Diabetes impairs the vascular effects of aldosterone mediated by G protein-coupled estrogen receptor activation

Frontiers in Pharmacology

Volumn 6, Issue MAR, 2015, Pages

  Ferreira, Nathanne S ^a   Cau, Stêfany B A ^b   Silva, Marcondes A B ^a   Manzato, Carla P ^a   Mestriner, Fabíola L A C ^a   Matsumoto, Takayuki ^c   Carneiro, Fernando S ^a   Tostes, Rita C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c HOSHI UNIVERSITY   (Japan)

Author keywords

Aldosterone; Diabetes; G protein coupled estrogen receptor; Mesenteric arteries; Mineralocorticoid receptor

Indexed keywords

ACETYLCHOLINE; ALDOSTERONE; EPLERENONE; ESTROGEN RECEPTOR; G PROTEIN COUPLED ESTROGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHENYLEPHRINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME PHOSPHORYLATION; FEMALE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MESENTERIC ARTERY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASOCONSTRICTION; VASODILATATION; WESTERN BLOTTING;

EID: 84926434861     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2015.00034     Document Type: Article

References (50)

1. Adam, L. P., Franklin, M. T., Raff, G. J., and Hathaway, D. R. (1995). Activation of mitogen-activated protein kinase in porcine carotid arteries. Circ. Res. 76, 183-190. doi: 10.1161/01.RES.76.2.183.
2. Adel, H., Taye, A., and Khalifa, M. M. (2014). Spironolactone improves endothelial dysfunction in streptozotocin-induced diabetic rats. Naunyn Schmiedebergs Arch. Pharmacol. 387, 1187-1197. doi: 10.1007/s00210-014-1048-3.
3. Barrett-Connor, E., and Wingard, D. L. (1983). Sex differential in ischemic heart disease mortality in diabetics: a prospective population-based study. Am. J. Epidemiol. 118, 489-496.
4. Bender, S. B., McGraw, A. P., Jaffe, I. Z., and Sowers, J. R. (2013). Mineralocorticoid receptor-mediated vascular insulin resistance: an early contributor to diabetes-related vascular disease? Diabetes 62, 313-319. doi: 10.2337/db12-090562/2/313.
5. Briet, M., and Schiffrin, E. L. (2012). Vascular actions of aldosterone. J. Vasc. Res. 50, 89-99. doi: 10.1159/000345243.
6. Briones, A. M., Nguyen Dinh Cat, A., Callera, G. E., Yogi, A., Burger, D., He, Y., et al. (2012). Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus-associated obesity and vascular dysfunction. Hypertension 59, 1069-1078. doi: 10.1161/HYPERTENSIONAHA.111.190223.
7. Callera, G. E., Touyz, R. M., Tostes, R. C., Yogi, A., He, Y., Malkinson, S., et al. (2005). Aldosterone activates vascular p38MAP kinase and NADPH oxidase via c-Src. Hypertension 45, 773-779. doi: 10.1161/01.HYP.0000154365.30593.d3.
8. Callera, G. E., Yogi, A., Briones, A. M., Montezano, A. C., He, Y., Tostes, R. C., et al. (2011). Vascular proinflammatory responses by aldosterone are mediated via c-Src trafficking to cholesterol-rich microdomains: role of PDGFR. Cardiovasc. Res. 91, 720-731. doi: 10.1093/cvr/cvr131.
9. Caroccia, B., Seccia, T. M., Campos, A. G., Gioco, F., Kuppusamy, M., Ceolotto, G., et al. (2014). GPER-1 and estrogen receptor-beta ligands modulate aldosterone synthesis. Endocrinology 155, 4296-4304. doi: 10.1210/en.2014-1416.
10. Cheng, S. B., Dong, J., Pang, Y., LaRocca, J., Hixon, M., Thomas, P., et al. (2014). Anatomical location and redistribution of G protein-coupled estrogen receptor-1 during the estrus cycle in mouse kidney and specific binding to estrogens but not aldosterone. Mol. Cell. Endocrinol. 382, 950-959. doi: 10.1016/j.mce.2013.11.005.
