Estrogen receptor beta dependent attenuation of cytokine-induced cyclooxygenase-2 by androgens in human brain vascular smooth muscle cells and rat mesenteric arteries

Steroids

Volumn 77, Issue 8-9, 2012, Pages 835-844

  Zuloaga, Kristen L ^a   O'Connor, Devin T ^a   Handa, Robert J ^a   Gonzales, Rayna J ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Androgen; Cyclooxygenase 2; Interleukin 1 beta; Vascular smooth muscle; Vasculature

Indexed keywords

ANDROSTANOLONE; CYCLOOXYGENASE 2; ESTROGEN RECEPTOR BETA; INTERLEUKIN 1BETA;

ADULT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ATTENUATION; CONTROLLED STUDY; ENZYME METABOLISM; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MALE; MESENTERIC ARTERY; NONHUMAN; PROTEIN EXPRESSION; RAT; SMOOTH MUSCLE FIBER;

ANDROGENS; ANIMALS; BLOTTING, WESTERN; BRAIN; CELLS, CULTURED; CYCLOOXYGENASE 2; CYTOKINES; ESTROGEN RECEPTOR BETA; HUMANS; MALE; MESENTERIC ARTERIES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANDROGEN;

RATTUS;

EID: 84861596021     PISSN: 0039128X     EISSN: 18785867     Source Type: Journal    
DOI: 10.1016/j.steroids.2012.04.013     Document Type: Article

References (66)

