Upregulation of store operated ca2+ channel orai1, Stimulation of Ca2+ Entry and triggering of cell membrane scrambling in platelets by Mineralocorticoid DOCA

Kidney and Blood Pressure Research

Volumn 38, Issue 1, 2014, Pages 21-30

  Liu, Guoxing ^a,b   Liu, Guilai ^a,b   Alzoubi, Kousi ^a   Umbach, Anja T ^a   Pelzl, Lisann ^a   Borst, Oliver ^a   Gawaz, Meinrad ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Department of Cardiology and Cardiovascular Medicine Eberhard Karls University of Tübingen ^*  (Germany)

Author keywords

EMD638683; Mineralocorticoids; Orai1; PI3K; SGK; SOCE

Indexed keywords

CALCIUM; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; DEOXYCORTICOSTERONE ACETATE; EMD 638683; LIPOCORTIN 5; PHOSPHATIDYLSERINE; PROTEIN SERINE THREONINE KINASE INHIBITOR; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG; CALCIUM CHANNEL; MINERALOCORTICOID; ORAI1 PROTEIN, MOUSE; ANTIBODY CONJUGATE; CALCIUM ION; FLUORESCEIN ISOTHIOCYANATE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL ISOLATION; CELL SURFACE; CELL VOLUME; CONCENTRATION (PARAMETERS); FEMALE; FLOW CYTOMETRY; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; THROMBOCYTE; THROMBOCYTE MEMBRANE; UPREGULATION; ANIMAL; BIOSYNTHESIS; CELL MEMBRANE; CELL SIZE; DRUG EFFECTS; GENETICS; METABOLISM; ULTRASTRUCTURE; CELL SWELLING; CONTROLLED STUDY; FLUORESCENCE;

ANIMALS; BLOOD PLATELETS; CALCIUM; CALCIUM CHANNELS; CELL MEMBRANE; CELL SIZE; DESOXYCORTICOSTERONE ACETATE; FEMALE; IN VITRO TECHNIQUES; MALE; MICE; MINERALOCORTICOIDS; PHOSPHATIDYLSERINES; UP-REGULATION;

EID: 84893636343     PISSN: 14204096     EISSN: 14230143     Source Type: Journal    
DOI: 10.1159/000355750     Document Type: Article

References (78)

