High-fructose diet downregulates long-chain acyl-CoA synthetase 3 expression in liver of hamsters via impairing LXR/RXR signaling pathway

Journal of Lipid Research

Volumn 54, Issue 5, 2013, Pages 1241-1254

  Dong, Bin ^a   Kan, Chin Fung Kelvin ^a   Singh, Amar B ^a   Liu, Jingwen ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Gene expression; Liver X receptor; Retinoid X receptor

Indexed keywords

ARACHIDONOYL COENZYME A; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; LONG CHAIN FATTY ACID COENZYME A LIGASE; LONG CHAIN FATTY ACID COENZYME A LIGASE 1; LONG CHAIN FATTY ACID COENZYME A LIGASE 2; LONG CHAIN FATTY ACID COENZYME A LIGASE 3; LONG CHAIN FATTY ACID COENZYME A LIGASE 4; LONG CHAIN FATTY ACID COENZYME A LIGASE 5; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; OLEOYL COENZYME A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RETINOID X RECEPTOR BETA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL STRAIN HEK293; CHOLESTEROL BLOOD LEVEL; COMPLEX FORMATION; CONTROLLED STUDY; DIET; DOWN REGULATION; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; GENE EXPRESSION REGULATION; HAMSTER; HIGH FRUCTOSE DIET; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPID LIVER LEVEL; LIPID STORAGE; LIVER CELL; LIVER METABOLISM; LIVER WEIGHT; MALE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRIACYLGLYCEROL BLOOD LEVEL;

ACYL COENZYME A; ANIMALS; COENZYME A LIGASES; CRICETINAE; DIET; FRUCTOSE; GENE EXPRESSION REGULATION; LIVER; ORPHAN NUCLEAR RECEPTORS; RETINOID X RECEPTOR BETA; SIGNAL TRANSDUCTION;

EID: 84876789513     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M032599     Document Type: Article

References (47)

