Transintestinal cholesterol excretion is an active metabolic process modulated by PCSK9 and statin involving ABCB1

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 7, 2013, Pages 1484-1493

  Le May, Cédric ^a   Berger, Jean Mathieu ^a   Lespine, Anne ^b   Pillot, Bruno ^a,c   Prieur, Xavier ^a,c   Letessier, Eric ^d   Hussain, M Mahmood ^e   Collet, Xavier ^f   Cariou, Bertrand ^a,d,e   Costet, Philippe ^a,d,e  

^a L INSTITUT DU THORAX   (France)

^b TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d NANTES UNIVERSITY HOSPITAL   (France)

^e SUNY Downstate Medical Center   (United States)

^f University Hospital of Toulouse   (France)

Author keywords

ATP binding cassette transporter B1; Lipoprotein; Low density lipoprotein receptor; PCSK9; Transintestinal cholesterol excretion

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN E; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; MEVINOLIN; MULTIDRUG RESISTANCE PROTEIN 1; PROPROTEIN CONVERTASE SUBTILISIN KEXIN TYPE 9; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DUODENUM; EX VIVO STUDY; EXPLANT; HUMAN; IN VIVO STUDY; JEJUNUM; METABOLIC DISORDER; NONHUMAN; PLASMA CLEARANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TRANSINTESTINAL CHOLESTEROL EXCRETION; UPREGULATION;

ATP-BINDING CASSETTE TRANSPORTER B1; LIPOPROTEIN; LOW-DENSITY LIPOPROTEIN RECEPTOR; PCSK9; TRANSINTESTINAL CHOLESTEROL EXCRETION;

ANIMALS; BIOPSY; CHOLESTEROL; CHOLESTEROL, HDL; CHOLESTEROL, LDL; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; JEJUNUM; LOVASTATIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; P-GLYCOPROTEIN; P-GLYCOPROTEINS; PROPROTEIN CONVERTASES; RECEPTORS, LDL; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES; TIME FACTORS;

EID: 84879079456     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300263     Document Type: Article

References (41)

