Ezetimibe promotes brush border membraneto-lumen cholesterol efflux in the small intestine

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Nakano, Takanari ^a   Inoue, Ikuo ^a   Takenaka, Yasuhiro ^a   Ono, Hiraku ^a   Katayama, Shigehiro ^a   Awata, Takuya ^b   Murakoshi, Takayuki ^a  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b International University of Health and Welfare   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ALKALINE PHOSPHATASE; ATP BINDING CASSETTE G5; ATP BINDING CASSETTE G8; CARRIER PROTEIN; EZETIMIBE; HYDROGEN; NIEMANN PICK C1 LIKE 1; PHYTOSTEROL; UNCLASSIFIED DRUG; CHOLESTEROL; NPC1L1 PROTEIN, MOUSE; TRITIUM;

ABSORPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; BRUSH BORDER MEMBRANE TO LUMEN CHOLESTEROL EFFLUX; CACO 2 CELL LINE; CELL DIFFERENTIATION; CELL SLOUGHING; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CHOLESTEROL ABSORPTION; CHOLESTEROL TRANSPORT; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; EX VIVO STUDY; GENE INACTIVATION; GENETIC TRANSFECTION; HEPG2 CELL LINE; INTESTINE BRUSH BORDER MEMBRANE; INTESTINE CELL; INTESTINE WALL; ISOTOPE LABELING; JEJUNUM; MALE; MOUSE; NONHUMAN; RADIOACTIVITY; REVERSE CHOLESTEROL TRANSPORT; SMALL INTESTINE; TRANSINTESTINAL CHOLESTEROL EFFLUX; ANIMAL; C57BL MOUSE; CACO-2 CELL LINE; DRUG EFFECTS; HEP-G2 CELL LINE; HUMAN; INTESTINE ABSORPTION; KNOCKOUT MOUSE; MEMBRANE; METABOLISM; MICROVILLUS; MUCUS; PERFUSION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CACO-2 CELLS; CELL DIFFERENTIATION; CHOLESTEROL; ENTEROCYTES; EZETIMIBE; HEP G2 CELLS; HUMANS; INTESTINAL ABSORPTION; INTESTINE, SMALL; MALE; MEMBRANE TRANSPORT PROTEINS; MEMBRANES; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROVILLI; MUCUS; PERFUSION; PHYTOSTEROLS; TRITIUM;

EID: 84977489118     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0152207     Document Type: Article

References (42)

1. Temel RE, Brown JM. A new model of reverse cholesterol transport: enTICEing strategies to stimulate intestinal cholesterol excretion. Trends in Pharmacological Sciences. 2015; 36(7):440-51. doi: 10.1016/j.tips.2015.04.002 PMID: 25930707
2. van der Velde AE, Vrins CL, van den Oever K, Kunne C, Oude Elferink RP, Kuipers F, et al. Direct intestinal cholesterol secretion contributes significantly to total fecal neutral sterol excretion in mice. Gastroenterology. 2007; 133(3):967-75. Epub 2007/09/15. doi: 10.1053/j.gastro.2007.06.019 PMID: 17854600.
3. Altmann SW, Davis HR Jr, Zhu LJ, Yao X, Hoos LM, Tetzloff G, et al. Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science. 2004; 303(5661):1201-4. PMID: 14976318.
4. Cannon CP, Blazing MA, Giugliano RP, McCagg A, White JA, Theroux P, et al. Ezetimibe Added to Statin Therapy after Acute Coronary Syndromes. New England Journal of Medicine. 2015; 372 (25):2387-97. doi: 10.1056/NEJMoa1410489 PMID: 26039521.
