Additive effects of low concentrations of estradiol-17β and progesterone on nitric oxide production by human vascular endothelial cells through shared signaling pathways

Journal of Steroid Biochemistry and Molecular Biology

Volumn 165, Issue , 2017, Pages 258-267

  Pang, Yefei ^a   Thomas, Peter ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Additive; Estradiol 17 ; HUVECs; Nitric oxide; Progesterone; Signaling pathways

Indexed keywords

1 (5 CHLORO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CYCLOOXYGENASE 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; MITOGEN ACTIVATED PROTEIN KINASE; PROGESTERONE RECEPTOR MODULATOR; PROSTACYCLIN SYNTHASE; SELUMETINIB; WORTMANNIN; CYTOCHROME P450; ESTRADIOL; ESTROGEN RECEPTOR ALPHA, HUMAN; G PROTEIN COUPLED RECEPTOR; GPER PROTEIN, HUMAN; MESSENGER RNA; NITRIC OXIDE; NOS3 PROTEIN, HUMAN; PROGESTERONE; PROGESTERONE RECEPTOR; PTGIS PROTEIN, HUMAN; PTGS1 PROTEIN, HUMAN;

ARTICLE; CARDIOVASCULAR EFFECT; ESTRADIOL BLOOD LEVEL; HORMONE SUBSTITUTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VIVO STUDY; POSTMENOPAUSE; PROGESTERONE BLOOD LEVEL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIAL CELL; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; ENDOTHELIUM CELL; METABOLISM; UMBILICAL CORD;

CELLS, CULTURED; CYCLOOXYGENASE 1; CYTOCHROME P-450 ENZYME SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; HORMONE REPLACEMENT THERAPY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PROGESTERONE; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PROGESTERONE; RNA, MESSENGER; SIGNAL TRANSDUCTION; UMBILICAL CORD;

EID: 84979643845     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2016.06.014     Document Type: Article

References (54)

