17β-Estradiol prevents cell death and mitochondrial dysfunction by an estrogen receptor-dependent mechanism in astrocytes after oxygen-glucose deprivation/reperfusion

Free Radical Biology and Medicine

Volumn 52, Issue 11-12, 2012, Pages 2151-2160

  Guo, Jiabin ^a,b,c   Duckles, Sue P ^a   Weiss, John H ^a   Li, Xuejun ^b   Krause, Diana N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PEKING UNIVERSITY   (China)

^c BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

Astrocyte; Estrogen; Free radicals; Ischemic injury; Mitochondria; Protection

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; GLUCOSE; LACTATE DEHYDROGENASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; CELL DEATH; CELL HYPOXIA; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ESTROGEN ACTIVITY; HORMONAL REGULATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; ASTROCYTES; CELLS, CULTURED; CYTOPROTECTION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GLUCOSE; L-LACTATE DEHYDROGENASE; MICE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; OXIDATIVE STRESS; PRIMARY CELL CULTURE; PYRAZOLES; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 84861414624     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.03.005     Document Type: Article

References (52)

1. S. Suzuki, C.M. Brown, and P.M. Wise Neuroprotective effects of estrogens following ischemic stroke Front. Neuroendocrinol. 30 2009 201 211
2. M. Liu, M.H. Kelley, P.S. Herson, and P.D. Hurn Neuroprotection of sex steroids Minerva Endocrinol. 35 2010 127 143
3. G.J. del Zoppo Stroke and neurovascular protection N. Engl. J. Med. 354 2006 553 555
4. E.H. Lo, T. Dalkara, and M.A. Moskowitz Mechanisms, challenges and opportunities in stroke Nat. Rev. Neurosci. 4 2003 399 415
5. Y. Persidsky, S.H. Ramirez, J. Haorah, and G.D. Kanmogne Blood-brain barrier: structural components and function under physiologic and pathologic conditions J. Neuroimmune Pharmacol. 1 2006 223 236
6. A.C. Yu, H.K. Wong, H.W. Yung, and L.T. Lau Ischemia-induced apoptosis in primary cultures of astrocytes Glia 35 2001 121 130
7. T. Takano, N. Oberheim, M.L. Cotrina, and M. Nedergaard Astrocytes and ischemic injury Stroke 40 2009 S8 S12
8. S. Guo, and E.H. Lo Dysfunctional cell-cell signaling in the neurovascular unit as a paradigm for central nervous system disease Stroke 40 2009 S4 S7
9. D.C. Wu, X.Q. Xiao, A.K. Ng, P.M. Chen, W. Chung, N.T. Lee, P.R. Carlier, Y.P. Pang, A.C. Yu, and Y.F. Han Protection against ischemic injury in primary cultured mouse astrocytes by bis(7)-tacrine, a novel acetylcholinesterase inhibitor [corrected] Neurosci. Lett. 288 2000 95 98
10. K.M. Dhandapani, and D.W. Brann Role of astrocytes in estrogen-mediated neuroprotection Exp. Gerontol. 42 2007 70 75
11. P. Micevych, G. Bondar, and J. Kuo Estrogen actions on neuroendocrine glia Neuroendocrinology 91 2010 211 222
12. M.A. Arevalo, M. Santos-Galindo, M.J. Bellini, I. Azcoitia, and L.M. Garcia-Segura Actions of estrogens on glial cells: implications for neuroprotection Biochim. Biophys. Acta 1800 2010 1106 1112
13. J.W. Gatson, J.W. Simpkins, K.D. Yi, A.H. Idris, J.P. Minei, and J.G. Wigginton Aromatase is increased in astrocytes in the presence of elevated pressure Endocrinology 152 2011 207 213
