Bile acids induce the expression of the human peroxisome proliferator-activated receptor α gene via activation of the farnesoid X receptor

Molecular Endocrinology

Volumn 17, Issue 2, 2003, Pages 259-272

  Torra, Inés Pineda ^a,b   Claudel, Thierry ^a,b   Duval, Caroline ^a,b   Kosykh, Vladimir ^c   Fruchart, Jean Charles ^a,b   Staels, Bart ^a,b  

^a INSTITUT PASTEUR DE LILLE   (France)

^b UNIV LILLE   (France)

^c INSTITUTE OF EXPERIMENTAL CARDIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

3 [2 [2 CHLORO 4 [3 (2,6 DICHLOROPHENYL) 5 ISOPROPYL 4 ISOXAZOLYLMETHOXY]PHENYL]VINYL]BENZOIC ACID; AGENTS AFFECTING LIPID METABOLISM; CARNITINE PALMITOYLTRANSFERASE; CELL NUCLEUS RECEPTOR; CHENODEOXYCHOLIC ACID; FARNESOID X RECEPTOR; FARNESOID X RECEPTOR AGONIST; LIGAND; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; RETINOID X RECEPTOR; TAUROCHOLIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; EVIDENCE BASED MEDICINE; GENE ACTIVATION; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HELA CELL; HEPATOMA CELL; HUMAN; HUMAN TISSUE; INCUBATION TIME; LIVER CELL; MALE; MOLECULAR MODEL; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SPECIES DIFFERENTIATION; UPREGULATION;

ANIMALS; BASE SEQUENCE; BILE ACIDS AND SALTS; CELLS, CULTURED; CHENODEOXYCHOLIC ACID; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; ISOXAZOLES; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); RECEPTOR CROSS-TALK; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, RETINOIC ACID; RESPONSE ELEMENTS; RETINOID X RECEPTORS; RNA, MESSENGER; SPECIES SPECIFICITY; TAUROCHOLIC ACID; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

ANIMALIA; EUKARYOTA; MURINAE;

EID: 0037315190     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2002-0120     Document Type: Article

References (69)

