Estrogen and the regulation of mitochondrial structure and function in the brain

Journal of Steroid Biochemistry and Molecular Biology

Volumn 131, Issue 1-2, 2012, Pages 2-9

  Arnold, Susanne ^a   Victor, Marion Barbara ^a   Beyer, Cordian ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Astroglia; ATP; CNS; Estrogen; Fusion and fission; Mitochondria; Neuron; Respiratory chain; ROS

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; CELL ENERGY; CELL FUNCTION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; DENDRITIC SPINE; ENERGY BALANCE; GENE EXPRESSION; HUMAN; INTRACELLULAR SIGNALING; MITOCHONDRION; NONHUMAN; REVIEW; SYNAPSE;

ANIMALS; BRAIN; ENERGY METABOLISM; ESTROGENS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 84859247743     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2012.01.012     Document Type: Review

References (101)

1. C. Beyer Estrogen and the developing mammalian brain Anat. Embryol. (Berl) 199 1999 379 390 (Pubitemid 29145836)
2. M.M. McCarthy Estradiol and the developing brain Physiol. Rev. 88 2008 91 124
3. M. Kipp, S. Karakaya, J. Pawlak, G. Araujo-Wright, S. Arnold, and C. Beyer Estrogen and the development and protection of midbrain dopaminergic neurons: concerted action of a multitude of signals, protective molecules, and growth factor Front. Neuroendocrinol. 27 2006 376 390 (Pubitemid 44738014)
4. C.L. Wright, J.S. Schwarz, S.L. Dean, and M.M. Mc Carthy Cellular mechanisms of estradiol-mediated sexual differentiation of the brain Trends Endocrinol. Metab. 21 2010 553 561
5. A.E. Kudwa, V. Michopoulos, J.D. Gatewood, and E.F. Rissman Roles of estrogen receptors alpha an beta in differentiation of mouse sexual behaviour Neuroscience 138 2006 921 928
6. P.M. Wise, M.J. Smith, D.B. Dubal, M.E. Woslon, S.W. Rau, A.B. Cashion, M. Böttner, and K.L. Rosewell Neuroendocrine modulation and repercussions of female reproductive aging Recent Prog. Horm. Res. 57 2002 235 256
7. D.E. Dluzen Unconventional effects of estrogen uncovered Trends Pharmacol. Sci. 26 2005 485 487 (Pubitemid 41338557)
8. R. Bosse, and T. DiPaolo The modulation of brain dopamine and GABAA receptors by estradiol: a clue for CNS changes occurring during menopause Cell. Mol. Neurobiol. 16 1996 199 212
9. T.A. Roepke, O.K. Ronneleiv, and M.J. Kelly Physiological consequences of membrane-initiated estrogen signaling in the brain Front. Biosci. 16 2011 1560 1573
10. T.C. Foster Role of estrogen receptor alpha an beta expression and signaling on cognitive function and aging Hippocampus 2011 [Epub ahead of print]
11. P. Acs, M. Kipp, S. Komoly, and C. Beyer 17β-estradiol and progesterone treatment prevents demyelinization in an experimental multiple sclerosis animal model Glia 57 2009 807 814
12. J. Dang, B. Mitkari, M. Kipp, and C. Beyer Gonadal steroids prevent cell damage and stimulate behavioral recovery after transient middle cerebral artery occlusion in male and female rats Brain Behav. Immun. 25 2011 715 726
13. H. Xu, G.K. Gouras, J.P. Greenfield, B. Vincent, J. Naslund, L. Mazzarelli, G. Fried, J.N. Jovanovic, M. Seeger, N.R. Relkin, F. Liao, F. Checler, J.D. Buxbaum, B.T. Chait, G. Thinakaran, S.S. Sisodia, R. Wang, P. Greengard, and S. Gandy Estrogen reduces neuronal generation of Alzheimer beta-amyloid peptides Nat. Med. 4 1998 447 451 (Pubitemid 28212761)
14. K.M. Dhandapani, and D.W. Brann Protective effects of estrogen and selective estrogen receptor modulators in the brain Biol. Reprod. 67 2002 1379 1385 (Pubitemid 35204912)
15. L.M. Garcia-Segura, I. Azcoitia, and L.L. DonCarlos Neuroprotection by estradiol Prog. Neurobiol. 63 2001 29 60