1. Pearce D, Bhargava A, Cole TJ: Aldosterone: its receptor, target genes, and actions. Vitam Horm 2003;66:29-76.
2. Pelzl L, Pakladok T, Pathare G, Fakhri H, Michael D, Wagner CA, Paulmichl M, Lang F: DOCA sensitive pendrin expression in kidney, heart, lung and thyroid tissues. Cell Physiol Biochem 2012;30:1491-1501.
3. Sakai RR, McEwen BS, Fluharty SJ, Ma LY: The amygdala: site of genomic and nongenomic arousal of aldosterone-induced sodium intake. Kidney Int 2000;57:1337-1345.
4. Vallon V, Huang DY, Grahammer F, Wyatt AW, Osswald H, Wulff P, Kuhl D, Lang F: SGK1 as a determinant of kidney function and salt intake in response to mineralocorticoid excess. Am J Physiol Regul Integr Comp Physiol 2005;289:R395-R401.
5. Funder JW: Aldosterone, hypertension and heart failure: insights from clinical trials. Hypertens Res 2010;33:872-875.
6. Xanthakis V, Vasan RS: Aldosterone and the risk of hypertension. Curr Hypertens Rep 2013;15:102-107.
7. Briet M, Schiffrin EL: Vascular actions of aldosterone. J Vasc Res 2013;50:89-99.
8. Fagart J, Huyet J, Pinon GM, Rochel M, Mayer C, Rafestin-Oblin ME: Crystal structure of a mutant mineralocorticoid receptor responsible for hypertension. Nat Struct Mol Biol 2005;12:554-555.
9. Fejes-Toth G, Naray-Fejes-Toth A: Early aldosterone-regulated genes in cardiomyocytes: clues to cardiac remodeling? Endocrinology 2007;148:1502-1510.
10. Latouche C, Sainte-Marie Y, Steenman M, Castro Chaves P, Naray-Fejes-Toth A, Fejes-Toth G, Farman N, Jaisser F: Molecular signature of mineralocorticoid receptor signaling in cardiomyocytes: from cultured cells to mouse heart. Endocrinology 2010;151:4467-4476.
11. Young M, Funder J: Mineralocorticoid action and sodium-hydrogen exchange: studies in experimental cardiac fibrosis. Endocrinology 2003;144:3848-3851.
12. Young M, Funder JW: Aldosterone and the heart. Trends Endocrinol Metab 2000;11:224-226.
13. Oberleithner H: Is the vascular endothelium under the control of aldosterone? Facts and hypothesis. Pflugers Arch 2007;454:187-193.
14. Oberleithner H, Kusche-Vihrog K, Schillers H: Endothelial cells as vascular salt sensors. Kidney Int 2010;77:490-494.
15. Oberleithner H, Ludwig T, Riethmuller C, Hillebrand U, Albermann L, Schafer C, Shahin V, Schillers H: Human endothelium: target for aldosterone. Hypertension 2004;43:952-956.
16. Sugiyama T, Yoshimoto T, Tsuchiya K, Gochou N, Hirono Y, Tateno T, Fukai N, Shichiri M, Hirata Y: Aldosterone induces angiotensin converting enzyme gene expression via a JAK2-dependent pathway in rat endothelial cells. Endocrinology 2005;146:3900-3906.
17. Lang F: Stiff endothelial cell syndrome in vascular inflammation and mineralocorticoid excess. Hypertension 2011;57:146-147.
18. Lacolley P, Challande P, Osborne-Pellegrin M, Regnault V: Genetics and pathophysiology of arterial stiffness. Cardiovasc Res 2009;81:637-648.
19. Jaffe IZ, Tintut Y, Newfell BG, Demer LL, Mendelsohn ME: Mineralocorticoid receptor activation promotes vascular cell calcification. Arterioscler Thromb Vasc Biol 2007;27:799-805.
20. Voelkl J, Alesutan I, Leibrock CB, Quintanilla-Martinez L, Kuhn V, Feger M, Mia S, Ahmed MS, Rosenblatt KP, Kuro OM, Lang F: Spironolactone ameliorates PIT1-dependent vascular osteoinduction in klothohypomorphic mice. J Clin Invest 2013;123:812-822.
21. de Kloet ER, Joels M, Holsboer F: Stress and the brain: from adaptation to disease. Nat Rev Neurosci 2005;6:463-475.
22. Deutsch SI, Mastropaolo J: Discriminative stimulus properties of midazolam are shared by a GABA-receptor positive steroid. Pharmacol Biochem Behav 1993;46:963-965.
23. Rupprecht R, Holsboer F: Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci 1999;22:410-416.
24. Firsov D: Revisiting sodium and water reabsorption with functional genomics tools. Curr Opin Nephrol Hypertens 2004;13:59-65.
25. Kellner M, Peiter A, Hafner M, Feuring M, Christ M, Wehling M, Falkenstein E, Losel R: Early aldosterone upregulated genes: new pathways for renal disease? Kidney Int 2003;64:1199-1207.
26. Sekizawa N, Yoshimoto T, Hayakawa E, Suzuki N, Sugiyama T, Hirata Y: Transcriptome analysis of aldosterone-regulated genes in human vascular endothelial cell lines stably expressing mineralocorticoid receptor. Mol Cell Endocrinol 2011;341:78-88.
27. Christ M, Sippel K, Eisen C, Wehling M: Non-classical receptors for aldosterone in plasma membranes from pig kidneys. Mol Cell Endocrinol 1994;99:R31-34.
28. Mohammed SF, Ohtani T, Korinek J, Lam CS, Larsen K, Simari RD, Valencik ML, Burnett JC, Jr., Redfield MM: Mineralocorticoid accelerates transition to heart failure with preserved ejection fraction via "nongenomic effects". Circulation 2010;122:370-378.
