Differential regulation of endothelium behavior by progesterone and medroxyprogesterone acetate

Journal of Endocrinology

Volumn 220, Issue 3, 2014, Pages 179-193

  Cutini, Pablo H ^a,b   Campelo, Adrián E ^a,b   Massheimer, Virginia L ^a,b  

^a UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Cell migration; Medroxyprogesterone acetate; Nitric oxide; Progesterone; Vascular tissue

Indexed keywords

CELL MIGRATION; MEDROXYPROGESTERONE ACETATE; NITRIC OXIDE; PROGESTERONE; VASCULAR TISSUE;

ANIMALS; CELL MOVEMENT; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; MEDROXYPROGESTERONE ACETATE; NITRIC OXIDE; PROGESTERONE; RATS; RATS, WISTAR;

EID: 84894334240     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0263     Document Type: Article

References (58)

1. van Baal WM, Kenemans P, Emeis JJ, Schalkwijk CG, Mijatovic V, van der Mooren MJ, Vischer UM & Stehouwer CD 1999 Long-term effects of combined hormone replacement therapy on markers of endothelial function and inflammatory activity in healthy postmenopausal women. Fertility and Sterility 71 663-670. (doi:10.1016/S0015- 0282(98)00513-5)
2. Campelo AE, Cutini PH & Massheimer VL 2012 Cellular actions of testosterone in vascular cells: mechanism independent of aromatization to estradiol. Steroids 77 1033-1040. (doi:10.1016/j.steroids.2012. 05.008)
3. Cartwright JE, Johnstone AP & Whitley GS 2000 Endogenously produced nitric oxide inhibits endothelial cell growth as demonstrated using novel antisense cell lines. British Journal of Pharmacology 131 131-137. (doi:10.1038/sj.bjp.0703539)
4. Chataigneau T, Zerr M, Chataigneau M, Hudlett F, Hirn C, Pernot F, Schini-Kerth VB 2004 Chronic treatment with progesterone but not medroxyprogesterone acetate restores the endothelial control of vascular tone in the mesenteric artery of ovariectomized rats. Menopause 11 255-263. (doi:10.1097/01.GME.0000097847.95550.E3)
5. Chen L, Salafranca MN & Mehta JL 1997 Cyclooxygenase inhibition decreases nitric oxide synthase activity in human platelets. American Journal of Physiology 273 H1854-H1859.
6. Chiu WC, Chiou TJ & Chiang AN 2012 b2-Glycoprotein I inhibits endothelial cell migration through the nuclear factor kB signalling pathway and endothelial nitric oxide synthase activation. Biochemical Journal 445 125-133. (doi:10.1042/BJ20111383)
7. Choy JC, Granville DJ, Hunt DW & McManus BM 2001 Endothelial cell apoptosis: biochemical characteristics and potential implications for atherosclerosis. Journal of Molecular and Cellular Cardiology 33 1673-1690. (doi:10.1006/jmcc.2001.1419)
8. Cutini PH & Massheimer VL 2010 Role of progesterone on the regulation of vascular muscle cells proliferation, migration and apoptosis. Steroids 75 355-361. (doi:10.1016/j.steroids.2010.01.017)
9. Cutini P, Selles J & Massheimer V 2009 Cross-talk between rapid and long term effects of progesterone on vascular tissue. Journal of Steroid Biochemistry and Molecular Biology 115 36-43. (doi:10.1016/j.jsbmb. 2009.02.014)
10. Cutini PH, Campelo AE, Agriello E, Sandoval MJ, Rauschemberger MB & Massheimer VL 2012 The role of sex steroids on cellular events involved in vascular disease. Journal of Steroid Biochemistry and Molecular Biology 132 322-330. (doi:10.1016/j.jsbmb.2012.08.001)
11. Duckles SP & Miller VM 2010 Hormonal modulation of endothelial NO production. Pflügers Archiv: European Journal of Physiology 459 841-851. (doi:10.1007/s00424-010-0797-1)
12. Forstermann U 2010 Nitric oxide and oxidative stress in vascular disease. Pflügers Archiv: European Journal of Physiology 459 923-939. (doi:10.1007/s00424-010-0808-2)