1. Faergeman, N. J., and J. Knudsen. 1997. Role of long-chain fatty acyl-coA esters in the regulation of metabolism and in cell signaling. Biochem. J. 323 : 1-12.
2. Coleman, R. A., T. M. Lewin, C. G. Van Horn, and M. R. Gonzalez-Baro. 2002. Do acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? J. Nutr. 132 : 2123-2126.
3. Soupene, E., and F. A. Kuypers. 2008. Mammalian long-chain acyl-CoA synthetases. Exp. Biol. Med. (Maywood). 233 : 507-521.
4. Mashek, D. G., and R. A. Coleman. 2007. Long-chain acyl-CoA synthetases and fatty acid channeling. Future Lipidol. 2 : 465-476.
5. Ellis, J. M., J. L. Frahm, L. O. Li, and R. A. Coleman. 2010. Acylcoenzyme A synthetases in metabolic control. Curr. Opin. Lipidol. 21 : 212-217.
6. Lewin, T. M., and C. G. Van Horn. 2002. Rat liver acyl-CoA synthetase 4 is a peripheral-membrane protein located in two distinct subcellular organelles, peroxisomes, and mitochondrial-associated membrane. Arch. Biochem. Biophys. 404 : 263-270.
7. Lobo, S., B. M. Wiczer, and D. A. Bernlohr. 2009. Functional analysis of long-chain acyl-CoA synthetase 1 in 3T3-L1 adipocytes. J. Biol. Chem. 284 : 18347-18356.
8. Parkes, H. A., E. Preston, D. Wilks, M. Ballesteros, L. Carpenter, L. Wood, E. W. Kraegen, S. M. Furler, and G. J. Cooney. 2006. Overexpression of acyl-CoA synthetase-1 increases lipid deposition in hepatic (HepG2) cells and rodent liver in vivo. Am. J. Physiol. Endocrinol. Metab. 291 : E737-E744.
9. Durgan, D. J., J. K. Smith, M. A. Hotze, O. Egbejimi, K. D. Cuthbert, V. G. Zaha, J. R. B. Dyck, E. D. Abel, and M. E. Young. 2006. Distinct transcriptional regulation of long-chain acyl-CoA synthetase isoforms and cytosolic thioesterase 1 in the rodent heart by fatty acids and insulin. Am. J. Physiol. Heart Circ. Physiol. 290 : H2480-H2497.
10. Marszalek, J. R., C. Ktidis, A. Dararutana, and H. F. Lodish. 2004. Acyl-coA synthetase 2 (ACSL2) over expression enhances fatty acid internalization and neurite outgrowth. J. Biol. Chem. 279 : 23882-23891.
11. Li, L. O., J. M. Ellis, H. A. Paich, S. Wang, N. Gong, G. Altshuller, R. J. Thresher, T. R. Koves, S. M. Watkins, D. M. Muoio, et al. 2009. Liver-specific loss of long chain acyl-CoA synthetase-1 decreases triacylglycerol synthesis and beta-oxidation and alters phospholipid fatty acid composition. J. Biol. Chem. 284 : 27816-27826.
12. Ellis, J. M., O. L. Li, P-C. Wu, T. R. Koves, O. I. Ikayeva, R. D. Stevens, S. M. Watkins, D. M. Muoio, and R. A. Coleman. 2010. Adipose acyl-CoA synthetase-1 directs fatty acids toward α-oxidation and is required for cold thermogenesis. Cell Metab. 12 : 53-64.
13. Ellis, J. M., S. M. Mentock, M. A. DePetrillo, T. R. Koves, S. Sen, S. M. Watkins, D. M. Muoio, G. W. Cline, H. Taegtmeyer, G. I. Shulman, et al. 2011. Mouse cardiac acyl coenzyme A synthetase 1 deficiency impairs fatty acid oxidation and induces cardiac hypertrophy. Mol. Cell. Biol. 31 : 1252-1262.
14. Golej, D. L., B. Askari, F. Kraemer, S. Barnhart, A. Vivekanandan-Giri, S. Pennathur, and K. E. Bornfeldt. 2011. Long-chain acyl-CoA synthetase 4 modulates prostaglandin E2 release from human arterial smooth muscle cells. J. Lipid Res. 52 : 782-793.
15. Mashek, D. G., L. O. Li, and R. A. Coleman. 2006. Rat long-chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet. J. Lipid Res. 47 : 2004-2010.
16. Wu, M., H. Liu, W. Chen, Y. Fujimoto, and J. Liu. 2009. Hepatic expression of long-chain acyl-CoA synthetase 3 is upregulated in hyperlipidemic hamsters. Lipids. 44 : 989-998.
