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Individual trans 18:1 Isomers are Metabolised Differently and Have Distinct Effects on Lipogenesis in 3T3-L1 Adipocytes

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Lipids

Abstract

The objective of this research was to study the metabolism of individual trans fatty acids (FAs) that can be found in ruminant fat or partially hydrogenated vegetable oils (PHVO) and determine their effects on FA composition and lipogenic gene expression in adipocytes. Differentiated 3T3-L1 adipocytes were treated with 200 µM of either trans-9-18:1, trans-11-18:1, trans-13-18:1, cis-9-18:1 or BSA vehicle control for 120 h. Trans-9-18:1 increased total cell FA content (µmole/well) compared to other FA treatments, which was mainly related to the accumulation of trans-9-18:1 in the cells. Adipocytes were able to desaturate a significant proportion of absorbed trans-11-18:1 and trans-13-18:1 (~20 and 30 % respectively) to cis-9,trans-11-18:2 and cis-9,trans-13-18:2, whereas trans-9-18:1 was mostly incorporated intact resulting in a greater lipophilic index (i.e. decreased mean FA fluidity) of adipocytes. Trans-9-18:1 up-regulated (P < 0.05) the expression of lipogenic genes including acetyl-CoA carboxylase (1.65 fold), FA synthase (1.45 fold), FA elongase-5 (1.52 fold) and stearoyl-CoA desaturase-1 (1.49 fold), compared to the control, whereas trans-11-18:1 and trans-13-18:1 did not affect the expression of these genes compared to control. Our results suggest that the metabolism and lipogenic properties of trans-11-18:1 and trans-13-18:1, typically the most abundant trans FA in beef from cattle fed forage-based diets, are similar and are different from those of trans-9-18:1, the predominant trans FA in PHVO.

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Abbreviations

ACC:

Acetyl-CoA carboxylase

AFABP:

Adipocyte fatty acid-binding protein

BHP:

Biohydrogenation products

c :

Cis

CLA:

Conjugated linoleic acid

CVD:

Cardiovascular disease

ELOVL5:

Elongation of very long chain fatty acids protein-5

FA:

Fatty acid

FAS:

Fatty acid synthase

LI:

Lipophilic index

MUFA:

Monounsaturated fatty acids

PHVO:

Partially hydrogenated vegetable oils

PPARγ:

Peroxisome proliferator-activated receptor gamma

PUFA:

Polyunsaturated fatty acids

SCD1:

Stearoyl-CoA desaturase-1

SFA:

Saturated fatty acids

SREBP-1:

Sterol regulatory element-binding proteins-1

t :

Trans

References

  1. Dugan MER, Aldai N, Aalhus JL, Rolland DC, Kramer JKG (2011) Review: trans-forming beef to provide healthier fatty acid profiles. Can J Anim Sci 91:545–556

    Article  CAS  Google Scholar 

  2. Yashodhara BM, Umakanth S, Pappachan JM, Bhat SK, Kamath R, Choo BH (2009) Omega-3 fatty acids: a comprehensive review of their role in health and disease. Postgrad Med J 85:84–90

    Article  CAS  PubMed  Google Scholar 

  3. Kelley NS, Hubbard NE, Erickson KL (2007) Conjugated linoleic acid isomers and cancer. J Nutr 137:2599–2607

    CAS  PubMed  Google Scholar 

  4. Jenkins TC, Wallace RJ, Moate PJ, Mosley EE (2008) Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J Anim Sci 86:397–412

    Article  CAS  PubMed  Google Scholar 

  5. Mapiye C, Aldai N, Turner TD, Aalhus JL, Rolland DC, Kramer JKG, Dugan MER (2012) The labile lipid fraction of meat: from perceived disease and waste to health and opportunity. Meat Sci 92:210–220

    Article  CAS  PubMed  Google Scholar 

  6. Santora JE, Palmquist DL, Roehrig KL (2000) Trans-vaccenic acid is desaturated to conjugated linoleic acid in mice. J Nutr 130:208–215

    CAS  PubMed  Google Scholar 

  7. Turpeinen AM, Mutanen M, Aro A, Salminen I, Basu S, Palmquist DL, Griinari JM (2002) Bioconversion of vaccenic acid to conjugated linoleic acid in humans. Am J Clin Nutr 76:504–510