16. I. Azcoitia, J.G. Yague, and L.M. Garcia-Segura Estradiol synthesis within the human brain Neuroscience 2011 [Epub ahead of print]
17. Y. Hojo, G. Murakami, H. Mukai, S. Higo, Y. Hatanaka, M. Ogiue-Ikeda, H. Ishii, T. Kimoto, and S. Kawato Estrogen synthesis in the brain-role in synaptic plasticity and memory Mol. Cell. Endocrinol. 13 2008 31 43
18. C. Beyer, S. Green, P.J. Baker, N.S. Huskisson, and J.B. Hutchison Aromatase is specifically localised to neurones of the developing mouse hypothalamus and cortex Brain Res. 638 1994 203 210 (Pubitemid 24063306)
19. A.J. Mhyre, and D.M. Dorsa Estrogen activates rapid signaling in the brain: role of estrogen receptor alpha and beta in neurons and glia Neuroscience 138 2006 851 858
20. P.J. Shughrue, M.V. Lane, and I. Merchenthaler Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system J. Comp. Neurol. 388 1997 507 525 (Pubitemid 27481288)
21. T. Funakoshi, A. Yanai, K. Shinoda, M.M. Kawano, and Y. Mizukami G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane Biochem. Biophys. Res. Commun. 346 2006 904 910
22. J.I. Luoma, M.I. Boulware, and P.G. Mermelstein Caveolin proteins and estrogen signaling in the brain Mol. Cell. Endocrinol. 290 2008 8 13
23. M. Schumacher, R. Guennoun, P. Robel, and E.E. Baulieu Neurosteroids in the hippocampus: neuronal plasticity and memory Stress 2 1997 65 78 (Pubitemid 28154817)
24. N. Romano, K. Lee, I.M. Abraham, C.L. Jasoni, and A.E. Herbison Nonclassical estrogen modulation of presynaptic GABA terminals modulates calcium dynamics in gonadotropin-releasing hormone neurons Endocrinology 149 2008 5335 5344
25. A. Dhir, and S.K. Kulkarni Antidepressant-like effect of 17beta-estradiol: involvement of dopaminergic, serotonergic, and (or) sigma-1 receptor systems Can. J. Physiol. Pharmacol. 86 2008 726 735
26. J. Pawlak, M. Karolczak, A. Krust, P. Chambon, and C. Beyer Estrogen receptor-alpha is associated with the plasma membrane of astrocytes and coupled to the MAP/Src-kinase pathway Glia 50 2005 270 275 (Pubitemid 40769856)
27. T. Ivanova, E. Küppers, J. Engele, and C. Beyer Estrogen stimulates brain-derived neurotrophic factor expression in embryonic mouse midbrain neurons through a membrane-mediated and calcium-dependent mechanism J. Neurosci. Res. 66 2001 221 230 (Pubitemid 32912291)
28. J.J. Watters, and D.M. Dorsa Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms J. Neurosci. 18 1998 6672 6680 (Pubitemid 28387999)
29. X. Zhen, S. Goswami, S.A. Abdali, M. Frankfurt, and E. Friedman Estrogen-modulated frontal cortical CaMKII activity and behavioral supersensitization induced by prolonged cocaine treatment in female rats Psychopharmacology (Berl) 191 2007 323 331 (Pubitemid 46354608)
30. Z. Zhao, C. Park, M.A. McDevitt, C. Gildewell-Kenney, P. Chambon, J. Weiss, J.L. Jameson, and J.E. Levine p21-activated kinase mediates rapid estradiol-negative feedback actions in the reproductive axis Proc. Natl. Acad. Sci. U. S. A. 106 2009 7221 7226
31. L. Raz, M.M. Khan, V.B. Mahesh, R.K. Vadlamudi, and D.W. Brann Rapid estrogen signaling in the brain Neurosignals 16 2008 140 153 (Pubitemid 351263221)
32. E.M. Szego, K. Barabas, J. Balog, N. Szilagyi, K.S. Korach, G. Juhasz, and I.M. Abraham Estrogen induces estrogen receptor alpha-dependent cAMP response element-binding protein phosphorylation via mitogen activated protein kinase pathway in basal forebrain cholinergic neurons in vivo J. Neurosci. 26 2006 4104 4110 (Pubitemid 44315431)
33. L.M. Garcia-Segura, M.A. Arevalo, and I. Azcoitia Interactions of estradiol and insulin-like growth factor signalling in the nervous system: new advances Prog. Brain Res. 181 2010 251 272