13. Fu XD, Flamini M, Sanchez AM, Goglia L, Giretti MS, Genazzani AR, Simoncini T 2008a Progestogens regulate endothelial actin cytoskeleton and cell movement via the actin-binding protein moesin. Molecular Human Reproduction 14 225-234. (doi:10.1093/molehr/gan010)
14. Fu XD, Giretti MS, Baldacci C, Garibaldi S, Flamini M, Sanchez AM, Gadducci A, Genazzani AR & Simoncini T 2008b Extra-nuclear signaling of progesterone receptor to breast cancer cell movement and invasion through the actin cytoskeleton. PLoS ONE 3 e2790. (doi:10.1371/journal.pone.0002790)
15. Gaillard T, Mulsch A, Klein H & Decker K 1992 Regulation by prostaglandin E2 of cytokine-elicited nitric oxide synthesis in rat liver macrophages. Biological Chemistry Hoppe-Seyler 373 897-902. (doi:10.1515/bchm3. 1992.373.2.897)
16. Garonna E, Botham KM, Birdsey GM, Randi AM, Gonzalez-Perez RR & Wheeler-Jones CP 2011 Vascular endothelial growth factor receptor-2 couples cyclo-oxygenase-2 with pro-angiogenic actions of leptin on human endothelial cells. PLoS ONE 6 e18823. (doi:10.1371/journal. pone.0018823)
17. Glusa E, Graser T, Wagner S & Oettel M 1997 Mechanisms of relaxation of rat aorta in response to progesterone and synthetic progestins. Maturitas 28 181-191. (doi:10.1016/S0378-5122(97)00057-1)
18. Grady D, Herrington D, Bittner V, Blumenthal R, Davidson M, Hlatky M, Hsia J, Hulley S, Herd A, Khan S et al. 2002 Cardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/ progestin Replacement Study follow-up (HERS II). Journal of the American Medical Association 288 49-57. (doi:10.1001/jama.288.1.49)
19. Harrison DG, Widder J, Grumbach I, Chen W, Weber M, Searles C 2006 Endothelial mechanotransduction, nitric oxide and vascular inflammation. Journal of Internal Medicine 259 351-363. (doi:10.1111/ j.1365-2796.2006.01621.x)
20. Hermenegildo C, Oviedo PJ, Garcia-Martinez MC, Garcia-Perez MA, Tarin JJ & Cano A 2005 Progestogens stimulate prostacyclin production by human endothelial cells. Human Reproduction 20 1554-1561. (doi:10.1093/humrep/deh803)
21. Hsieh HL, Lin CC, Chan HJ, Yang CM & Yang CM 2012 c-Src-dependent EGF receptor transactivation contributes to ET-1-induced COX-2 expression in brain microvascular endothelial cells. Journal of Neuroinflammation 9 152. (doi:10.1186/1742-2094-9-152)
22. Hulley S, Grady D, Bush T, Furberg C, Herrington D, Riggs B & Vittinghoff E 1998 Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. Journal of the American Medical Association 280 605-613. (doi:10.1001/jama.280.7.605)
23. Ignarro LJ 1989 Biological actions and properties of endothelium-derived nitric oxide formed and released from artery and vein. Circulation Research 65 1-21. (doi:10.1161/01.RES.65.1.1)
24. Jiang CW, Sarrel PM, Lindsay DC, Poole-Wilson PA, Collins P 1992 Progesterone induces endothelium-independent relaxation of rabbit coronary artery in vitro. European Journal of Pharmacology 211 163-167. (doi:10.1016/0014-2999(92)90524-8)
25. Joswig M, Hach-Wunderle V, Ziegler R & Nawroth PP 1999 Postmenopausal hormone replacement therapy and the vascular wall: mechanisms of 17b-estradiol's effects on vascular biology. Experimental and Clinical Endocrinology & Diabetes 107 477-487. (doi:10.1055/s-0029-1232556)
26. Kikuta K, Sawamura T,Miwa S, Hashimoto N &Masaki T 1998 High-affinity arginine transport of bovine aortic endothelial cells is impaired by lysophosphatidylcholine. Circulation Research 83 1088-1096. (doi:10.1161/01.RES.83.11.1088)
27. Kim SF 2011 The role of nitric oxide in prostaglandin biology; update. Nitric Oxide 25 255-264. (doi:10.1016/j.niox.2011.07.002)
