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BioMed Research International
Volume 2015, Article ID 535982, 10 pages
http://dx.doi.org/10.1155/2015/535982
Research Article

Individual CLA Isomers, c9t11 and t10c12, Prevent Excess Liver Glycogen Storage and Inhibit Lipogenic Genes Expression Induced by High-Fructose Diet in Rats

1Department of Human Nutrition, Faculty of Food Technology, Agricultural University of Krakow, Balicka 122, 30-149 Krakow, Poland
2Jagiellonian Centre for Experimental Therapeutics (JCET), Jagiellonian University, Bobrzynskiego 14, 30-348 Krakow, Poland
3Department of Chemistry, Faculty of Food Science, Wroclaw University of Environmental and Life Sciences, C. K. Norwida 25, 50-375 Wroclaw, Poland
4Department of Clinical and Experimental Pathomorphology, Jagiellonian University Medical College, Grzegorzecka 16, 31-531 Krakow, Poland
5Department of Experimental Pharmacology, Jagiellonian University Medical College, Grzegorzecka 16, 31-531 Krakow, Poland

Received 10 October 2014; Revised 12 January 2015; Accepted 26 February 2015

Academic Editor: Maria J. Martins

Copyright © 2015 Edyta Maslak et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Kotronen, J. Westerbacka, R. Bergholm, K. H. Pietiläinen, and H. Yki-Järvinen, “Liver fat in the metabolic syndrome,” Journal of Clinical Endocrinology and Metabolism, vol. 92, no. 9, pp. 3490–3497, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Marchesini, E. Bugianesi, G. Forlani et al., “Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome,” Hepatology, vol. 37, no. 4, pp. 917–923, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. J. S. Lim, M. Mietus-Snyder, A. Valente, J.-M. Schwarz, and R. H. Lustig, “The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome,” Nature Reviews Gastroenterology and Hepatology, vol. 7, no. 5, pp. 251–264, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. O. Lee, W. R. Bruce, Q. Dong, J. Bruce, R. Mehta, and P. J. O'Brien, “Fructose and carbonyl metabolites as endogenous toxins,” Chemico-Biological Interactions, vol. 178, no. 1–3, pp. 332–339, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. R. B. Kostogrys and P. M. Pisulewski, “Effect of conjugated linoleic acid (CLA) on lipid profile and liver histology in laboratory rats fed high-fructose diet,” Environmental Toxicology and Pharmacology, vol. 30, no. 3, pp. 245–250, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. F. G. S. Toledo, A. D. Sniderman, and D. E. Kelley, “Influence of hepatic steatosis (fatty liver) on severity and composition of dyslipidemia in type 2 diabetes,” Diabetes Care, vol. 29, no. 8, pp. 1845–1850, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. C. Martin and K. Valeille, “Conjugated linoleic acids: all the same or to everyone its own function?” Reproduction Nutrition Development, vol. 42, no. 6, pp. 525–536, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. M. W. Pariza, Y. Park, and M. E. Cook, “The biologically active isomers of conjugated linoleic acid,” Progress in Lipid Research, vol. 40, no. 4, pp. 283–298, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. P. L. Mitchell and R. S. McLeod, “Conjugated linoleic acid and atherosclerosis: studies in animal models,” Biochemistry and Cell Biology, vol. 86, no. 4, pp. 293–301, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. J. W. Ryder, C. P. Portocarrero, X. M. Song et al., “Isomer-specific antidiabetic properties of conjugated linoleic acid: improved glucose tolerance, skeletal muscle insulin action, and UCP-2 gene expression,” Diabetes, vol. 50, no. 5, pp. 1149–1157, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Noto, P. Zahradka, N. R. Ryz, N. Yurkova, X. Xie, and C. G. Taylor, “Dietary conjugated linoleic acid preserves pancreatic function and reduces inflammatory markers in obese, insulin-resistant rats,” Metabolism: Clinical and Experimental, vol. 56, no. 1, pp. 142–151, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. X.-R. Zhou, C.-H. Sun, J.-R. Liu, and D. Zhao, “Dietary conjugated linoleic acid increases PPARγ gene expression in adipose tissue of obese rat, and improves insulin resistance,” Growth Hormone and IGF Research, vol. 18, no. 5, pp. 361–368, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Kennedy, K. Martinez, S. Schmidt, S. Mandrup, K. LaPoint, and M. McIntosh, “Antiobesity mechanisms of action of conjugated linoleic acid,” The Journal of Nutritional Biochemistry, vol. 21, no. 3, pp. 171–179, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. L. D. Whigham, A. C. Watras, and D. A. Schoeller, “Efficacy of conjugated linoleic acid for reducing fat mass: a meta-analysis in humans,” The American Journal of Clinical Nutrition, vol. 85, no. 5, pp. 1203–1211, 2007. View at Google Scholar · View at Scopus