1. Russell DW 1999 Nuclear orphan receptors control cholesterol catabolism. Cell 97:539-542
2. Repa JJ, Mangelsdorf DJ 2000 The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. Annu Rev Cell Dev Biol 16:459-481
3. Wang H, Chen J, Hollister K, Sowers LC, Forman BM 1999 Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol Cell 3:543-553
4. Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, Stimmel JB, Willson TM, Zavacki AM, Moore DD, Lehmann JM 1999 Bile acids: natural ligands for an orphan nuclear receptor. Science 284:1365-1368
5. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, Hull MV, Lustig KD, Mangelsdorf DJ, Shan B 1999 Identification of a nuclear receptor for bile acids. Science 284:1362-1365
6. Forman BM, Goode E, Chen J, Oro AE, Bradley DJ, Perlmann T, Nooman DJ, Burka LT, McMorris T, Lamph WW, Evans RM, Weinberger C 1995 Identification of a nuclear receptor that is activated by farnesol metabolites. Cell 81:687-693
7. Song CS, Echchgadda I, Baek BS, Ahn SC, Oh T, Roy AK, Chatterjee B 2001 Dehydroepiandrosterone sulfotransferase gene induction by bile acid activated famesoid X receptor. J Biol Chem 276:42549-42556
8. Zavacki AM, Lehmann JM, Seol W, Willson TM, Kliewer SA, Moore DD 1997 Activation of the orphan receptor RIP14 by retinoids. Proc Natl Acad Sci USA 94:7909-7914
9. Lafitte BA, Kast HR, Nguyen CM, Zavacki AM, Moore DD, Edwards PA 2000 Identification of the DNA binding specificity and potential target genes for the farnesoid X-activated receptor. J Biol Chem 275:10638-10647
10. Kast HR, Goodwin B, Tarr PT, Jones SA, Anisfeld AM, Stoltz CM, Tontonoz P, Kliewer S, Willson TM, Edwards PA 2002 Regulation of multidrug resistance-associated protein 2 (ABCC2) by the nuclear receptors pregnane X receptor, farnesoid X-activated receptor, and constitutive androstane receptor. J Biol Chem 277:2908-2915
11. Claudel T, Sturm E, Duez H, Pineda Torra I, Sirvent A, Kosykh V, Fruchart JC, Dallongeville J, Hum DW, Kuipers F, Staels B 2002 Bile acid-activated nuclear receptor FXR suppresses apolipoprotein A-I transcription via a negative FXR response element. J Clin Invest 109:961-971
12. Princen HMG, Post SM, Twisk J 1997 Regulation of bile acid biosynthesis. Curr Pharm Des 3:59-84
13. Sinai CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ 2000 Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 102:731-744
14. Lu TT, Makishima M, Repa JJ, Schoonjans K, Kerr TA, Auwerx J, Mangelsdorf DJ 2000 Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol Cell 6:507-515
15. Goodwin B, Jones SA, Price RR, Watson MA, McKee DD, Moore LB, Galardi C, Wilson JG, Lewis MC, Roth ME, Maloney PR, Willson TM, Kliewer SA 2000 A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol Cell 6:517-526
16. Vlahcevic ZR, Eggertsen G, Bjorkhem I, Hylemon PB, Redford K, Pandak WM 2000 Regulation of sterol 12α-hydroxylase and cholic acid biosynthesis in the rat. Gastroenterology 118:599-607
17. del Castillo-Olivares A, Gil G 2000 α1-Fetoprotein transcription factor is required for the expression of sterol 12α-hydroxylase, the specific enzyme for cholic acid synthesis. Potential role in the bile acid-mediated regulation of gene transcription. J Biol Chem 275:17793-17799
18. Love MW, Dawson PA 1998 New insights into bile acid transport. Curr Opin Lipidol 9:225-229
19. Grober J, Zaghini I, Fujii H, Jones SA, Kliewer SA, Willson TM, Ono T, Besnard P 1999 Identification of a bile acid-responsive element in the human ileal bile acid-binding protein gene. Involvement of the farnesoid X receptor/9-cis-retinoic acid receptor heterodimer. J Biol Chem 274:29749-29754