1. G.J. del Zoppo, and T. Mabuchi Cerebral microvessel responses to focal ischemia J Cereb Blood Flow Metab 23 2003 879 894 (Pubitemid 36959394)
2. H.C.A. Emsley, and P.J. Tyrrell Inflammation and infection in clinical stroke J Cereb Blood Flow Metab 22 2002 1399 1419 (Pubitemid 35424925)
3. A. Brooks, N. Menzies-Gow, S. Bailey, F. Cunningham, and J. Elliott Endotoxin-induced HIF-1α stabilisation in equine endothelial cells: synergistic action with hypoxia Inflammat Res 9 2010 689 698
4. Q. Wang, X.N. Tang, and M.A. Yenari The inflammatory response in stroke J Neuroimmunol 184 2007 53 68 (Pubitemid 46365991)
5. K.L. Osterlund, R.J. Handa, and R.J. Gonzales Dihydrotestosterone alters cyclooxygenase-2 levels in human coronary artery smooth muscle cells Am J Physiol Endocrinol Metab 298 2010 E838 E845
6. K.L. Zuloaga, and R.J. Gonzales Dihydrotestosterone attenuates hypoxia inducible factor-1alpha and cyclooxygenase-2 in cerebral arteries during hypoxia or hypoxia with glucose deprivation Am J Physiol Heart Circ Physiol 301 2011 H1882 H1890
7. G.D. Norata, G. Tibolla, P.M. Seccomandi, A. Poletti, and A.L. Catapano Dihydrotestosterone decreases tumor necrosis factor-alpha and lipopolysaccharide-induced inflammatory response in human endothelial cells J Clin Endocrinol Metab 91 2006 546 554 (Pubitemid 43236925)
8. C.J. Malkin, P.J. Pugh, R.D. Jones, T.H. Jones, and K.S. Channer Testosterone as a protective factor against atherosclerosis-immunomodulation and influence upon plaque development and stability J Endocrinol 178 2003 373 380 (Pubitemid 37220164)
9. D. Xing, W. Feng, A.P. Miller, N.M. Weathington, Y.-F. Chen, and L. Novak Estrogen modulates TNF-{alpha}-induced inflammatory responses in rat aortic smooth muscle cells through estrogen receptor-beta activation Am J Physiol Heart Circ Physiol 292 2007 H2607 H2612
10. A.K. Death, K.C.Y. McGrath, M.A. Sader, S. Nakhla, W. Jessup, and D.J. Handelsman Dihydrotestosterone promotes vascular cell adhesion molecule-1 expression in male human endothelial cells via a nuclear factor-{kappa}B- dependent pathway Endocrinology 145 2004 1889 1897 (Pubitemid 38402398)
11. J.A. McCrohon, W. Jessup, D.J. Handelsman, and D.S. Celermajer Androgen exposure increases human monocyte adhesion to vascular endothelium and endothelial cell expression of vascular cell adhesion molecule-1 Circulation 99 1999 2317 2322 (Pubitemid 29201140)
12. E.D. Lephart, T.D. Lund, and T.L. Horvath Brain androgen and progesterone metabolizing enzymes: biosynthesis, distribution and function Brain Res Brain Res Rev 37 2001 25 37 (Pubitemid 34020719)
13. R.J. Handa, H.L. Stadelman, and J.A. Resko Effect of estrogen on androgen receptor dynamics in female rat pituitary Endocrinology 121 1987 84 89 (Pubitemid 17089264)
14. C.E. Roselli, L.E. Horton, and J.A. Resko Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system Endocrinology 117 1985 2471 2477 (Pubitemid 16194078)
15. G.G. Kuiper, J.G. Lemmen, B. Carlsson, J.C. Corton, S.H. Safe, and P.T. van der Saag Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta Endocrinology 139 1998 4252 4263 (Pubitemid 28513713)
16. G.G. Kuiper, B. Carlsson, K. Grandien, E. Enmark, J. Haggblad, and S. Nilsson Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta Endocrinology 138 1997 863 870 (Pubitemid 27089735)
17. G.G. Kuiper, E. Enmark, M. Pelto-Huikko, S. Nilsson, and J.A. Gustafsson Cloning of a novel receptor expressed in rat prostate and ovary Proc Natl Acad Sci USA 93 1996 5925 5930 (Pubitemid 26190778)
18. Z. Weihua, R. Lathe, M. Warner, and J.A. Gustafsson An endocrine pathway in the prostate, ERbeta, AR, 5alpha-androstane-3beta,17beta-diol, and CYP7B1, regulates prostate growth Proc Natl Acad Sci USA 99 2002 13589 13594 (Pubitemid 35221316)
19. A. Gangloff, R. Shi, V. Nahoum, and S.X. Lin Pseudo-symmetry of C19 steroids, alternative binding orientations, and multispecificity in human estrogenic 17beta-hydroxysteroid dehydrogenase FASEB J 17 2003 274 276
20. S. Torn, P. Nokelainen, R. Kurkela, A. Pulkka, M. Menjivar, and S. Ghosh Production, purification, and functional analysis of recombinant human and mouse 17beta-hydroxysteroid dehydrogenase type 7 Biochem Biophys Res Commun 305 2003 37 45 (Pubitemid 36535406)
21. Y. Jin, and T.M. Penning Steroid 5alpha-reductases and 3alpha-hydroxysteroid dehydrogenases: key enzymes in androgen metabolism Best Pract Res Clin Endocrinol Metab 15 2001 79 94 (Pubitemid 32544611)
22. S. Steckelbroeck, Y. Jin, S. Gopishetty, B. Oyesanmi, and T.M. Penning Human cytosolic 3alpha-hydroxysteroid dehydrogenases of the aldo-keto reductase superfamily display significant 3beta-hydroxysteroid dehydrogenase activity: implications for steroid hormone metabolism and action J Biol Chem 279 2004 10784 10795 (Pubitemid 38379543)
