Estrogen receptors α and β mediate distinct pathways of vascular gene expression, including genes involved in mitochondrial electron transport and generation of reactive oxygen species

Molecular Endocrinology

Volumn 21, Issue 6, 2007, Pages 1281-1296

  O'Lone, Raegan ^a   Knorr, Katrin ^d   Jaffe, Iris Z ^d   Schaffer, Michael E ^b   Martini, Paolo G V ^f   Karas, Richard H ^d   Bienkowska, Jadwiga ^c,e   Mendelsohn, Michael E ^d   Hansen, Ulla ^a,b,g  

^a Boston University   (United States)

^b BOSTON UNIVERSITY   (United States)

^c Boston University   (United States)

^d TUFTS MEDICAL CENTER   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f UNIVERSITY OF MILAN   (Italy)

^g NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; RECEPTOR SUBTYPE; SCLEROPROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ELECTRON TRANSPORT; ESTROGEN THERAPY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC CODE; INTRACELLULAR TRANSPORT; KNOCKOUT GENE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR GENE; RESPIRATORY CHAIN; WILD TYPE;

ANIMALS; AORTA; DOWN-REGULATION; ELECTRON TRANSPORT; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIGANDS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; OXIDOREDUCTASES; PROMOTER REGIONS (GENETICS); REACTIVE OXYGEN SPECIES; RNA, MESSENGER; TRANSCRIPTION FACTORS; UP-REGULATION;

MUS;

EID: 34347248822     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2006-0497     Document Type: Article

References (71)