1. Pertsemlidis D, Kirchman EH, Ahrens EH Jr. Regulation of cholesterol metabolism in the dog. I. Effects of complete bile diversion and of cholesterol feeding on absorption, synthesis, accumulation, and excretion rates measured during life. J Clin Invest. 1973;52:2353-2367.
2. Bandsma RH, Stellaard F, Vonk RJ, Nagel GT, Neese RA, Hellerstein MK, Kuipers F. Contribution of newly synthesized cholesterol to rat plasma and bile determined by mass isotopomer distribution analysis: bile-salt flux promotes secretion of newly synthesized cholesterol into bile. Biochem J. 1998;329 (pt 3):699-703.
3. Deckelbaum RJ, Lees RS, Small DM, Hedberg SE, Grundy SM. Failure of complete bile diversion and oral bile acid therapy in the treatment of homozygous familial hypercholesterolemia. N Engl J Med. 1977;296:465-470.
4. Kruit JK, Plösch T, Havinga R, Boverhof R, Groot PH, Groen AK, Kuipers F. Increased fecal neutral sterol loss upon liver X receptor activation is independent of biliary sterol secretion in mice. Gastroenterology. 2005;128:147-156.
5. Temel RE, Sawyer JK, Yu L, Lord C, Degirolamo C, McDaniel A, Marshall S, Wang N, Shah R, Rudel LL, Brown JM. Biliary sterol secretion is not required for macrophage reverse cholesterol transport. Cell Metab. 2010;12:96-102.
6. Brown JM, Bell TA III, Alger HM, Sawyer JK, Smith TL, Kelley K, Shah R, Wilson MD, Davis MA, Lee RG, Graham MJ, Crooke RM, Rudel LL. Targeted depletion of hepatic ACAT2-driven cholesterol esterification reveals a non-biliary route for fecal neutral sterol loss. J Biol Chem. 2008;283:10522-10534.
7. van der Velde AE, Brufau G, Groen AK. Transintestinal cholesterol efflux. Curr Opin Lipidol. 2010;21:167-171.
8. van der Veen JN, van Dijk TH, Vrins CL, van Meer H, Havinga R, Bijsterveld K, Tietge UJ, Groen AK, Kuipers F. Activation of the liver X receptor stimulates trans-intestinal excretion of plasma cholesterol. J Biol Chem. 2009;284:19211-19219.
9. van der Velde AE, Vrins CL, van den Oever K, Seemann I, Oude Elferink RP, van Eck M, Kuipers F, Groen AK. Regulation of direct transintestinal cholesterol excretion in mice. Am J Physiol Gastrointest Liver Physiol. 2008;295:G203-G208.
10. Vrins CL, van der Velde AE, van den Oever K, Levels JH, Huet S, Oude Elferink RP, Kuipers F, Groen AK. Peroxisome proliferator-activated receptor delta activation leads to increased transintestinal cholesterol efflux. J Lipid Res. 2009;50:2046-2054.
11. Goldstein JL, Brown MS. The LDL receptor. Arterioscler Thromb Vasc Biol. 2009;29:431-438.
12. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 1996;271:518-520.
13. Fong LG, Bonney E, Kosek JC, Cooper AD. Immunohistochemical localization of low density lipoprotein receptors in adrenal gland, liver, and intestine. J Clin Invest. 1989;84:847-856.
14. Stange EF, Dietschy JM. Cholesterol synthesis and low density lipoprotein uptake are regulated independently in rat small intestinal epithelium. Proc Natl Acad Sci USA. 1983;80:5739-5743.
15. Zhang DW, Lagace TA, Garuti R, Zhao Z, McDonald M, Horton JD, Cohen JC, Hobbs HH. Binding of proprotein convertase subtilisin/kexin type 9 to epidermal growth factor-like repeat A of low density lipoprotein receptor decreases receptor recycling and increases degradation. J Biol Chem. 2007;282:18602-18612.
16. Rashid S, Curtis DE, Garuti R, Anderson NN, Bashmakov Y, Ho YK, Hammer RE, Moon YA, Horton JD. Decreased plasma cholesterol and hypersensitivity to statins in mice lacking Pcsk9. Proc Natl Acad Sci USA. 2005;102:5374-5379.
17. Le May C, Kourimate S, Langhi C, Chétiveaux M, Jarry A, Comera C, Collet X, Kuipers F, Krempf M, Cariou B, Costet P. Proprotein convertase subtilisin kexin type 9 null mice are protected from postprandial triglyceridemia. Arterioscler Thromb Vasc Biol. 2009;29:684-690.
18. Hui DY, Labonté ED, Howles PN. Development and physiological regulation of intestinal lipid absorption. III. Intestinal transporters and cholesterol absorption. Am J Physiol Gastrointest Liver Physiol. 2008;294:G839-G843.
19. Chan LM, Lowes S, Hirst BH. The ABCs of drug transport in intestine and liver: efflux proteins limiting drug absorption and bioavailability. Eur J Pharm Sci. 2004;21:25-51.
20. Honig SM, Fu S, Mao X, Yopp A, Gunn MD, Randolph GJ, Bromberg JS. FTY720 stimulates multidrug transporter-and cysteinyl leukotriene-dependent T cell chemotaxis to lymph nodes. J Clin Invest. 2003;111:627-637.
21. Aye IL, Singh AT, Keelan JA. Transport of lipids by ABC proteins: interactions and implications for cellular toxicity, viability and function. Chem Biol Interact. 2009;180:327-339.