17. Achouri, Y., B. D. Hegarty, D. Allanic, D. Becard, I. Hainault, and F. Foufelle. 2005. Long chain fatty acyl-CoA synthetase 5 expression is induced by insulin and glucose: Involvement of sterol regulatory element-binding protein-1c. Biochimie. 87 : 1149-1155.
18. Schoonjans, K., M. Watanabe, H. Suzuki, A. Mahfoudi, G. Krey, W. Wahli, P. Grimaldi, B. Staels, T. Yamamoto, and J. Auwerx. 1995. Induction of the acyl-coenzyme A synthetase gene by fi brates and fatty acids is mediated by a peroxisome proliferator response element in the C promoter. J. Biol. Chem. 270 : 19269-19276.
19. Martin, G., K. Schoonjans, A-M. Lefebvre, B. Staels, and J. Auwerx. 1997. Coordinate regulation of the expression of the fatty acid transport protein and acyl-CoA synthetase genes by PPAR α and PPAR α activators. J. Biol. Chem. 272 : 28210-28217.
20. Gerhold, D. L., F. Liu, G. Jiang, Z. Li, J. Xu, M. Lu, J. R. Sachs, A. Bagchi, A. Fridman, and D. J. Holder. 2002. Gene expression profile of adipocyte differentiation and its regulation by peroxisome proliferator-activated receptor-gamma agonists. Endocrinology. 143 : 2106-2118.
21. Cao, A., H. Li, Y. Zhou, M. Wu, and J. Liu. 2010. Long chain acyl-CoA synthetase-3 is a molecular target for peroxisome proliferatoractivated receptor α in HepG2 hepatoma cells. J. Biol. Chem. 285 : 16664-16674.
22. Apfel, R., D. Benbrook, E. Lernhardt, M. A. Ortiz, G. Salbert, and M. Pfahl. 1994. A novel orphan receptor specific for a subset of thyroid hormone-responsive elements and its interaction with the retinoid/thyroid hormone receptor subfamily. Mol. Cell. Bio. 14 : 7025-7035.
23. Boergesen, M., T. A. Pedersen, B. Gross, S. J. van Heeinggen, D. Hagenbeek, C. Bindesboll, S. Caron, F. Lalloyer, K. R. Steffensen, H. I. Nebb, et al. 2012. Genome-wide profi ling of liver-X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor α in mouse liver reveals extensive sharing of binding sites. Mol. Cell. Biol. 32 : 852-867.
24. Dawson, M. I., and Z. Xia. 2012. The retinoid X receptors and their ligands. Biochem. Biophys. Acta. 1821 : 21-56.
25. Jakobsson, T., E. Treuter, J. A. Gustafsson, and K. R. Steffensen. 2012. Liver X receptor biology and pharmacology: New pathways, challenges and opportunities. Trends Pharmacol. Sci. 33 : 394-404.
26. Maxwell, K. N., R. E. Soccio, E. M. Duncan, E. Sehayek, and J. L. Reslow. 2003. Novel putative SREBP and LXR target genes identified by microarray analysis in liver of cholesterol-fed mice. J. Lipid Res. 44 : 2109-2119.
27. Weedon-Fekjaer, M. S., K. T. Dalen, K. Solaas, A. C. Staff, A. K. Dutaroy, and H. I. Nebb. 2010. Activation of LXR increases acyl-CoA synthetase activity through direct regulation of ACSL3 in human placental trophoblast cells. J. Lipid Res. 51 : 1886-1896.
28. Srivastava, R. A. K. 2011. Evaluation of anti-atheroclerotic activities of PPAR α, PPAR α, and LXR agonists in hyperlipidemic atherosclerosis-susceptible F1B hamsters. Atherosclerosis. 214 : 86-93.
29. Srivastava, R. A., and S. He. 2010. Anti-hyperlipidemic and insulin sensitizing activities of fenofi brate reduces aortic lipid deposition in hyperlipidemic Golden Syrian hamster. Mol. Cell. Biochem. 345 : 197-206.
30. Ohtani, H., K. Hayashi, Y. Hirata, S. Dojo, K. Nakashima, E. Nishio, H. Kurushima, M. Saeki, and G. Kajiyama. 1990. Effects of dietary cholesterol and fatty acids on plasma cholesterol level and hepatic lipoprotein metabolism. J. Lipid Res. 31 : 1413-1422.
31. Liu, G., L. Fan, and R. Redinger. 1991. The association of hepatic apolipoprotein and lipid metabolism in hamsters and rats. Comp. Biochem. Physiol. A. Comp. Physiol. 99 : 223-228.