1. Mendelsohn ME, Karas RH 2005 Molecular and cellular basis of cardiovascular gender differences. Science 308:1583-1587
2. Mendelsohn ME, Karas RH 1999 The protective effects of estrogen on the cardiovascular system. N Engl J Med 340:1801-1811
3. Pare G, Krust A, Karas RH, Dupont S, Aronovitz M, Chambon P, Mendelsohn ME 2002 Estrogen receptor-α mediates the protective effects of estrogen against vascular injury. Circ Res 90:1087-1092
4. Zhu Y, Bian Z, Lu P, Karas RH, Bao L, Cox D, Hodgin J, Shaul PW, Thorén P, Smithies O, Gustafsson JÅ, Mendelsohn ME 2002 Abnormal vascular function and hypertension in mice deficient in estrogen receptor β. Science 295:505-508
5. Shearman AM, Cupples LA, Demissie S, Peter I, Schmid CH, Karas RH, Mendelsohn ME, Housman DE, Levy D 2003 Association between estrogen receptor α gene variation and cardiovascular disease. JAMA 290:2263-2270
6. Peter I, Shearman AM, Vasan RS, Zucker DR, Schmid CH, Demissie S, Cupples LA, Kuvin JT, Karas RH, Mendelsohn ME, Housman DE, Benjamin EJ 2005 Association of estrogen receptor β gene polymorphisms with left ventricular mass and wall thickness in women. Am J Hypertens 18:1388-1395
7. Peter I, Shearman AM, Zucker DR, Schmid CH, Demissie S, Cupples LA, Larson MG, Vasan RS, D'Agostino RB, Karas RH, Mendelsohn ME, Housman DE, Levy D 2005 Variation in estrogen-related genes and cross-sectional and longitudinal blood pressure in the Framingham Heart Study. J Hypertens 23:2193-2200
8. Björnström L, Sjöberg M 2005 Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 19:833-842
9. Mendelsohn ME 2000 Nongenomic, estrogen receptor-mediated activation of endothelial nitric oxide synthase: how does it work? What does it mean? Circ Res 87:956-960
10. Mendelsohn ME 2000 Mechanisms of estrogen action in the cardiovascular system. J Steroid Biochem Mol Biol 74:337-343
11. Losordo DW, Isner JM 2001 Estrogen and angiogenesis: a review. Arterioscler Thromb Vasc Biol 21:6-12
12. Spyridopoulos I, Sullivan AB, Kearney M, Isner JM, Losordo DW 1997 Estrogen-receptor-mediated inhibition of human endothelial cell apoptosis. Estradiol as a survival factor. Circulation 95:1505-1514
13. Garmy-Susini B, Delmas E, Gourdy P, Zhou M, Bossard C, Bugler B, Bayard F, Krust A, Prats AC, Doetschman T, Prats H, Arnal JF 2004 Role of fibroblast growth factor-2 isoforms in the effect of estradiol on endothelial cell migration and proliferation. Circ Res 94:1301-1309
14. Suzuki A, Mizuno K, Ino Y, Okada M, Kikkawa F, Mizutani S, Tomoda Y 1996 Effects of 17β-estradiol and progesterone on growth-factor-induced proliferation and migration in human female aortic smooth muscle cells in vitro. Cardiovasc Res 32:516-523
15. Takeda-Matsubara Y, Nakagami H, Iwai M, Cui T-X, Shiuchi T, Akishita M, Nahmias C, Ito M, Horiuchi M 2002 Estrogen activates phosphatases and antagonizes growth-promoting effect of angiotensin II. Hypertension 39:41-45
16. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J 2003 TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374-378
17. Zhang B, Schmoyer D, Kirov S, Snoddy J 2004 GOTree Machine (GOTM): a web-based platform for interpreting sets of interesting genes using Gene Ontology hierarchies. BMC Bioinformatics 5:16
18. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M 2006 From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354-D357
19. Sauer H, Wartenberg M, Hescheler J 2001 Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 11:173-186
20. Cho S, Park E-M, Febbraio M, Anrather J, Park L, Racchumi G, Silverstein RL, Iadecola C 2005 The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J Neurosci 25:2504-2512
21. Hayes JD, Flanagan JU, Jowsey IR 2005 Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51-88
22. Gonzalez FJ 2005 Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat Res 569:101-110
23. Chance B, Sies H, Boveris A 1979 Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527-605
24. Hashimoto M, Hsu LJ, Rockenstein E, Takenouchi T, Mallory M, Masliah E 2002 α-Synuclein protects against oxidative stress via inactivation of the c-Jun N-terminal kinase stress-signaling pathway in neuronal cells. J Biol Chem 277:11465-11472