    CAS  PubMed  Google Scholar 

  8. Field CJ, Blewett HH, Proctor S, Vine D (2009) Human health benefits of vaccenic acid. Appl Physiol Nutr Metab 34:979–991

    Article  CAS  PubMed  Google Scholar 

  9. Chilliard Y, Glasser F, Ferlay A, Bernard L, Rouel J, Doreau M (2007) Diet, rumen biohydrogenation and nutritional quality of cow and goat milk fat. Eur J Lipid Sci Technol 109:828–855

    Article  CAS  Google Scholar 

  10. Stender S, Astrup A, Dyerberg J (2008) Ruminant and industrially produced trans fatty acids: health aspects. Food Nutr Res. doi:10.3402/fnr.v52i0.1651

    PubMed Central  PubMed  Google Scholar 

  11. Mozaffarian D, Aro A, Willett WC (2009) Health effects of trans-fatty acids: experimental and observational evidence. Eur J Clin Nutr 63:S5–S21

    Article  CAS  PubMed  Google Scholar 

  12. Mapiye C, Aalhus JL, Turner TD, Rolland DC, Basarab JA, Baron VS, McAllister TA, Block HC, Uttaro B, Lopez-Campos O, Proctor SD, Dugan MER (2013) Effects of feeding flaxseed or sunflower-seed in high-forage diets on beef production, quality and fatty acid composition. Meat Sci 95:98–109

    Article  CAS  PubMed  Google Scholar 

  13. Sterk A, Johansson BE, Taweel HZ, Murphy M, van Vuuren AM, Hendriks WH, Dijkstra J (2011) Effects of forage type, forage to concentrate ratio, and crushed linseed supplementation on milk fatty acid profile in lactating dairy cows. J Dairy Sci 94:6078–6091

    Article  CAS  PubMed  Google Scholar 

  14. Juárez M, Dugan MER, Aalhus JL, Aldai N, Basarab JA, Baron VS, McAllister TA (2011) Effects of vitamin E and flaxseed on rumen-derived fatty acid intermediates in beef intramuscular fat. Meat Sci 88:434–440

    Article  PubMed  Google Scholar 

  15. Wood R (1979) Incorporation of dietary cis and trans octadecenoate isomers in the lipid classes of various rat tissues. Lipids 14:975–982

    Article  CAS  PubMed  Google Scholar 

  16. Gruffat D, De La Torre A, Chardigny JM, Durand D, Loreau O, Bauchart D (2005) Vaccenic acid metabolism in the liver of rat and bovine. Lipids 40:295–301

    Article  CAS  PubMed  Google Scholar 

  17. Kuhnt K, Kraft J, Moeckel P, Jahreis G (2006) Trans-11-18:1 is effectively Δ9-desaturated compared with trans-12-18:1 in humans. Br J Nutr 95:752–761

    Article  CAS  PubMed  Google Scholar 

  18. Evans M, Geigerman C, Cook J, Curtis L, Kuebler B, McIntosh M (2000) Conjugated linoleic acid suppresses triglyceride accumulation and induces apoptosis in 3T3-L1 preadipocytes. Lipids 35:899–910

    Article  CAS  PubMed  Google Scholar 

  19. Evans M, Park Y, Pariza M, Curtis L, Kuebler B, McIntosh M (2001) Trans-10, cis-12 conjugated linoleic acid reduces triglyceride content while differentially affecting peroxisome proliferator activated receptor gamma2 and aP2 expression in 3T3-L1 preadipocytes. Lipids 36:1223–1232

    Article  CAS  PubMed  Google Scholar 

  20. Sera RK, McBride JH, Higgins SA, Rodgerson DO (1994) Evaluation of reference ranges for fatty acids in serum. J Clin Lab Anal 8:81–85

    Article  CAS  PubMed  Google Scholar 

  21. Shaw B, Lambert S, Wong MHT, Ralston JC, Stryjecki C, Mutch DM (2013) Individual saturated and monounsaturated fatty acids trigger distinct transcriptional networks in differentiated 3T3-L1 preadipocytes. J Nutrigenet Nutrigenomics 6:1–15

    Article  CAS  PubMed  Google Scholar 

  22. Cruz-Hernandez C, Deng Z, Zhou J, Hill AR, Yurawecz MP, Delmonte P, Mossoba MM, Dugan MER, Kramer JKG (2004) Methods for analysis of conjugated linoleic acids and trans-18:1 isomers in dairy fats by using a combination of gas chromatography, silver-ion thin-layer chromatography/gas chromatography, and silver-ion liquid chromatography. J AOAC Int 87:545–562