14. P.E. Micevych, V. Chaban, J. Ogi, P. Dewing, J.K. Lu, and K. Sinchak Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures Endocrinology 148 2007 782 789
15. K. Sinchak, R.H. Mills, L. Tao, P. LaPolt, J.K. Lu, and P. Micevych Estrogen induces de novo progesterone synthesis in astrocytes Dev. Neurosci. 25 2003 343 348
16. M.A. Sortino, M. Chisari, S. Merlo, C. Vancheri, M. Caruso, F. Nicoletti, P.L. Canonico, and A. Copani Glia mediate the neuroprotective action of estradiol on β-amyloid-induced neuronal death Endocrinology 145 2004 5080 5086
17. K.M. Dhandapani, F.M. Wade, V.B. Mahesh, and D.W. Brann Astrocyte-derived transforming growth factor-β mediates the neuroprotective effects of 17β-estradiol: involvement of nonclassical genomic signaling pathways Endocrinology 146 2005 2749 2759
18. M. Tomas-Camardiel, J.L. Venero, A.J. Herrera, R.M. De Pablos, J.A. Pintor-Toro, A. Machado, and J. Cano Blood-brain barrier disruption highly induces aquaporin-4 mRNA and protein in perivascular and parenchymal astrocytes: protective effect by estradiol treatment in ovariectomized animals J. Neurosci. Res. 80 2005 235 246
19. S.W. Rau, D.B. Dubal, M. Bottner, L.M. Gerhold, and P.M. Wise Estradiol attenuates programmed cell death after stroke-like injury J. Neurosci. 23 2003 11420 11426
20. D.B. Dubal, M.L. Kashon, L.C. Pettigrew, J.M. Ren, S.P. Finklestein, S.W. Rau, and P.M. Wise Estradiol protects against ischemic injury J. Cereb. Blood Flow Metab. 18 1998 1253 1258
21. M. Liu, P.D. Hurn, C.E. Roselli, and N.J. Alkayed Role of P450 aromatase in sex-specific astrocytic cell death J. Cereb. Blood Flow Metab. 27 2007 135 141
22. M.E. Wilson, D.B. Dubal, and P.M. Wise Estradiol protects against injury-induced cell death in cortical explant cultures: a role for estrogen receptors Brain Res. 873 2000 235 242
23. N. Sharifi, A.E. Reuss, and S. Wray Prenatal LHRH neurons in nasal explant cultures express estrogen receptor β transcript Endocrinology 143 2002 2503 2507
24. L. Fester, J. Prange-Kiel, H. Jarry, and G.M. Rune Estrogen synthesis in the hippocampus Cell Tissue Res. 345 2011 285 294
25. N.R. Sims, and H. Muyderman Mitochondria, oxidative metabolism and cell death in stroke Biochim. Biophys. Acta 1802 2010 80 91
26. J.W. Simpkins, and J.A. Dykens Mitochondrial mechanisms of estrogen neuroprotection Brain Res. Rev. 57 2008 421 430
27. S.P. Duckles, and D.N. Krause Cerebrovascular effects of oestrogen: multiplicity of action Clin. Exp. Pharmacol. Physiol. 34 2007 801 808
28. S.P. Duckles, D.N. Krause, C. Stirone, and V. Procaccio Estrogen and mitochondria: a new paradigm for vascular protection? Mol. Interv. 6 2006 26 35
29. 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 α in brain endothelial cells J. Pharmacol. Exp. Ther. 325 2008 782 790
30. 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
31. 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
32. 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
33. 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
34. 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
35. M.A. Zorrilla Zubilete, L.R. Guelman, D.G. Maur, L.G. Caceres, H. Rios, L.M. Zieher, and A.M. Genaro Partial neuroprotection by 17-β-estradiol in neonatal γ-irradiated rat cerebellum Neurochem. Int. 58 2011 273 280
