Heterodimerization with the prostacyclin receptor triggers thromboxane receptor relocation to lipid rafts

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 1, 2013, Pages 60-66

  Ibrahim, Salam ^a   McCartney, Ann ^a   Markosyan, Nune ^a   Smyth, Emer M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

dimerization; G protein coupled receptor; lipid raft; prostacyclin; thromboxane

Indexed keywords

CHOLESTEROL; FLUORESCENT DYE; G PROTEIN COUPLED RECEPTOR; PROSTACYCLIN RECEPTOR; RENILLA LUCIFERIN 2 MONOOXYGENASE; THROMBOXANE RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL STRAIN COS7; CONTROLLED STUDY; DIMERIZATION; ENERGY TRANSFER; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; LIPID RAFT; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ANIMALS; CERCOPITHECUS AETHIOPS; CHOLESTEROL; COS CELLS; CYCLIC AMP; DIMERIZATION; DISEASE MODELS, ANIMAL; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; HUMANS; HYPERCHOLESTEROLEMIA; LUCIFERASES, RENILLA; MACROPHAGES, PERITONEAL; MEMBRANE MICRODOMAINS; MICE; MYOCYTES, SMOOTH MUSCLE; PROTEIN TRANSPORT; RECEPTORS, PROSTAGLANDIN; RECEPTORS, THROMBOXANE A2, PROSTAGLANDIN H2; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84871749242     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300536     Document Type: Article

References (62)