    CAS  PubMed  Google Scholar 

  23. Kramer JK, Hernandez M, Cruz-Hernandez C, Kraft J, Dugan ME (2008) Combining results of two GC separations partly achieves determination of all cis and trans 16:1, 18:1, 18:2 and 18:3 except CLA isomers of milk fat as demonstrated using Ag-ion SPE fractionation. Lipids 43:259–273

    Article  CAS  PubMed  Google Scholar 

  24. Toledo E, Campos H, Ding EL, Wu H, Hu FB, Sun Q, Baylin A (2013) A novel fatty acid profile index-the lipophilic index-and risk of myocardial infarction. Am J Epidemiol 178:392–400

    Article  PubMed Central  PubMed  Google Scholar 

  25. Vahmani P, Glover KE, Fredeen AH (2014) Effects of pasture versus confinement and marine oil supplementation on the expression of genes involved in lipid metabolism in mammary, liver, and adipose tissues of lactating dairy cows. J Dairy Sci 97:4174–4183

    Article  CAS  PubMed  Google Scholar 

  26. Arsenijevic T, Grégoire F, Delforge V, Delporte C, Perret J (2012) Murine 3T3-L1 adipocyte cell differentiation model: validated reference genes for qPCR gene expression analysis. PLoS One 7:e37517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:Research0034

    Article  PubMed Central  PubMed  Google Scholar 

  28. Wu H, Ding EL, Toledo ET, Campos H, Baylin A, Hu FB, Sun Q (2013) A novel fatty acid lipophilic index and risk of CHD in US men: the health professionals follow-up study. Br J Nutr 110:466–474

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Muramatsu K, Maitani Y, Takayama K, Nagai T (1999) The relationship between the rigidity of the liposomal membrane and the absorption of insulin after nasal administration of liposomes modified with an enhancer containing insulin in rabbits. Drug Dev Ind Pharm 25:1099–1105

    Article  CAS  PubMed  Google Scholar 

  30. Pilch PF, Thompson PA, Czech MP (1980) Coordinate modulation of d-glucose transport activity and bilayer fluidity in plasma membranes derived from control and insulin-treated adipocytes. Proc Natl Acad Sci USA 77:915–918

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Ibrahim A, Natarajan S, Ghafoorunissa (2005) Dietary trans-fatty acids alter adipocyte plasma membrane fatty acid composition and insulin sensitivity in rats. Metabolism 54:240–246

    Article  CAS  PubMed  Google Scholar 

  32. Emken EA (1984) Nutrition and biochemistry of trans and positional fatty acid isomers in hydrogenated oils. Annu Rev Nutr 4:339–376

    Article  CAS  PubMed  Google Scholar 

  33. Yu W, Liang X, Ensenauer RE, Vockley J, Sweetman L, Schulz H (2004) Leaky beta-oxidation of a trans-fatty acid: incomplete beta-oxidation of elaidic acid is due to the accumulation of 5-trans-tetradecenoyl-CoA and its hydrolysis and conversion to 5-trans-tetradecenoylcarnitine in the matrix of rat mitochondria. J Biol Chem 279:52160–52167

    Article  CAS  PubMed  Google Scholar 

  34. Banni S (2002) Conjugated linoleic acid metabolism. Curr Opin Lipidol 13:261–266

    Article  CAS  PubMed  Google Scholar 

  35. Wood R, Chumbler F, Wiegand R (1977) Incorporation of dietary cis and trans isomers of octadecenoate in lipid classes of liver and hepatoma. J Biol Chem 252:1965–1970

    CAS  PubMed  Google Scholar 

  36. Du ZY, Degrace P, Gresti J, Loreau O, Clouet P (2010) Dissimilar properties of vaccenic versus elaidic acid in β-oxidation activities and gene regulation in rat liver cells. Lipids 45:581–591

    Article  CAS  PubMed  Google Scholar 

  37. Kadegowda AKG, Burns TA, Miller MC, Duckett SK (2013) Cis-9, trans-11 conjugated linoleic acid is endogenously synthesized from palmitelaidic (C16:1 trans-9) acid in bovine adipocytes. J Anim Sci 91:1614–1623