22. Le Goff W, Settle M, Greene DJ, Morton RE, Smith JD. Reevaluation of the role of the multidrug-resistant P-glycoprotein in cellular cholesterol homeostasis. J Lipid Res. 2006;47:51-58.
23. Garrigues A, Escargueil AE, Orlowski S. The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc Natl Acad Sci USA. 2002;99:10347-10352.
24. van der Velde AE, Vrins CL, van den Oever K, Kunne C, Oude Elferink RP, Kuipers F, Groen AK. Direct intestinal cholesterol secretion contributes significantly to total fecal neutral sterol excretion in mice. Gastroenterology. 2007;133:967-975.
25. Grefhorst A, McNutt MC, Lagace TA, Horton JD. Plasma PCSK9 preferentially reduces liver LDL receptors in mice. J Lipid Res. 2008;49:1303-1311.
26. Schmidt RJ, Beyer TP, Bensch WR, Qian YW, Lin A, Kowala M, Alborn WE, Konrad RJ, Cao G. Secreted proprotein convertase subtilisin/kexin type 9 reduces both hepatic and extrahepatic low-density lipoprotein receptors in vivo. Biochem Biophys Res Commun. 2008;370:634-640.
27. Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest. 1993;92:883-893.
28. Truong TQ, Auger A, Denizeau F, Brissette L. Analysis of low-density lipoprotein catabolism by primary cultures of hepatic cells from normal and low-density lipoprotein receptor knockout mice. Biochim Biophys Acta. 2000;1484:307-315.
29. Foucaud-Vignault M, Soayfane Z, Ménez C, Bertrand-Michel J, Martin PG, Guillou H, Collet X, Lespine A. P-glycoprotein dysfunction contributes to hepatic steatosis and obesity in mice. PLoS ONE. 2011;6:e23614.
30. Qadir M, O'Loughlin KL, Fricke SM, Williamson NA, Greco WR, Minderman H, Baer MR. Cyclosporin A is a broad-spectrum multidrug resistance modulator. Clin Cancer Res. 2005;11:2320-2326.
31. Vrins CL, Ottenhoff R, van den Oever K, de Waart DR, Kruyt JK, Zhao Y, van Berkel TJ, Havekes LM, Aerts JM, van Eck M, Rensen PC, Groen AK. Trans-intestinal cholesterol efflux is not mediated through high density lipoprotein. J Lipid Res. 2012;53:2017-2023.
32. Moestrup SK, Gliemann J, Pallesen G. Distribution of the alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein in human tissues. Cell Tissue Res. 1992;269:375-382.
33. Poirier S, Mayer G, Benjannet S, Bergeron E, Marcinkiewicz J, Nassoury N, Mayer H, Nimpf J, Prat A, Seidah NG. The proprotein convertase PCSK9 induces the degradation of low density lipoprotein receptor (LDLR) and its closest family members VLDLR and ApoER2. J Biol Chem. 2008;283:2363-2372.
34. Strong A, Ding Q, Edmondson AC, et al. Hepatic sortilin regulates both apolipoprotein B secretion and LDL catabolism. J Clin Invest. 2012;122:2807-2816.
35. Ji ZS, Sanan DA, Mahley RW. Intravenous heparinase inhibits remnant lipoprotein clearance from the plasma and uptake by the liver: in vivo role of heparan sulfate proteoglycans. J Lipid Res. 1995;36:583-592.
36. Ishibashi S, Perrey S, Chen Z, Osuga Ji, Shimada M, Ohashi K, Harada K, Yazaki Y, Yamada N. Role of the low density lipoprotein (LDL) receptor pathway in the metabolism of chylomicron remnants. A quantitative study in knockout mice lacking the LDL receptor, apolipoprotein E, or both. J Biol Chem. 1996;271:22422-22427.
37. Sberna AL, Assem M, Xiao R, Ayers S, Gautier T, Guiu B, Deckert V, Chevriaux A, Grober J, Le Guern N, Pais de Barros JP, Moore DD, Lagrost L, Masson D. Constitutive androstane receptor activation decreases plasma apolipoprotein B-containing lipoproteins and atherosclerosis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2011;31:2232-2239.
38. Vantourout P, Radojkovic C, Lichtenstein L, Pons V, Champagne E, Martinez LO. Ecto-F-ATPase: a moonlighting protein complex and an unexpected apoA-I receptor. World J Gastroenterol. 2010;16:5925-5935.
39. Jeannesson E, Siest G, Bastien B, Albertini L, Aslanidis C, Schmitz G, Visvikis-Siest S. Association of ABCB1 gene polymorphisms with plasma lipid and apolipoprotein concentrations in the STANISLAS cohort. Clin Chim Acta. 2009;403:198-202.
40. Kajinami K, Brousseau ME, Ordovas JM, Schaefer EJ. Polymorphisms in the multidrug resistance-1 (MDR1) gene influence the response to atorvastatin treatment in a gender-specific manner. Am J Cardiol. 2004;93:1046-1050.
41. Rodrigues AC, Rebecchi IM, Bertolami MC, Faludi AA, Hirata MH, Hirata RD. High baseline serum total and LDL cholesterol levels are associated with MDR1 haplotypes in Brazilian hypercholesterolemic individuals of European descent. Braz J Med Biol Res. 2005;38:1389-1397.