Chenodeoxycholic acid suppresses the activation of acetyl-coenzyme A carboxylase-α gene transcription by the liver X receptor agonist T0-901317

Journal of Lipid Research

Volumn 48, Issue 12, 2007, Pages 2647-2663

  Talukdar, Saswata ^a   Bhatnagar, Sushant ^a   Dridi, Sami ^a   Hillgartner, F Bradley ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Extracellular signal regulated kinase; Fatty acid synthesis; Fibroblast growth factor 19; p38 mitogen activated protein kinase; Peroxisome proliferator activated receptor coactivator 1 ; Sterol regulatory element binding protein

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ABC TRANSPORTER A1; ACETYL COENZYME A CARBOXYLASE; CHENODEOXYCHOLIC ACID; FARNESOID X RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 19; HISTONE H3; HISTONE H4; LIVER X RECEPTOR AGONIST; MITOGEN ACTIVATED PROTEIN KINASE; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SB 600126; SP 600126; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG; UO 126;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHICK; CONTROLLED STUDY; DRUG INHIBITION; DRUG PROTEIN BINDING; FATTY ACID SYNTHESIS; FATTY LIVER; GEL MOBILITY SHIFT ASSAY; GENE ACTIVATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HYPERLIPIDEMIA; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ISOLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACETYL-COA CARBOXYLASE; ANIMALS; BINDING SITES; CHENODEOXYCHOLIC ACID; CHICK EMBRYO; DNA-BINDING PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; SULFONAMIDES; TRANS-ACTIVATION (GENETICS);

EID: 37249028156     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M700189-JLR200     Document Type: Article

References (72)

1. Seol, W., H. S. Choi, and D. D. Moore. 1995. Isolation of proteins that interact specifically with the retinoid X receptor: two novel orphan receptors. Mol. Endocrinol. 9: 72-85.
2. Willy, P. J., K. Umesono, E. S. Ong, R. M. Evans, R. A. Heyman, and D. J. Mangelsdorf. 1995. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 9: 1033-1045.
3. Teboul, M., E. Enmark, Q. Li, A. C. Wikstrom, M. Pelto-Huikko, and J. A. Gustafsson. 1995. OR-1, a member of the nuclear receptor superfamily that interacts with the 9-cis-retinoic acid receptor. Proc. Natl. Acad. Sci. USA. 92: 2096-2100.
4. Xu, L., C. K. Glass, and M. G. Rosenfeld. 1999. Coactivator and corepressor complexes in nuclear receptor function. Curr. Opin. Genet. Dev. 9: 140-147.
5. Wiebel, F. F., K. R. Steffensen, E. Treuter, D. Feltkamp, and J. A. Gustafsson. 1999. Ligand-independent coregulator recruitment by the triply activatable OR1/retinoid X receptor-a nuclear receptor heterodimer. Mol. Endocrinol. 13: 1105-1118.
6. Oberkofler, H., E. Schraml, F. Krempler, and W. Patsch. 2003. Potentiation of liver X receptor transcriptional activity by peroxisome-proliferator-activated receptor gamma co-activator 1α. Biochem. J. 371: 89-96.
7. Janowski, B. A., P. J. Willy, T. R. Devi, J. R. Falck, and D. J. Mangelsdorf. 1996. An oxysterol signalling pathway mediated by the nuclear receptor LXRα. Nature. 383: 728-731.
8. Lehmann, J. M., S. A. Kliewer, L. B. Moore, T. A. Smith-Oliver, B. B. Oliver, J. L. Su, S. S. Sundseth, D. A. Winegar, D. E. Blanchard, T. A. Spencer, et al. 1997. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J. Biol. Chem. 272: 3137-3140.
9. Edwards, P. A., H. R. Kast, and A. M. Anisfeld. 2002. BAREing it all: the adoption of LXR and FXR and their roles in lipid homeostasis. J. Lipid Res. 43: 2-12.
10. Repa, J. J., and D. J. Mangelsdorf. 2002. The liver X receptor gene team: potential new players in atherosclerosis. Nat. Med. 8: 1243-1248.