    Article  CAS  PubMed  Google Scholar 

  38. Mahfouz MM, Valicenti AJ, Holman RT (1980) Desaturation of isomeric trans-octadecenoic acids by rat liver microsomes. Biochim Biophys Acta 618:1–12

    Article  CAS  PubMed  Google Scholar 

  39. Pollard MR, Gunstone FD, James AT, Morris LJ (1980) Desaturation of positional and geometric isomers of monoenoic fatty acids by microsomal preparations from rat liver. Lipids 15:306–314

    Article  CAS  PubMed  Google Scholar 

  40. Kadegowda AKG, Connor EE, Teter BB, Sampugna J, Delmonte P, Piperova LS, Erdman RA (2010) Dietary trans fatty acid isomers differ in their effects on mammary lipid metabolism as well as lipogenic gene expression in lactating mice. J Nutr 140:919–924

    Article  CAS  PubMed  Google Scholar 

  41. Bauchart D, Roy A, Lorenz S, Chardigny J-M, Ferlay A, Gruffat D, Sébédio J-L, Chilliard Y, Durand D (2007) Butters Varying in trans 18:1 and cis-9, trans-11 conjugated linoleic acid modify plasma lipoproteins in the hypercholesterolemic rabbit. Lipids 42:123–133

    Article  CAS  PubMed  Google Scholar 

  42. Meijer GW, van Tol A, van Berkel TJ, Weststrate JA (2001) Effect of dietary elaidic versus vaccenic acid on blood and liver lipids in the hamster. Atherosclerosis 157:31–40

    Article  CAS  PubMed  Google Scholar 

  43. Willett WC, Stampfer MJ, Manson JE, Colditz GA, Speizer FE, Rosner BA, Sampson LA, Hennekens CH (1993) Intake of trans fatty acids and risk of coronary heart disease among women. Lancet 341:581–585

    Article  CAS  PubMed  Google Scholar 

  44. Kameda K, Valicenti AJ, Holman RT (1980) Chain elongation of trans-octadecenoic acid isomers in rat liver microsomes. Biochim Biophys Acta 618:13–17

    Article  CAS  PubMed  Google Scholar 

  45. Shao F, Ford DA (2014) Elaidic acid increases hepatic lipogenesis by mediating sterol regulatory element binding protein-1c activity in HuH-7 cells. Lipids 49:403–413

    Article  CAS  PubMed  Google Scholar 

  46. Vendel Nielsen L, Krogager TP, Young C, Ferreri C, Chatgilialoglu C, Nørregaard Jensen O, Enghild JJ (2013) Effects of elaidic acid on lipid metabolism in HepG2 cells, investigated by an integrated approach of lipidomics, transcriptomics and proteomics. PLoS One 8:e7428

    Article  Google Scholar 

  47. Minville-Walz M, Gresti J, Pichon L, Bellenger S, Bellenger J, Narce M, Rialland M (2012) Distinct regulation of stearoyl-CoA desaturase 1 gene expression by cis and trans C18:1 fatty acids in human aortic smooth muscle cells. Genes Nutr 7:209–216

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Ntambi JM, Miyazaki M (2004) Regulation of stearoyl-CoA desaturases and role in metabolism. Prog Lipid Res 43:91–104

    Article  CAS  PubMed  Google Scholar 

  49. Collins JM, Neville MJ, Hoppa MB, Frayn KN (2010) De novo lipogenesis and stearoyl-CoA desaturase are coordinately regulated in the human adipocyte and protect against palmitate-induced cell injury. J Biol Chem 285:6044–6052

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Ntambi JM, Bene H (2001) Polyunsaturated fatty acid regulation of gene expression. J Mol Neurosci 16:273–278 (discussion 279–284)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Study funding was provided through the AAFC-Peer Review program. T.D. Turner and C. Mapiye acknowledge NSERC Post-Doctoral funding provided by the Alberta Livestock and Meat Association (ALMA). P. Vahmani acknowledges NSERC post-doctoral funding provided by the AAFC-Peer Review program.

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Correspondence to M. E. R. Dugan.

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Vahmani, P., Meadus, W.J., Turner, T.D. et al. Individual trans 18:1 Isomers are Metabolised Differently and Have Distinct Effects on Lipogenesis in 3T3-L1 Adipocytes. Lipids 50, 195–204 (2015). https://doi.org/10.1007/s11745-014-3982-8

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  • DOI: https://doi.org/10.1007/s11745-014-3982-8

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