1. Smyth EM, Grosser T, Wang M, Yu Y, FitzGerald GA. Prostanoids in health and disease. J Lipid Res. 2009;50(Suppl):S423-S428.
2. Cheng Y, Wang M, Yu Y, Lawson J, Funk CD, Fitzgerald GA. Cyclooxygenases, microsomal prostaglandin E synthase-1, and cardiovascular function. J Clin Invest. 2006;116:1391-1399.
3. Egan KM, Lawson JA, Fries S, Koller B, Rader DJ, Smyth EM, Fitzgerald GA. COX-2-derived prostacyclin confers atheroprotection on female mice. Science. 2004;306:1954-1957.
4. Francois H, Athirakul K, Howell D, Dash R, Mao L, Kim HS, Rockman HA, Fitzgerald GA, Koller BH, Coffman TM. Prostacyclin protects against elevated blood pressure and cardiac fibrosis. Cell Metab. 2005;2:201-207.
5. Kobayashi T, Tahara Y, Matsumoto M, Iguchi M, Sano H, Murayama T, Arai H, Oida H, Yurugi-Kobayashi T, Yamashita JK, Katagiri H, Majima M, Yokode M, Kita T, Narumiya S. Roles of thromboxane A(2) and prostacyclin in the development of atherosclerosis in apoE-deficient mice. J Clin Invest. 2004;114:784-794.
6. Nakahata N. Thromboxane A2: physiology/pathophysiology, cellular signal transduction and pharmacology. Pharmacol Ther. 2008;118:18-35.
7. Baigent C, Patrono C. Selective cyclooxygenase 2 inhibitors, aspirin, and cardiovascular disease: a reappraisal. Arthritis Rheum. 2003;48:12-20.
8. Kinsella BT. Thromboxane A2 signalling in humans: a 'Tail' of two receptors. Biochem Soc Trans. 2001;29(Pt 6):641-654.
9. Habib A, FitzGerald GA, Maclouf J. Phosphorylation of the thromboxane receptor alpha, the predominant isoform expressed in human platelets. J Biol Chem. 1999;274:2645-2651.
10. Wilson SJ, Roche AM, Kostetskaia E, Smyth EM. Dimerization of the human receptors for prostacyclin and thromboxane facilitates thromboxane receptor-mediated cAMP generation. J Biol Chem. 2004;279:53036-53047.
11. Yaqoob P. The nutritional significance of lipid rafts. Annu Rev Nutr. 2009;29:257-282.
12. Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol. 2010;11:688-699.
13. Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science. 2010;327:46-50.
14. Patel HH, Murray F, Insel PA. G-protein-coupled receptor-signaling components in membrane raft and caveolae microdomains. Handb Exp Pharmacol. 2008;167-184.
15. Levitt ES, Clark MJ, Jenkins PM, Martens JR, Traynor JR. Differential effect of membrane cholesterol removal on mu-and delta-opioid receptors: a parallel comparison of acute and chronic signaling to adenylyl cyclase. J Biol Chem. 2009;284:22108-22122.
16. Pontier SM, Percherancier Y, Galandrin S, Breit A, Galés C, Bouvier M. Cholesterol-dependent separation of the beta2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J Biol Chem. 2008;283:24659-24672.
17. Chini B, Parenti M. G-protein-coupled receptors, cholesterol and palmitoylation: facts about fats. J Mol Endocrinol. 2009;42:371-379.
18. Michel V, Bakovic M. Lipid rafts in health and disease. Biol Cell. 2007;99:129-140.
19. Jiao X, Zhang N, Xu X, Oppenheim JJ, Jin T. Ligand-induced partitioning of human CXCR1 chemokine receptors with lipid raft microenvironments facilitates G-protein-dependent signaling. Mol Cell Biol. 2005;25:5752-5762.
20. Rouquette-Jazdanian AK, Pelassy C, Breittmayer JP, Aussel C. Revaluation of the role of cholesterol in stabilizing rafts implicated in T cell receptor signaling. Cell Signal. 2006;18:105-122.
21. Storey SM, Gallegos AM, Atshaves BP, McIntosh AL, Martin GG, Parr RD, Landrock KK, Kier AB, Ball JM, Schroeder F. Selective cholesterol dynamics between lipoproteins and caveolae/lipid rafts. Biochemistry. 2007;46:13891-13906.
22. Blair A, Shaul PW, Yuhanna IS, Conrad PA, Smart EJ. Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. J Biol Chem. 1999;274:32512-32519.
23. Murphy AJ, Woollard KJ, Hoang A, Mukhamedova N, Stirzaker RA, McCormick SP, Remaley AT, Sviridov D, Chin-Dusting J. High-density lipoprotein reduces the human monocyte inflammatory response. Arterioscler Thromb Vasc Biol. 2008;28:2071-2077.
24. Ma Y, Ashraf MZ, Podrez EA. Scavenger receptor BI modulates platelet reactivity and thrombosis in dyslipidemia. Blood. 2010;116:1932-1941.
25. Stuart MJ, Gerrard JM, White JG. Effect of cholesterol on production of thromboxane b2 by platelets in vitro. N Engl J Med. 1980;302:6-10.
26. Murphy AJ, Akhtari M, Tolani S, Pagler T, Bijl N, Kuo CL, Wang M, Sanson M, Abramowicz S, Welch C, Bochem AE, Kuivenhoven JA, Yvan-Charvet L, Tall AR. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J Clin Invest. 2011;121:4138-4149.
27. Liu X, Thangavel M, Sun SQ, Kaminsky J, Mahautmr P, Stitham J, Hwa J, Ostrom RS. Adenylyl cyclase type 6 overexpression selectively enhances beta-adrenergic and prostacyclin receptor-mediated inhibition of cardiac fibroblast function because of colocalization in lipid rafts. Naunyn Schmiedebergs Arch Pharmacol. 2008;377:359-369.
28. Ibrahim S, Tetruashvily M, Frey AJ, Wilson SJ, Stitham J, Hwa J, Smyth EM. Dominant negative actions of human prostacyclin receptor variant through dimerization: implications for cardiovascular disease. Arterioscler Thromb Vasc Biol. 2010;30:1802-1809.
29. Miggin SM, Lawler OA, Kinsella BT. Palmitoylation of the human prostacyclin receptor. Functional implications of palmitoylation and isoprenylation. J Biol Chem. 2003;278:6947-6958.
30. O'Meara SJ, Kinsella BT. Investigation of the effect of the farnesyl protein transferase inhibitor R115777 on isoprenylation and intracellular signalling by the prostacyclin receptor. Br J Pharmacol. 2004;143:318-330.
31. Reid HM, Kinsella BT. Palmitoylation of the TPbeta isoform of the human thromboxane A2 receptor. Modulation of G protein: effector coupling and modes of receptor internalization. Cell Signal. 2007;19:1056-1070.