34. C. Behl Oestrogen as a neuroprotective hormone Nat. Rev. Neurosci. 3 2002 433 442 (Pubitemid 135711799)
35. J.L. Spencer, E.M. Waters, R.D. Romeo, G.E. Wood, T.A. Milner, and B.S. McEwen Uncovering the mechanisms of estrogen effects on hippocampal neurons Front. Neuroendocrinol. 29 2008 219 237
36. O.K. Ronnekleiv, A. Malyala, and M.J. Kelly Membrane-initiated signaling of estrogen in the brain Semin. Reprod. Med. 25 2007 165 177 (Pubitemid 46676903)
37. S. Arnold, and C. Beyer Neuroprotection by estrogen in the brain: the mitochondrial compartment as presumed therapeutic target J. Neurochem. 110 2009 1 11
38. E.R. Levin Plasma membrane estrogen receptors Trends Endocrinol. Metab. 20 2009 477 482
39. J.-Q. Chen, M. Delannoy, C. Cooke, and J.D. Yager Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells Am. J. Physiol. Endocrinol. Metab. 286 2004 E1011 E1022
40. P. Monje, and R. Boland Subcellular distribution of native estrogen receptor alpha and beta isoforms in rabbit uterus and ovary J. Cell. Biochem. 82 2001 467 479 (Pubitemid 32729410)
41. A. Razmara, L. Sunday, C. Stirone, X.B. Wang, D.N. Krause, S.P. Duckles, and V. Procaccia Mitochondrial effects of estrogen are mediated by estrogen receptor a in brain endothelial cells J. Pharmacol. Exp. Ther. 325 2008 782 790 (Pubitemid 351724313)
42. S.H. Yang, R. Liu, E.J. Perez, Y. Wen, S.M. Stevens, T. Valencia, A.M. Brun-Zinkernagel, L. Prokai, Y. Will, J. Dykens, P. Koulen, and J.W. Simpkins Mitochondrial location of estrogen receptor beta Proc. Natl. Acad. Sci. U. S. A. 102 2004 4130 4135 (Pubitemid 38410620)
43. T.A. Milner, K. Ayoola, C.T. Drake, S.P. Herrick, N.E. Rabori, B.S. McEwen, S. Warrier, and S.E. Alves Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation J. Comp. Neurol. 491 2005 81 95 (Pubitemid 41263413)
44. C. Alvarez-Delgado, C.A. Mendoza-Rodriguez, O. Picazo, and M. Cerbon Different expression of alpha and beta mitochondrial estrogen receptors in the aging rat brain: interaction with respiratory complex V Exp. Gerontol. 45 2010 580 585
45. P.R. Cammarata, S. Chu, A. Moor, Z. Wang, S.H. Yang, and J.W. Simpkins Subcellular distribution of native estrogen receptor alpha and beta subtypes in cultured human lens epithelial cells Exp. Eye Res. 78 2004 861 871 (Pubitemid 38252962)
46. A. Grossman, J. Oppenheim, G. Grondin, P. St Jean, and A.R. Beaudoin Immunocytochemical localization of [3H]estradiol-binding protein in rat pancreatic acinar cells Endocrinology 124 1989 2857 2866 (Pubitemid 19154119)
47. J. Zheng, and V.D. Ramirez Rapid inhibition of rat brain mitochondrial proton F0F1-ATPase activity by estrogens: comparison with Na+, K+ -ATPase of porcine cortex Eur. J. Pharmacol. 368 1999 95 102 (Pubitemid 29106419)
48. J. Zheng, and V.D. Ramirez Purification and identification of an estrogen binding protein from rat brain: oligomycin sensitivity-conferring protein (OSCP, a subunit of mitochondrial F0F1-ATPase/ATP synthase J. Steroid Biochem. Mol. Biol. 68 1999 65 75 (Pubitemid 29130387)
49. J.L. Kipp, and V.D. Ramirez Effect of estradiol, diethylstilbestrol, and resveratrol on F0F1-ATPase activity from mitochondrial preparations of rat heart, liver, and brain Endocrine 15 2001 165 175 (Pubitemid 32977326)
50. A. Horvat, S. Petrovic, N. Nedeljikovic, J.N. Martinovic, and G. Nikezic Estradiol affect Na-dependent Ca2+ efflux from synaptosomal mitochondria Gen. Physiol. Biophys. 19 2000 59 71
51. L. Hernandez-Esquivel, N. Pavon, C. Zazueta, N. Garcia, F. Correa, and E. Chavez Protective action of tamoxifen on carboxyatractyloside-induced mitochondrial permeability transition Life Sci. 88 2011 681 687