  15. B. A. Watkins, Y. Li, H. E. Lippman, S. Reinwald, and M. F. Seifert, “A test of Ockham's razor: implications of conjugated linoleic acid in bone biology,” The American Journal of Clinical Nutrition, vol. 79, supplement 6, pp. 1175S–1185S, 2004. View at Google Scholar · View at Scopus
  16. I. Platt, L. G. Rao, and A. El-Sohemy, “Isomer-specific effects of conjugated linoleic acid on mineralized bone nodule formation from human osteoblast-like cells,” Experimental Biology and Medicine, vol. 232, no. 2, pp. 246–252, 2007. View at Google Scholar · View at Scopus
  17. S. W. Ing and M. A. Belury, “Impact of conjugated linoleic acid on bone physiology: proposed mechanism involving inhibition of adipogenesis,” Nutrition Reviews, vol. 69, no. 3, pp. 123–131, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Purushotham, G. E. Shrode, A. A. Wendel, L.-F. Liu, and M. A. Belury, “Conjugated linoleic acid does not reduce body fat but decreases hepatic steatosis in adult Wistar rats,” Journal of Nutritional Biochemistry, vol. 18, no. 10, pp. 676–684, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. P. M. Coen, P. M. Cummins, Y. A. Birney, R. Devery, and P. A. Cahill, “Modulation of nitric oxide and 6-keto-prostaglandin F-1alpha production in bovine aortic endothelial cells by conjugated linoleic acid,” Endothelium, vol. 11, no. 3-4, pp. 211–220, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. A. P. Torres-Duarte and J. Y. Vanderhoek, “Conjugated linoleic acid exhibits stimulatory and inhibitory effects on prostanoid production in human endothelial cells and platelets,” Biochimica et Biophysica Acta: Molecular Cell Research, vol. 1640, no. 1, pp. 69–76, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. P. G. Reeves, F. H. Nielsen, and G. C. Fahey Jr., “AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet,” Journal of Nutrition, vol. 123, no. 11, pp. 1939–1951, 1993. View at Google Scholar · View at Scopus
  22. J. Folch, M. Lees, and G. H. S. Stanley, “A simple method for the isolation and purification of total lipides from animal tissues,” The Journal of Biological Chemistry, vol. 226, no. 1, pp. 497–509, 1957. View at Google Scholar · View at Scopus
  23. R. Wirasnita, T. Hadibarata, Y. M. Novelina, A. R. M. Yusoff, and Z. Yusop, “A modified methylation method to determine fatty acid content by gas chromatography,” Bulletin of the Korean Chemical Society, vol. 34, no. 11, pp. 3239–3242, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Bartuś, M. Łomnicka, R. B. Kostogrys et al., “1-Methylnicotinamide (MNA) prevents endothelial dysfunction in hypertriglyceridemic and diabetic rats,” Pharmacological Reports, vol. 60, no. 1, pp. 127–138, 2008. View at Google Scholar · View at Scopus
  25. K. L. Stanhope and P. J. Havel, “Fructose consumption: potential mechanisms for its effects to increase visceral adiposity and induce dyslipidemia and insulin resistance,” Current Opinion in Lipidology, vol. 19, no. 1, pp. 16–24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. A. L. Fracanzani, L. Valenti, E. Bugianesi et al., “Risk of severe liver disease in nonalcoholic fatty liver disease with normal aminotransferase levels: a role for insulin resistance and diabetes,” Hepatology, vol. 48, no. 3, pp. 792–798, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. H. S. Uslusoy, S. G. Nak, M. Gülten, and Z. Biyikli, “Non-alcoholic steatohepatitis with normal aminotransferase values,” World Journal of Gastroenterology, vol. 15, no. 15, pp. 1863–1868, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. M. E. Bocarsly, E. S. Powell, N. M. Avena, and B. G. Hoebel, “High-fructose corn syrup causes characteristics of obesity in rats: Increased body weight, body fat and triglyceride levels,” Pharmacology Biochemistry and Behavior, vol. 97, no. 1, pp. 