Inhibition of cholesterol absorption associated with a PPARα -dependent increase in ABC binding cassette transporter A1 in mice

Journal of Lipid Research

Volumn 44, Issue 11, 2003, Pages 2049-2058

  Knight, Brian L ^a   Patel, Dilip D ^a   Humphreys, Sandy M ^b   Wiggins, David ^b   Gibbons, Geoffrey F ^b  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

3 unsaturated fatty acid; Intestine; Liver X receptor; Peroxisome proliferator activated receptor null mice; Sterol regulatory element binding protein

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A1; CHOLESTEROL; LIVER X RECEPTOR ALPHA; MESSENGER RNA; OXYSTEROL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIRINIXIC ACID; RECEPTOR PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL DIET; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG EFFECT; DRUG MECHANISM; GENE TARGETING; INTESTINE; LIPID ABSORPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ABSORPTION; ANIMAL FEED; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CCAAT-ENHANCER-BINDING PROTEINS; CHOLESTEROL; CHOLESTEROL, DIETARY; DIETARY SUPPLEMENTS; DNA-BINDING PROTEINS; INTESTINAL ABSORPTION; INTESTINES; LIVER; MALE; MICE; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION; PYRIMIDINES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION FACTORS;

EID: 0344236149     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M300042-JLR200     Document Type: Article

References (55)