5. Davidson MH, Voogt J, Luchoomun J, Decaris J, Killion S, Boban D, et al. Inhibition of intestinal cholesterol absorption with ezetimibe increases components of reverse cholesterol transport in humans. Atherosclerosis. 2013; 230(2):322-9. doi: 10.1016/j.atherosclerosis.2013.08.006 PMID: 24075764
6. Jakulj L, Vissers MN, van Roomen CP, van der Veen JN, Vrins CLJ, Kunne C, et al. Ezetimibe stimulates faecal neutral sterol excretion depending on abcg8 function in mice. FEBS Letters. 2010; 584 (16):3625-8. doi: 10.1016/j.febslet.2010.07.035 PMID: 20659465
7. Vrins CLJ, van der Velde AE, van den Oever K, Levels JHM, Huet S, Oude Elferink RPJ, et al. Peroxisome proliferator-activated receptor delta activation leads to increased transintestinal cholesterol efflux. Journal of Lipid Research. 2009; 50(10):2046-54. doi: 10.1194/jlr.M800579-JLR200 PMID: 19439761
8. Van Heek M, Farley C, Compton DS, Hoos L, Alton KB, Sybertz EJ, et al. Comparison of the activity and disposition of the novel cholesterol absorption inhibitor, SCH58235, and its glucuronide, SCH60663. British Journal of Pharmacology. 2000; 129(8):1748-54. doi: 10.1038/sj.bjp.0703235 PMID: 10780982
9. Hawes BE, O'Neill KA, Yao X, Crona JH, Davis HR, Graziano MP, et al. In Vivo Responsiveness to Ezetimibe Correlates with Niemann-Pick C1 Like-1 (NPC1L1) Binding Affinity: Comparison of Multiple Species NPC1L1 Orthologs. Molecular Pharmacology. 2007; 71(1):19-29. doi: 10.1124/mol.106. 027896 PMID: 17005902
10. Igel M, Giesa U, Lütjohann D, von Bergmann K. Comparison of the intestinal uptake of cholesterol, plant sterols, and stanols in mice. Journal of Lipid Research. 2003; 44(3):533-8. doi: 10.1194/jlr. M200393-JLR200 PMID: 12562824
11. 2 in membrane-raft budding and fission. Biochim Biophys Acta. 2009; 1788(10):2222-8. Epub 2009/08/01. S0005-2736(09)00243-0 [pii] doi: 10.1016/j.bbamem.2009.07.015 PMID: 19643079.
12. Haidari M, Leung N, Mahbub F, Uffelman KD, Kohen-Avramoglu R, Lewis GF, et al. Fasting and postprandial overproduction of intestinally derived lipoproteins in an animal model of insulin resistance. Evidence that chronic fructose feeding in the hamster is accompanied by enhanced intestinal de novo lipogenesis and ApoB48-containing lipoprotein overproduction. J Biol Chem. 2002; 277(35):31646-55. Epub 2002/06/19. doi: 10.1074/jbc.M200544200 [pii]. PMID: 12070142.
13. Chateau D, Pauquai T, Delers F, Rousset M, Chambaz J, Demignot S. Lipid micelles stimulate the secretion of triglyceride-enriched apolipoprotein B48-containing lipoproteins by Caco-2 cells. J Cell Physiol. 2005; 202(3):767-76. PMID: 15389567.
14. Nakano T, Inoue I, Koyama I, Kanazawa K, Nakamura K, Narisawa S, et al. Disruption of the murine intestinal alkaline phosphatase gene Akp3 impairs lipid transcytosis and induces visceral fat accumulation and hepatic steatosis. Am J Physiol. 2006; 292(5):G1439-49.
15. Nakano T, Inoue I, Alpers DH, Akiba Y, Katayama S, Shinozaki R, et al. Role of lysophosphatidylcholine in brush-border intestinal alkaline phosphatase release and restoration. Am J Physiol Gastrointest Liver Physiol. 2009; 297(1):G207-14. Epub 2009/05/02. 90590.2008 [pii] doi: 10.1152/ajpgi.90590. 2008 PMID: 19407215.
16. Nakano T, Inoue I, Katayama S, Seo M, Takahashi S, Hokari S, et al. Lysophosphatidylcholine for efficient intestinal lipid absorption and lipoprotein secretion in caco-2 cells. J Clin Biochem Nutr. 2009; 45 (2):227-34. Epub 2009/10/02. doi: 10.3164/jcbn.09-25 PMID: 19794933.
17. Hernell O, Staggers JE, Carey MC. Physical-chemical behavior of dietary and biliary lipids during intestinal digestion and absorption. 2. Phase analysis and aggregation states of luminal lipids during duodenal fat digestion in healthy adult human beings. Biochemistry. 1990; 29(8):2041-56. PMID: 2328238.
