PI3Kβ Plays a Key Role in Apolipoprotein A-I-Induced Endothelial Cell Proliferation Through Activation of the Ecto-F 1 -ATPase/P2Y 1 Receptors

Cellular Physiology and Biochemistry

Volumn 42, Issue 2, 2017, Pages 579-593

  Castaing Berthou, Audrey ^a,b   Malet, Nicole ^a,b   Radojkovic, Claudia ^c   Cabou, Cendrine ^a,b   Gayral, Stéphanie ^a,b   Martinez, Laurent Olivier ^a,b   Laffargue, Muriel ^a,b  

^a CHU RANGUEIL   (France)

^b Université de Toulouse   (France)

^c UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

Apolipoprotein A I; ATP synthase; Endothelial cell; HDL; Phosphoinositide 3 kinase; Purinergic signaling

Indexed keywords

APOLIPOPROTEIN A1; FIBRINOGEN; OLIGOMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE BETA; PURINERGIC P2Y1 RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE; APOA1 PROTEIN, HUMAN; HIGH DENSITY LIPOPROTEIN; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE; PIK3C2B PROTEIN, HUMAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ARTICLE; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; GENE SILENCING; HEART PROTECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; ARTERY; BIOSYNTHESIS; CELL WALL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

ADENOSINE DIPHOSPHATE; APOLIPOPROTEIN A-I; ARTERIES; CELL PROLIFERATION; CELL WALL; CLASS II PHOSPHATIDYLINOSITOL 3-KINASES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIPOPROTEINS, HDL; ONCOGENE PROTEIN V-AKT; PROTON-TRANSLOCATING ATPASES; RECEPTORS, PURINERGIC P2Y1;

EID: 85020444446     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000477607     Document Type: Article

References (68)

