Increased atherosclerosis in P2Y13/apolipoprotein e double-knockout mice: Contribution of P2Y13 to reverse cholesterol transport

Cardiovascular Research

Volumn 106, Issue 2, 2015, Pages 314-323

  Lichtenstein, Laeticia ^a,b   Serhan, Nizar ^a,b   Espinosa Delgado, Sara ^a,b   Fabre, Aurélie ^a,b   Annema, Wijtske ^c   Tietge, Uwe J F ^c   Robaye, Bernard ^d   Boeynaems, Jean Marie ^d   Laffargue, Muriel ^a,b   Perret, Bertrand ^a,b,e   Martinez, Laurent O ^a,b,e,f  

^a University Hospital of Toulouse   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e CHU PURPAN   (France)

^f CHU RANGUEIL   (France)

Author keywords

ATP synthase; Bile acids; Cholesterol; High density lipoprotein; Purinergic receptor

Indexed keywords

APOLIPOPROTEIN E; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PURINERGIC P2Y13 RECEPTOR; ABC TRANSPORTER; HIGH DENSITY LIPOPROTEIN; P2RY13 PROTEIN, MOUSE; PURINERGIC P2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA SINUS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BILIARY EXCRETION; BLOOD CELL; BONE MARROW TRANSPLANTATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DISEASE COURSE; FECES; GENE EXPRESSION; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; STEROL EXCRETION; ANIMAL; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; DISEASE MODELS, ANIMAL; LIPOPROTEINS, HDL; LIVER; MACROPHAGES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, PURINERGIC P2;

EID: 84929085806     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv109     Document Type: Article

References (40)