29. Pietranera L, Saravia FE, McEwen BS, Lucas LL, Johnson AK, De Nicola AF: Changes in Fos expression in various brain regions during deoxycorticosterone acetate treatment: relation to salt appetite, vasopressin mRNA and the mineralocorticoid receptor. Neuroendocrinology 2001;74:396-406.
30. Roy JW, Hill E, Ruan YC, Vedovelli L, Paunescu TG, Brown D, Breton S: Circulating aldosterone induces the apical accumulation of the proton pumping V-ATPase and increases proton secretion in clear cells in the caput epididymis. Am J Physiol Cell Physiol 2013;305:C436-446.
31. Wehling M, Christ M, Theisen K: Membrane receptors for aldosterone: a novel pathway for mineralocorticoid action. Am J Physiol 1992;263:E974-979.
32. Wendler A, Albrecht C, Wehling M: Nongenomic actions of aldosterone and progesterone revisited. Steroids 2012;77:1002-1006.
33. Williams JS: Evolving research in nongenomic actions of aldosterone. Curr Opin Endocrinol Diabetes Obes 2013;20:198-203.
34. Liu SL, Schmuck S, Chorazcyzewski JZ, Gros R, Feldman RD: Aldosterone regulates vascular reactivity: short-term effects mediated by phosphatidylinositol 3-kinase-dependent nitric oxide synthase activation. Circulation 2003;108:2400-2406.
35. Mutoh A, Isshiki M, Fujita T: Aldosterone enhances ligand-stimulated nitric oxide production in endothelial cells. Hypertens Res 2008;31:1811-1820.
36. Oh-hashi S, Takata M, Ueno H, Tomoda F, Yasumoto K, Iida H, Sasayama S: Cytosolic free calcium concentration in platelets in patients with renovascular hypertension and primary aldosteronism. J Hum Hypertens 1992;6:71-74.
37. Gawaz M: Role of platelets in coronary thrombosis and reperfusion of ischemic myocardium. Cardiovasc Res 2004;61:498-511.
38. Borst O, Schmidt EM, Munzer P, Schonberger T, Towhid ST, Elvers M, Leibrock C, Schmid E, Eylenstein A, Kuhl D, May AE, Gawaz M, Lang F: The serum-and glucocorticoid-inducible kinase 1 (SGK1) influences platelet calcium signaling and function by regulation of Orai1 expression in megakaryocytes. Blood 2012;119:251-261.
39. Bigalke B, Stellos K, Geisler T, Kremmer E, Seizer P, May AE, Lindemann S, Melms A, Luft A, Gawaz M: Expression of platelet glycoprotein VI is associated with transient ischemic attack and stroke. Eur J Neurol 2010;17:111-117.
40. Borst O, Munzer P, Gatidis S, Schmidt EM, Schonberger T, Schmid E, Towhid ST, Stellos K, Seizer P, May AE, Lang F, Gawaz M: The inflammatory chemokine CXC motif ligand 16 triggers platelet activation and adhesion via CXC motif receptor 6-dependent phosphatidylinositide 3-kinase/Akt signaling. Circ Res 2012;111:1297-1307.
41. Bergmeier W, Stefanini L: Novel molecules in calcium signaling in platelets. J Thromb Haemost 2009;7:187-190.
42. Rink TJ, Sage SO: Calcium signaling in human platelets. Annu Rev Physiol 1990;52:431-449.
43. Sage SO: Three routes for receptor-mediated Ca2+ entry. Curr Biol 1992;2:312-314.
44. Varga-Szabo D, Braun A, Nieswandt B: Calcium signaling in platelets. J Thromb Haemost 2009;7:1057-1066.
45. Shuttleworth TJ, Thompson JL, Mignen O: STIM1 and the noncapacitative ARC channels. Cell Calcium 2007;42:183-191.
46. Wang Y, Deng X, Gill DL: Calcium signaling by STIM and Orai: intimate coupling details revealed. Sci Signal 2010;3:e42.
47. Parekh AB: Store-operated CRAC channels: function in health and disease. Nat Rev Drug Discov 2010;9:399-410.
48. Braun A, Vogtle T, Varga-Szabo D, Nieswandt B: STIM and Orai in hemostasis and thrombosis. Front Biosci (Landmark Ed) 2011;16:2144-2160.
49. Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, Bosl M, Stoll G, Nieswandt B: Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 2009;113:2056-2063.
50. Bearer EL, Prakash JM, Li Z: Actin dynamics in platelets. Int Rev Cytol 2002;217:137-182.
51. Varga-Szabo D, Braun A, Nieswandt B: STIM and Orai in platelet function. Cell Calcium 2011;50:270-278.
52. Bucki R, Pastore JJ, Giraud F, Janmey PA, Sulpice JC: Involvement of the Na+/H+ exchanger in membrane phosphatidylserine exposure during human platelet activation. Biochim Biophys Acta 2006;1761:195-204.
53. Schmidt EM, Kraemer BF, Borst O, Munzer P, Schonberger T, Schmidt C, Leibrock C, Towhid ST, Seizer P, Kuhl D, Stournaras C, Lindemann S, Gawaz M, Lang F: SGK1 sensitivity of platelet migration. Cell Physiol Biochem 2012;30:259-268.
54. Schmid E, Bhandaru M, Nurbaeva MK, Yang W, Szteyn K, Russo A, Leibrock C, Tyan L, Pearce D, Shumilina E, Lang F: SGK3 regulates Ca(2+) entry and migration of dendritic cells. Cell Physiol Biochem 2012;30:1423-1435.