32. Quest AF, Leyton L, Párraga M. Caveolins, caveolae, and lipid rafts in cellular transport, signaling, and disease. Biochem Cell Biol. 2004;82:129-144.
33. Zidovetzki R, Levitan I. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim Biophys Acta. 2007;1768:1311-1324.
34. Ayoub MA, Couturier C, Lucas-Meunier E, Angers S, Fossier P, Bouvier M, Jockers R. Monitoring of ligand-independent dimerization and ligand-induced conformational changes of melatonin receptors in living cells by bioluminescence resonance energy transfer. J Biol Chem. 2002;277:21522-21528.
35. Salahpour A, Angers S, Mercier JF, Lagacé M, Marullo S, Bouvier M. Homodimerization of the beta2-adrenergic receptor as a prerequisite for cell surface targeting. J Biol Chem. 2004;279:33390-33397.
36. Terrillon S, Bouvier M. Roles of G-protein-coupled receptor dimerization. EMBO Rep. 2004;5:30-34.
37. Fessler MB, Parks JS. Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling. J Immunol. 2011;187:1529-1535.
38. Nguyen DH, Espinoza JC, Taub DD. Cellular cholesterol enrichment impairs T cell activation and chemotaxis. Mech Ageing Dev. 2004;125:641-650.
39. Zhuang L, Kim J, Adam RM, Solomon KR, Freeman MR. Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts. J Clin Invest. 2005;115:959-968.
40. Fredrickson DS, Steinberg D. Inhibitors of cholesterol biosynthesis and the problem of hypercholesterolemia. Ann N Y Acad Sci. 1956;64:579-589.
41. LaRosa JC, Hunninghake D, Bush D, Criqui MH, Getz GS, Gotto AM Jr, Grundy SM, Rakita L, Robertson RM, Weisfeldt ML. The cholesterol facts. A summary of the evidence relating dietary fats, serum cholesterol, and coronary heart disease. A joint statement by the American Heart Association and the National Heart, Lung, and Blood Institute. The Task Force on Cholesterol Issues, American Heart Association. Circulation. 1990;81:1721-1733.
42. 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.
43. Bhandaru R, Srinivasan SR, Radhakrisnamurthy B, Berenson GS. Effects of diabetes and high fat-high cholesterol diet on plasma lipid levels and on erythrocyte membrane composition. Atherosclerosis. 1982;42:263-272.
44. Sun JV, Tepperman HM, Tepperman J. Lipid composition of liver plasma membranes isolated from rats fed a high glucose or a high fat diet. J Nutr. 1979;109:193-201.
45. Shanmugasundaram KR, Visvanathan A, Dhandapani K, Srinivasan N, Rasappan P, Gilbert R, Alladi S, Kancharla S, Vasanthi N. Effect of high-fat diet on cholesterol distribution in plasma lipoproteins, cholesterol esterifying activity in leucocytes, and erythrocyte membrane components studied: importance of body weight. Am J Clin Nutr. 1986;44:805-815.
46. Jaschonek K, Funck M, Muller CP, Schmidt H. Modulation of platelet [3H] iloprost binding by cholesterol, dibucaine and pentoxifylline. Prog Clin Biol Res. 1989;301:321-325.
47. Chabanel A, Flamm M, Sung KL, Lee MM, Schachter D, Chien S. Influence of cholesterol content on red cell membrane viscoelasticity and fluidity. Biophys J. 1983;44:171-176.
48. Sharma DK, Brown JC, Choudhury A, Peterson TE, Holicky E, Marks DL, Simari R, Parton RG, Pagano RE. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol Biol Cell. 2004;15:3114-3122.
49. Resh MD. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci STKE. 2006;2006:re14.
50. Leslie M. Mysteries of the cell. Do lipid rafts exist? Science. 2011;334:1046-1047.
51. Oh P, Schnitzer JE. Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol Biol Cell. 2001;12:685-698.
52. Fallahi-Sichani M, Linderman JJ. Lipid raft-mediated regulation of G-protein coupled receptor signaling by ligands which influence receptor dimerization: a computational study. PLoS ONE. 2009;4:e6604.
53. Ayoub MA, Pfleger KD. Recent advances in bioluminescence resonance energy transfer technologies to study GPCR heteromerization. Curr Opin Pharmacol. 2010;10:44-52.
54. Oh H, Mohler ER III, Tian A, Baumgart T, Diamond SL. Membrane cholesterol is a biomechanical regulator of neutrophil adhesion. Arterioscler Thromb Vasc Biol. 2009;29:1290-1297.
55. Cheng Y, Austin SC, Rocca B, Koller BH, Coffman TM, Grosser T, Lawson JA, FitzGerald GA. Role of prostacyclin in the cardiovascular response to thromboxane A2. Science. 2002;296:539-541.
56. Marquer C, Devauges V, Cossec JC, Liot G, Lécart S, Saudou F, Duyckaerts C, Lévêque-Fort S, Potier MC. Local cholesterol increase triggers amyloid precursor protein-Bace1 clustering in lipid rafts and rapid endocytosis. FASEB J. 2011;25:1295-1305.
57. Dalrymple MB, Pfleger KD, Eidne KA. G protein-coupled receptor dimers: functional consequences, disease states and drug targets. Pharmacol Ther. 2008;118:359-371.
58. Milligan G. G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br J Pharmacol. 2009;158:5-14.
59. Teitler M, Klein MT. A new approach for studying GPCR dimers: drug-induced inactivation and reactivation to reveal GPCR dimer function in vitro, in primary culture, and in vivo. Pharmacol Ther. 2012;133:205-217.
60. AbdAlla S, Lother H, el Massiery A, Quitterer U. Increased AT(1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat Med. 2001;7:1003-1009.
61. Chakrabarti S, Liu NJ, Gintzler AR. Formation of mu-/kappa-opioid receptor heterodimer is sex-dependent and mediates female-specific opioid analgesia. Proc Natl Acad Sci USA. 2010;107:20115-20119.
62. Wong AH, Liu F. Uncoupling the dopamine D1-D2 receptor complex: a novel target for antidepressant treatment. Clin Pharmacol Ther. 2012;91: 298-302.