52. M. Christophe, and S. Nicolas Mitochondria: a target for neuroprotective interventions in cerebral ischemia-reperfusion Curr. Pharm. Des. 12 2006 739 757
53. W.L. Miller Role of mitochondria in steroidogenesis Endocr. Dev. 20 2011 1 19
54. R. Guevara, M. Gianotti, P. Roca, and J. Oliver Age and sex-related changes in rat brain mitochondrial function Cell. Physiol. Biochem. 27 2011 201 206
55. D.G. Nicholls Mitochondrial calcium function and dysfunction in the central nervous system Biochim. Biophys. Acta 1787 2009 1416 1424
56. M. Karbowski, and R.J. Youle Dynamics of mitochondrial morphology in healthy cells and during apoptosis Cell Death Differ. 10 2003 870 880 (Pubitemid 36939697)
57. A. Santel, and S. Frank Shaping mitochondria: the complex posttranslational regulation of the mitochondrial fission protein DRP1 IUBMB Life 60 2008 448 455
58. A. Santel, and M.T. Fuller Control of mitochondrial morphology by a human mitofusion J. Cell Sci. 114 2001 867 874 (Pubitemid 32266258)
59. D.C. Chan Mitochondrial dynamics in disease J. Med. 359 2007 1707 1709 (Pubitemid 46658702)
60. M.P. Yaffe The machinery of mitochondrial inheritance and behavior Science 283 1999 1493 1497
61. S. Zuchner, I.V. Mersiyanova, M. Muglia, N. Bissar-Tadmouri, J. Rochelle, E.L. Dadali, M. Zappa, E. Nelis, A. Patitucci, J. Senderek, Y. Parman, O. Evgrafov, P.D. Jonghe, Y. Takahashi, S. Tsulli, M.A. Pericak-Vance, A. Quattrone, E. Battaloglu, A.V. Polyakov, V. Timmermann, J.M. Schröder, and J.M. Vance Mutations in mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A Nat. Genet. 36 2004 449 451 (Pubitemid 38620027)
62. C. Alexander, M. Votruba, U.E. Pesch, D.L. Thiselton, S. Mayer, A. Moore, M. Rodriguez, U. Kellner, B. Leo-Kottler, G. Auburger, S.S. Bhattacharya, and B. Wissinger OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28 Nat. Genet. 26 2000 211 215
63. R. Sugioka, S. Shimizu, and Y. Tsujimoto Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis J. Biol. Chem. 279 2004 52726 52734 (Pubitemid 39656648)
64. Z. Liz, K. Okamoto, Y. Hayashi, and M. Sheng The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses Cell 119 2004 873 887 (Pubitemid 40017692)
65. A.M. Motley, and E.H. Hettema Yeast peroxisomes multiply by growth and division J. Cell Biol. 178 2007 399 410 (Pubitemid 47196149)
66. J. Yao, R. Hamilton, E. Cadenas, and R.D. Brinton Decline in mitochondrial bioenergetics and shift to ketogenic profile in brain during reproductive senescence Biochim. Biophys. Acta 1800 2010 1121 1126
67. S. Arnold, G. Wright de Araujo, and C. Beyer Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones J. Mol. Endocrinol. 41 2008 289 300
68. G.W. Araujo, C. Beyer, and S. Arnold Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes J. Neuroendocrinol. 20 2008 930 941 (Pubitemid 351859111)
69. A. Zorzano Regulation of mitofusin-2 expression in skeletal muscle Appl. Physiol. Nutr. Metab. 34 2009 433 439
70. R. Cartoni, B. leger, M.B. Hock, M. Praz, A. Crettenand, S. Pitch, J.L. Ziltener, F. Luthi, O. Deriaz, A. Zorzano, C. Gobelet, A. Kralli, and A.P. Russell Mitofusins and ERRalpha expression are increased in human skeletal muscle after physical exercise J. Physiol. 567 2005 349 358 (Pubitemid 41167327)
71. A. Wagatasuma, N. Kotake, T. Kawachi, M. Shiozuka, S. Yamada, and R. Matsuda Mitochondrial adaptations in skeletal muscle to hindlimb unloading Mol. Cell. Biochem. 350 2011 1 11