25. Ellis CE, Murphy EJ, Mitchell DC, Golovko MY, Scaglia F, Barceló-Coblijn GC, Nussbaum RL 2005 Mitochondrial lipid abnormality and electron transport chain impairment in mice lacking α-synuclein. Mol Cell Biol 25:10190-10201
26. Hurlin PJ, Steingrimsson E, Copeland NG, Jenkins NA, Eisenman RN 1999 Mga, a dual-specificity transcription factor that interacts with Max and contains a T-domain DNA-binding motif. EMBO J 18:7019-7028
27. Sun X-H, Copeland NG, Jenkins NA, Baltimore D 1991 Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 11:5603-5611
28. Forrest S, McNamara C 2004 Id family of transcription factors and vascular lesion formation. Arterioscler Thromb Vasc Biol 24:2014-2020
29. Ruzinova MB, Benezra R 2003 Id proteins in development, cell cycle and cancer. Trends Cell Biol 13:410-418
30. INK4a expression during cellular senescence. Nature 409:1067-1070
31. Roberts EC, Deed RW, Inoue T, Norton JD, Sharrocks AD 2001 Id helix-loop-helix proteins antagonize Pax transcription factor activity by inhibiting DNA binding. Mol Cell Biol 21:524-533
32. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M 2005 Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122:33-43
33. Odom DT, Zizlsperger N, Gordon DB, Bell GW, Rinaldi NJ, Murray HL, Volkert TL, Schreiber J, Rolfe PA, Gifford DK, Fraenkel E, Bell GI, Young RA 2004 Control of pancreas and liver gene expression by HNF transcription factors. Science 303:1378-1381
34. 2/M checkpoints. Genes Dev 16:245-256
35. Katzenellenbogen BS, Choi I, Delage-Mourroux R, Ediger TR, Martini PGV, Montano M, Sun J, Weis K, Katzenellenbogen JA 2000 Molecular mechanisms of estrogen action: selective ligands and receptor pharmacology. J Steroid Biochem Mol Biol 74:279-285
36. Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson J-Å 2001 Mechanisms of estrogen action. Physiol Rev 81:1535-1565
37. Hewitt SC, Deroo BJ, Hansen K, Collins J, Grissom S, Afshari CA, Korach KS 2003 Estrogen receptor-dependent genomic responses in the uterus mirror the biphasic physiological response to estrogen. Mol Endocrinol 17:2070-2083
38. Jelinsky SA, Harris HA, Brown EL, Flanagan K, Zhang X, Tunkey C, Lai K, Lane MV, Simcoe DK, Evans MJ 2003 Global transcription profiling of estrogen activity: estrogen receptor α regulates gene expression in the kidney. Endocrinology 144:701-710
39. Weihua Z, Mäkelä S, Andersson LC, Salmi S, Saji S, Webster JI, Jensen EV, Nilsson S, Warner M, Gustafsson J-Å 2001 A role for estrogen receptor β in the regulation of growth of the ventral prostate. Proc Natl Acad Sci USA 98:6330-6335
40. Weihua Z, Saji S, Mäkinen S, Cheng G, Jensen EV, Warner M, Gustafsson J-Å 2000 Estrogen receptor (ER) β, a modulator of ERα in the uterus. Proc Natl Acad Sci USA 97:5936-5941
41. Chen J-Q, Yager JD, Russo J 2005 Regulation of mitochondrial respiratory chain structure and function by estrogens/ estrogen receptors and potential physiological/ pathophysiological implications. Biochim Biophys Acta 1746:1-17
42. Watanabe T, Inoue S, Hiroi H, Orimo A, Kawashima H, Muramatsu M 1998 Isolation of estrogen-responsive genes with a CpG island library. Mol Cell Biol 18:442-449
43. Chen J, Schwartz DA, Young TA, Norris JS, Yager JD 1996 Identification of genes whose expression is altered during mitosuppression in livers of ethinyl estradiol-treated female rats. Carcinogenesis 17:2783-2786
44. Thompson CJ, Tam NNC, Joyce JM, Leav I, Ho S-M 2002 Gene expression profiling of testosterone and estradiol-17β-induced prostatic dysplasia in Noble rats and response to the antiestrogen ICI 182,780. Endocrinology 143:2093-2105
45. Stirone C, Duckles SP, Krause DN, Procaccio V 2005 Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 68:959-965
46. Chen J, Gokhale M, Li Y, Trush MA, Yager JD 1998 Enhanced levels of several mitochondrial mRNA transcripts and mitochondrial superoxide production during ethinyl estradiol-induced hepatocarcinogenesis and after estrogen treatment of HepG2 cells. Carcinogenesis 19:2187-2193
47. Psarra A-MG, Solakidi S, Sekeris CE 2006 The mitochondrion as a primary site of action of steroid and thyroid hormones: presence and action of steroid and thyroid hormone receptors in mitochondria of animal cells. Mol Cell Endocrinol 246:21-33