55. Lang F, Bohmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V: (Patho)physiological significance of the serum-and glucocorticoid-inducible kinase isoforms. Physiol Rev 2006;86:1151-1178.
56. Spinelli SL, Maggirwar SB, Blumberg N, Phipps RP: Nuclear emancipation: a platelet tour de force. Sci Signal 2010;3:e37.
57. Denis MM, Tolley ND, Bunting M, Schwertz H, Jiang H, Lindemann S, Yost CC, Rubner FJ, Albertine KH, Swoboda KJ, Fratto CM, Tolley E, Kraiss LW, McIntyre TM, Zimmerman GA, Weyrich AS: Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 2005;122:379-391.
58. Pabla R, Weyrich AS, Dixon DA, Bray PF, McIntyre TM, Prescott SM, Zimmerman GA: Integrin-dependent control of translation: engagement of integrin alphaIIbbeta3 regulates synthesis of proteins in activated human platelets. J Cell Biol 1999;144:175-184.
59. Weyrich AS, Schwertz H, Kraiss LW, Zimmerman GA: Protein synthesis by platelets: historical and new perspectives. J Thromb Haemost 2009;7:241-246.
60. Lindemann S, Tolley ND, Eyre JR, Kraiss LW, Mahoney TM, Weyrich AS: Integrins regulate the intracellular distribution of eukaryotic initiation factor 4E in platelets. A checkpoint for translational control. J Biol Chem 2001;276:33947-33951.
61. Schwertz H, Tolley ND, Foulks JM, Denis MM, Risenmay BW, Buerke M, Tilley RE, Rondina MT, Harris EM, Kraiss LW, Mackman N, Zimmerman GA, Weyrich AS: Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J Exp Med 2006;203:2433-2440.
62. Munzer P, Tolios A, Pelzl L, Schmid E, Schmidt EM, Walker B, Frohlich H, Borst O, Gawaz M, Lang F: Thrombin-sensitive expression of the store operated Ca(2+) channel Orai1 in platelets. Biochem Biophys Res Commun 2013;436:25-30.
63. Martin V, Guillermet-Guibert J, Chicanne G, Cabou C, Jandrot-Perrus M, Plantavid M, Vanhaesebroeck B, Payrastre B, Gratacap MP: 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.
64. Zhang J, Fry MJ, Waterfield MD, Jaken S, Liao L, Fox JE, Rittenhouse SE: Activated phosphoinositide 3-kinase associates with membrane skeleton in thrombin-exposed platelets. J Biol Chem 1992;267:4686-4692.
65. Weyrich AS, Dixon DA, Pabla R, Elstad MR, McIntyre TM, Prescott SM, Zimmerman GA: Signal-dependent translation of a regulatory protein, Bcl-3, in activated human platelets. Proc Natl Acad Sci USA 1998;95:5556-5561.
66. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG: Orai1 is an essential pore subunit of the CRAC channel. Nature 2006;443:230-233.
67. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP: CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 2006;312:1220-1223.
68. Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD: STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 2005;437:902-905.
69. Varga-Szabo D, Braun A, Kleinschnitz C, Bender M, Pleines I, Pham M, Renne T, Stoll G, Nieswandt B: The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med 2008;205:1583-1591.
70. Rosenwald IB, Pechet L, Han A, Lu L, Pihan G, Woda B, Chen JJ, Szymanski I: Expression of translation initiation factors elF-4E and elF-2alpha and a potential physiologic role of continuous protein synthesis in human platelets. Thromb Haemost 2001;85:142-151.
71. Ackermann TF, Boini KM, Beier N, Scholz W, Fuchss T, Lang F: EMD638683, a novel SGK inhibitor with antihypertensive potency. Cell Physiol Biochem 2011;28:137-146.
72. Galan C, Zbidi H, Bartegi A, Salido GM, Rosado JA: STIM1, Orai1 and hTRPC1 are important for thrombinand ADP-induced aggregation in human platelets. Arch Biochem Biophys 2009;490:137-144.
73. Gawaz M: The evolving science of atherothrombotic disease. Eur Heart J 2008;10:I4-I7.
74. Mahaut-Smith MP: A role for platelet TRPC channels in the Ca2+ response that induces procoagulant activity. Sci Signal 2013;6:pe23.
75. Harper MT, Poole AW: Store-operated calcium entry and non-capacitative calcium entry have distinct roles in thrombin-induced calcium signalling in human platelets. Cell Calcium 2011;50:351-358.
76. Mushtaq M, Nam TS, Kim UH: Critical role for CD38-mediated Ca2+ signaling in thrombin-induced procoagulant activity of mouse platelets and hemostasis. J Biol Chem 2011;286:12952-12958.
77. Wolfs JL, Comfurius P, Rasmussen JT, Keuren JF, Lindhout T, Zwaal RF, Bevers EM: Activated scramblase and inhibited aminophospholipid translocase cause phosphatidylserine exposure in a distinct platelet fraction. Cell Mol Life Sci 2005;62:1514-1525.
78. Badlou BA, Wu YP, Smid WM, Akkerman JW: Platelet binding and phagocytosis by macrophages. Transfusion 2006;46:1432-1443.