1. Gordon DJ, Probstfield JL, Garrison RJ, Neaton JD, Castelli WP, Knoke JD, Jacobs DR Jr, Bangdiwala S, Tyroler HA. High-density lipoprotein cholesterol and cardiovascular disease. Four prospective American studies. Circulation 1989;79:8-15.
2. Rigotti A, Miettinen HE, Krieger M. The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr Rev 2003;24: 357-387.
3. Mineo C, Shaul PW. Functions of scavenger receptor class B, type I in atherosclerosis. Curr Opin Lipidol 2012;23:487-493.
4. Martinez LO, Jacquet S, Esteve JP, Rolland C, Cabezon E, Champagne E, Pineau T, Georgeaud V, Walker JE, Terce F, Collet X, Perret B, Barbaras R. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 2003;421:75-79.
5. Garcia A, Barbaras R, Collet X, Bogyo A, Chap H, Perret B, Collet R. High density lipo-protein3 (HDL3) receptor-dependent endocytosis pathway in a human hepatoma cell line (HepG2). Biochemistry 1996;35:13064-13070.
6. Jacquet S, Malaval C, Martinez LO, Sak K, Rolland C, Perez C, Nauze M, Champagne E, Terce F, Gachet C, Perret B, Collet X, Boeynaems JM, Barbaras R. The nucleotide receptor P2Y13 is a key regulator of hepatic high-density lipoprotein (HDL) endocytosis. Cell Mol Life Sci 2005;62:2508-2515.
7. Malaval C, Laffargue M, Barbaras R, Rolland C, Peres C, Champagne E, Perret B, Tercé F, Collet X, Martinez LOO, Terce F. RhoA/ROCK I signalling downstream of the P2Y13 ADP-receptor controls HDL endocytosis in human hepatocytes. Cell Signal 2009;21: 120-127.
8. Zhang FL, Luo L, Gustafson E, Palmer K, Qiao X, Fan X, Yang S, Laz TM, Bayne M, Monsma F Jr. P2Y(13): identification and characterization of a novel Galphai-coupled ADP receptor from human and mouse. J Pharmacol Exp Ther 2002;301:705-713.
9. Ben Addi A, Lefort A, Hua X, Libert F, Communi D, Ledent C, Macours P, Tilley SL, Boeynaems J-M, Robaye B. Modulation of murine dendritic cell function by adenine nucleotides and adenosine: involvement of the A(2B) receptor. Eur J Immunol 2008; 38:1610-1620.
10. Ben Addi A, Cammarata D, Conley PB, Boeynaems J-M, Robaye B. Roleofthe P2Y12re-ceptor in the modulation of murine dendritic cell function by ADP. J Immunol 2010;185: 5900-5906.
11. Fabre ACC, Malaval C, Ben Addi A, Verdier C, Pons V, Serhan N, Lichtenstein L, Combes G, Huby T, Briand F, Collet X, Nijstad N, Tietge UJFJ, Robaye B, Perret B, Boeynaems J-MM, Martinez LOO. P2Y13 receptor is critical for reverse cholesterol transport. Hepatology 2010;52:1477-1483.
12. Blom D, Yamin T-TT, Champy M-FF, Selloum M, Bedu E, Carballo-Jane E, Gerckens L, Luell S, Meurer R, Chin J, Mudgett J, Puig O. Altered lipoprotein metabolism in P2Y(13) knockout mice. Biochim Biophys Acta 2010;1801:1349-1360.
13. Lichtenstein L, Serhan N, Annema W, Combes G, Robaye B, Boeynaems J-M, Perret B, Tietge UJ, Laffargue M, Martinez LO. Lack of P2Y13 in mice fed a high cholesterol diet results indecreased hepatic cholesterol content, biliary lipid secretion and reverse cholesterol transport. Nutr Metab (Lond) 2013;10:67.
14. Kapourchali FR, Surendiran G, Chen L, Uitz E, Bahadori B, Moghadasian MH. Animal models of atherosclerosis. World J Clin Cases 2014;2:126-132.
15. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL, Aalto-Setälä K. Severe hypercholesterolemia and atherosclerosisin apolipo-protein E-deficient mice createdby homologous recombination in ES cells. Cell 1992;71: 343-353.
16. Gayral S, Garnotel R, Castaing-Berthou A, Blaise S, Fougerat A, Berge E, Montheil A, Malet N, Wymann MP, Maurice P, Debelle L, Martiny L, Martinez LO, Pshezhetsky AV, Duca L, Laffargue M. Elastin-derived peptides potentiate atherosclerosis through the immune Neu1-PI3Kg pathway. Cardiovasc Res 2014;102:118-127.
17. Serhan N, Cabou C, Verdier C, Lichtenstein L, Malet N, Perret B, Laffargue M, Martinez LO. Chronic pharmacological activation of P2Y13 receptor in mice decreases HDL-cholesterol level by increasing hepatic HDL uptake and bile acid secretion. Biochim Biophys Acta 2013;1831:719-725.
18. Dullaart RPF, Annema W, de Boer JF, Tietge UJF. Pancreatic b-cell function relates positively to HDL functionality in well-controlled type 2 diabetes mellitus. Atherosclerosis 2012;222:567-573.
19. Nijstad N, deBoer JF, Lagor WR, Toelle M, Usher D, Annema W, der Giet Mv, Rader DJ, Tietge UJF. Overexpression of apolipoprotein O does not impact on plasma HDL levels or functionality in human apolipoprotein A-I transgenic mice. Biochim Biophys Acta 2011; 1811:294-299.
20. Martinez LO, Georgeaud V, Rolland C, Collet X, Tercé F, Perret B, Barbaras R. Characterization of two high-density lipoprotein binding sites on porcine hepatocyte plasma membranes: contribution of scavenger receptor class B type I (SR-BI) to the low-affinity component. Biochemistry 2000;39:1076-1082.