1. Forte A, Rinaldi B, Berrino L, Rossi F, Galderisi U, Cipollaro M: Novel potential targets for prevention of arterial restenosis: insights from the pre-clinical research. Clin Sci (Lond) 2014;127: 615-634.
2. Zhu T, Yao Q, Hu X, Chen C, Yao H, Chao J: The Role of MCPIP1 in Ischemia/Reperfusion Injury-Induced HUVEC Migration and Apoptosis. Cell Physiol Biochem 2015;37: 577-591.
3. Chapman MJ, Ginsberg HN, Amarenco P, Andreotti F, Borén J, Catapano AL, Descamps OS, Fisher E, Kovanen PT, Kuivenhoven JA, Lesnik P, Masana L, Nordestgaard BG, Ray KK, Reiner Z, Taskinen M-R, Tokgözoglu L, Tybjærg-Hansen A, Watts GF: Triglyceride-rich lipoproteins and high-density lipoprotein cholesterol in patients at high risk of cardiovascular disease: evidence and guidance for management. Eur Heart J 2011;32: 1345-1361.
4. Rye K-A, Barter PJ: Cardioprotective functions of HDLs. J Lipid Res 2014;55: 168-79.
5. Kratzer A, Giral H, Landmesser U: High-density lipoproteins as modulators of endothelial cell functions: alterations in patients with coronary artery disease. Cardiovasc Res 2014;103: 350-361.
6. Riwanto M, Landmesser U: High density lipoproteins and endothelial functions: mechanistic insights and alterations in cardiovascular disease. J Lipid Res 2013;54: 3227-3243.
7. Tran-Dinh A, Diallo D, Delbosc S, Varela-Perez LM, Dang QB, Lapergue B, Burillo E, Michel JB, Levoye A, Martin-Ventura JL, Meilhac O: HDL and endothelial protection. Br J Pharmacol 2013;169: 493-511.
8. von Eckardstein A, Rohrer L: HDLs in crises. Curr Opin Lipidol 2016;27: 264-273.
9. Strong A, Rader DJ: Clinical Implications of Lipid Genetics for Cardiovascular Disease. Curr Cardiovasc Risk Rep 2010;4: 461-468.
10. Voight BF, Peloso GM, Orho-Melander M, Frikke-Schmidt R, Barbalic M, Jensen MK, Hindy G, Hólm H, Ding EL, Johnson T, Schunkert H, Samani NJ, Clarke R, Hopewell JC, Thompson JF, Li M, Thorleifsson G, Newton-Cheh C, Musunuru K, Pirruccello JP, Saleheen D, Chen L, Stewart AFR, Schillert A, Thorsteinsdottir U, Thorgeirsson G, Anand S, Engert JC, Morgan T, Spertus J, et al.: Plasma HDL cholesterol and risk of myocardial infarction: a mendelian randomisation study. Lancet 2012;380: 572-580.
11. 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.
12. Riwanto M, Rohrer L, von Eckardstein A, Landmesser U: Dysfunctional HDL: from structure-function-relationships to biomarkers. Handb Exp Pharmacol 2015;224: 337-366.
13. Tauber JP, Cheng J, Gospodarowicz D: Effect of high and low density lipoproteins on proliferation of cultured bovine vascular endothelial cells. J Clin Invest 1980;66: 696-708.
14. Tauber JP, Cheng J, Massoglia S, Gospodarowicz D: High density lipoproteins and the growth of vascular endothelial cells in serum-free medium. In Vitro 1981;17: 519-530.
15. Suc I, Escargueil-Blanc I, Troly M, Salvayre R, Negre-Salvayre A: HDL and ApoA prevent cell death of endothelial cells induced by oxidized LDL. Arter Thromb Vasc Biol 1997;17: 2158-2166.
16. Seetharam D, Mineo C, Gormley AK, Gibson LL, Vongpatanasin W, Chambliss KL, Hahner LD, Cummings ML, Kitchens RL, Marcel YL, Rader DJ, Shaul PW: High-density lipoprotein promotes endothelial cell migration and reendothelialization via scavenger receptor-B type I. Circ Res 2006;98: 63-72.
17. Kimura T, Sato K, Malchinkhuu E, Tomura H, Tamama K, Kuwabara A, Murakami M, Okajima F: High-density lipoprotein stimulates endothelial cell migration and survival through sphingosine 1-phosphate and its receptors. Arter Thromb Vasc Biol 2003;23: 1283-1288.
