simmental bulls. Meat Sci 87:344–348

    Article  PubMed  Google Scholar 

  17. Bernard L, Leroux C, Chilliard Y (2008) Expression and nutritional regulation of lipogenic genes in the ruminant lactating mammary gland. Adv Exp Med Biol 606:67–108

    Article  PubMed  CAS  Google Scholar 

  18. Dervishi E, Serrano C, Joy M, Serrano M, Rodellar C, Calvo JH (2010) Effect of the feeding system on the fatty acid composition, expression of the Δ9-desaturase, peroxisome proliferator-activated receptor alpha, gamma, and sterol regulatory element binding protein 1 genes in the semitendinosus muscle of light lambs of the Rasa Aragonesa breed. BMC Vet Res 6:1–11

    Article  Google Scholar 

  19. Herdmann A, Nuernberg K, Martin J, Nuernberg G, Doran O (2010) Effect of dietary fatty acids on expression of lipogenic enzymes and fatty acid profile in tissues of bulls. Anim 4:755–762

    Article  CAS  Google Scholar 

  20. Ward RE, Woodward B, Otter N, Doran O (2010) Relationship between the expression of key lipogenic enzymes, fatty acid composition, and intramuscular fat content of Limousin and Aberdeen Angus cattle. Livestock Sci 127:22–29

    Article  Google Scholar 

  21. Waters SM, Kelly JP, O’Boyle P, Moloney AP, Kenny DA (2009) Effect of level and duration of dietary n-3 polyunsaturated fatty acid supplementation on the transcriptional regulation of {Delta}9-desaturase in muscle of beef cattle. J Anim Sci 87:244–252

    Article  PubMed  CAS  Google Scholar 

  22. Vasta V, Priolo A, Scerra M, Hallett KG, Wood JD, Doran O (2009) Δ9 desaturase protein expression and fatty acid composition of longissimus muscle in lambs fed green herbage or concentrate with or without added tannins. Meat Sci 82:357–364

    Article  CAS  Google Scholar 

  23. Herdmann A, Martin J, Nuernberg G, Dannenberger D, Nuernberg K (2010) Effect of dietary n-3 and n-6 PUFA on lipid composition of different tissues of German Holstein bulls and the fate of bioactive fatty acids during processing. J Agric Food Chem 58:8314–8321

    Article  PubMed  CAS  Google Scholar 

  24. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:1–10

    Article  Google Scholar 

  25. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  26. Dannenberger D, Nuernberg G, Scollan N, Schabbel W, Steinhart H, Ender K, Nuernberg K (2004) Effect of diet on the deposition of n-3 fatty acids conjugated linoleic- and C18:1 trans fatty acid isomers in muscle lipids of German Holstein bulls. J Agric Food Chem 52:6607–6615

    Article  PubMed  CAS  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. Kim S, Moustaid-Moussa N (2000) Secretory, endocrine and autocrine/paracrine function of the adipocyte. J Nutr 130:3110S–3115S

    PubMed  CAS  Google Scholar 

  29. Taniguchi M, Mannen H, Oyama K, Shimakura Y, Oka A, Watanabe H, Kojima T, Komatsu M, Harper GS, Tsuji S (2004) Differences in stearoyl-CoA desaturase mRNA levels between Japanese Black and Holstein cattle. Livestock Prod Sci 87:215–220

    Article  Google Scholar 

  30. Dance LJE, Matthews KR, Doran O (2009) Effect of breed on fatty acid composition and stearoyl-CoA desaturase protein expression in the semimembranosus muscle and subcutaneous adipose tissue of cattle. Livestock Sci 125:291–297

    Article  Google Scholar 

  31. Doran O, Moule SK, Teye GA, Whittington FM, Hallett KG, Wood JD (2006) A reduced protein diet induces stearoyl-CoA desaturase protein expression in pig muscle but not in subcutaneous adipose tissue: relationship with intramuscular lipid formation. Br J Nutr 95:609–617

    Article  PubMed  CAS  Google Scholar 

  32. Cánovas A, Estany J, Tor M, Pena RN, Doran O (2009) Acetyl-CoA carboxylase and stearoyl-CoA desaturase protein expression in subcutaneous adipose tissue is reduced in pigs selected for decreased backfat thickness at constant intramuscular fat content. J Anim Sci 87:3905–3914

    Article  PubMed  Google Scholar 

  33. Kokta TA, Dodsonb MV, Gertler A, Hill RA (2004) Intercellular signalling between adipose tissue and muscle tissue. Dom Anim Endocrinol 27:303–331

    Article  CAS  Google Scholar 

  34. Ohsaki H, Sawa T, Sasazaki S, Kano K, Taniguchi M, Mukai F, Mannen H (2007) Stearoyl-CoA desaturase mRNA expression during bovine adipocyte differentiation in primary culture derived from Japanese Black and Holstein cattle. Comp Biochem Physiol A 148:629–634

    Article  CAS  Google Scholar 

  35. Wang YH, Bower NI, Reverter A, Tan SH, De Jager N, Wang R, McWilliam SM, Café LM, Greenwood PL, Lehnert SA (2009) Gene expression patterns during intramuscular fat development in cattle. J Anim Sci 87:119–130

    Article  PubMed  CAS  Google Scholar 

  36. Chung KY, Lunt DK, Kawachi H, Yano H, Smith SB (2007) 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 85:380–387

    Article  PubMed  CAS  Google Scholar 

  37. Guixuan Zhou G, Wang S, Wang Z, Zhu X, Shu G, Liao W, Yu K, Gao P, Xi Q, Wang X, Zhang Y, Yuan L, Jiang Q (2010) Global comparison of gene expression profiles between intramuscular and subcutaneous adipocytes of neonatal landrace pig using microarray. Meat Sci 86:440–450