11. Alberti, S., G. Schuster, P. Parini, D. Feltkamp, U. Diczfalusy, M. Rudling, B. Angelin, I. Bjorkhem, S. Pettersson, and J. A. Gustafsson. 2001. Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXRb-deficient mice. J. Clin. Invest. 107: 565-573.
12. Peet, D. J., S. D. Turley, W. Ma, B. A. Janowski, J. M. Lobaccaro, R. E. Hammer, and D. J. Mangelsdorf. 1998. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXRα. Cell. 93: 693-704.
13. Joseph, S. B., B. A. Laffitte, P. H. Patel, M. A. Watson, K. E. Matsukuma, R. Walczak, J. L. Collins, T. F. Osborne, and P. Tontonoz. 2002. Direct and indirect mechanisms for regulation of fatty acid synthase gene expression by liver X receptors. J. Biol. Chem. 277: 11019-11025.
14. Schultz, J. R., H. Tu, A. Luk, J. J. Repa, J. C. Medina, L. Li, S. Schwendner, S. Wang, M. Thoolen, D. J. Mangelsdorf, et al. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14: 2831-2838.
15. Talukdar, S., and F. B. Hillgartner. 2006. The mechanism mediating the activation of acetyl-coenzyme A carboxylase-α gene transcription by the liver X receptor agonist T0-901317. J. Lipid Res. 47: 2451-2461.
16. Repa, J. J., G. Liang, J. Ou, Y. Bashmakov, J. M. Lobaccaro, I. Shimomura, B. Shan, M. S. Brown, J. L. Goldstein, and D. J. Mangelsdorf. 2000. Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRα and LXRβ. Genes Dev. 14: 2819-2830.
17. Briel, M., A. J. Nordmann, and H. C. Bucher. 2005. Statin therapy for prevention and treatment of acute and chronic cardiovascular disease: update on recent trials and metaanalyses. Curr. Opin. Lipidol. 16: 601-605.
18. Collins, J. L., A. M. Fivush, M. A. Watson, C. M. Galardi, M. C. Lewis, L. B. Moore, D. J. Parks, J. G. Wilson, T. K. Tippin, J. G. Binz, et al. 2002. Identification of a nonsteroidal liver X receptor agonist through parallel array synthesis of tertiary amines. J. Med. Chem. 45: 1963-1966.
19. Joseph, S. B., E. McKilligin, L. Pei, M. A. Watson, A. R. Collins, B. A. Laffitte, M. Chen, G. Noh, J. Goodman, G. N. Hagger, et al. 2002. Synthetic LXR ligand inhibits the development of atherosclerosis in mice. Proc. Natl. Acad. Sci. USA. 99: 7604-7609.
20. Terasaka, N., A. Hiroshima, T. Koieyama, N. Ubukata, Y. Morikawa, D. Nakai, and T. Inaba. 2003. T-0901317, a synthetic liver X receptor ligand, inhibits development of atherosclerosis in LDL receptor-deficient mice. FEBS Lett. 536: 6-11.
21. Grefhorst, A., T. H. van Dijk, A. Hammer, F. H. van der Sluijs, R. Havinga, L. M. Havekes, J. A. Romijn, P. H. Groot, D. J. Reijngoud, and F. Kuipers. 2005. Differential effects of pharmacological liver X receptor activation on hepatic and peripheral insulin sensitivity in lean and ob/ob mice. Am. J. Physiol. Endocrinol. Metab. 289: E829-E838.
22. Laffitte, B. A., L. C. Chao, J. Li, R. Walczak, S. Hummasti, S. B. Joseph, A. Castrillo, D. C. Wilpitz, D. J. Mangelsdorf, J. L. Collins, et al. 2003. Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc. Natl. Acad. Sci. USA. 100: 5419-5424.
23. Grefhorst, A., B. M. Elzinga, P. J. Voshol, T. Plosch, T. Kok, V. W. Bloks, F. H. van der Sluijs, L. M. Havekes, J. A. Romijn, H. J. Verkade, et al. 2002. Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J. Biol. Chem. 277: 34182-34190.
24. Goodridge, A. G. 1973. Regulation of fatty acid synthesis in isolated hepatocytes prepared from the livers of neonatal chicks. J. Biol. Chem. 248: 1924-1931.