18. Radojkovic C, Genoux A, Pons V, Combes G, de Jonge H, Champagne E, Rolland C, Perret B, Collet X, Terce F, Martinez LO: Stimulation of Cell Surface F1-ATPase Activity by Apolipoprotein A-I Inhibits Endothelial Cell Apoptosis and Promotes Proliferation. Arter Thromb Vasc Biol 2009;29: 1125-1130.
19. González-Pecchi V, Valdés S, Pons V, Honorato P, Martinez LO, Lamperti L, Aguayo C, Radojkovic C: Apolipoprotein A-I enhances proliferation of human endothelial progenitor cells and promotes angiogenesis through the cell surface ATP synthase. Microvasc Res 2015;98: 9-15.
20. 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.
21. 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.
22. 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 LO: P2Y13 receptor is critical for reverse cholesterol transport. Hepatology 2010;52: 1477-1483.
23. Lichtenstein L, Serhan N, Espinosa-Delgado S, Fabre A, Annema W, Tietge UJF, Robaye B, Boyenaems J-M, Laffargue M, Perret B, Martinez LO: Increased Atherosclerosis in P2Y13/Apolipoprotein E Double-Knockout Mice: Contribution of P2Y13 to Reverse Cholesterol Transport. Cardiovasc Res 2015;106: 315-323.
24. Goffinet M, Tardy C, Boubekeur N, Cholez G, Bluteau GA, 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.
25. 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.
26. Cabezon E, Butler PJ, Runswick MJ, Walker JE: Modulation of the oligomerization state of the bovine F1-ATPase inhibitor protein, IF1, by pH. J Biol Chem 2000;275: 25460-25464.
27. Fabre AC, Vantourout P, Champagne E, Terce F, Rolland C, Perret B, Collet X, Barbaras R, Martinez LO: Cell surface adenylate kinase activity regulates the F1-ATPase/P2Y13-mediated HDL endocytosis pathway on human hepatocytes. Cell Mol Life Sci 2006;63: 2829-2837.
28. Moser TL, Stack MS, Asplin I, Enghild JJ, Hojrup P, Everitt L, Hubchak S, Schnaper HW, Pizzo S V: Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc Natl Acad Sci USA 1999;96: 2811-2816.
29. Linnett PE, Beechey RB: Inhibitors of the ATP synthethase system. Methods Enzym 1979;55: 472-518.
30. 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.
31. Martinez LO, Cabou C, Pons V, Malaval C: P2Y receptors in atherosclerosis: from lipid metabolism to vascular functions. WIREs Membr Transp Signal 2012;1: 743-754.
32. Martinez LO, Najib S, Perret B, Cabou C, Lichtenstein L: Ecto-F1-ATPase/P2Y pathways in metabolic and vascular functions of high density lipoproteins. Atherosclerosis 2015;238: 89-100.
33. Shen J, DiCorleto PE: ADP stimulates human endothelial cell migration via P2Y1 nucleotide receptor-mediated mitogen-activated protein kinase pathways. Circ Res 2008;102: 448-456.
34. Lupieri A, Smirnova N, Malet N, Gayral S, Laffargue M: PI3K signaling in arterial diseases: Non redundant functions of the PI3K isoforms. Adv Biol Regul 2015;59: 4-18.
35. Wymann MP, Zvelebil M, Laffargue M: Phosphoinositide 3-kinase signalling-which way to target? Trends Pharmacol Sci 2003;24: 366-376.
36. Guillermet-Guibert J, Bjorklof K, Salpekar A, Gonella C, Ramadani F, Bilancio A, Meek S, Smith AJH, Okkenhaug K, Vanhaesebroeck B: The p110beta isoform of phosphoinositide 3-kinase signals downstream of G protein-coupled receptors and is functionally redundant with p110gamma. Proc Natl Acad Sci USA 2008;105: 8292-8297.
37. Nofer J-R: Signal transduction by HDL: agonists, receptors, and signaling cascades. Handb Exp Pharmacol 2015;224: 229-256.
38. Martinez LO, Jacquet S, Terce F, Collet X, Perret B, Barbaras R: New insight on the molecular mechanisms of high-density lipoprotein cellular interactions. Cell Mol Life Sci 2004;61: 2343-2360.