    Article  PubMed  Google Scholar 

  38. Bartoň L, Kott T, Bureš D, Řehák D, Zahrádková R, Kottová B (2010) The polymorphisms of stearoyl-CoA desaturase (SCD1) and sterol regulatory element binding protein-1 (SREBP-1) genes and their association with the fatty acid profile of muscle and subcutaneous fat in Fleckvieh bulls. Meat Sci 85:15–20

    Article  PubMed  Google Scholar 

  39. Smith SB, Kawachi H, Choi CB, Choi CW, Wu G, Sawyer JE (2009) Cellular regulation of bovine intramuscular adipose tissue development and composition. J Anim Sci 87:E72–E82

    Article  PubMed  CAS  Google Scholar 

  40. Pavan E, Duckett SK (2007) Corn oil supplementation to steers grazing endophyte-free tall fescue. II. Effects on longissimus muscle and subcutaneous adipose fatty acid composition and stearoyl-CoA desaturase activity and expression. J Anim Sci 85:1731–1740

    Article  PubMed  CAS  Google Scholar 

  41. Dridi S, Taouis M, Gertler A, Decuypere E, Buyse J (2007) The regulation of stearoyl-CoA desaturase gene expression is tissue specific in chickens. J Endocrinol 192:229–236

    Article  PubMed  CAS  Google Scholar 

  42. Matsuhashi T, Maruyama S, Uemoto Y, Kobayashi N, Mannen H, Abe T, Sakaguchi S, Kobayashi E (2011) Effects of bovine fatty acid synthase, stearoyl-coenzyme A desaturase, sterol regulatory element-binding protein 1, and growth hormone gene polymorphisms on fatty acid composition and carcass traits in Japanese Black cattle. J Anim Sci 89:12–22

    Article  PubMed  CAS  Google Scholar 

  43. Serra A, Mele M, La Comba F, Conte G, Buccioni A, Secchiari P (2009) Conjugated linoleic acid (CLA) content of meat from three muscles of Massese suckling lambs slaughtered at different weights. Meat Sci 81:396–404

    Article  CAS  Google Scholar 

  44. Daniel ZC, Wynn RJ, Salter AM, Buttery PJ (2004) 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 82:747–758

    PubMed  CAS  Google Scholar 

  45. Deiuliis J, Shin J, Murphy E, Kronberg SL, Eastridge ML, Suh Y, Yoon JT, Lee K (2010) Bovine adipose triglyceride lipase is not altered and adipocyte fatty acid-binding protein is increased by dietary flaxseed. Lipids 45:963–973

    Article  PubMed  CAS  Google Scholar 

  46. Joseph SJ, Robbins KR, Pavan E, Pratt SL, Duckett SK, Rekaya R (2010) Effect of diet supplementation on the expression of bovine genes associated with fatty acid synthesis and metabolism. Bioinform Biol Insights 4:19–31

    Article  PubMed  CAS  Google Scholar 

  47. Lee S-H, Cho Y-M, Lee S-H, Kim B-S, Kim N-K, Choy Y-H, Kim K-H, Yoon D, Im S-K, Oh S-J, Park E-W (2008) Identification of marbling-related candidate genes in M. longissimus dorsi of high- and low marbled Hanwoo (Korean Native Cattle) steers. BMB reports 41:846–851

    PubMed  CAS  Google Scholar 

  48. Dobrzyn A, Dobrzyn P (2006) Stearoyl-CoA desaturase—a new player in skeletal muscle metabolism regulation. J Physiol Pharmacol 57(S10):31–42

    PubMed  Google Scholar 

  49. Sampath H, Miyazaki M, Dobrzyn A, Ntambi JM (2007) Stearoyl-CoA desaturase-1 mediates the pro-lipogenic effects of dietary saturated fat. J Biol Chem 282:2483–2493

    Article  PubMed  CAS  Google Scholar 

  50. Geetha CJ, Herbein JH (2000) Healthier dairy fat using trans-vaccenic acid. Nutr Food Sci 30:304–309

    Article  Google Scholar 

  51. Bonnet M, Faulconnier Y, Leroux C, Jurie C, Cassar-Malek I, Bauchart D, Boulesteix P, Pethick D, Hocquette JF, Chilliard Y (2007) Glucose-6-phosphate dehydrogenase and leptin are related to marbling differences among Limousin and Angus or Japanese Black × Angus steers. J Anim Sci 85:2882–2894

    Article  PubMed  CAS  Google Scholar 

  52. Underwood KR, Tong J, Zhu MJ, Shen QW, Means WJ, Ford SP, Paisley SI, Hess BW, Du M (2007) Relationship between kinase phosphorylation, muscle fiber typing, and glycogen accumulation in longissimus muscle of beef cattle with high and low intramuscular fat. J Agric Food Chem 55:9698–9703

    Article  PubMed  CAS  Google Scholar 

  53. Wells T (2009) Ghrelin—defender of fat. Prog Lipid Res 48:257–274

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The study was conducted and financially supported within the framework of EU Project ProSafeBeef (Project No. FOOD-CT-2006-36241). The authors kindly thank B. Jentz and M. Dahm for their excellent technical assistance.

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Authors and Affiliations

  1. Research Unit Muscle Biology and Growth, Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany

    Beate Hiller, Andrea Herdmann & Karin Nuernberg

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  1. Beate Hiller
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  2. Andrea Herdmann
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  3. Karin Nuernberg
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Correspondence to Beate Hiller.

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Hiller, B., Herdmann, A. & Nuernberg, K. Dietary n-3 Fatty Acids Significantly Suppress Lipogenesis in Bovine Muscle and Adipose Tissue: A Functional Genomics Approach. Lipids 46, 557–567 (2011). https://doi.org/10.1007/s11745-011-3571-z

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