1. Hayden, M. R., S. M. Clee, W. A. Brooks, J. J. Genest, A. Attie, and J. J. Kastelein. 2000. Cholesterol efflux regulatory protein, Tangier disease and familial high-density lipoprotein deficiency. Curr. Opin. Lipidol. 11: 117-122.
2. Brooks, W. A., M. Marcil, S. M. Clee, L. H. Zhang, K. Roomp, M. van Dam, L. Yu, C. Brewer, J. A. Collins, H. O. Molhuizen, O. Loubser, B. F. Oulette, K. Fichter, E. K. Ashbourne, C. W. Sensen, S. Scherer, S. Mott, M. Denis, D. Martindale, J. Frohlich, K. Morgan, B. Koop, S. Pimstone, J. J. Kastelein, and M. R. Hayden. 1999. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22: 336-345.
3. Bodzioch, M., E. Orso, J. Klucken, T. Langmann, A. Bottcher, W. Diederich, W. Drobnik, S. Barlage, C. Buchler, O. M. Porsch, W. E. Kaminski, H. W. Hahmann, K. Oette, G. Rothe, C. Asianidis, K. J. Lackner, and G. Schmitz. 1999. The gene encoding ATP-binding cassette transporter1 is mutated in Tangier disease. Nat. Genet. 22: 347-351.
4. Rust, S., M. Rosier, H. Funke, J. Real, Z. Amoura, J. C. Piette, J. F. Deleuze, H. B. Brewer, N. Duverger, P. Denefle, and G. Assmann. 1999. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter1. Nat. Genet. 22: 352-355.
5. Lawn, R. M., D. P. Wade, M. R. Garvin, X. Wang, K. Schwartz, J. G. Porter, J. J. Seilhamer, A. M. Vaughan, and J. F. Oram. 1999. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J. Clin. Invest. 104: 25-31.
6. Hobbs, H. H., and D.J. Rader. 1999. ABC1: connecting yellow tonsils, neuropathy, and very low HDL. J. Clin. Invest. 104: 1015-1017.
7. Costet, P., Y. Luo, N. Wang, and A. R. Tall. 2000. Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J. Biol. Chem. 275: 28240-28245.
8. Repa, J. J., S. D. Turley, J. A. Lobaccaro, J. Medina, L. Li, K. Lustig, B. Shan, R. A. Heyman, J. M. Dietschy, and D. J. Mangelsdorf. 2000. Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science. 289: 1524-1529.
9. Venkateswaran, A., B. A. Laffitte, S. B. Joseph, P. A. Mak, D. C. Wilpitz, P. A. Edwards, and P. Tontonoz. 2000. Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXRα. Proc. Natl. Acad. Sci. USA. 97: 12097-12102.
10. McNeish, J., R. J. Aiello, D. Guyot, T. Turi, C. Gabel, C. Aldinger, K. L. Hoppe, M. L. Roach, L. J. Royer, J. De Wet, C. Broccardo, C. Chimini, and O. L. Francone. 2000. High density lipoprotein deficiency and foam cell accumulation in mice with targeted disruption of ATP-binding cassette transporter-1. Proc. Natl. Acad. Sci. USA. 97: 4245-4250.
11. Drobnik, W., B. Lindenthal, B. Lieser, M. Ritter, C. T. Weber, G. Liebisch, U. Giesa, M. Igel, H. Borsukova, and C. Buchler. 2001. ATP-binding cassette transporter A1 (ABCA1) affects total body sterol metabolism. Gastroenterology. 120: 1203-1211.
12. Schwartz, K., R. M. Lawn, and D. P. Wade. 2000. ABC1 gene expression and ApoA-I-mediated cholesterol efflux are regulated by LXR. Biochem. Biophys. Res. Commun. 274: 794-802.
13. Chinetti, G., S. Lestavel, V. Bocher, A. T. Remaley, B. Neve, I. P. Torra, E. Teissier, A. Minnich, M. Jaye, N. Duverger, H. B. Brewer, J. C. Fruchart, V. Clavey, and B. Staels. 2001. PPAR-α and PPAR-α activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat. Med. 7: 53-58.
14. Schoonjans, K., B. Staels, and J. Auwerx. 1996. Role of the peroxisome proliferator-activated receptor (PPAR) in mediating the effects of fibrates and fatty acids on gene expression. J. Lipid Res. 37: 907-925.
15. Pineda Torra, I., P. Gervois, and B. Staels. 1999. Peroxisome proliferator-activated receptor α in metabolic disease, inflammation, atherosclerosis and aging. Curr. Opin. Lipidol. 10: 151-159.
16. Umeda, Y., Y. Kako, K. Mizutani, Y. Iikura, M. Kawamura, M. Seishima, and H. Hayashi. 2001. Inhibitory action of gemfibrozil on cholesterol absorption in rat intestine. J. Lipid Res. 42: 1214-1219.
17. Lee, S. S., T. Pineau, J. Drago, E.J. Lee, J. W. Owens, D. L. Kroetz, S. P. Fernandez, H. Westphal, and F. J. Gonzalez. 1995. Targeted disruption of the alpha isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators. Mol. Cell. Biol. 15: 3012-3022.