39. Cavelier C, Rohrer L, von Eckardstein A: ATP-Binding cassette transporter A1 modulates apolipoprotein A-I transcytosis through aortic endothelial cells. Circ Res 2006;99: 1060-1066.
40. Vaisman BL, Demosky SJ, Stonik JA, Ghias M, Knapper CL, Sampson ML, Dai C, Levine SJ, Remaley AT: Endothelial expression of human ABCA1 in mice increases plasma HDL cholesterol and reduces diet-induced atherosclerosis. J Lipid Res 2012;53: 158-167.
41. Westerterp M, Tsuchiya K, Tattersall IW, Fotakis P, Bochem AE, Molusky MM, Ntonga V, Abramowicz S, Parks JS, Welch CL, Kitajewski J, Accili D, Tall AR: Deficiency of ATP-Binding Cassette Transporters A1 and G1 in Endothelial Cells Accelerates Atherosclerosis in Mice. Arterioscler Thromb Vasc Biol 2016;36: 1328-1337.
42. Argraves KM, Argraves WS: HDL serves as a S1P signaling platform mediating a multitude of cardiovascular effects. J Lipid Res 2007;48: 2325-2333.
43. Boeynaems J-M, Communi D, Robaye B: Overview of the pharmacology and physiological roles of P2Y receptors. WIREs Membr Transp Signal 2012;1: 581-588.
44. Malaval C, Laffargue M, Barbaras R, Rolland C, Peres C, Champagne E, Perret B, Tercé F, Collet X, Martinez LO: RhoA/ROCK I signalling downstream of the P2Y13 ADP-receptor controls HDL endocytosis in human hepatocytes. Cell Signal 2009;21: 120-127.
45. Blom D, Yamin T-T, Champy M-F, 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.
46. Laplante MA, Monassier L, Freund M, Bousquet P, Gachet C: The purinergic P2Y1 receptor supports leptin secretion in adipose tissue. Endocrinology 2010;151: 2060-2070.
47. Lee H, Jun DJ, Suh BC, Choi BH, Lee JH, Do MS, Suh BS, Ha H, Kim KT: Dual roles of P2 purinergic receptors in insulin-stimulated leptin production and lipolysis in differentiated rat white adipocytes. J Biol Chem 2005;280: 28556-28563.
48. Kim BW, Choo HJ, Lee JW, Kim JH, Ko YG: Extracellular ATP is generated by ATP synthase complex in adipocyte lipid rafts. Exp Mol Med 2004;36: 476-485.
49. Arakaki N, Kita T, Shibata H, Higuti T: Cell-surface H+-ATP synthase as a potential molecular target for anti-obesity drugs. FEBS Lett 2007;581: 3405-3409.
50. Howard AD, Verghese PB, Arrese EL, Soulages JL: The beta-subunit of ATP synthase is involved in cellular uptake and resecretion of apoA-I but does not control apoA-I-induced lipid efflux in adipocytes. Mol Cell Biochem 2011;348: 155-164.
51. Guns PJ, Korda A, Crauwels HM, Assche T Van, Robaye B, Boeynaems JM, Bult H: Pharmacological characterization of nucleotide P2Y receptors on endothelial cells of the mouse aorta. Br J Pharmacol 2005;146: 288-295.
52. Wihlborg A-K, Malmsjö M, Eyjolfsson A, Gustafsson R, Jacobson K, Erlinge D: Extracellular nucleotides induce vasodilatation in human arteries via prostaglandins, nitric oxide and endothelium-derived hyperpolarising factor. Br J Pharmacol 2003;138: 1451-1458.
53. Hechler B, Freund M, Ravanat C, Magnenat S, Cazenave JP, Gachet C: Reduced atherosclerotic lesions in P2Y1/apolipoprotein E double-knockout mice: the contribution of non-hematopoietic-derived P2Y1 receptors. Circulation 2008;118: 754-763.
54. Zerr M, Hechler B, Freund M, Magnenat S, Lanois I, Cazenave JP, Leon C, Gachet C: Major contribution of the P2Y1 receptor in purinergic regulation of TNFalpha-induced vascular inflammation. Circulation 2011;123: 2404-2413.
55. Haddad G, Zhabyeyev P, Farhan M, Zhu LF, Kassiri Z, Rayner DC, Vanhaesebroeck B, Oudit GY, Murray AG: Phosphoinositide 3-kinase β mediates microvascular endothelial repair of thrombotic microangiopathy. Blood 2014;124: 2142-2149.