25. Seglen, P. O. 1973. Preparation of rat liver cells. III. Enzymatic requirements for tissue dispersion. Exp. Cell Res. 82: 391-398.
26. Stabile, L. P., S. A. Klautky, S. M. Minor, and L. M. Salati. 1998. Polyunsaturated fatty acids inhibit the expression of the glucose-6-phosphate dehydrogenase gene in primary rat hepatocytes by a nuclear posttranscriptional mechanism. J. Lipid Res. 39: 1951-1963.
27. Lowenstein, J. M., H. Brunengraber, and M. Wadke. 1975. Measurement of rates of lipogenesis with deuterated and tritiated water. Methods Enzymol. 35: 279-287.
28. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
29. Zhang, Y., L. Yin, and F. B. Hillgartner. 2001. Thyroid hormone stimulates acetyl-CoA carboxylase-a transcription in hepatocytes by modulating the composition of nuclear receptor complexes bound to a thyroid hormone response element. J. Biol. Chem. 276: 974-983.
30. Yin, L., Y. Zhang, and F. B. Hillgartner. 2002. Sterol regulatory element-binding protein-1 interacts with the nuclear thyroid hormone receptor to enhance acetyl-CoA carboxylase-α transcription in hepatocytes. J. Biol. Chem. 277: 19554-19565.
31. Baillie, R. A., S. A. Klautky, and A. G. Goodridge. 1993. Transient transfection of chick-embryo hepatocytes. J. Nutr. Biochem. 4: 431-439.
32. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2: 1044-1051.
33. Sedmak, J. J., and S. E. Grossberg. 1977. A rapid, sensitive, and versatile assay for protein using Coomassie Brilliant Blue G250. Anal. Biochem. 79: 544-552.
34. Yin, L., Y. Wang, S. Dridi, C. Vinson, and F. B. Hillgartner. 2005. Role of CCAAT/enhancer-binding protein, histone acetylation, and coactivator recruitment in the regulation of malic enzyme transcription by thyroid hormone. Mol. Cell. Endocrinol. 245: 43-52.
35. Mulligan, J. D., M. T. Flowers, A. Tebon, J. J. Bitgood, C. Wellington, M. R. Hayden, and A. D. Attie. 2003. ABCA1 is essential for efficient basolateral cholesterol efflux during the absorption of dietary cholesterol in chickens. J. Biol. Chem. 278: 13356-13366.
36. Back, D. W., S. B. Wilson, S. M. Morris, Jr., and A. G. Goodridge. 1986. Hormonal regulation of lipogenic enzymes in chick embryo hepatocytes in culture. Thyroid hormone and glucagon regulate malic enzyme mRNA level at post-transcriptional steps. J. Biol. Chem. 261: 12555-12561.
37. Hillgartner, F. B., and T. Charron. 1997. Arachidonate and medium-chain fatty acids inhibit transcription of the acetyl-CoA carboxylase gene in hepatocytes in culture. J. Lipid Res. 38: 2548-2557.
38. Hillgartner, F. B., T. Charron, and K. A. Chesnut. 1997. Triiodothyronine stimulates and glucagon inhibits transcription of the acetyl-CoA carboxylase gene in chick embryo hepatocytes: glucose and insulin amplify the effect of triiodothyronine. Arch. Biochem. Biophys. 337: 159-168.
39. Roncero, C., and A. G. Goodridge. 1992. Hexanoate and octanoate inhibit transcription of the malic enzyme and fatty acid synthase genes in chick embryo hepatocytes in culture. J. Biol. Chem. 267: 14918-14927.
40. Miller, N. E., and P. J. Nestel. 1974. Triglyceride-lowering effect of chenodeoxycholic acid in patients with endogenous hypertriglyceridaemia. Lancet. 2: 929-931.
41. Bilz, S., V. Samuel, K. Morino, D. Savage, C. S. Choi, and G. I. Shulman. 2006. Activation of the farnesoid X receptor improves lipid metabolism in combined hyperlipidemic hamsters. Am. J. Physiol. Endocrinol. Metab. 290: E716-E722.
42. Watanabe, M., S. M. Houten, L. Wang, A. Moschetta, D. J. Mangelsdorf, R. A. Heyman, D. D. Moore, and J. Auwerx. 2004. Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J. Clin. Invest. 113: 1408-1418.