20. Ananthanarayanan M, Balasubramanian N, Makishima M, Mangelsdorf DJ, Suchy FJ 2001 Human bile salt export pump promoter is transactivated by the farnesoid X receptor/bile acid receptor. J Biol Chem 276:28857-28865
21. Kast HR, Nguyen CM, Sinal CJ, Jones SA, Laffitte BA, Reue K, Gonzalez FJ, Willson TM, Edwards PA 2001 Farnesoid X-activated receptor induces apolipoprotein C-II transcription: a molecular mechanism linking plasma triglyceride levels to bile acids. Mol Endocrinol 15:1720-1728
22. Maloney PR, Parks DJ, Haffner CD, Fivush AM, Chandra G, Plunker KD, Creech KL, Moore LB, Wilson JG, Lewis MC, Jones SA, Willson TM 2000 Identification of a chemical tool for the orphan nuclear receptor FXR. J Med Chem 43:2971-2974
23. Urizar NL, Dowhan DH, Moore DD 2000 The farnesoid X-activated receptor mediates bile acid activation of phospholipid transfer protein gene expression. J Biol Chem 275:39313-39317
24. Jiang XC, Bruce C, Mar J, Lin M, Ji Y, Francone OL, Tall AR 1999 Targeted mutation of plasma phospholipid transfer protein gene markedly reduces high-density lipoprotein levels. J Clin Invest 103:907-914
25. Desvergne B, Wahli W 1999 Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev 20:649-688
26. Willson TM, Brown PJ, Sternbach DD, Henke BR 2000 The PPARs: from orphan receptors to drug discovery. J Med Chem 43:527-550
27. Staels B, Dallongeville J, Auwerx J, Schoonjans K, Leitersdorf E, Fruchart J-C 1998 Mechanism of action of fibrates on lipid and lipoprotein metabolism. Circulation 98:2088-2093
28. Chinetti G, Gbaguidi FG, Griglio S, Mallat Z, Antonucci M, Poulain P, Chapman J, Fruchart JC, Tedgui A, Najib-Fruchart J, Staels B 2000 CLA-1/SR-BI is expressed in atherosclerotic lesion macrophages and regulated by activators of peroxisome proliferator-activated receptors. Circulation 101:2411-2417
29. Chinetti G, Lestavel S, Bocher V, Remaley AT, Neve B, Pineda Torra I, Teissier E, Minnich A, Jaye M, Duverger N, Brewer HB, Fruchart JC, Clavey V, Staels B 2001 PPAR-α and PPAR-γ activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nature Med 7:53-58
30. Guerre-Millo M, Gervois P, Raspe E, Madsen L, Poulain P, Derudas B, Herbert JM, Winegar DA, Willson TM, Fruchart JC, Berge RK, Staels B 2000 Peroxisome proliferator-activated receptor α activators improve insulin sensitivity and reduce adiposity. J Biol Chem 275:16638-16642
31. Ye JM, Doyle PJ, Iglesias MA, Watson DG, Cooney GJ, Kraegen EW 2001 Peroxisome proliferator-activated receptor (PPAR)-α activation lowers muscle lipids and improves insulin sensitivity in high fat-fed rats: comparison with PPAR-γ activation. Diabetes 50:411-417
32. Chinetti G, Fruchart JC, Staels B 2000 Peroxisome proliferator-activated receptors (PPARs): nuclear receptors at the crossroads between lipid metabolism and inflammation. Inflamm Res 49:497-505
33. Ericsson CG, Hamsten A, Nilsson J, Grip L, Svane B, Defaire U 1996 Angiographic assessment of effects of bezafibrate on progression of coronary artery disease in young male postinfarction patients. Lancet 347:849-853
34. Frick MH, Syvanne M, Nieminen MS, Kauma H, Majahalme S, Virtanen V, Kesaniemi YA, Pasternak A, Taskinen MR 1997 Prevention of the angiographic progression of coronary and vein-graft atherosclerosis by gemfibrozil after coronary bypass surgery in men with low levels of HDL cholesterol. Circulation 96:2137-2143
35. Rubins HB, Robins SJ, Collins D, Fye CL, Anderson JW, Elam MB, Faas FH, Linares E, Schaefer EJ, Schectman G, Wilt TJ, Wittes J 1999 Gemfibrozil for the secondary prevention of coronary heart disease in men with low levels of high-density lipoprotein cholesterol. Veterans Affairs High-Density Lipoprotein Cholesterol intervention Trial Study Group. N Engl J Med 341:410-418