56. Logan SK, Falasca M, Hu P, Schlessinger J: Phosphatidylinositol 3-kinase mediates epidermal growth factor-induced activation of the c-Jun N-terminal kinase signaling pathway. Mol Cell Biol 1997;17: 5784-5790.
57. Murga C, Fukuhara S, Gutkind JS: A novel role for phosphatidylinositol 3-kinase beta in signaling from G protein-coupled receptors to Akt. J Biol Chem 2000;275: 12069-12073.
58. Kurosu H, Maehama T, Okada T, Yamamoto T, Hoshino S, Fukui Y, Ui M, Hazeki O, Katada T: Heterodimeric phosphoinositide 3-kinase consisting of p85 and p110beta is synergistically activated by the betagamma subunits of G proteins and phosphotyrosyl peptide. J Biol Chem 1997;272: 24252-24256.
59. Igarashi J, Michel T: Sphingosine 1-phosphate and isoform-specific activation of phosphoinositide 3-kinase beta. Evidence for divergence and convergence of receptor-regulated endothelial nitric-oxide synthase signaling pathways. J Biol Chem 2001;276: 36281-36288.
60. Heller R, Chang Q, Ehrlich G, Hsieh SN, Schoenwaelder SM, Kuhlencordt PJ, Preissner KT, Hirsch E, Wetzker R: Overlapping and distinct roles for PI3Kbeta and gamma isoforms in S1P-induced migration of human and mouse endothelial cells. Cardiovasc Res 2008;80: 96-105.
61. Uruno A, Sugawara A, Kanatsuka H, Kagechika H, Saito A, Sato K, Kudo M, Takeuchi K, Ito S.: Upregulation of nitric oxide production in vascular endothelial cells by all-trans retinoic acid through the phosphoinositide 3-kinase/Akt pathway. Circulation 2005;112: 727-736.
62. Tibolla G, Piñeiro R, Chiozzotto D, Mavrommati I, Wheeler AP, Norata GD, Catapano AL, Maffucci T, Falasca M: Class II phosphoinositide 3-kinases contribute to endothelial cells morphogenesis. PLoS One 2013;8:e53808.
63. Fougerat A, Gayral S, Gourdy P, Schambourg A, Ruckle T, Schwarz MK, Rommel C, Hirsch E, Arnal JF, Salles JP, Perret B, Breton-Douillon M, Wymann MP, Laffargue M: Genetic and pharmacological targeting of phosphoinositide 3-kinase-gamma reduces atherosclerosis and favors plaque stability by modulating inflammatory processes. Circulation 2008;117: 1310-1317.
64. Smirnova NF, Gayral S, Pedros C, Loirand G, Vaillant N, Malet N, Kassem S, Calise D, Goudounèche D, Wymann MP, Hirsch E, Gadeau A-P, Martinez LO, Saoudi A, Laffargue M: Targeting PI3Kγ activity decreases vascular trauma-induced intimal hyperplasia through modulation of the Th1 response. J Exp Med 2014;211: 1779-1792.
65. Puri KD, Doggett TA, Huang C-Y, Douangpanya J, Hayflick JS, Turner M, Penninger J, Diacovo TG: The role of endothelial PI3Kgamma activity in neutrophil trafficking. Blood 2005;106: 150-157.
66. Jackson SP, Schoenwaelder SM, Goncalves I, Nesbitt WS, Yap CL, Wright CE, Kenche V, Anderson KE, Dopheide SM, Yuan Y, Sturgeon SA, Prabaharan H, Thompson PE, Smith GD, Shepherd PR, Daniele N, Kulkarni S, Abbott B, Saylik D, Jones C, Lu L, Giuliano S, Hughan SC, Angus JA, Robertson AD, Salem HH: PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat Med 2005;11: 507-514.
67. Canobbio I, Stefanini L, Cipolla L, Ciraolo E, Gruppi C, Balduini C, Hirsch E, Torti M: Genetic evidence for a predominant role of PI3Kbeta catalytic activity in ITAM-and integrin-mediated signaling in platelets. Blood 2009;114: 2193-2196.
68. Martin V, Guillermet-Guibert J, Chicanne G, Cabou C, Jandrot-Perrus M, Plantavid M, Vanhaesebroeck B, Payrastre B, Gratacap M-P: Deletion of the p110beta isoform of phosphoinositide 3-kinase in platelets reveals its central role in Akt activation and thrombus formation in vitro and in vivo. Blood 2010; 115: 2008-2013.