28. Ladurner A, Schmitt CA, Schachner D, Atanasov AG, Werner ER, Dirsch VM, Heiss EH 2012 Ascorbate stimulates endothelial nitric oxide synthase enzyme activity by rapid modulation of its phosphorylation status. Free Radical Biology &Medicine 52 2082-2090. (doi:10.1016/j.freeradbiomed. 2012.03.022)
29. L'hermite M, Simoncini T, Fuller S & Genazzani AR 2008 Could transdermal estradiol C progesterone be a safer postmenopausal HRT?. A review Maturitas 60 185-201. (doi:10.1016/j.maturitas.2008.07.007)
30. Lowry OH, Rosebrough NJ, Farr AL & Randall RJ 1951 Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193 265-275.
31. Manson JE,Hsia J, Johnson KC, RossouwJE, Assaf AR, Lasser NL, TrevisanM, Black HR, Heckbert SR, Detrano R et al. 2003 Estrogen plus progestin and the risk of coronary heart disease. New England Journal of Medicine 349 523-534. (doi:10.1056/NEJMoa030808)
32. Mendiberri J, Rauschemberger MB, Selles J, Massheimer V 2006 Involvement of phosphoinositide-3-kinase and phospholipase C transduction systems in the non-genomic action of progesterone in vascular tissue. International Journal of Biochemistry & Cell Biology 38 288-296. (doi:10.1016/j.biocel.2005.09.012)
33. Moreno PR, Sanz J & Fuster V 2009 Promoting mechanisms of vascular health: circulating progenitor cells, angiogenesis, and reverse cholesterol transport. Journal of the American College of Cardiology 53 2315-2323. (doi:10.1016/j.jacc.2009.02.057)
34. Nilsen J & Brinton RD 2003 Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. PNAS 100 10506-10511. (doi:10.1073/ pnas.1334098100)
35. Oishi A, Takahashi K, Ohmichi M, Mochizuki Y, Inaba N & Kurachi H 2011 Role of glucocorticoid receptor in the inhibitory effect of medroxyprogesterone acetate on the estrogen-induced endothelial nitric oxide synthase phosphorylation in human umbilical vein endothelial cells. Fertility and Sterility 95 1168-1170. (doi:10.1016/j.fertnstert. 2010.09.041)
36. Okada H, Okamoto R, Tsuzuki T, Tsuji S, Yasuda K & Kanzaki H 2011 Progestins inhibit estradiol-induced vascular endothelial growth factor and stromal cell-derived factor 1 in human endometrial stromal cells. Fertility and Sterility 96 786-791. (doi:10.1016/j.fertnstert.2011.06.048)
37. Otsuki M, Saito H, Xu X, Sumitani S, Kouhara H, Kishimoto T & Kasayama S 2001 Progesterone, but not medroxyprogesterone, inhibits vascular cell adhesion molecule-1 expression in human vascular endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 21 243-248. (doi:10.1161/01.ATV.21.2.243)
38. OviedoPJ, SobrinoA,Novella S,RiusC,Laguna-FernandezA,Garcia-PerezMA, Tarin JJ, Cano A & Hermenegildo C 2011 Progestogens reduce thromboxaneproductionbyculturedhumanendothelial cells. Climacteric 14 41-48. (doi:10.3109/13697131003602496)
39. Pedram A, Razandi M, Aitkenhead M, Hughes CC & Levin ER 2002 Integration of the non-genomic and genomic actions of estrogen. Membrane-initiated signaling by steroid to transcription and cell biology. Journal of Biological Chemistry 277 50768-50775. (doi:10.1074/ jbc.M210106200)
40. Perrot-Applanat M, Groyer-Picard MT, Garcia E, Lorenzo F & Milgrom E 1988 Immunocytochemical demonstration of estrogen and progesterone receptors in muscle cells of uterine arteries in rabbits and humans. Endocrinology 123 1511-1519. (doi:10.1210/endo-123-3-1511)
41. Ross R 1999 Atherosclerosis - an inflammatory disease. New England Journal of Medicine 340 115-126. (doi:10.1056/NEJM1999011 43400207)
42. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC et al. 2002 Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. Journal of the American Medical Association 288 321-333. (doi:10.1001/jama.288.3.321)