72. F.X. Soriano, M. Liesa, D. Bach, D.C. Chan, M. Palacin, and A. Zorzano Evidence for a mitochondrial regulatory pathway defined by peroxisome proliferator-activated receptor gamma coactivator-1 alpha, estrogen-related receptor-alpha, and mitofusin 2 Diabetes 55 2006 1783 1791 (Pubitemid 44324133)
73. K. Tahara, D. Tsuchimoto, Y. Tominaga, S. Asoh, S. Ohta, M. Kitagawa, H. Horie, T. Kadoya, and Y. Nakabeppu DeltaFosB, but not FosB, induces delayed apoptosis independent of cell proliferation in the Rat1a embryo cell line Cell Death Differ. 10 2003 496 507 (Pubitemid 36656639)
74. J.-Q. Chen, J.D. Yager, and J. Russo Regulation of mitochondrial respiratory chain structure and function by estrogen/estrogen receptors and potential physiological/pathophysiological implications Biochim. Biophys. Acta 1746 2005 1 17 (Pubitemid 41484081)
75. P. Vic, F. Vignon, D. Derocq, and H. Rochefort Effect of estradiol on the ultrastructure of the mcf7 human breast cancer cells in culture Cancer Res. 42 1982 667 673 (Pubitemid 12173611)
76. M. Alkhalaf, G. Chaminadas, A.Y. proper, and G.L. Adessi Ultrastructural changes induced by oestradiol-17 beta, progesterone and oestrone-3-sulphate in guinea-pig endometrial glandular cells grown in primary culture J. Endocrinol. 122 1989 439 444 (Pubitemid 19199913)
77. P. Zai, T.E. Eurell, P.S. Cooke, D.B. Lubahn, and D.R. Gross Myocardial ischemia-reperfusion injury in estrogen receptor-alpha knockout and wild-type mice Am. J. Physiol. Heart Circ. Physiol. 278 2000 H1640 H1647
78. K. Toda, K. Takeda, T. Okada, S. Akira, T. Saibara, T. Kaname, K. Yamamura, S. Onishi, and Y. Shizuta Targeted disruption of the aromatase p450 gene (cyp19) in mice and their ovarian and uterine responses to 17beta-oestradiol J. Endocrinol. 170 2001 99 111 (Pubitemid 32677571)
79. M.M. Gonzalez-Barroso, C. Fleury, M.A. Jimenez, M.A. Sanz, A. Romero, F. Bouillaud, and E. Rial Structural and functional study of a conserved region in the uncoupling protein UCP1: the three matrix loops are involved in the control of transport J. Mol. Biol. 292 1999 137 149 (Pubitemid 29425659)
80. R. Jusato, J. Boada, M. Frontera, J. Oliver, J. Bermudez, and M. Gianotti Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis Am. J. Physiol. Cell Physiol. 289 2005 C372 C378
81. J. Yao, R. Irwin, S. Chen, R. Hamilton, E. Cadenas, and R.D. Brinton Ovarian hormone loss induces bioenergetic deficits and mitochondrial β-amyloid Neurobiol. Aging 2011 [Epub ahead of print]
82. R.W. Irwin, J. Yao, R.T. Hamilton, E. Cadenas, R.D. Brinton, and J. Nilsen Progesterone and estrogen regulate oxidative metabolism in brain mitochondria Endocrinology 149 2008 3167 3175 (Pubitemid 351724522)
83. J. Nilsen, R.W. Irwin, T.K. Gallaher, and R.D. Brinton Estradiol in vivo regulation of brain mitochondrial proteome J. Neurosci. 27 2007 14069 14077 (Pubitemid 351377854)
84. J.Q. Chen, P.A. Russo, C. Cooke, I.H. Russo, and J. Russo ERbeta shifts from mitochondria to nucleus during estrogen-induced neoplastic transformation of human breast epithelial cells and is involved in estrogen-induced synthesis of mitochondrial respiratory chain proteins Biochim. Biophys. Acta 1773 2007 1732 1746 (Pubitemid 350191975)
85. Y.C. Hsieh, H.P. Yu, T. Suzuki, M.A. Choudhry, M.G. Schwacha, K.I. Bland, and I.H. Chaudry Upregulation of mitochondrial respiratory complex IV by estrogen receptor-beta is critical for inhibiting mitochondrial apoptotic signaling and restoring cardiac functions following trauma-hemorrhage J. Mol. Cell. Cardiol. 41 2006 511 521 (Pubitemid 44344281)
86. D. Jonsson, J. Nilsson, M. Odenlund, G. Bratthall, J. Broman, E. Ekblad, M.L. Lydrup, and B.O. Nilsson Demonstration of mitochondrial oestrogen receptor beta and oestrogen-induced attenuation of cytochrome c oxidase subunit I expression in human periodontal ligament cells Arch. Oral Biol. 52 2007 669 676 (Pubitemid 46678944)