36. B. Gabryel, A. Pudelko, and A. Malecki Erk1/2 and Akt kinases are involved in the protective effect of aniracetam in astrocytes subjected to simulated ischemia in vitro Eur. J. Pharmacol. 494 2004 111 120
37. K. Rasakham, and L.Y. Liu-Chen Sex differences in κ opioid pharmacology Life Sci. 88 2011 2 16
38. R.G. Giffard, and R.A. Swanson Ischemia-induced programmed cell death in astrocytes Glia 50 2005 299 306
39. V.M. Miller, and S.P. Duckles Vascular actions of estrogens: functional implications Pharmacol. Rev. 60 2008 210 241
40. V.V. Chaban, A.J. Lakhter, and P. Micevych A membrane estrogen receptor mediates intracellular calcium release in astrocytes Endocrinology 145 2004 3788 3795
41. W.R. Harrington, S. Sheng, D.H. Barnett, L.N. Petz, J.A. Katzenellenbogen, and B.S. Katzenellenbogen Activities of estrogen receptor α- and β-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression Mol. Cell. Endocrinol. 206 2003 13 22
42. L.A. Voloboueva, M. Duan, Y. Ouyang, J.F. Emery, C. Stoy, and R.G. Giffard Overexpression of mitochondrial Hsp70/Hsp75 protects astrocytes against ischemic injury in vitro J. Cereb. Blood Flow Metab. 28 2008 1009 1016
43. D.J. Stone, Y. Song, C.P. Anderson, K.K. Krohn, C.E. Finch, and I. Rozovsky Bidirectional transcription regulation of glial fibrillary acidic protein by estradiol in vivo and in vitro Endocrinology 139 1998 3202 3209
44. J. Wang, P.S. Green, and J.W. Simpkins Estradiol protects against ATP depletion, mitochondrial membrane potential decline and the generation of reactive oxygen species induced by 3-nitroproprionic acid in SK-N-SH human neuroblastoma cells J. Neurochem. 77 2001 804 811
45. S.D. Edmands, and A.C. Hall Role for metallothioneins-I/II in isoflurane preconditioning of primary murine neuronal cultures Anesthesiology 110 2009 538 547
46. Z. Feng, and J.T. Zhang Long-term melatonin or 17β-estradiol supplementation alleviates oxidative stress in ovariectomized adult rats Free Radic. Biol. Med. 39 2005 195 204
47. L. Prokai, K. Prokai-Tatrai, P. Perjesi, A.D. Zharikova, E.J. Perez, R. Liu, and J.W. Simpkins Quinol-based cyclic antioxidant mechanism in estrogen neuroprotection Proc. Natl. Acad. Sci. USA 100 2003 11741 11746
48. D.B. Dubal, S.W. Rau, P.J. Shughrue, H. Zhu, J. Yu, A.B. Cashion, S. Suzuki, L.M. Gerhold, M.B. Bottner, S.B. Dubal, I. Merchanthaler, M.S. Kindy, and P.M. Wise Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERα in estradiol-mediated protection against delayed cell death Endocrinology 147 2006 3076 3084
49. S. Suzuki, C.M. Brown, C.D. Dela Cruz, E. Yang, D.A. Bridwell, and P.M. Wise Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions Proc. Natl. Acad. Sci. USA 104 2007 6013 6018
50. D.B. Dubal, H. Zhu, J. Yu, S.W. Rau, P.J. Shughrue, I. Merchenthaler, M.S. Kindy, and P.M. Wise Estrogen receptor α, not β, is a critical link in estradiol-mediated protection against brain injury Proc. Natl. Acad. Sci. USA 98 2001 1952 1957
51. M.D. Al-Bader, S.A. Malatiali, and Z.B. Redzic Expression of estrogen receptor α and β in rat astrocytes in primary culture: effects of hypoxia and glucose deprivation Physiol. Res. 60 2011 951 960
52. J. Kuo, N. Hamid, G. Bondar, E.R. Prossnitz, and P. Micevych Membrane estrogen receptors stimulate intracellular calcium release and progesterone synthesis in hypothalamic astrocytes J. Neurosci. 30 2010 12950 12957