Endothelial mineralocorticoid receptor activation enhances endothelial protein C receptor and decreases vascular thrombosis in mice

FASEB Journal

Volumn 28, Issue 5, 2014, Pages 2062-2072

  Lagrange, Jérémy ^a,b   Li, Zhenlin ^c   Fassot, Céline ^c,d   Bourhim, Mustapha ^a,b   Louis, Huguette ^a,b   Nguyen Dinh Cat, Aurélie ^c,d   Parlakian, Ara ^c   Wahl, Denis ^a,b,e   Lacolley, Patrick ^a,b,e   Jaisser, Fréderic ^c,d,e   Regnault, Véronique ^a,b,e  

^a INSERM   (France)

^b UNIVERSITÉ DE LORRAINE   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d CENTRE DE RECHERCHE DES CORDELIERS   (France)

^e UNIVERSITY HOSPITAL OF NANCY   (France)

Author keywords

Aldosterone; Smooth muscle cell; SP1; Thrombin; Transcriptional regulation

Indexed keywords

ACTIVATED PROTEIN C; ALDOSTERONE; ENDOTHELIAL PROTEIN C RECEPTOR; FERRIC CHLORIDE; MINERALOCORTICOID RECEPTOR; RNA; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTIC ENDOTHELIAL CELL; ARTERY THROMBOSIS; ARTICLE; BLOOD CLOTTING; CARDIOVASCULAR RISK; CONTROLLED STUDY; CORTICOSTEROID THERAPY; DOWN REGULATION; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RNA ISOLATION; SMOOTH MUSCLE FIBER; THROMBOCYTE POOR PLASMA; UPREGULATION; VASCULAR ENDOTHELIUM; WILD TYPE;

ALDOSTERONE; SMOOTH MUSCLE CELL; SP1; THROMBIN; TRANSCRIPTIONAL REGULATION;

ALDOSTERONE; ANIMALS; AORTA; BLOOD COAGULATION FACTORS; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENES, REPORTER; GENETIC VECTORS; HUMANS; MALE; MICE; MICE, TRANSGENIC; PLASMIDS; PROTEIN C; RECEPTORS, CELL SURFACE; RECEPTORS, MINERALOCORTICOID; RNA; THROMBIN; THROMBOSIS;

EID: 84901070317     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-238188     Document Type: Article

References (43)