101–106, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Basaranoglu, G. Basaranoglu, T. Sabuncu, and H. Sentürk, “Fructose as a key player in the development of fatty liver disease,” World Journal of Gastroenterology, vol. 19, no. 8, pp. 1166–1172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. K. S. Collison, S. M. Saleh, R. H. Bakheet et al., “Diabetes of the liver: the link between nonalcoholic fatty liver disease and HFCS-55,” Obesity (Silver Spring), vol. 17, no. 11, pp. 2003–2013, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Araya, R. Rodrigo, L. A. Videla et al., “Increase in long-chain polyunsaturated fatty acid n-6/n-3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease,” Clinical Science, vol. 106, no. 6, pp. 635–643, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. L. A. Videla, R. Rodrigo, J. Araya, and J. Poniachik, “Oxidative stress and depletion of hepatic long-chain polyunsaturated fatty acids may contribute to nonalcoholic fatty liver disease,” Free Radical Biology and Medicine, vol. 37, no. 9, pp. 1499–1507, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Sigruener, M. E. Kleber, S. Heimerl, G. Liebisch, G. Schmitz, and W. Maerz, “Glycerophospholipid and sphingolipid species and mortality: the Ludwigshafen risk and cardiovascular health (LURIC) study,” PLoS ONE, vol. 9, no. 1, Article ID e85724, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Staiger, H. Staiger, C. Weigert, C. Haas, H.-U. Häring, and M. Kellerer, “Saturated, but not unsaturated, fatty acids induce apoptosis of human coronary artery endothelial cells via nuclear factor-κB activation,” Diabetes, vol. 55, no. 11, pp. 3121–3126, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Kadotani, Y. Tsuchiya, H. Hatakeyama, H. Katagiri, and M. Kanzaki, “Different impacts of saturated and unsaturated free fatty acids on COX-2 expression in C2C12 myotubes,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 297, no. 6, pp. E1291–E1303, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. L. W. Xing, L. Zhang, K. Youker et al., “Free fatty acids inhibit insulin signaling-stimulated endothelial nitric oxide synthase activation through upregulating PTEN or inhibiting Akt kinase,” Diabetes, vol. 55, no. 8, pp. 2301–2310, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. X.-Y. Xie, Z.-X. Chen, M.-X. Lei et al., “Ceramide mediates inhibition of the AKT/eNOS signaling pathway by palmitate in human vascular endothelial cells,” Medical Science Monitor, vol. 15, no. 9, pp. BR254–BR261, 2009. View at Google Scholar · View at Scopus
  38. H. B. Eccleston, K. K. Andringa, A. M. Betancourt et al., “Chronic exposure to a high-fat diet induces hepatic steatosis, impairs nitric oxide bioavailability, and modifies the mitochondrial proteome in mice,” Antioxidants and Redox Signaling, vol. 15, no. 2, pp. 447–459, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Pasarín, J. G. Abraldes, A. Rodríguez-Vilarrupla, V. La Mura, J. C. García-Pagán, and J. Bosch, “Insulin resistance and liver microcirculation in a rat model of early NAFLD,” Journal of Hepatology, vol. 55, no. 5, pp. 1095–1102, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Dobrzyn and J. M. Ntambi, “The role of stearoyl-CoA desaturase in the control of metabolism,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 73, no. 1, pp. 35–41, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. P. O. Bonetti, L. O. Lerman, and A. Lerman, “Endothelial dysfunction: a marker of atherosclerotic risk,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 23, no. 2, pp. 168–175, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Bartuś, M. Łomnicka, B. Lorkowska et al., “Hypertriglyceridemia but not hypercholesterolemia induces endothelial dysfunction in the rat,” Pharmacological Reports, vol. 57, supplement, pp. 127–137, 2005. View at Google Scholar · View at Scopus