1. [1] Mendelsohn, M.E., Karas, R.H., Molecular and cellular basis of cardiovascular gender differences. Science 308 (2005), 1583–1587.
2. [2] Wenner, M.M., Stachenfeld, N.S., Blood pressure and water regulation: understanding sex hormone effects within and between men and women. J. Physiol. 590 (2012), 5949–5961.
3. [3] Wilson, M., Morganti, A.A., Zervoudakis, I., Letcher, R.L., Romney, B.M., Von Oeyon, P., Papera, S., Sealey, J.E., Laragh, J.H., Blood pressure, the renin-aldosterone system and sex steroids throughout normal pregnancy. Am. J. Med. 68 (1980), 97–104.
4. [4] Stevenson, J.C., Crook, D., Godsland, I.F., Collins, P., Whitehead, M.I., Hormone replacement therapy and the cardiovascular system. Nonlipid effects Drugs 47:Suppl. 2 (1994), 35–41.
5. [5] Orshal, J.M., Khalil, R.A., Gender, sex hormones, and vascular tone. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 (2004), R233–249.
6. [6] Reckelhoff, J.F., Sex steroids, cardiovascular disease, and hypertension: unanswered questions and some speculations. Hypertension 45 (2005), 170–174.
7. [7] Guetta, V., Cannon, R.O. 3rd, Cardiovascular effects of estrogen and lipid-lowering therapies in postmenopausal women. Circulation 93 (1996), 1928–1937.
8. [8] Levenson, J.W., Skerrett, P.J., Gaziano, J.M., Reducing the global burden of cardiovascular disease: the role of risk factors. Prev. Cardiol. 5 (2002), 188–199.
9. [9] Tsai, S.A., Stefanick, M.L., Stafford, R.S., Trends in menopausal hormone therapy use of US office-based physicians, 2000–2009. Menopause 18 (2011), 385–392.
10. [10] Felmeden, D.C., Lip, G.Y., Hormone replacement therapy and hypertension. Blood Press. 9 (2000), 246–249.
11. [11] Ettinger, B., Rationale for use of lower estrogen doses for postmenopausal hormone therapy. Maturitas 57 (2007), 81–84.
12. [12] Jazbutyte, V., Arias-Loza, P.A., Hu, K., Widder, J., Govindaraj, V., von Poser-Klein, C., Bauersachs, J., Fritzemeier, K.H., Hegele-Hartung, C., Neyses, L., Ertl, G., Pelzer, T., Ligand-dependent activation of ER{beta} lowers blood pressure and attenuates cardiac hypertrophy in ovariectomized spontaneously hypertensive rats. Cardiovasc. Res. 77 (2008), 774–781.
13. [13] Roesch, D.M., Keller-Wood, M., Progesterone rapidly reduces arterial pressure in ewes. Am. J. Physiol. 272 (1997), H386–391.
14. [14] Brandin, L.M., Gustafsson, H., Ghanoum, B., Milsom, I., Manhem, K., Effects of estrogen plus progesterone on hemodynamic and vascular reactivity in hypertensive postmenopausal women. Blood Press. 19 (2010), 156–163.
15. [15] Pang, Y., Dong, J., Thomas, P., Progesterone increases nitric oxide synthesis in human vascular endothelial cells through activation of membrane progesterone receptor-alpha. Am. J. Physiol. Endocrinol. Metab. 308 (2015), E899–911.
16. [16] Grady, D., Herrington, D., Bittner, V., Blumenthal, R., Davidson, M., Hlatky, M., Hsia, J., Hulley, S., Herd, A., Khan, S., Newby, L.K., Waters, D., Vittinghoff, E., Wenger, N., Cardiovascular disease outcomes during 6.8 years of hormone therapy: heart and estrogen/progestin replacement study follow-up (HERS II). JAMA 288 (2002), 49–57.
17. [17] Rossouw, J.E., Anderson, G.L., Prentice, R.L., LaCroix, A.Z., Kooperberg, C., Stefanick, M.L., Jackson, R.D., Beresford, S.A., Howard, B.V., Johnson, K.C., Kotchen, J.M., Ockene, J., Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 288 (2002), 321–333.
18. [18] Hermsmeyer, R.K., Thompson, T.L., Pohost, G.M., Kaski, J.C., Cardiovascular effects of medroxyprogesterone acetate and progesterone: a case of mistaken identity?. Nat. Clin. Pract. Cardiovasc. Med. 5 (2008), 387–395.
19. [19] Simoncini, T., Mannella, P., Fornari, L., Caruso, A., Willis, M.Y., Garibaldi, S., Baldacci, C., Genazzani, A.R., Differential signal transduction of progesterone and medroxyprogesterone acetate in human endothelial cells. Endocrinology 145 (2004), 5745–5756.