11. Christ, M., Meyer, C., Sippel, K., and Wehling, M. (1995). Rapid aldosterone signaling in vascular smooth muscle cells: involvement of phospholipase, C., diacylglycerol and protein kinase C alpha. Biochem. Biophys. Res. Commun. 213, 123-129. doi: 10.1006/bbrc.1995.2106.
12. Christensen, K. L., and Mulvany, M. J. (2001). Location of resistance arteries. J. Vasc. Res. 38, 1-12. doi: 10.1159/000051024.
13. Davies, J., Gavin, A., Band, M., Morris, A., and Struthers, A. (2005). Spironolactone reduces brachial pulse wave velocity and PIIINP levels in hypertensive diabetic patients. Br. J. Clin. Pharmacol. 59, 520-523. doi: 10.1111/j.1365-2125.2005.02363.x.
14. Davies, J., and Struthers, A. (2002). The potential benefits of aldosterone antagonism in Type 2 diabetes mellitus. J. Renin Angiotensin Aldosterone Syst. 3, 150-155. doi: 10.3317/jraas.2002.034.
15. De Vriese, A. S., Verbeuren, T. J., Van de Voorde, J., Lameire, N. H., and Vanhoutte, P. M. (2000). Endothelial dysfunction in diabetes. Br. J. Pharmacol. 130, 963-974. doi: 10.1038/sj.bjp.0703393.
16. Feldman, R. D., and Gros, R. (2013). Vascular effects of aldosterone: sorting out the receptors and the ligands. Clin. Exp. Pharmacol. Physiol. 40, 916-921. doi: 10.1111/1440-1681.12157.
17. Garg, R., Rao, A. D., Baimas-George, M., Hurwitz, S., Foster, C., Shah, R. V., et al. (2014). Mineralocorticoid receptor blockade improves coronary microvascular function in individuals with Type 2 diabetes mellitus. Diabetes 64, 236-242. doi: 10.2337/db14-0670.
18. Garris, D. R. (1985). Diabetes-associated alterations in uterine structure in the C57BL/KsJ mouse: relationship to changes in estradiol accumulation, circulating ovarian steroid levels, and age. Anat. Rec. 211, 414-419. doi: 10.1002/ar.1092110407.
19. Garris, D. R., West, R. L., and Pekala, P. H. (1986). Ultrastructural and metabolic changes associated with reproductive tract atrophy and adiposity in diabetic female mice. Anat. Rec. 216, 359-366. doi: 10.1002/ar.1092160304.
20. Goel, A., Thor, D., Anderson, L., and Rahimian, R. (2008). Sexual dimorphism in rabbit aortic endothelial function under acute hyperglycemic conditions and gender-specific responses to acute 17beta-estradiol. Am. J. Physiol. Heart Circ. Physiol. 294, H2411-H2420. doi: 10.1152/ajpheart.01217.2007.
21. Goel, A., Zhang, Y., Anderson, L., and Rahimian, R. (2007). Gender difference in rat aorta vasodilation after acute exposure to high glucose: involvement of protein kinase C beta and superoxide but not of Rho kinase. Cardiovasc. Res. 76, 351-360. doi: S0008-6363(07)00309-4.
22. Gros, R., Ding, Q., Liu, B., Chorazyczewski, J., and Feldman, R. D. (2013). Aldosterone mediates its rapid effects in vascular endothelial cells through Gper/Gpr30 activation. Am. J. Physiol. Cell Physiol. 304, C532-C540. doi: 10.1152/ajpcell.00203.2012.
23. Gros, R., Ding, Q., Sklar, L. A., Prossnitz, E. E., Arterburn, J. B., Chorazyczewski, J., et al. (2011). GPR30 expression is required for the mineralocorticoid receptor-independent rapid vascular effects of aldosterone. Hypertension 57, 442-451. doi: 10.1161/HYPERTENSIONAHA.110.161653.