43. Rawson, R. B. 2003. Control of lipid metabolism by regulated intramembrane proteolysis of sterol regulatory element binding proteins (SREBPs). Biochem. Soc. Symp. 70: 221-231.
44. Yabe, D., R. Komuro, G. Liang, J. L. Goldstein, and M. S. Brown. 2003. Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis. Proc. Natl. Acad. Sci. USA. 100: 3155-3160.
45. Sinal, C. J., M. Tohkin, M. Miyata, J. M. Ward, G. Lambert, and F. J. Gonzalez. 2000. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell. 102: 731-744.
46. Privalsky, M. L. 2004. The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu. Rev. Physiol. 66: 315-360.
47. Lee, F. Y., H. Lee, M. L. Hubbert, P. A. Edwards, and Y. Zhang. 2006. FXR, a multipurpose nuclear receptor. Trends Biochem. Sci. 31: 572-580.
48. Goodwin, B., S. A. Jones, R. R. Price, M. A. Watson, D. D. McKee, L. B. Moore, C. Galardi, J. G. Wilson, M. C. Lewis, M. E. Roth, et al. 2000. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell. 6: 517-526.
49. Lu, T. T., M. Makishima, J. J. Repa, K. Schoonjans, T. A. Kerr, J. Auwerx, and D. J. Mangelsdorf. 2000. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol. Cell. 6: 507-515.
50. Brendel, C., K. Schoonjans, O. A. Botrugno, E. Treuter, and J. Auwerx. 2002. The small heterodimer partner interacts with the liver X receptor a and represses its transcriptional activity. Mol. Endocrinol. 16: 2065-2076.
51. Oberkofler, H., E. Schraml, F. Krempler, and W. Patsch. 2004. Restoration of sterol-regulatory-element-binding protein-1c gene expression in HepG2 cells by peroxisome-proliferator-activated receptor-gamma co-activator-1α. Biochem. J. 381: 357-363.
52. Ma, K., P. K. Saha, L. Chan, and D. D. Moore. 2006. Farnesoid X receptor is essential for normal glucose homeostasis. J. Clin. Invest. 116: 1102-1109.
53. Wallberg, A. E., S. Yamamura, S. Malik, B. M. Spiegelman, and R. G. Roeder. 2003. Coordination of p300-mediated chromatin remodeling and TRAP/mediator function through coactivator PGC-1α. Mol. Cell. 12: 1137-1149.
54. Holt, J. A., G. Luo, A. N. Billin, J. Bisi, Y. Y. McNeill, K. F. Kozarsky, M. Donahee, Y. Wang, T. A. Mansfield, S. A. Kliewer, et al. 2003. Definition of a novel growth factor-dependent signal cascade for the suppression of bile acid biosynthesis. Genes Dev. 17: 1581-1591.
55. Grambihler, A., H. Higuchi, S. F. Bronk, and G. J. Gores. 2003. cFLIP-L inhibits p38 MAPK activation: an additional anti-apoptotic mechanism in bile acid-mediated apoptosis. J. Biol. Chem. 278: 26831-26837.
56. Nakahara, M., H. Fujii, P. R. Maloney, M. Shimizu, and R. Sato. 2002. Bile acids enhance low density lipoprotein receptor gene expression via a MAPK cascade-mediated stabilization of mRNA. J. Biol. Chem. 277: 37229-37234.
57. Zhang, Y., L. W. Castellani, C. J. Sinal, F. J. Gonzalez, and P. A. Edwards. 2004. Peroxisome proliferator-activated receptor-gamma coactivator 1a (PGC-1a) regulates triglyceride metabolism by activation of the nuclear receptor FXR. Genes Dev. 18: 157-169.
58. Denson, L. A., E. Sturm, W. Echevarria, T. L. Zimmerman, M. Makishima, D. J. Mangelsdorf, and S. J. Karpen. 2001. The orphan nuclear receptor, shp, mediates bile acid-induced inhibition of the rat bile acid transporter, ntcp. Gastroenterology. 121: 140-147.
59. Boulias, K., N. Katrakili, K. Bamberg, P. Underhill, A. Greenfield, and I. Talianidis. 2005. Regulation of hepatic metabolic pathways by the orphan nuclear receptor SHP. EMBO J. 24: 2624-2633.