18. Peters, J. M., N. Hennuyer, B. Staels, J. C. Fruchart, C. Fievet, F. J. Gonzalez, and J. Auwerx. 1997. Alterations in lipoprotein metabolism in peroxisome proliferator-activated receptor alpha-deficient mice. J. Biol. Chem. 272: 27307-27312.
19. Aoyama, T., J. M. Peters, N. Iritani, T. Nakajima, K. Furihata, T. Hashimoto, and F. J. Gonzalez. 1998. Altered constitutive expression of fatty acid-metabolizing enzymes in mice lacking the peroxisome proliferator-activated receptor alpha (PPARalpha). J. Biol. Chem. 273: 5678-5684.
20. Kersten, S., J. Seydoux, J. M. Peters, F. J. Gonzalez, B. Desvergne, and W. Wahli. 1999. Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J. Clin. Invest. 103: 1489-1498.
21. Leone, T. C., C. J. Winheimer, and D. P. Kelly. 1999. A critical role for the peroxisome proliferator-activated receptor alpha (PPAR alpha) in the cellular fasting response: the PPAR alpha-null mouse as a model of fatty acid oxidation disorders. Proc. Natl. Acad. Sci. USA. 96: 7473-7478.
22. Patel, D. D., B. L. Knight, D. Wiggins, S. M. Humphreys, and G. F. Gibbons. 2001. Disturbances in the normal regulation of SREBP-sensitive genes in peroxisome proliferator-activated receptor alpha (PPAR α) deficient mice. J. Lipid Res. 42: 328-337.
23. Sambrook, J., E. F. Frisch, and T. Maniatis. 1989. Molecular Cloning; A Laboratory Manual. 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Rosenberg, M. F., G. Verlade, R. C. Ford, C. Martin, G. Berridge, I. D. Kerr, R. Callaghan, A. Schmidlin, C. Wooding, K. J. Linton, and C. F. Higgins. 2001. Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J. 20: 5615-5625.
25. Schwarz, M., D. W. Russell, J. M. Dietschy, and S. D. Turley. 1998. Marked reduction in bile acid synthesis in cholesterol 7-alpha-hydroxylase-deficient mice does not lead to diminished tissue cholesterol turnover or to hypercholesterolemia. J. Lipid Res. 39: 1833-1843.
26. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509.
27. Goldfarb, S., T. A. Barber, M. W. Pariza, and D. D. Pugh. 1978. Lipid synthesis and ultrastructure of adult rat hepatocytes during their first twenty-four hours in culture. Exp. Cell Res. 117: 39-46.
28. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
29. Schultz, J. R., H. Tu, A. Luk, J. J. Repa, J. C. Medina, L. Li, S. Schwender, S. Wang, M. Thoolen, D. J. Mangelsdorf, K. D. Lustig, and B. Shan. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14: 2831-2838.
30. Oram, J. F., and R. M. Lawn. 2002. ABCA1: the gatekeeper for eliminating excess tissue cholesterol. J. Lipid Res. 42: 1173-1179.
31. Santamarina, F. S., K. Peterson, C. Knapper, Y. Qiu, L. Freeman, J. F. Cheng, J. Osorio, A. Remaley, X. P. Yang, C. Haudenschild, C. Prades, G. Chimini, E. Blackmon, T. Francois, N. Duverger, E. M. Rubin, M. Rosier, P. Denefle, D. S. Fredickson, and H. B. Brewer. 2000. Complete genomic sequence of the human ABCA1 gene: analysis of the human and mouse ATP-binding cassette A promoter. Proc. Natl. Acad. Sci. USA. 97: 7987-7992.
32. Janowski, B. A., M. J. Grogan, S. A. Jones, G. B. Wisely, S. A. Kleiwer, E. J. Corey, and D. J. Mangelsdorf. 1999. Structural requirements of ligands for the oxysterol liver X receptors LXRα and LXRβ. Proc. Natl. Acad. Sci. USA. 96: 266-271.
33. Bjorkhem, I. 2002. Do oxysterols control cholesterol homeostasis? J. Clin. Invest. 110: 725-730.
34. Saucier, S. E., A. A. Kandutsch, A. K. Gayen, D. K. Swahn, and T. A. Spencer. 1989. Oxysterol regulators of 3-hydroxy-3-methylglutaryl-CoA reductase in liver. Effect of dietary cholesterol. J. Biol. Chem. 264: 6863-6869.
35. 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.
36. Repa, J. J., G. Liang, J. Ou, Y. Bashmakov, J. M. A. 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, LXR α and LXR α. Genes Dev. 14: 2819-2830.
37. Miyata, K. S., S. E. McCaw, H. V. Patel, R. A. Rachubinski, and J. A. Capone. 1996. The orphan nuclear hormone receptor LXRα interacts with the peroxisome proliferator-activated receptor and inhibits peroxisome proliferator signaling. J. Biol. Chem. 271: 9189-9192.