48. Pedram A, Razandi M, Wallace DC, Levin ER 2006 Functional estrogen receptors in the mitochondria of breast cancer cells. Mol Biol Cell 17:2125-2137
49. Kelly DP, Scarpulla RC 2004 Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18:357-368
50. Turrens JF 2003 Mitochondrial formation of reactive oxygen species. J Physiol 552:335-344
51. de Nigris F, Lerman A, Ignarro LJ, Williams-Ignarro S, Sica V, Baker AH, Lerman LO, Geng YJ, Napoli C 2003 Oxidation-sensitive mechanisms, vascular apoptosis and atherosclerosis. Trends Mol Med 9:351-359
52. Griendling KK, Ushio-Fukai M 2000 Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept 91:21-27
53. Rao GN, Berk BC 1992 Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ Res 70:593-599
54. Ruiz-Ginés JA, López-Ongil S, González-Rubio M, González-Santiago L, Rodríguez-Puyol M, Rodr?́guez-Puyol D 2000 Reactive oxygen species induce proliferation of bovine aortic endothelial cells. J Cardiovasc Pharmacol 35:109-113
55. Strehlow K, Rotter S, Wassmann S, Adam O, Grohé C, Laufs K, Böhm M, Nickenig G 2003 Modulation of antioxidant enzyme expression and function by estrogen. Circ Res 93:170-177
56. Wu X, Pang S-T, Sahlin L, Blanck A, Norstedt G, Flores-Morales A 2003 Gene expression profiling of the effects of castration and estrogen treatment in the rat uterus. Biol Reprod 69:1308-1317
57. Deroo BJ, Hewitt SC, Peddada SD, Korach KS 2004 Estradiol regulates the thioredoxin antioxidant system in the mouse uterus. Endocrinology 145:5485-5492
58. Scarpulla RC 2002 Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576:1-14
59. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M 2000 Effect of single and compound knockouts of estrogen receptors α (ERα) and β (ERβ) on mouse reproductive phenotypes. Development 127:4277-4291
60. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson J-Å, Smithies O 1998 Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc Natl Acad Sci USA 95:15677-15682
61. Wu Z, Irizarry RA 2005 Stochastic models inspired by hybridization theory for short oligonucleotide arrays. J Comput Biol 12:882-893
62. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP 2003 Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264
63. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80
64. Chomczynski P, Sacchi N 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159
65. Zhong S, Tian L, Li C, Storch K-F, Wong WH 2004 Comparative analysis of gene sets in the Gene Ontology space under the multiple hypothesis testing framework. Proc IEEE Comput Syst Bioinform Conf 425-435
66. Tullai JW, Schaffer ME, Mullenbrock S, Kasif S, Cooper GM 2004 Identification of transcription factor binding sites upstream of human genes regulated by the phosphatidylinositol 3-kinase and MEK/ERK signaling pathways. J Biol Chem 279:20167-20177
67. Kel AE, Gossling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, Wingender E 2003 MATCH: a tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31:3576-3579
68. Wingender E, Chen X, Hehl R, Karas H, Liebich I, Matys V, Meinhardt T, Pruss M, Reuter I, Schacherer F 2000 TRANSFAC: an integrated system for gene expression regulation. Nucleic Acids Res 28:316-319
69. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Church DM, DiCuccio M, Edgar R, Federhen S, Helmberg W, Kenton DL, Khovayko O, Lipman DJ, Madden TL, Maglott DR, Ostell J, Pontius JU, Pruitt KD, Schuler GD, Schriml LM, Sequeira E, Sherry ST, Sirotkin K, Starchenko G, Suzek TO, Tatusov R, Tatusova TA, Wagner L, Yaschenko E 2005 Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 33:D39-D45
70. Hinrichs AS, Karolchik D, Baertsch R, Barber GP, Bejerano G, Clawson H, Diekhans M, Furey TS, Harte RA, Hsu F, Hillman-Jackson J, Kuhn RM, Pedersen JS, Pohl A, Raney BJ, Rosenbloom KR, Siepel A, Smith KE, Sugnet CW, Sultan-Qurraie A, Thomas DJ, Trumbower H, Weber RJ, Weirauch M, Zweig AS, Haussler D, Kent WJ 2006 The UCSC Genome Browser Database: update 2006. Nucleic Acids Res 34:D590-D598
71. Maglott D, Ostell J, Pruitt KD, Tatusova T 2005 Entrez Gene: gene-centered information at NCBI. Nucleic Acids Res 33:D54-D58