20. [20] Thomas, P., Pang, Y., Protective actions of progesterone in the cardiovascular system: potential role of membrane progesterone receptors (mPRs) in mediating rapid effects. Steroids, 2013.
21. [21] Cutini, P.H., Campelo, A.E., Massheimer, V.L., Differential regulation of endothelium behavior by progesterone and medroxyprogesterone acetate. J. Endocrinol. 220 (2014), 179–193.
22. [22] Olie, V., Canonico, M., Scarabin, P.Y., Postmenopausal hormone therapy and venous thromboembolism. Thromb. Res. 127:Suppl. 3 (2011), S26–S29.
23. [23] L'Hermite, M., HRT optimization using transdermal estradiol plus micronized progesterone, a safer HRT. Climacteric 16:Suppl. 1 (2013), 44–53.
24. [24] Simon, J.A., What if the Women's Health Initiative had used transdermal estradiol and oral progesterone instead?. Menopause 21 (2014), 769–783.
25. [25] Giles, T.D., Sander, G.E., Nossaman, B.D., Kadowitz, P.J., Impaired vasodilation in the pathogenesis of hypertension: focus on nitric oxide, endothelial-derived hyperpolarizing factors, and prostaglandins. J. Clin. Hypertens. (Greenwich) 14 (2012), 198–205.
26. [26] Duckles, S.P., Miller, V.M., Hormonal modulation of endothelial NO production. Pflugers Arch. 459 (2010), 841–851.
27. [27] Chen, Z., Yuhanna, I.S., Galcheva-Gargova, Z., Karas, R.H., Mendelsohn, M.E., Shaul, P.W., Estrogen receptor alpha mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J. Clin. Invest. 103 (1999), 401–406.
28. [28] Haynes, M.P., Sinha, D., Russell, K.S., Collinge, M., Fulton, D., Morales-Ruiz, M., Sessa, W.C., Bender, J.R., Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ. Res. 87 (2000), 677–682.
29. [29] Hisamoto, K., Ohmichi, M., Kurachi, H., Hayakawa, J., Kanda, Y., Nishio, Y., Adachi, K., Tasaka, K., Miyoshi, E., Fujiwara, N., Taniguchi, N., Murata, Y., Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J. Biol. Chem. 276 (2001), 3459–3467.
30. [30] Florian, M., Lu, Y., Angle, M., Magder, S., Estrogen induced changes in Akt-dependent activation of endothelial nitric oxide synthase and vasodilation. Steroids 69 (2004), 637–645.
31. [31] Chambliss, K.L., Yuhanna, I.S., Mineo, C., Liu, P., German, Z., Sherman, T.S., Mendelsohn, M.E., Anderson, R.G., Shaul, P.W., Estrogen receptor alpha and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circ. Res. 87 (2000), E44–52.
32. [32] Lindsey, S.H., Carver, K.A., Prossnitz, E.R., Chappell, M.C., Vasodilation in response to the GPR30 agonist G-1 is not different from estradiol in the mRen2. Lewis female rat. J. Cardiovasc. Pharmacol. 57 (2011), 598–603.
33. [33] Arefin, S., Simoncini, T., Wieland, R., Hammarqvist, F., Spina, S., Goglia, L., Kublickiene, K., Vasodilatory effects of the selective GPER agonist G-1 is maximal in arteries of postmenopausal women. Maturitas 78 (2014), 123–130.
34. [34] Meyer, M.R., Fredette, N.C., Howard, T.A., Hu, C., Ramesh, C., Daniel, C., Amann, K., Arterburn, J.B., Barton, M., Prossnitz, E.R., G protein-coupled estrogen receptor protects from atherosclerosis. Sci. Rep., 4, 2014, 7564.
35. [35] Akishita, M., Kozaki, K., Eto, M., Yoshizumi, M., Ishikawa, M., Toba, K., Orimo, H., Ouchi, Y., Estrogen attenuates endothelin-1 production by bovine endothelial cells via estrogen receptor. Biochem. Biophys. Res. Commun. 251 (1998), 17–21.
36. [36] Jun, S.S., Chen, Z., Pace, M.C., Shaul, P.W., Estrogen upregulates cyclooxygenase-1 gene expression in ovine fetal pulmonary artery endothelium. J. Clin. Invest. 102 (1998), 176–183.
37. [37] Vanhoutte, P.M., COX-1 and vascular disease. Clin. Pharmacol. Ther. 86 (2009), 212–215.