87. K.A. Mattingly, M.M. Ivanova, K.A. Riggs, N.S. Wickramasinghe, M.J. Barch, and C.M. Klinge Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis Mol. Endocrinol. 22 2008 609 622 (Pubitemid 351397789)
88. J.Q. Chen, T.R. Brown, and J. Russo Regulation of energy metabolism pathways by estrogens and estrogenic chemicals and potential implications in obesity associated with increased exposure to endocrine disruptors Biochim. Biophys. Acta 1793 2009 1128 1143
89. S. Johann, M. Dahm, M. Kipp, C. Beyer, and S. Arnold Oestrogen regulates mitochondrial respiratory chain enzyme transcription in the mouse spinal cord J. Neuroendocrinol. 22 2010 926 935
90. C. Stirone, S.P. Duckles, D.N. Krause, and V. Procaccio Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels Mol. Pharmacol. 68 2005 959 965 (Pubitemid 41345787)
91. T. Kanki, K. Ohgaki, M. Gaspari, C.M. Gustafsson, A. Fukuoh, N. Sasaki, N. Hamasaki, and D. Kang Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA Mol. Cell. Biol. 24 2004 9823 9834 (Pubitemid 39458810)
92. C. Demonacos, R. Djordjevic-Markovic, N. Tsawdaroglou, and C.E. Sekeris The mitochondrion as a primary site of action of glucocorticoids: the interaction of the glucocorticoid receptor with mitochondrial DNA sequences showing partial similarity to the nuclear glucocorticoid responsive elements J. Steroid Biochem. Mol. Biol. 55 1995 43 55
93. C.E. Sekeris The mitochondrial genome: a possible primary site of action of steroid hormones In Vivo 4 1990 317 320
94. R. O'Lone, K. Knorr, I.Z. Jaffe, M.E. Schaffer, P.G. Martini, R.H. Karas, J. Bienkowska, M.E. Mendelsohn, and U. Hansen Estrogen receptors alpha and beta mediate distinct pathways of vascular gene expression, including genes involved in mitochondrial electron transport and generation of reactive oxygen species Mol. Endocrinol. 21 2007 1281 1296 (Pubitemid 46991958)
95. C.J. Thompson, N.N. Tam, J.M. Joyce, I. Leav, and S.M. Ho Gene expression profiling of testosterone and estradiol-17 beta-induced prostatic dysplasia in Noble rats and response to the antiestrogen ICI 182,780 Endocrinology 143 2002 2093 2105 (Pubitemid 34521557)
96. J.W. Simpkins, K.D. Yi, S.H. Yang, and J.A. Dykens Mitochondrial mechanisms of estrogen neuroprotection Biochim. Biophys. Acta 1800 2010 1113 1120
97. C. Borras, J. Gambini, M.C. Gomez-Cabrera, J. Sastre, F.V. Pallardó, G.E. Mann, and J. Viña 17beta-oestradiol up-regulates longevity-related, antioxidant enzyme expression via the ERK1 and ERK2[MAPK]/NFkappaB cascade Aging Cell 4 2005 113 118 (Pubitemid 41602744)
98. A. Razmara, S.P. Duckles, D.N. Krause, and V. Procaccio Estrogen suppresses brain mitochondrial oxidative stress in female and male rats Brain Res. 1176 2007 71 81 (Pubitemid 47553127)
99. X. Wang, J.W. Simpkins, J.A. Dykens, and P.R. Cammarata Oxidative damage to human lens epithelial cells in culture: estrogen protection of mitochondrial potential, ATP, and cell viability Invest. Ophthalmol. Vis. Sci. 44 2003 2067 2075 (Pubitemid 36520301)
100. A. Giddabasappa, M. Bauler, M. Yepuru, E. Chaum, J.T. Dalton, and J. Eswaraka 17-β estradiol protects ARPE-19 cells from oxidative stress through estrogen receptor-β Invest. Ophthalmol. Vis. Sci. 51 2010 5278 5287
101. A. Razmara, L. Sunday, C. Stirone, X.B. Wang, D.N. Krause, S.P. Duckles, and V. Procaccio Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain endothelial cells J. Pharmacol. Exp. Ther. 325 2008 782 790 (Pubitemid 351724313)