32. Sullivan, M. P., J. J. Cerda, F. L. Robbins, C. W. Burgin, and R. J. Beatty. 1993. The gerbil, hamster, and guinea pig as rodent models for hyperlipidemia. Lab. Anim. Sci. 43 : 575-578.
33. Dong, B., M. Wu, H. Li, F. B. Kraemer, K. Adeli, N. G. Seidah, S. W. Park, and J. Liu. 2010. Strong induction of PCSK9 gene expression through HNF1 α and SREBP2: Mechanism for the resistance to LDL-cholesterol lowering effect of statins in dyslipidemic hamsters. J. Lipid Res. 51 : 1486-1495.
34. Basciano, H., E. M. Abigale, M. Naples, C. Baker, R. Kohen, E. Xu, Q. Su, E. M. Allister, M. B. Wichael, and K. Adeli. 2009. Metabolic effects of dietary cholesterol in an animal model of insulin resistance and hepatic steatosis. Am. J. Physiol. Endocrinol. Metab. 297 : E462-E473.
35. Koo, H. Y., M. A. Wallig, B. H. Chung, T. Y. Nara, B. H. Cho, and M. T. Nakamura. 2008. Dietary fructose induces a wide range of genes with distinct shift in carbohydrate and lipid metabolism in fed and fasted rat liver. Biochim. Biophys. Acta. 1782 : 341-348.
36. Koo, H. Y., M. Miyashita, B. H. Cho, and M. T. Nakamura. 2009. Replacing dietary glucose with fructose increases ChREBP activity and SREBP-1 protein in rat liver nucleus. Biochem. Biophys. Res. Commun. 390 : 285-289.
37. Tappy, L., and K. A. Le. 2010. Metabolic effects of fructose and the worldwide increase in obesity. Physiol. Rev. 90 : 23-46.
38. Fujino, T., M. J. Kang, H. Suzuki, H. Iijima, and T. Yamamoto. 1996. Molecular characterization and expression of rat acyl-CoA synthetase 3. J. Biol. Chem. 271 : 16748-16752.
39. Yvan-Charvet, L., M. Ranalletta, N. Wang, S. Han, N. Terasaka, R. Li, C. Wesch, and A. R. Tall. 2007. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J. Clin. Invest. 117 : 3900-3908.
40. Groot, P. H., N. J. Pearce, J. W. Yates, C. Stocker, C. Sauermelch, C. P. Doe, R. N. Willette, A. Olzinski, T. Peters, D. d'Epagnier, et al. 2005. Synthetic LXR agonists increase LDL in CETP species. J. Lipid Res. 46 : 2182-2191.
41. Briand, F., M. Treguier, A. Andre, D. Grillot, M. Issandou, K. Ouguerram, and T. Sulpice. 2010. Liver X receptor activation promotes macrophage-to-feces reverse cholesterol transport in a dyslipidemic hamster model. J. Lipid Res. 51 : 763-770.
42. Quinet, E. M., M. D. Basso, A. R. Halpern, D. W. Yates, R. J. Steffan, V. Clerin, C. Resmini, J. C. Keith, T. J. Berrodin, I. Feingold, et al. 2009. LXR ligand lowers LDL cholesterol in primates, is lipid neutral in hamster, and reduces atherosclerosis in mouse. J. Lipid Res. 50 : 2358-2370.
43. Li, L. O., D. G. Mashek, J. An, S. D. Doughman, C. B. Newgard, and R. A. Coleman. 2006. Overexpression of rat long chain acyl-CoA synthetase 1 alters fatty acid metabolism in rat primary hepatocytes. J. Biol. Chem. 281 : 37246-37255.
44. Brasaemle, D. L., G. Dolios, L. Shapiro, and R. Wang. 2004. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279 : 46835-46842.
45. Poppelreuther, M., B. Rudolph, C. Du, R. Großmann, M. Becker, C. Thiele, R. Ehehalt, and J. Füllekrug. 2012. The N-terminal region of acyl-CoA synthetase 3 is essential for both the localizationon lipid droplets and the function in fatty acid uptake. J. Lipid Res. 53 : 888-900.
46. Bu, S. Y., M. T. Mashek, and D. G. Mashek. 2009. Suppression of long chain acyl-CoA synthetase 3 decreases hepatic de novo fatty acid synthesis through decreased transcriptional activity. J. Biol. Chem. 284 : 30474-30483.
47. Wu, M., A. Cao, B. Dong, and J. Liu. 2011. Reduction of serum free fatty acids and triglycerides by liver-targeted expression of long chain acyl-CoA synthetase 3. Int. J. Mol. Med. 27 : 655-662.