38. [38] Thomas, P., Pang, Y., Dong, J., Groenen, P., Kelder, J., de Vlieg, J., Zhu, Y., Tubbs, C., Steroid and G protein binding characteristics of the seatrout and human progestin membrane receptor alpha subtypes and their evolutionary origins. Endocrinology 148 (2007), 705–718.
39. [39] Henmi, N., Takahashi, K., Amita, M., Takata, K., Ohta, T., Tsutsumi, S., Takahashi, T., Kurachi, H., Effect of dienogest on estrogen-induced nitric oxide production in human umbilical vein endothelial cells and endothelium-dependent vasodilatation in postmenopausal women. Menopause 17 (2010), 615–621.
40. [40] Oishi, A., Ohmichi, M., Takahashi, K., Takahashi, T., Mori-Abe, A., Kawagoe, J., Otsu, R., Mochizuki, Y., Inaba, N., Kurachi, H., Medroxyprogesterone acetate attenuates estrogen-induced nitric oxide production in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 324 (2004), 193–198.
41. [41] Klinge, C.M., Wickramasinghe, N.S., Ivanova, M.M., Dougherty, S.M., Resveratrol stimulates nitric oxide production by increasing estrogen receptor alpha-Src-caveolin-1 interaction and phosphorylation in human umbilical vein endothelial cells. FASEB J. 22 (2008), 2185–2197.
42. [42] Simoncini, T., Fornari, L., Mannella, P., Varone, G., Caruso, A., Garibaldi, S., Genazzani, A.R., Differential estrogen signaling in endothelial cells upon pulsed or continuous administration. Maturitas 50 (2005), 247–258.
43. [43] Chambliss, K.L., Shaul, P.W., Rapid activation of endothelial NO synthase by estrogen: evidence for a steroid receptor fast-action complex (SRFC) in caveolae. Steroids 67 (2002), 413–419.
44. [44] Darblade, B., Pendaries, C., Krust, A., Dupont, S., Fouque, M.J., Rami, J., Chambon, P., Bayard, F., Arnal, J.F., Estradiol alters nitric oxide production in the mouse aorta through the alpha- but not beta-, estrogen receptor. Circ. Res. 90 (2002), 413–419.
45. [45] Chakrabarti, S., Morton, J.S., Davidge, S.T., Mechanisms of estrogen effects on the endothelium: an overview. Can. J. Cardiol. 30 (2014), 705–712.
46. [46] Lindsey, S.H., Liu, L., Chappell, M.C., Vasodilation by GPER in mesenteric arteries involves both endothelial nitric oxide and smooth muscle cAMP signaling. Steroids 81 (2014), 99–102.
47. [47] Gros, R., Ding, Q., Liu, B., Chorazyczewski, J., Feldman, R.D., Aldosterone mediates its rapid effects in vascular endothelial cells through GPER activation. Am. J. Physiol. Cell Physiol. 304 (2013), C532–540.
48. [48] Cheng, S.B., Dong, J., Pang, Y., LaRocca, J., Hixon, M., Thomas, P., Filardo, E.J., 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 (2014), 950–959.
49. [49] Wei, Y., Zhang, Z., Liao, H., Wu, L., Wu, X., Zhou, D., Xi, X., Zhu, Y., Feng, Y., Nuclear estrogen receptor-mediated Notch signaling and GPR30-mediated PI3K/AKT signaling in the regulation of endometrial cancer cell proliferation. Oncol. Rep. 27 (2012), 504–510.
50. [50] Filardo, E.J., Quinn, J.A., Frackelton, A.R. Jr., Bland, K.I., Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16 (2002), 70–84.
51. [51] Wong, S.L., Wong, W.T., Tian, X.Y., Lau, C.W., Huang, Y., Prostaglandins in action indispensable roles of cyclooxygenase-1 and −2 in endothelium-dependent contractions. Adv. Pharmacol. 60 (2010), 61–83.
52. [52] Hermenegildo, C., Oviedo, P.J., Garcia-Martinez, M.C., Garcia-Perez, M.A., Tarin, J.J., Cano, A., Progestogens stimulate prostacyclin production by human endothelial cells. Hum. Reprod. 20 (2005), 1554–1561.
53. [53] Oviedo, P.J., Sobrino, A., Novella, S., Rius, C., Laguna-Fernandez, A., Garcia-Perez, M.A., Tarin, J.J., Cano, A., Hermenegildo, C., Progestogens reduce thromboxane production by cultured human endothelial cells. Climacteric 14 (2011), 41–48.
54. [54] Pedersen, S.H., Nielsen, L.B., Pedersen, N.G., Nilas, L., Ottesen, B., Hormone therapy modulates ET(A) mRNA expression in the aorta of ovariectomised New Zealand White rabbits. Gynecol. Endocrinol. 25 (2009), 175–182.