24. Guo, Z., Su, W., Allen, S., Pang, H., Daugherty, A., Smart, E., et al. (2005). COX-2 up-regulation and vascular smooth muscle contractile hyperreactivity in spontaneous diabetic db/db mice. Cardiovasc. Res. 67, 723-735. doi: 10.1016/j.cardiores.2005.04.008.
25. Haas, E., Meyer, M. R., Schurr, U., Bhattacharya, I., Minotti, R., Nguyen, H. H., et al. (2007). Differential effects of 17beta-estradiol on function and expression of estrogen receptor alpha, estrogen receptor beta, and GPR30 in arteries and veins of patients with atherosclerosis. Hypertension 49, 1358-1563. doi: 10.1161/HYPERTENSIONAHA.107.089995.
26. Hollenberg, N. K., Stevanovic, R., Agarwal, A., Lansang, M. C., Price, D. A., Laffel, L. M., et al. (2004). Plasma aldosterone concentration in the patient with diabetes mellitus. Kidney Int. 65, 1435-1439. doi: 10.1111/j.1523-1755.2004.00524.x.
27. International Diabetes Federation [IDF]. (2013). International Diabetes Federation-Diabetes Atlas, 6th Edn. Aalst: IDF Publications.
28. Ishizawa, K., Izawa, Y., Ito, H., Miki, C., Miyata, K., Fujita, Y., et al. (2005). Aldosterone stimulates vascular smooth muscle cell proliferation via big mitogen-activated protein kinase 1 activation. Hypertension 46, 1046-1052. doi: 10.1161/01.HYP.0000172622.51973.f5.
29. Jin, H. M., Zhou, D. C., Gu, H. F., Qiao, Q. Y., Fu, S. K., Liu, X. L., et al. (2013). Antioxidant N-acetylcysteine protects pancreatic beta-cells against aldosterone-induced oxidative stress and apoptosis in female db/db mice and insulin-producing MIN6 cells. Endocrinology 154, 4068-4077. doi: 10.1210/en.2013-1115.
30. Katoch, S. S., and Moreland, R. S. (1995). Agonist and membrane depolarization induced activation of MAP kinase in the swine carotid artery. Am. J. Physiol. 269(1 Pt 2), H222-H229.
31. Krug, A. W., Grossmann, C., Schuster, C., Freudinger, R., Mildenberger, S., Govindan, M. V., et al. (2003). Aldosterone stimulates epidermal growth factor receptor expression. J. Biol. Chem. 278, 43060-43066. doi: 10.1074/jbc.M308134200.
32. Legato, M. J., Gelzer, A., Goland, R., Ebner, S. A., Rajan, S., Villagra, V., et al. (2006). Gender-specific care of the patient with diabetes: review and recommendations. Gend. Med. 3, 131-158. doi: 10.1016/S1550-8579(06)80202-0.
33. Leopold, J. A. (2009). Rapid aldosterone signaling and vascular reactivity: relax or don't do it. J. Cardiovasc. Pharmacol. 54, 465-467. doi: 10.1097/FJC.0b013e3181c37ddc.
34. Li, Z. L., Liu, J. C., Liu, S. B., Li, X. Q., Yi, D. H., and Zhao, M. G. (2012). Improvement of vascular function by acute and chronic treatment with the GPR30 agonist G1 in experimental diabetes mellitus. PLoS ONE 7:e38787. doi: 10.1371/journal.pone.0038787.
35. Lindsey, S. H., Carver, K. A., Prossnitz, E. R., and Chappell, M. C. (2011). Vasodilation in response to the GPR30 agonist G-1 is not different from estradiol in the mRen2. Lewis female rat. J. Cardiovasc. Pharmacol. 57, 598-603. doi: 10.1097/FJC.0b013e3182135f1c.
36. Lindsey, S. H., da Silva, A. S., Silva, M. S., and Chappell, M. C. (2013). Reduced vasorelaxation to estradiol and G-1 in aged female and adult male rats is associated with GPR30 downregulation. Am. J. Physiol. Endocrinol. Metab. 305, E113-E118. doi: 10.1152/ajpendo.00649.2012.