18. Knöpfel M, Davies JP, Duong PT, Kværnø L, Carreira EM, Phillips MC, et al. Multiple plasma membrane receptors but not NPC1L1 mediate high-affinity, ezetimibe-sensitive cholesterol uptake into the intestinal brush border membrane. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids. 2007; 1771(9):1140-7. doi: 10.1016/j.bbalip.2007.05.011
19. Beaumier-Gallon G, Dubois C, Senft M, Vergnes M-F, Pauli A-M, Portugal H, et al. Dietary cholesterol is secreted in intestinally derived chylomicrons during several subsequent postprandial phases in healthy humans. The American Journal of Clinical Nutrition. 2001; 73(5):870-7. PMID: 11333839
20. Yu L, Li-Hawkins J, Hammer RE, Berge KE, Horton JD, Cohen JC, et al. Overexpression of ABCG5 and ABCG8 promotes biliary cholesterol secretion and reduces fractional absorption of dietary cholesterol. The Journal of Clinical Investigation. 2002; 110(5):671-80. PMID: 12208868
21. Ge L, Wang J, Qi W, Miao H-H, Cao J, Qu Y-X, et al. The Cholesterol Absorption Inhibitor Ezetimibe Acts by Blocking the Sterol-Induced Internalization of NPC1L1. Cell Metabolism. 2008; 7(6):508-19. doi: 10.1016/j.cmet.2008.04.001 PMID: 18522832
22. Yamanashi Y, Takada T, Suzuki H. Niemann-Pick C1-like 1 overexpression facilitates ezetimibe-sensitive cholesterol and beta-sitosterol uptake in CaCo-2 cells. J Pharmacol Exp Ther. 2007; 320(2):559-64. PMID: 17135346.
23. Wang J, Sun F, Zhang D-w, Ma Y, Xu F, Belani JD, et al. Sterol Transfer by ABCG5 and ABCG8: IN VITRO ASSAY AND RECONSTITUTION. Journal of Biological Chemistry. 2006; 281(38):27894-904. doi: 10.1074/jbc.M605603200 PMID: 16867993
24. Chang T-Y, Chang C. Ezetimibe Blocks Internalization of the NPC1L1/Cholesterol Complex. Cell Metabolism. 2008; 7(6):469-71. doi: 10.1016/j.cmet.2008.05.001 PMID: 18522826
25. Wang J, Chu B-B, Ge L, Li B-L, Yan Y, Song B-L. Membrane topology of human NPC1L1, a key protein in enterohepatic cholesterol absorption. Journal of Lipid Research. 2009; 50(8):1653-62. doi: 10.1194/jlr.M800669-JLR200 PMID: 19325169
26. Xie C, Zhou Z-S, Li N, Bian Y, Wang Y-J, Wang L-J, et al. Ezetimibe blocks the internalization of NPC1L1 and cholesterol in mouse small intestine. Journal of Lipid Research. 2012; 53(10):2092-101. doi: 10.1194/jlr.M027359 PMID: 22811412
27. Yu L, von Bergmann K, Lütjohann D, Hobbs HH, Cohen JC. Ezetimibe normalizes metabolic defects in mice lacking ABCG5 and ABCG8. Journal of Lipid Research. 2005; 46(8):1739-44. doi: 10.1194/jlr. M500124-JLR200 PMID: 15930515
28. Tang W, Ma Y, Jia L, Ioannou YA, Davies JP, Yu L. Genetic inactivation of NPC1L1 protects against sitosterolemia in mice lacking ABCG5/ABCG8. Journal of Lipid Research. 2009; 50(2):293-300. doi: 10.1194/jlr.M800439-JLR200 PMID: 18796403
29. Orlowski S, Coméra C, Tercé F, Collet X. Lipid rafts: dream or reality for cholesterol transporters? Eur Biophys J. 2007; 36(8):869-85. doi: 10.1007/s00249-007-0193-8 PMID: 17576551
30. Sarkadi B, Homolya L, Szakács G, Váradi A. Human Multidrug Resistance ABCB and ABCG Transporters: Participation in a Chemoimmunity Defense System. Physiological Reviews. 2006; 86(4):1179-236. doi: 10.1152/physrev.00037.2005 PMID: 17015488