23. M. Sundin, M. Warner, T. Haaparanta, and J.A. Gustafsson Isolation and catalytic activity of cytochrome P-450 from ventral prostate of control rats J Biol Chem 262 1987 12293 12297
24. R.J. Gonzales, S. Ansar, S.P. Duckles, and D.N. Krause Androgenic/estrogenic balance in the male rat cerebral circulation: metabolic enzymes and sex steroid receptors J Cereb Blood Flow Metab 27 2007 1841 1852 (Pubitemid 47624548)
25. G.D. Snyder, U.M. Krishna, J.R. Falck, and A.A. Spector Evidence for a membrane site of action for 14,15-EET on expression of aromatase in vascular smooth muscle Am J Physiol Heart Circ Physiol 283 2002 H1936 H1942
26. H.-C. Shih, C.-L. Lin, S.-C. Wu, A.-L. Kwan, Y.-R. Hong, and S.-L. Howng Upregulation of estrogen receptor alpha and mediation of 17beta-estradiol vasoprotective effects via estrogen receptor alpha in basilar arteries in rats after experimental subarachnoid hemorrhage J Neurosurg 109 2008 92 99 (Pubitemid 351930526)
27. Y. Nakamura, T. Suzuki, T. Inoue, C. Tazawa, T. Moriya, and H. Saito 3beta-Hydroxysteroid dehydrogenase in human aorta Endocr J 52 2005 111 115
28. T.C. Register, and M.R. Adams Coronary artery and cultured aortic smooth muscle cells express mRNA for both the classical estrogen receptor and the newly described estrogen receptor beta J Steroid Biochem Mol Biol 64 1998 187 191 (Pubitemid 28200991)
29. Y. Ma, X. Qiao, A.E. Falone, O.M. Reslan, S.J. Sheppard, and R.A. Khalil Gender-specific reduction in contraction is associated with increased estrogen receptor expression in single vascular smooth muscle cells of female rat Cell Physiol Biochem 26 2010 457 470
30. S. Chakrabarti, and S.T. Davidge High glucose-induced oxidative stress alters estrogen effects on ERα and ERβ in human endothelial cells: reversal by AMPK activator J Steroid Biochem Mol Biol 117 2009 99 106
31. G.D. Norata, P. Cattaneo, A. Poletti, and A.L. Catapano The androgen derivative 5alpha-androstane-3beta,17beta-diol inhibits tumor necrosis factor alpha and lipopolysaccharide induced inflammatory response in human endothelial cells and in mice aorta Atherosclerosis 212 2010 100 106
32. K. Sugimoto, and C. Iadecola Delayed effect of administration of COX-2 inhibitor in mice with acute cerebral ischemia Brain Res 960 2003 273 276 (Pubitemid 36044587)
33. Ribaudo R, Gilman M, Kingston RE, Choczynski P, Sacchi N. Preparation of RNA from tissues and cells. Curr Protoc Immunol 2001;Chapter 10:Unit 10 1.
34. N.F. González-Cadavid, D. Vernet, A.F. Navarro, J. Rodriguez, R.S. Swerdloff, and J. Rajfer Up-regulation of the levels of androgen receptor and its mRNA by androgens in smooth-muscle cells from rat penis Mol Cell Endocrinol 90 1993 219 229 (Pubitemid 23024651)
35. M. Oka, V. Karoor, N. Homma, T. Nagaoka, E. Sakao, and S.M. Golembeski Dehydroepiandrosterone upregulates soluble guanylate cyclase and inhibits hypoxic pulmonary hypertension Cardiovascular Res 74 2007 377 387 (Pubitemid 46693699)
36. Z.K. Li, L. Shen, H. Ke, F. Li, L.M. Ni, and Q.H. Li Effects of androgen on the expression of brain aromatase cytopigment and nerve growth factor in neonatal rats with hypoxic-ischemic brain damage Zhongguo Dang Dai Er Ke Za Zhi 10 2008 441 446
37. M. Uchida, J.M. Palmateer, P.S. Herson, A.C. Devries, J. Cheng, and P.D. Hurn Dose-dependent effects of androgens on outcome after focal cerebral ischemia in adult male mice J Cereb Blood Flow Metab 29 2009 1454 1462
38. Y. Pan, H. Zhang, A.B. Acharya, P.H. Patrick, D. Oliver, and J.E. Morley Effect of testosterone on functional recovery in a castrate male rat stroke model Brain Res 1043 2005 195 204 (Pubitemid 40603387)
39. J. Cheng, W. Hu, T.J. Toung, Z. Zhang, S.M. Parker, and C.E. Roselli Age-dependent effects of testosterone in experimental stroke J Cereb Blood Flow Metab 29 2008 486 494
40. J. Cheng, M. Uchida, W. Zhang, M.R. Grafe, P.S. Herson, and P.D. Hurn Role of salt-induced kinase 1 in androgen neuroprotection against cerebral ischemia J Cereb Blood Flow Metab 31 2010 339 350
41. B.B. Yeap, Z. Hyde, O.P. Almeida, P.E. Norman, S.A.P. Chubb, and K. Jamrozik Lower testosterone levels predict incident stroke and transient ischemic attack in older men J Clin Endocrinol Metab 94 2009 2353 2359
42. L.L. Jeppesen, H.S. Jorgensen, H. Nakayama, H.O. Raaschou, T.S. Olsen, and K. Winther Decreased serum testosterone in men with acute ischemic stroke Arterioscler Thromb Vasc Biol 16 1996 749 754 (Pubitemid 26179363)
43. H. Hatakeyama, M. Nishizawa, A. Nakagawa, S. Nakano, T. Kigoshi, and K. Uchida Testosterone inhibits tumor necrosis factor-alpha-induced vascular cell adhesion molecule-1 expression in human aortic endothelial cells FEBS Lett 530 2002 129 132 (Pubitemid 35248198)
44. H. Jin, W.B. Qiu, Y.F. Mei, D.M. Wang, Y.G. Li, and X.R. Tan Testosterone alleviates tumor necrosis factor-alpha-mediated tissue factor pathway inhibitor downregulation via suppression of nuclear factor-kappa B in endothelial cells Asian J Androl 11 2009 266 271