38. Gbaguidi, G. F., and L. B. Agellon. 2002. The atypical interaction of peroxisome proliferator-activated receptor α with liver X receptor α antagonizes the stimulatory effect of their respective ligands on the murine cholesterol 7α-hydroxylase gene promoter. Biochim. Biophys. Acta. 1583: 229-236.
39. Ou, J., H. Tu, B. Shan, A. Luk, R. A. DeBose-Boyd, Y. Bashmakov, J. L. Goldstein, and M. S. Brown. 2001. Unsaturated fatty acids inhibit transcription of the sterol regulatory element-binding protein-1c (SREBP-1c) gene by antagonizing ligand-dependent activation of the LXR. Proc. Natl. Acad. Sci. USA. 98: 6027-6032.
40. Johnson, T. E., and B. J. Ledwith. 2001. Peroxisome proliferators and fatty acids negatively regulate liver X receptor-mediated activity and sterol biosynthesis. J. Steroid Biochem. Mol. Biol. 77: 59-71.
41. Yoshikawa, T., H. Shimano, N. Yahagi, T. Ide, M. Amemiya-Kudo, T. Matsuzaka, M. Nakakuki, S. Tomita, H. Okazaki, Y. Tamura, Y. Iizuka, K. Ohashi, A. Takahashi, H. Sone, J. Osuga, T. Gotoda, S. Ishibashi, and N. Yamada. 2002. Polyunsaturated fatty acids suppress sterol regulatory element-binding protein 1c promoter activity by inhibition of liver X receptor (LXR) binding to LXR response elements. J. Biol. Chem. 277: 1705-1711.
42. Tobin, K. A. R., H. H. Steineger, S. Alberti, O. Spydevold, J. Auwerx, J-A. Gustafsson, and H. I. Nebb. 2000. Cross-talk between fatty acid and cholesterol metabolism mediated by liver X receptor-α. Mol. Endocrinol. 14: 741-752.
43. Lund, E. G., J. M. Guileyardo, and D. W. Russell. 1999. cDNA cloning of cholesterol 24-hydroxylase, a mediator of cholesterol homeostasis in the brain. Proc. Natl. Acad. Sci. USA. 96: 7238-7243.
44. Brown, A. J., G. F. Watts, J. R. Burnett, R. T. Dean, and W. Jessup. 2000. Sterol 27-hydroxylase acts on 7-ketocholesterol in human atherosclerotic lesions and macrophages in culture. J. Biol. Chem. 275: 27627-27633.
45. Gibbons, G. F., C. R. Pullinger, H. W. Chen, W. K. Cavenee, and A. A. Kandutsch. 1980. Regulation of cholesterol synthesis in cultured cells by probable natural precursor sterols. J. Biol. Chem. 255: 375-400.
46. Gibbons, G. F., D. D. Patel, D. Wiggins, and B. L. Knight. 2002. The functional efficiency of lipogenic and cholesterogenic gene expression in normal mice and in mice lacking the peroxisomal proliferator-activated receptor α (PPAR α). Adv. Enzyme Regul. 42: 227-247.
47. Patel, D. D., B. L. Knight, A. K. Soutar, G. F. Gibbons, and D. P. Wade. 2000. The effect of peroxisome-proliferator-activated receptor-α on the activity of the cholesterol 7α-hydroxylase gene. Biochem. J. 351: 747-753.
48. Post, S. M., H. Duez, P. P. Gervois, B. Staels, F. Kuipers, and H. M. G. Princen. 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.
49. Brousseau, M. E. 2003. ATP-binding cassette transporter A1, fatty acids and cholesterol absorption. Curr. Opin. Lipidol. 14: 35-40.
50. Repa, J. J., K. E. Berge, C. Pomajzl, J. A. Richardson, H. Hobbs, and D. J. Mangelsdorf. 2002. Regulation of ATP-binding cassette transporters ABCG5 and ABCG8 by the liver X receptors α and β. J. Biol. Chem. 277: 18793-18800.
51. Repa, J. J., J. M. Dietschy, and S. D. Turley. 2002. Inhibition of cholesterol absorption by SCH 58053 in the mouse is not mediated via changes in the expression of mRNA for ABCA1, ABCG5, or ABCG8 in the enterocyte. J. Lipid Res. 43: 1864-1874.
52. Devchand, P. R., H. Keller, J. M. Peters, M. Vazquez, F. J. Gonzalez, and W. Wahli. 1996. The PPAR-alpha-leukotriene B4 pathway to inflammation control. Nature. 384: 39-43.
53. Parks, J. S., and J. R. Crouse. 1992. Reduction of cholesterol absorption by dietary oleinate and fish oil in African green monkeys. J. Lipid Res. 33: 559-568.
54. Oliver, W. R., J. L. Shenk, M. R. Snaith, C. S. Russell, K. D. Plunket, N. L. Bodkin, M. C. Lewis, D. A. Winegar, M. L. Sznaidman, M. H. Lambert, H. E. Xu, D. D. Sternbach, S. A. Kliewer, B. C. Hansen, and T. M. Willson. 2001. A selective peroxisome proliferator-activated receptor delta agonist promotes reverse cholesterol transport. Proc. Natl. Acad. Sci. USA. 98: 5306-5311.
55. Turley, S. D. 2002. State of the art in cholesterol management: targeting multiple pathways. Am. J. Manag. Care. 8: S29-S32.