  43. D. S. Celermajer, “Endothelial dysfunction: does it matter? Is it reversible?” Journal of the American College of Cardiology, vol. 30, no. 2, pp. 325–333, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. E. Stachowska, A. Siennicka, M. Baśkiewcz-Hałasa, J. Bober, B. MacHalinski, and D. Chlubek, “Conjugated linoleic acid isomers may diminish human macrophages adhesion to endothelial surface,” International Journal of Food Sciences and Nutrition, vol. 63, no. 1, pp. 30–35, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. V. DeClercq, C. G. Taylor, J. Wigle, B. Wright, L. Tworek, and P. Zahradka, “Conjugated linoleic acid improves blood pressure by increasing adiponectin and endothelial nitric oxide synthase activity,” Journal of Nutritional Biochemistry, vol. 23, no. 5, pp. 487–493, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. O. A. Gudbrandsen, E. Rodríguez, H. Wergedahl et al., “Trans-10, cis-12-conjugated linoleic acid reduces the hepatic triacylglycerol content and the leptin mRNA level in adipose tissue in obese Zucker fa/fa rats,” British Journal of Nutrition, vol. 102, no. 6, pp. 803–815, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. M. F. Andreoli, P. G. Illesca, M. A. González, and C. A. Bernal, “Conjugated linoleic acid reduces hepatic steatosis and restores liver triacylglycerol secretion and the fatty acid profile during protein repletion in rats,” Lipids, vol. 45, no. 11, pp. 1035–1045, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. P. Priore, A. M. Giudetti, F. Natali, G. V. Gnoni, and M. J. H. Geelen, “Metabolism and short-term metabolic effects of conjugated linoleic acids in rat hepatocytes,” Biochimica et Biophysica Acta: Molecular and Cell Biology of Lipids, vol. 1771, no. 10, pp. 1299–1307, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Noto, P. Zahradka, N. Yurkova et al., “Conjugated linoleic acid reduces hepatic steatosis, improves liver function, and favorably modifies lipid metabolism in obese insulin-resistant rats,” Lipids, vol. 41, no. 2, pp. 179–188, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. J.-L. Sébédio, E. Angioni, J. M. Chardigny, S. Grégoire, P. Juanéda, and O. Berdeaux, “The effect of conjugated linoleic acid isomers on fatty acid profiles of liver and adipose tissues and their conversion to isomers of 16:2 and 18:3 conjugated fatty acids in rats,” Lipids, vol. 36, no. 6, pp. 575–582, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Choi, Y.-C. Kim, Y.-B. Han, Y. Park, M. W. Pariza, and J. M. Ntambi, “The trans-10,cis-12 isomer of conjugated linoleic acid downregulates stearoyl-CoA desaturase 1 gene expression in 3T3-L1 Adipocytes,” Journal of Nutrition, vol. 130, no. 8, pp. 1920–1924, 2000. View at Google Scholar · View at Scopus
  52. J. M. Arbonés-Mainar, M. A. Navarro, S. Acín et al., “Trans-10, cis-12- and cis-9, trans-11-conjugated linoleic acid isomers selectively modify HDL-apolipoprotein composition in apolipoprotein E knockout mice,” Journal of Nutrition, vol. 136, no. 2, pp. 353–359, 2006. View at Google Scholar · View at Scopus
  53. B. De Roos, G. Rucklidge, M. Reid et al., “Divergent mechanisms of cis9, trans11-and trans10, cis12-conjugated linoleic acid affecting insulin resistance and inflammation in apolipoprotein E knockout mice: a proteomics approach,” The FASEB Journal, vol. 19, no. 12, pp. 1746–1748, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. D. M. Stringer, P. Zahradka, V. C. DeClercq et al., “Modulation of lipid droplet size and lipid droplet proteins by trans-10,cis-12 conjugated linoleic acid parallels improvements in hepatic steatosis in obese, insulin-resistant rats,” Biochimica et Biophysica Acta—Molecular and Cell Biology of Lipids, vol. 1801, no. 12, pp. 1375–1385, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Férézou, M. Combettes-Souverain, M. Souidi et al., “Cholesterol, bile acid, and lipoprotein metabolism in two strains of hamster, one resistant, the other sensitive (LPN) to sucrose-induced cholelithiasis,” Journal of Lipid Research, vol. 41, no. 12, pp. 2042–2054, 2000. View at Google Scholar · View at Scopus
  56. J. M. Peters, Y. Park, F. J. Gonzalez, and M. W. Pariza, “Influence of conjugated linoleic acid on body composition and target gene expression in peroxisome proliferator-activated receptor alpha-null mice,” Biochimica et Biophysica Acta—Molecular and Cell Biology of Lipids, vol. 1533, no. 3, pp. 233–242, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. S. M. Rahman, Y.-M. Wang, H. Yotsumoto et al., “Effects of conjugated linoleic acid on serum leptin concentration, body-fat accumulation, and β-oxidation of fatty acid in OLETF rats,” Nutrition, vol. 17, no. 5, pp. 385–390, 2001. View at Publisher · View at Google Scholar · View at Scopus