21. Mezdour H, Clavey V, Kora I, Koffigan M, Barkia A, Fruchart JC. Anion-exchange fast protein liquid chromatographic characterization and purification of apolipoproteins A-I A-II C-I C-II C-III-0 C-III-1 C-III-2 and E from human plasma. J Chromatogr 1987; 414:35-46.
22. Goffinet M, Tardy C, Boubekeur N, Cholez G, Bluteau A, Oniciu DC, Lalwani ND, Dasseux J-LH, Barbaras R, Baron R. P2Y13 receptor regulates HDL metabolism and atherosclerosis in vivo. PLoS ONE 2014;9:e95807.
23. Naik SU, Wang X, DaSilva JS, Jaye M, Macphee CH, Reilly MP, Billheimer JT, Rothblat GH, Rader DJ. Pharmacological activation of liver X receptors promotes reverse cholesterol transport in vivo. Circulation 2006;113:90-97.
24. Cavelier C, Ohnsorg PM, Rohrer L, von Eckardstein A. The beta-chain of cell surface F0F1 ATPase modulates ApoA-I and HDL transcytosis through aortic endothelial cells. Arter Thromb Vasc Biol 2012;32:131-139.
25. Van Eck M, Twisk J, Hoekstra M, Van Rij BT, Van der Lans CA, Bos IS, Kruijt JK, Kuipers F, VanBerkel TJ. Differential effectsofscavenger receptorBIdeficiencyonlipid metabolism in cells of the arterial wall and in the liver. J Biol Chem 2003;278:23699-23705.
26. Kozarsky KF, Donahee MH, Rigotti A, Iqbal SN, Edelman ER, Krieger M. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 1997; 387:414-417.
27. Wang N, Arai T, Ji Y, Rinninger F, Tall AR. Liver-specific overexpression of scavenger receptor BI decreases levels of very low density lipoprotein Apo B, low density lipoprotein Apo B, and high density lipoprotein in transgenic mice. J Biol Chem 1998;273: 32920-32926.
28. Calvo D, Gomez-Coronado D, Lasuncion MA, Vega MA. CLA-1an85-kD plasma membrane glycoprotein that acts as a high-affinity receptor for both native (HDL, LDL, and VLDL) and modified (ox LDL, AcLDL) lipoproteins. Arter Thromb Vasc Biol 1997;17: 2341-2349.
29. Stangl H, Hyatt M, Hobbs HH. Transport of lipids from high and low density lipoproteins via scavenger receptor-BI. J Biol Chem 1999;274:32692-32698.
30. Röhrl C, Fruhwürth S, Schreier SMM, Lohninger A, Dolischka A, Hüttinger M, Zemann N, Hermann M, Strobl W, Stangl H, Rohrl C, Fruhwurth S, Huttinger M. Scavenger receptor, class B, typeIprovidesanalternative means for beta-VLDL uptake independentofthe LDL receptor in tissue culture. Biochim Biophys Acta 2010;1801:198-204.
31. Ueda Y, Royer L, Gong E, Zhang J, Cooper PN, Francone O, Rubin EM. Lower plasma levels and accelerated clearance of high density lipoprotein (HDL) and non-HDL cholesterol in scavenger receptor class B type I transgenic mice. J Biol Chem 1999;274: 7165-7171.
32. Van Eck M, Hoekstra M, Out R, Bos IST, Kruijt JK, Hildebrand RB, Van Berkel TJC. Scavenger receptorBIfacilitates the metabolismof VLDL lipoproteinsin vivo.JLipid Res2008; 49:136-146.
33. Yesilaltay A, Kocher O, Rigotti A, Krieger M. Regulation of SR-BI-mediated high-density lipoprotein metabolism by the tissue-specific adaptor protein PDZK1. Curr Opin Lipidol 2005;16:147-152.
34. Kozarsky KF, Donahee MH, Glick JM, Krieger M, Rader DJ. Gene transfer and hepatic overexpression of the HDL receptor SR-BI reduces atherosclerosis in the cholesterol-fed LDL receptor-deficient mouse. Arterioscler Thromb Vasc Biol 2000;20: 721-727.
35. Arai T, Wang N, Bezouevski M, Welch C, Tall AR. Decreased atherosclerosis in heterozygous low density lipoprotein receptor-deficient mice expressing the scavenger receptor BI transgene. J Biol Chem 1999;274:2366-2371.
36. Zhang Y, Da Silva JR, Reilly M, Billheimer JT, Rothblat GH, Rader DJ. Hepatic expression of scavenger receptor classB type I(SR-BI) is a positive regulatorof macrophage reverse cholesterol transport in vivo. J Clin Invest 2005;115:2870-2874.
37. Arai T, Rinninger F, Varban L, Fairchild-Huntress V, Liang CP, Chen W, Seo T, Deckelbaum R, Huszar D, Tall AR. Decreased selective uptake of high density lipopro-tein cholesteryl esters in apolipoprotein E knock-out mice. Proc Natl Acad Sci USA 1999; 96:12050-12055.
38. Annema W, Tietge UJ. Regulation of reverse cholesterol transport-a comprehensive appraisal of available animal studies. Nutr Metab (Lond) 2012;9:25.
39. Verdier C, Martinez LO, Ferrières J, Elbaz M, Genoux A, Perret B. Targeting high-density lipoproteins: update on a promising therapy. Arch Cardiovasc Dis 2013;106:601-611.
40. Kingwell BA, Chapman MJ, Kontush A, Miller NE. HDL-targetedtherapies: progress, failures and future. Nat Rev Drug Discov 2014;13:445-464.