36. Steiner G, Hamsten A, Hosking A, Stewart J, McLaugdstone P, Sole M, Syvanne M 2001 Effect of fenofibrate on progression of coronary-artery disease in type 2 diabetes: the Diabetes Atherosclerosis Intervention Study, a randomised study. Lancet 357:905-910
37. Stahlberg D, Angelin B, Einarsson K 1989 Effects of treatment with clofibrate, bezafibrate, and ciprofibrate on the metabolism of cholesterol in rat liver microsomes. J Lipid Res 30:953-958
38. Stahlberg D, Reihner E, Rudling M, Berglund L, Einarsson K, Angelin B 1995 Influence of bezafibrate on hepatic cholesterol metabolism in gallstone patients: reduced activity of cholesterol 7 α-hydroxylase. Hepatology 21:1025-1030
39. Bertolotti M, Concari M, Loria P, Abate N, Pinetti A, Guicciardi ME, Carulli N 1995 Effects of different phenotypes of hyperlipoproteinemia and of treatment with fibric acid derivatives on the rates of cholesterol 7 α-hydroxylation in humans. Arterioscler Thromb Vasc Biol 15:1064-1069
40. Odman B, Ericsson S, Lindmark M, Berglund L, Angelin B 1991 Gemfibrozil in familial combined hyperlipidaemia: effect of added low-dose cholestyramine on plasma and biliary lipids. Eur J Clin Invest 21:344-349
41. Marrapodi M, Chiang JY 2000 Peroxisome proliferator-activated receptor α (PPARα) and agonist inhibit cholesterol 7α-hydroxylase gene (CYP7A1) transcription. J Lipid Res 41:514-520
42. Patel DD, Knight BL, Soutar AK, Gibbons GF, Wade DP 2000 The effect of peroxisome-proliferator-activated receptor-α on the activity of the cholesterol 7α-hydroxylase gene. Biochem J 351:747-753
43. Post SM, Duez H, Gervois PP, Staels B, Kuipers F, Princen HM 2001 Fibrates suppress bile acid synthesis via peroxisome proliferator-activated receptor-α-mediated downregulation of cholesterol 7α-hydroxylase and sterol 27-hydroxylase expression. Arterioscler Thromb Vasc Biol 21:1840-1845
44. Hunt MC, Yang YZ, Eggertsen G, Carneheim CM, Gafvels M, Einarsson C, Alexson SE 2000 The peroxisome proliferator-activated receptor α (PPARα) regulates bile acid biosynthesis. J Biol Chem 275:28947-28953
45. Sinal CJ, Yoon M, Gonzalez FJ 2001 Antagonism of the actions of peroxisome proliferator-activated receptor-α by bile acids. J Biol Chem 276:47154-47162
46. Quandt K, Frech K, Karas H, Wingender E, Werner T 1995 MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23:4878-4884
47. Brown PJ, Stuart LW, Hurley KP, Lewis MC, Winegar DA, Wilson JG, Wilkinson WO, Ittoop OR, Willson TM 2001 Identification of a subtype selective human PPARα agonists through parallel-array synthesis. Bioorg Med Chem Lett 11:1225-1227
48. Hsu MH, Palmer CNA, Song W, Griffin KJ, Johnson EF 1998 A carboxyl-terminal extension of the zinc finger domain contributes to the specificity and polarity of peroxisome proliferator-activated receptor DNA binding. J Biol Chem 273:27988-27997
49. Lawrence JW, Li Y, Chen S, DeLuca JG, Berger JP, Umbenhauer DR, Moller DE, Zhou G 2001 Differential gene regulation in human vs. rodent hepatocytes by peroxisome proliferator-activated receptor (PPAR) α. PPAR α fails to induce peroxisome proliferation-associated genes in human cells independently of the level of receptor expression. J Biol Chem 276:31521-31527
50. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W 1999 Peroxisome proliferator-activated receptor α mediates the adaptive response to fasting. J Clin Invest 103:1489-1498
51. Edwards PA, Kast HR, Anisfeld AM 2002 BAREing it all. The adoption of LXR and FXR and their roles in lipid homeostasis. J Lipid Res 43:2-12
52. Cheema SK, Agellon LB 2000 The murine and human cholesterol 7α-hydroxylase gene promoters are differentially responsive to regulation by fatty acids mediated via peroxisome proliferator-activated receptor α. J Biol Chem 275:12530-12536