1. Simpson, S. A., Tait, J. F., Wettstein, A., Neher, R., Von Euw, J., and Reichstein, T. (1953) [Isolation from the adrenals of a new crystalline hormone with especially high effectiveness on mineral metabolism]. Experientia 9, 333-335
2. Brilla, C. G., Pick, R., Tan, L. B., Janicki, J. S., and Weber, K. T. (1990) Remodeling of the rat right and left ventricles in experimental hypertension. Circ. Res. 67, 1355-1364
3. Messaoudi, S., Azibani, F., Delcayre, C., and Jaisser, F. (2012) Aldosterone, mineralocorticoid receptor, and heart failure. Mol. Cell. Endocrinol. 350, 266-272
4. Pitt, B., Remme, W., Zannad, F., Neaton, J., Martinez, F., Roniker, B., Bittman, R., Hurley, S., Kleiman, J., and Gatlin, M. (2003) Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N. Engl. J. Med. 348, 1309-1321
5. Zannad, F., McMurray, J. J., Krum, H., van Veldhuisen, D. J., Swedberg, K., Shi, H., Vincent, J., Pocock, S. J., and Pitt, B. (2011) Eplerenone in patients with systolic heart failure and mild symptoms. N. Engl. J. Med. 364, 11-21
6. Funder, J. W. (2004) Is aldosterone bad for the heart? Trends Endocrinol. Metab. 15, 139-142
7. Messaoudi, S., Milliez, P., Samuel, J. L., and Delcayre, C. (2009) Cardiac aldosterone overexpression prevents harmful effects of diabetes in the mouse heart by preserving capillary density. FASEB J. 23, 2176-2185
8. Skott, O., Uhrenholt, T. R., Schjerning, J., Hansen, P. B., Rasmussen, L. E., and Jensen, B. L. (2006) Rapid actions of aldosterone in vascular health and disease-friend or foe? Pharmacol. Ther. 111, 495-507
9. Zhao, M., Celerier, I., Bousquet, E., Jeanny, J. C., Jonet, L., Savoldelli, M., Offret, O., Curan, A., Farman, N., Jaisser, F., and Behar-Cohen, F. (2012) Mineralocorticoid receptor is involved in rat and human ocular chorioretinopathy. J. Clin. Invest. 122, 2672-2679
10. Nguyen Dinh Cat, A., Griol-Charhbili, V., Loufrani, L., Labat, C., Benjamin, L., Farman, N., Lacolley, P., Henrion, D., and Jaisser, F. (2010) The endothelial mineralocorticoid receptor regulates vasoconstrictor tone and blood pressure. FASEB J. 24, 2454-2463
11. Bodary, P. F., Sambaziotis, C., Wickenheiser, K. J., Rajagopalan, S., Pitt, B., and Eitzman, D. T. (2006) Aldosterone promotes thrombosis formation after arterial injury in mice. Arterioscler. Thromb. Vasc. Biol. 26, 233
12. Stankiewicz, A., Gromotowicz, A., Szemraj, J., Wojewodzka-Zelezniakowicz, M., Skrzypkowski, P., and Chabielska, E. (2007) Acute aldosterone infusion enhances thrombosis development in normotensive rats. Thromb. Haemost. 98, 697-699
13. Gromotowicz, A., Szemraj, J., Stankiewicz, A., Zakrzeska, A., Mantur, M., Jaroszewicz, E., Rogowski, F., and Chabielska, E. (2011) Study of the mechanisms of aldosterone prothrombotic effect in rats. J. Renin Angiotensin Aldosterone Syst. 12, 430-439
14. Schafer, A., Fraccarollo, D., Hildemann, S., Christ, M., Eigenthaler, M., Kobsar, A., Walter, U., and Bauersachs, J. (2003) Inhibition of platelet activation in congestive heart failure by aldosterone receptor antagonism and ACE inhibition. Thromb. Haemost. 89, 1024-1030
15. Schafer, A., Vogt, C., Fraccarollo, D., Widder, J., Flierl, U., Hildemann, S. K., Ertl, G., and Bauersachs, J. (2010) Eplerenone improves vascular function and reduces platelet activation in diabetic rats. J. Physiol. Pharmacol. 61, 45-52
16. Ducros, E., Berthaut, A., Mirshahi, S. S., Faussat, A. M., Soria, J., Agarwal, M. K., and Mirshahi, M. (2008) Aldosterone modifies hemostasis via upregulation of the protein-C receptor in human vascular endothelium. Biochem. Biophys. Res. Commun. 373, 192-196
17. Regnault, V., Rivat, C., Pfister, M., and Stoltz, J. F. (1991) Monoclonal antibodies against human plasma protein C and their uses for immunoaffinity chromatography. Thromb. Res. 63, 629-640
18. Tchaikovski, S. N., van Vlijmen, B. J., Rosing, J., and Tans, G. (2007) Development of a calibrated automated thrombography based thrombin generation test in mouse plasma. J. Thromb. Haemost. 5, 2079-2086
19. Hemker, H. C., Giesen, P., Al Dieri, R., Regnault, V., de Smedt, E., Wagenvoord, R., Lecompte, T., and Beguin, S. (2003) Calibrated automated thrombin generation measurement in clotting plasma. Pathophysiol. Haemost. Thromb. 33, 4-15
20. Regnault, V., Hemker, H. C., Wahl, D., and Lecompte, T. (2004) Phenotyping the haemostatic system by thrombography-potential for the estimation of thrombotic risk. Thromb. Res. 114, 539-545
21. Hackeng, T. M., Tans, G., Koppelman, S. J., de Groot, P. G., Rosing, J., and Bouma, B. N. (1996) Protein C activation on endothelial cells by prothrombin activation products generated in situ: meizothrombin is a better protein C activator than alpha-thrombin. Biochem. J. 319(Pt. 2), 399-405