43. Saitoh M, Ohmichi M, Takahashi K, Kawagoe J, Ohta T, Doshida M, Takahashi T, Igarashi H, Mori-Abe A, Du B et al. 2005 Medroxyprogesterone acetate induces cell proliferation through up-regulation of cyclin D1 expression via phosphatidylinositol 3-kinase/Akt/nuclear factor-kB cascade in human breast cancer cells. Endocrinology 146 4917-4925. (doi:10.1210/en.2004-1535)
44. Salvemini D 1997 Regulation of cyclooxygenase enzymes by nitric oxide. Cellular and Molecular Life Sciences 53 576-582. (doi:10.1007/ s000180050074)
45. Schwalm S, Pfeilschifter J, Huwiler A 2010 Sphingosine kinase 1 is critically involved in nitric oxide-mediated human endothelial cell migration and tube formation. British Journal of Pharmacology 160 1641-1651. (doi:10.1111/j.1476-5381.2010.00818.x)
46. Selles J, Polini N, Alvarez C & Massheimer V 2002 Nongenomic action of progesterone in rat aorta: role of nitric oxide and prostaglandins. Cellular Signalling 14 431-436. (doi:10.1016/S0898-6568(01)00265-0)
47. Selles J, Polini N, Alvarez C & Massheimer V 2005 Novel action of estrone on vascular tissue: regulation of NOS and COX activity. Steroids 70 251-256. (doi:10.1016/j.steroids.2004.10.012)
48. Simoncini T, Mannella P, Fornari L, Caruso A, Varone G & Genazzani AR 2003 In vitro effects of progesterone and progestins on vascular cells. Steroids 68 831-836. (doi:10.1016/j.steroids.2003.08.006)
49. Simoncini T, Mannella P, Fornari L, Caruso A, Willis MY, Garibaldi S, Baldacci C & Genazzani AR 2004 Differential signal transduction of progesterone and medroxyprogesterone acetate in human endothelial cells. Endocrinology 145 5745-5756. (doi:10.1210/en.2004-0510)
50. Simoncini T, Caruso A, Garibaldi S, Fu XD, Giretti MS, Baldacci C, Scorticati C, Fornari L, Mannella P & Genazzani AR 2006 Activation of nitric oxide synthesis in human endothelial cells using nomegestrol acetate. Obstetrics & Gynecology 108 969-978. (doi:10.1097/01.AOG.0000233184.64531.84)
51. Sitruk-Ware R 2000 Progestins and cardiovascular risk markers. Steroids 65 651-658. (doi:10.1016/S0039-128X(00)00174-4)
52. Tegenge MA, Rockel TD, Fritsche E, Bicker G 2011 Nitric oxide stimulates human neural progenitor cell migration via cGMP-mediated signal transduction. Cellular and Molecular Life Sciences 68 2089-2099. (doi:10.1007/s00018-010-0554-9)
53. Thomas T, Rhodin J, Clark L & Garces A 2003 Progestins initiate adverse events of menopausal estrogen therapy. Climacteric 6 293-301. (doi:10.1082/cmt.6.4.293.301)
54. Tsao PS, Lewis NP, Alpert S & Cooke JP 1995 Exposure to shear stress alters endothelial adhesiveness. Role of nitric oxide. Circulation 92 3513-3519. (doi:10.1161/01.CIR.92.12.3513)
55. Vazquez F, Rodriguez-Manzaneque JC, Lydon JP, Edwards DP, O'Malley BW & Iruela-Arispe ML 1999 Progesterone regulates proliferation of endothelial cells. Journal of Biological Chemistry 274 2185-2192. (doi:10.1074/jbc.274.4.2185)
56. Yeh YC, Hwang GY, Liu IP & Yang VC 2002 Identification and expression of scavenger receptor SR-BI in endothelial cells and smooth muscle cells of rat aorta in vitro and in vivo. Atherosclerosis 161 95-103. (doi:10.1016/ S0021-9150(01)00642-6)
57. Zheng S, Huang J, Zhou K, Xiang Q, Zhang Y, Tan Z, Simoncini T, Fu X & Wang T 2012 Progesterone enhances vascular endothelial cell migration via activation of focal adhesion kinase. Journal of Cellular and Molecular Medicine 16 296-305. (doi:10.1111/j.1582-4934.2011. 01305.x)
58. Zhu Y, Rice CD, Pang Y, Pace M & Thomas P 2003 Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. PNAS 100 2231-2236. (doi:10.1073/pnas.0336132100)