45. T.K. Mukherjee, H. Dinh, G. Chaudhuri, and L. Nathan Testosterone attenuates expression of vascular cell adhesion molecule-1 by conversion to estradiol by aromatase in endothelial cells: Implications in atherosclerosis Proc Natl Acad Sci USA 99 2002 4055 4060 (Pubitemid 34252228)
46. C.J. Malkin, P.J. Pugh, R.D. Jones, D. Kapoor, K.S. Channer, and T.H. Jones The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men J Clin Endocrinol Metab 89 2004 3313 3318 (Pubitemid 38951897)
47. B.B. Yeap Are declining testosterone levels a major risk factor for ill-health in aging men Int J Impot Res 21 2008 24 36
48. R.J. Gonzales, S.P. Duckles, and D.N. Krause Dihydrotestosterone stimulates cerebrovascular inflammation through NFkappaB, modulating contractile function J Cereb Blood Flow Metab 29 2009 244 253
49. A. Razmara, D.N. Krause, and S.P. Duckles Testosterone augments endotoxin-mediated cerebrovascular inflammation in male rats Am J Physiol Heart Circ Physiol 289 2005 H1843 H1850
50. X. Zhang, L.Y. Wang, T.Y. Jiang, H.P. Zhang, Y. Dou, and J.H. Zhao Effects of testosterone and 17-beta-estradiol on TNF-alpha-induced E-selectin and VCAM-1 expression in endothelial cells. Analysis of the underlying receptor pathways Life Sci. 71 2002 15 29 (Pubitemid 34518626)
51. H.V. Carswell, I.M. Macrae, L. Gallagher, E. Harrop, and K.J. Horsburgh Neuroprotection by a selective estrogen receptor beta agonist in a mouse model of global ischemia Am J Physiol Heart Circ Physiol 287 2004 H1501 H1504
52. N.R. Miller, T. Jover, H.W. Cohen, R.S. Zukin, and A.M. Etgen Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death Endocrinology 146 2005 3070 3079 (Pubitemid 41002816)
53. T. Pelzer, P.A. Loza, K. Hu, B. Bayer, C. Dienesch, and L. Calvillo Increased mortality and aggravation of heart failure in estrogen receptor-beta knockout mice after myocardial infarction Circulation 111 2005 1492 1498 (Pubitemid 40470643)
54. I. Nikolic, D. Liu, J.A. Bell, J. Collins, C. Steenbergen, and E. Murphy Treatment with an estrogen receptor-beta-selective agonist is cardioprotective J Mol Cell Cardiol 42 2007 769 780 (Pubitemid 46527602)
55. M. Wang, P.R. Crisostomo, T. Markel, Y. Wang, K.D. Lillemoe, and D.R. Meldrum Estrogen receptor beta mediates acute myocardial protection following ischemia Surgery 144 2008 233 238
56. M. Wang, Y. Wang, B. Weil, A. Abarbanell, J. Herrmann, and J. Tan Estrogen receptor beta mediates increased activation of PI3K/Akt signaling and improved myocardial function in female hearts following acute ischemia Am J Physiol Regul Integr Comp Physiol 296 2009 R972 R978
57. N.D. Vornehm, M. Wang, A. Abarbanell, J. Herrmann, B. Weil, and J. Tan Acute postischemic treatment with estrogen receptor-alpha agonist or estrogen receptor-beta agonist improves myocardial recovery Surgery 146 2009 145 154
58. J. Guo, D.N. Krause, J. Horne, J.H. Weiss, X. Li, and S.P. Duckles Estrogen-receptor-mediated protection of cerebral endothelial cell viability and mitochondrial function after ischemic insult in vitro J Cereb Blood Flow Metab 30 2010 545 554
59. K. Saijo, G. Collier Jana, C. Li Andrew, A. Katzenellenbogen John, and K. Glass Christopher An ADIOL-ER[beta]-CtBP transrepression pathway negatively regulates microglia-mediated inflammation Cell 145 2011 584 595
60. N. Fortunati, F. Fissore, A. Fazzari, M. Becchis, A. Comba, and M.G. Catalano Sex steroid binding protein exerts a negative control on estradiol action in MCF-7 cells (human breast cancer) through cyclic adenosine 3′,5′-monophosphate and protein kinase A Endocrinology 137 1996 686 692
61. A.M. Nakhla, and W. Rosner Stimulation of prostate cancer growth by androgens and estrogens through the intermediacy of sex hormone-binding globulin Endocrinology 137 1996 4126 4129 (Pubitemid 26321856)
62. W.P. Benten, M. Lieberherr, G. Giese, C. Wrehlke, O. Stamm, and C.E. Sekeris Functional testosterone receptors in plasma membranes of T cells FASEB J 13 1999 123 133 (Pubitemid 29038282)
63. W.P. Benten, M. Lieberherr, O. Stamm, C. Wrehlke, Z. Guo, and F. Wunderlich Testosterone signaling through internalizable surface receptors in androgen receptor-free macrophages Mol Biol Cell 10 1999 3113 3123 (Pubitemid 29489549)
64. E.F. Konoplya, and E.H. Popoff Identification of the classical androgen receptor in male rat liver and prostate cell plasma membranes Int J Biochem 24 1992 1979 1983
65. C.A. Heinlein, and C. Chang The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions Mol Endocrinol 16 2002 2181 2187 (Pubitemid 35155532)
66. J. Thyberg, J. Roy, P.K. Tran, K. Blomgren, A. Dumitrescu, and U. Hedin Expression of caveolae on the surface of rat arterial smooth muscle cells is dependent on the phenotypic state of the cells Lab Invest 77 1997 93 101 (Pubitemid 27328363)