22. Regnault, V., de Maistre, E., Geschier, C., Briquel, M. E., André, E., Stoltz, J. F., and Lecompte, T. (1995) A new fast one-step immunopreparation for activated protein C. Thromb. Haemost. 73, 1365
23. Mao, X., Said, R., Louis, H., Max, J. P., Bourhim, M., Challande, P., Wahl, D., Li, Z., Regnault, V., and Lacolley, P. (2012) Cyclic stretch-induced thrombin generation by rat vascular smooth muscle cells is mediated by the integrin alphavbeta3 pathway. Cardiovasc. Res. 96, 513-523
24. Parlakian, A., Gomaa, I., Solly, S., Arandel, L., Mahale, A., Born, G., Marazzi, G., and Sassoon, D. (2010) Skeletal muscle phenotypically converts and selectively inhibits metastatic cells in mice. PLoS One 5, e9299
25. Jeong, Y., Chaupin, D. F., Matsushita, K., Yamakuchi, M., Cameron, S. J., Morrell, C. N., and Lowenstein, C. J. (2009) Aldosterone activates endothelial exocytosis. Proc. Natl. Acad. Sci. U. S. A. 106, 3782-3787
26. Esmon, C. T. (2004) Structure and functions of the endothelial cell protein C receptor. Crit. Care Med. 32, S298-301
27. Weiler, H. (2011) Multiple receptor-mediated functions of activated protein C. Hamostaseologie 31, 185-195
28. Van 't Veer, C., Golden, N. J., Kalafatis, M., and Mann, K. G. (1997) Inhibitory mechanism of the protein C pathway on tissue factor-induced thrombin generation. Synergistic effect in combination with tissue factor pathway inhibitor. J. Biol. Chem. 272, 7983-7994
29. McCurley, A., and Jaffe, I. Z. (2012) Mineralocorticoid receptors in vascular function and disease. Mol. Cell. Endocrinol. 350, 256-265
30. Mollica, L. R., Crawley, J. T., Liu, K., Rance, J. B., Cockerill, P. N., Follows, G. A., Landry, J. R., Wells, D. J., and Lane, D. A. (2006) Role of a 5'-enhancer in the transcriptional regulation of the human endothelial cell protein C receptor gene. Blood 108, 1251-1259
31. Meinel, S., Ruhs, S., Schumann, K., Stratz, N., Trenkmann, K., Schreier, B., Grosse, I., Keilwagen, J., Gekle, M., and Grossmann, C. (2013) Mineralocorticoid receptor interaction with SP1 generates a new response element for pathophysiologically relevant gene expression. Nucleic Acids Res. 41, 8045-8060
32. Qu, D., Wang, Y., Esmon, N. L., and Esmon, C. T. (2007) Regulated endothelial protein C receptor shedding is mediated by tumor necrosis factor-alpha converting enzyme/ADAM17. J. Thromb. Haemost. 5, 395-402
33. Barr, J. D., Chauhan, A. K., Schaeffer, G. V., Hansen, J. K., and Motto, D. G. (2013) Red blood cells mediate the onset of thrombosis in the ferric chloride murine model. Blood 121, 3733-3741
34. Li, W., Zheng, X., Gu, J., Hunter, J., Ferrell, G. L., Lupu, F., Esmon, N. L., and Esmon, C. T. (2005) Overexpressing endothelial cell protein C receptor alters the hemostatic balance and protects mice from endotoxin. J. Thromb. Haemost. 3, 1351-1359
35. Centelles, M. N., Puy, C., Lopez-Sagaseta, J., Fukudome, K., Montes, R., and Hermida, J. (2010) Blocking endothelial protein C receptor (EPCR) accelerates thrombus development in vivo. Thromb. Haemost. 103, 1239-1244
36. Itoh, Y., Toriumi, H., Yamada, S., Hoshino, H., and Suzuki, N. (2010) Resident endothelial cells surrounding damaged arterial endothelium reendothelialize the lesion. Arterioscler. Thromb. Vasc. Biol. 30, 1725-1732
37. Newfell, B. G., Iyer, L. K., Mohammad, N. N., McGraw, A. P., Ehsan, A., Rosano, G., Huang, P. L., Mendelsohn, M. E., and Jaffe, I. Z. (2011) Aldosterone regulates vascular gene transcription via oxidative stress-dependent and -independent pathways. Arterioscler. Thromb. Vasc. Biol. 31, 1871-1880
38. Burger, D., and Touyz, R. M. (2012) Cellular biomarkers of endothelial health: microparticles, endothelial progenitor cells, and circulating endothelial cells. J. Am. Soc. Hypertens. 6, 85-99
39. Deanfield, J. E., Halcox, J. P., and Rabelink, T. J. (2007) Endothelial function and dysfunction: testing and clinical relevance. Circulation. 115, 1285-1295
40. Lidegaard, O., Lokkegaard, E., Jensen, A., Skovlund, C. W., and Keiding, N. (2012) Thrombotic stroke and myocardial infarction with hormonal contraception. N. Engl. J. Med. 366, 2257-2266
41. Lidegaard, O., Nielsen, L. H., Skovlund, C. W., Skjeldestad, F. E., and Lokkegaard, E. (2011) Risk of venous thromboembolism from use of oral contraceptives containing different progestogens and oestrogen doses: Danish cohort study, 2001-2009. BMJ 343, d6423
42. Wu, C., Grandi, S., Filion, K., Abenhaim, H., Joseph, L., and Eisenberg, M. (2013) Drospirenone-containing oral contraceptive pills and the risk of venous and arterial thrombosis: a systematic review. BJOG 120, 801-810
43. Kolkhof, P., and Borden, S. A. (2012) Molecular pharmacology of the mineralocorticoid receptor: prospects for novel therapeutics. Mol. Cell. Endocrinol. 350, 310-317