31. von Bergmann K, Sudhop T, Lütjohann D. Cholesterol and Plant Sterol Absorption: Recent Insights. The American Journal of Cardiology. 2005; 96(1, Supplement):10-4. doi: 10.1016/j.amjcard.2005.03. 014
32. Salen G, von Bergmann K, Lütjohann D, Kwiterovich P, Kane J, Patel SB, et al. Ezetimibe Effectively Reduces Plasma Plant Sterols in Patients With Sitosterolemia. Circulation. 2004; 109(8):966-71. doi: 10.1161/01.cir.0000116766.31036.03 PMID: 14769702
33. Salen G, Starc T, Sisk CM, Patel SB. Intestinal Cholesterol Absorption Inhibitor Ezetimibe Added to Cholestyramine for Sitosterolemia and Xanthomatosis. Gastroenterology. 2006; 130(6):1853-7. doi: 10.1053/j.gastro.2006.02.027 PMID: 16697747
34. Musliner T, Cselovszky D, Sirah W, McCrary Sisk C, Sapre A, Salen G, et al. Efficacy and safety of ezetimibe 40 mg vs. ezetimibe 10 mg in the treatment of patients with homozygous sitosterolaemia. International Journal of Clinical Practice. 2008; 62(7):995-1000. doi: 10.1111/j.1742-1241.2008.01786.x PMID: 18484971
35. Brufau G, Kuipers F, Lin Y, Trautwein EA, Groen AK. A Reappraisal of the Mechanism by Which Plant Sterols Promote Neutral Sterol Loss in Mice. PLoS ONE. 2011; 6(6):e21576. doi: 10.1371/journal. pone.0021576 PMID: 21738715
36. Bonamassa B, Moschetta A. Atherosclerosis: lessons from LXR and the intestine. Trends in Endocrinology & Metabolism. 2013; 24(3):120-8. doi: 10.1016/j.tem.2012.10.004
37. Kruit JK, Plösch T, Havinga R, Boverhof R, Groot PHE, Groen AK, et al. Increased fecal neutral sterol loss upon liver X receptor activation is independent of biliary sterol secretion in mice. Gastroenterology. 2005; 128(1):147-56. doi: 10.1053/j.gastro.2004.10.006 PMID: 15633131
38. Breevoort SR, Angdisen J, Schulman IG. Macrophage-Independent Regulation of Reverse Cholesterol Transport by Liver X Receptors. Arteriosclerosis, Thrombosis, and Vascular Biology. 2014; 34 (8):1650-60. doi: 10.1161/atvbaha.114.303383 PMID: 24947527
39. Sehayek E, Hazen SL. Cholesterol Absorption From the Intestine Is a Major Determinant of Reverse Cholesterol Transport From Peripheral Tissue Macrophages. Arteriosclerosis, Thrombosis, and Vascular Biology. 2008; 28(7):1296-7. doi: 10.1161/atvbaha.108.165803 PMID: 18420997
40. Uto-Kondo H, Ayaori M, Sotherden GM, Nakaya K, Sasaki M, Yogo M, et al. Ezetimibe enhances macrophage reverse cholesterol transport in hamsters: Contribution of hepato-biliary pathway. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids. 2014; 1841(9):1247-55. doi: 10.1016/j.bbalip.2014.05.009
41. Vrins CLJ, Ottenhoff R, van den Oever K, de Waart DR, Kruyt JK, Zhao Y, et al. Trans-intestinal cholesterol efflux is not mediated through high density lipoprotein. Journal of Lipid Research. 2012; 53 (10):2017-23. doi: 10.1194/jlr.M022194 PMID: 22802462
42. Le May C, Berger JM, Lespine A, Pillot B, Prieur X, Letessier E, et al. Transintestinal Cholesterol Excretion Is an Active Metabolic Process Modulated by PCSK9 and Statin Involving ABCB1. Arteriosclerosis, Thrombosis, and Vascular Biology. 2013; 33(7):1484-93. doi: 10.1161/atvbaha.112.300263 PMID: 23559630