53. Leiss O, von Bergmann K 1982 Different effects of chenodeoxycholic acid and ursodeoxycholic acid on serum lipoprotein concentrations in patients with radiolucent gallstones. Scand J Gastroenterol 17:587-592
54. Bard JM, Parra HJ, Douste-Blazy P, Fruchart JC 1990 Effect of pravastatin, an HMG CoA reductase inhibitor, and cholestyramine, a bile acid sequestrant, on lipoprotein particles defined by their apolipoprotein composition. Metabolism 39:269-273
55. Betteridge DJ, Bhatnager D, Bing RF, Durrington PN, Evans GR, Flax H, Jay RH, Lewis-Barned N, Mann J, Matthews DR, Miller JP, Reckless JPD, Sturley R, Taylor KG, Winder AF 1992 Treatment of familial hypercholesterolaemia. United Kingdom lipid clinics study of pravastatin and cholestyramine. BMJ 304:1335-1338
56. Angelin B 1995 1994 Mack-Forster Award Lecture. Review. Studies on the regulation of hepatic cholesterol metabolism in humans. Eur J Clin Invest 25:215-224
57. Angelin B, Einarsson K, Hellstrom K, Leijd B 1978 Effects of cholestyramine and chenodeoxycholic acid on the metabolism of endogenous triglyceride in hyperlipoproteinemia. J Lipid Res 19:1017-1024
58. Duez HM, Poulain P, Fievet C, Fruchart J-C, Staels B 2000 Peroxisome proliferator activated-receptor α (PPARα) is required for the in vivo regulation of apo A-I gene expression by fibrates. Circulation 102:11-47
59. Lemberger T, Saladin R, Vazquez M, Assimacopoulos F, Staels B, Desvergne B, Wahli W, Auwerx J 1996 Expression of the peroxisome proliferator-activated receptor α gene is stimulated by stress and follows a diurnal rhythm. J Biol Chem 271:1764-1769
60. Lemberger T, Staels B, Saladin R, Desvergne B, Auwerx J, Wahli W 1994 Regulation of the peroxisome proliferator-activated receptor α gene by glucocorticoids. J Biol Chem 269:24527-24530
61. Peet DJ, Turley SD, Ma W, Janowski BA, Lobaccaro J-MA, Hammer RE, Mangelsdof DJ 1998 Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXRα. Cell 93:693-704
62. Chiang JY, Kimmel R, Stroup D 2001 Regulation of cholesterol 7α-hydroxylase gene (CYP7A1) transcription by the liver orphan receptor (LXRα). Gene 262:257-265
63. Cali JJ, Hsieh CL, Francke U, Russell DW 1991 Mutations in the bile acid biosynthetic enzyme sterol 27-hydroxylase underlie cerebrotendinous xanthomatosis. J Biol Chem 266:7779-7783
64. Rosen H, Reshef A, Maeda N, Lippoldt A, Shpizen S, Triger L, Eggertsen G, Bjorkhem I, Leitersdorf E 1998 Markedly reduced bile acid synthesis but maintained levels of cholesterol and vitamin D metabolites in mice with disrupted sterol 27-hydroxylase gene. J Biol Chem 273:14805-14812
65. Bjorkhem I, Eggertsen G 2001 Genes involved in initial steps of bile acid synthesis. Curr Opin Lipidol 12:97-103
66. Gervois P, Pineda Torra I, Chinetti G, Grotzinger T, Dubois G, Fruchart JC, Fruchart-Najib J, Leitersdorf E, Staels B 1999 A truncated human peroxisome proliferator-activated receptor α splice variant with dominant negative activity. Mol Endocrinol 13:1535-1549
67. Staels B, Vu-Dac N, Kosykh VA, Saladin R, Fruchart JC, Dallongeville J, Auwerx J 1995 Fibrates downregulate apolipoprotein C-III expression independent of induction of peroxisomal acyl coenzyme A oxidase. A potential mechanism for the hypolipidemic action of fibrates. J Clin Invest 95:705-712
68. Pineda Torra I, Jamshidi Y, Flavell DM, Fruchart J-C, Staels B 2002 Characterization of the human PPARa promoter: identification of a functional nuclear receptor response element. Mol Endocrinol 16:1013-1028
69. Bonazzi A, Mastyugin V, Mieyal PA, Dunn MW, Laniado-Schwartman M 2000 Regulation of cyclooxygenase-2 by hypoxia and peroxisome proliferators in the corneal epithelium. J Biol Chem 275:2837-2844