60. Inagaki, T., M. Choi, A. Moschetta, L. Peng, C. L. Cummins, J. G. McDonald, G. Luo, S. A. Jones, B. Goodwin, J. A. Richardson, et al. 2005. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab. 2: 217-225.
61. Tomlinson, E., L. Fu, L. John, B. Hultgren, X. Huang, M. Renz, J. P. Stephan, S. P. Tsai, L. Powell-Braxton, D. French, et al. 2002. Transgenic mice expressing human fibroblast growth factor-19 display increased metabolic rate and decreased adiposity. Endocrinology. 143: 1741-1747.
62. Fu, L., L. M. John, S. H. Adams, X. X. Yu, E. Tomlinson, M. Renz, P. M. Williams, R. Soriano, R. Corpuz, B. Moffat, et al. 2004. Fibroblast growth factor 19 increases metabolic rate and reverses dietary and leptin-deficient diabetes. Endocrinology. 145: 2594-2603.
63. Unger, R. H. 2003. Lipid overload and overflow: metabolic trauma and the metabolic syndrome. Trends Endocrinol. Metab. 14: 398-403.
64. Savage, D. B., C. S. Choi, V. T. Samuel, Z. X. Liu, D. Zhang, A. Wang, X. M. Zhang, G. W. Cline, X. X. Yu, J. G. Geisler, et al. 2006. Reversal of diet-induced hepatic steatosis and hepatic insulin resistance by antisense oligonucleotide inhibitors of acetyl-CoA carboxylases 1 and 2. J. Clin. Invest. 116: 817-824.
65. Zhang, Y., F. Y. Lee, G. Barrera, H. Lee, C. Vales, F. J. Gonzalez, T. M. Willson, and P. A. Edwards. 2006. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice. Proc. Natl. Acad. Sci. USA. 103: 1006-1011.
66. Langmann, T., M. Porsch-Ozcurumez, S. Heimerl, M. Probst, C. Moehle, M. Taher, H. Borsukova, D. Kielar, W. E. Kaminski, E. Dittrich-Wengenroth, et al. 2002. Identification of sterol-independent regulatory elements in the human ATP-binding cassette transporter A1 promoter: role of Sp1/3, E-box binding factors, and an oncostatin M-responsive element. J. Biol. Chem. 277: 14443-14450.
67. Xiong, Y., Q. F. Collins, J. An, E. Lupo, Jr., H. Y. Liu, D. Liu, J. Robidoux, Z. Liu, and W. Cao. 2007. p38 mitogen-activated protein kinase plays an inhibitory role in hepatic lipogenesis. J. Biol. Chem. 282: 4975-4982.
68. Botolin, D., Y. Wang, B. Christian, and D. B. Jump. 2006. Docosahexaneoic acid (22:6,n-3) regulates rat hepatocyte SREBP-1 nuclear abundance by Erk- and 26S proteasome-dependent pathways. J. Lipid Res. 47: 181-192.
69. Talukdar, I., W. Szeszel-Fedorowicz, and L. M. Salati. 2005. Arachidonic acid inhibits the insulin induction of glucose-6-phosphate dehydrogenase via p38 MAP kinase. J. Biol. Chem. 280: 40660-40667.
70. Fan, M., J. Rhee, J. St-Pierre, C. Handschin, P. Puigserver, J. Lin, S. Jaeger, H. Erdjument-Bromage, P. Tempst, and B. M. Spiegelman. 2004. Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1α: modulation by p38 MAPK. Genes Dev. 18: 278-289.
71. Cao, W., K. W. Daniel, J. Robidoux, P. Puigserver, A. V. Medvedev, X. Bai, L. M. Floering, B. M. Spiegelman, and S. Collins. 2004. p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol. Cell. Biol. 24: 3057-3067.
72. Oberkofler, H., H. Esterbauer, V. Linnemayr, A. D. Strosberg, F. Krempler, and W. Patsch. 2002. Peroxisome proliferator-activated receptor (PPAR) gamma coactivator-1 recruitment regulates PPAR subtype specificity. J. Biol. Chem. 277: 16750-16757.