37. Liu, S. L., Schmuck, S., Chorazcyzewski, J. Z., Gros, R., and Feldman, R. D. (2003). Aldosterone regulates vascular reactivity: short-term effects mediated by phosphatidylinositol 3-kinase-dependent nitric oxide synthase activation. Circulation 108, 2400-2406. doi: 10.1161/01.CIR.0000093188.53554.
38. McCollum, M., Hansen, L. S., Lu, L., and Sullivan, P. W. (2005). Gender differences in diabetes mellitus and effects on self-care activity. Gend. Med. 2, 246-254. doi: 10.1016/S1550-8579(05)80054-3.
39. McFarlane, S. I., and Sowers, J. R. (2003). Cardiovascular endocrinology 1: aldosterone function in diabetes mellitus: effects on cardiovascular and renal disease. J. Clin. Endocrinol. Metab. 88, 516-523. doi: 10.1210/jc.2002-021443.
40. Meyer, M. R., Baretella, O., Prossnitz, E. R., and Barton, M. (2010). Dilation of epicardial coronary arteries by the G protein-coupled estrogen receptor agonists G-1 and ICI 182, 780. Pharmacology 86, 58-64. doi: 10.1159/000315497.
41. Pannirselvam, M., Verma, S., Anderson, T. J., and Triggle, C. R. (2002). Cellular basis of endothelial dysfunction in small mesenteric arteries from spontaneously diabetic (db/db-/-) mice: role of decreased tetrahydrobiopterin bioavailability. Br. J. Pharmacol. 136, 255-263. doi: 10.1038/sj.bjp.0704683.
42. Prossnitz, E. R., and Barton, M. (2014). Estrogen biology: new insights into GPER function and clinical opportunities. Mol. Cell. Endocrinol. 389, 71-83. doi: 10.1016/j.mce.2014.02.002.
43. Schafer, A., Vogt, C., Fraccarollo, D., Widder, J., Flierl, U., Hildemann, S. K., et al. (2010). Eplerenone improves vascular function and reduces platelet activation in diabetic rats. J. Physiol. Pharmacol. 61, 45-52.
44. Schiffrin, E. L. (2006). Effects of aldosterone on the vasculature. Hypertension 47, 312-318. doi: 10.1161/01.HYP.0000201443.63240.a7.
45. Sowers, J. R. (1998). Diabetes mellitus and cardiovascular disease in women. Arch. Intern. Med. 158, 617-621. doi: 10.1001/archinte.158.6.617.
46. Swaminathan, K., Davies, J., George, J., Rajendra, N. S., Morris, A. D., and Struthers, A. D. (2008). Spironolactone for poorly controlled hypertension in type 2 diabetes: conflicting effects on blood pressure, endothelial function, glycaemic control and hormonal profiles. Diabetologia 51, 762-768. doi: 10.1007/s00125-008-0972-5.
47. Szymanski, P., Klisiewicz, A., Lubiszewska, B., Lipczynska, M., Kowalski, M., Janas, J., et al. (2011). Gender differences in angiotensin II and aldosterone secretion in patients with pressure overloaded systemic right ventricles are similar to those observed in systemic arterial hypertension. Int. J. Cardiol. 147, 366-370. doi: 10.1016/j.ijcard.2009.09.535.
48. Toledo, D. P., Akamine, E., Nigro, D., Passaglia, R. C., Carvalho, M. H., and Fortes, Z. B. (2003). Microvascular reactivity in experimental diabetes: responses of male and female rats. Inflamm. Res. 52, 191-198. doi: 10.1007/s000110300071.
49. Whaley-Connell, A., and Sowers, J. R. (2011). Aldosterone and risk for insulin resistance. Hypertension 58, 998-1000. doi: 10.1161/HYPERTENSIONAHA.111.182782.
50. Yu, X., Ma, H., Barman, S. A., Liu, A. T., Sellers, M., Stallone, J. N., et al. (2011). Activation of G protein-coupled estrogen receptor induces endothelium-independent relaxation of coronary artery smooth muscle. Am. J. Physiol. Endocrinol. Metab. 301, E882-E888. doi: 10.1152/ajpendo.00037.