Neuroprotection by estrogen in the brain: The mitochondrial compartment as presumed therapeutic target

Journal of Neurochemistry

Volumn 110, Issue 1, 2009, Pages 1-11

  Arnold, Susanne ^a   Beyer, Cordian ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Astroglia; Estrogen; Mitochondria; Neurodegeneration; Neuroprotection; Reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATE; ESTROGEN; GROWTH FACTOR; REACTIVE OXYGEN METABOLITE; SEX HORMONE;

APOPTOSIS; BRAIN DEGENERATION; BRAIN MITOCHONDRION; CELL SURVIVAL; DRUG TARGETING; HUMAN; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BRAIN; CYTOPROTECTION; ENERGY METABOLISM; ESTROGENS; HUMANS; MITOCHONDRIA; NERVE GROWTH FACTORS; NEUROPROTECTIVE AGENTS; SIGNAL TRANSDUCTION;

EID: 67449116583     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06133.x     Document Type: Review

References (134)

1. Adams M. M., Fink S. E., Shah R. A. et al. (2002) Estrogen and aging affect the sub cellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J. Neurosci. 22, 3014 3608.
2. Alkayed N. J., Harukuni I., Kimes A. S. et al. (1998) Gender-linked brain injury in experimental stroke. Stroke 29, 159 166. (Pubitemid 28046959)
3. Amantea D., Russo R., Bagetta G. et al. (2005) From clinical evidence to molecular mechanisms underlying neuroprotection afforded by estrogens. Pharmacol. Res. 52, 119 132. (Pubitemid 40828362)
4. Araujo G. W., Beyer C. Arnold S. (2008) Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes. J. Neuroendocrinol. 20, 930 941. (Pubitemid 351859111)
5. Arnold S., Wright-Araujo G. Beyer C. (2008) Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones. J. Mol. Endocrinol. 41, 289 300.
6. Beal M. F. Ferrante R. J. (2004) Experimental therapeutics in transgenic mouse models of Huntington's disease. Nat. Rev. Neurosci. 5, 373 384. (Pubitemid 38568498)
7. Behl C. (2002) Oestrogen as a neuroprotective hormone. Nat. Rev. Neurosci. 3, 433 442. (Pubitemid 135711799)
8. Berry C., Brosnan M. J., Fennell J. et al. (2001) Oxidative stress and vascular damage in hypertension. Curr. Opin. Nephrol. Hypertens. 10, 247 255. (Pubitemid 32221768)
9. Bettini E. Maggi A. (1992) Estrogen induction of cytochrome c oxidase subunit II in rat hippocampus. J. Neurochem. 58, 1923 1929.
10. Beyer C., Reisert I. Pilgrim C. (1991) Dopamine content and metabolism in mesencephalic and diencephalic cultures: sex differences and effects of sex steroids. J. Neurosci. 11, 1325 1333.
11. Beyer C., Pawlak J., Brito V. et al. (2003a) Regulation of gene expression in the developing midbrain by estrogen. Ann. NY Acad. Sci. 1007, 17 28.
12. Beyer C., Pawlak J. Karolczak M. (2003b) Membrane receptors for oestrogen in the brain. J. Neurochem. 87, 545 550. (Pubitemid 37310621)
13. G93A in astrocytes induces functional deficits in motoneuron mitochondria. J. Neurochem. 107, 1271 1283.
14. Bonilla E., Tanji K., Hirano M. et al. (1999) Mitochondrial involvement in Alzheimer's disease. Biochim. Biophys. Acta 1410, 171 182. (Pubitemid 29078603)
15. Borras C., Gambini J. Vina J. (2007) Mitochondrial oxidant generation is involved in determining why females live longer than males. Front. Biosci. 12, 1008 1023.
16. Bosetti F., Frizzi F., Barogi S. et al. (2002) Cytochrome c oxidase and mitochondrial F1F0-ATPase (ATP synthase) activities in platelets and brain from patients with Alzheimer's disease. Neurobiol. Aging 23, 37 376.
17. Brinton R. D. (2008) The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci. 31, 529 537.
18. Browne S. E., Bowling A. C., Baik M. J. et al. (1998) Metabolic dysfunction in familial, but not sporadic, amyotrophic lateral sclerosis. J. Neurochem. 71, 281 287. (Pubitemid 28292560)
19. Bryant D. N., Sheldahl L. C., Marriott L. K. et al. (2006) Multiple pathways transmit neuroprotective effects of gonadal steroids. Endocr. 29, 199 207. (Pubitemid 44097363)
20. Burris T. P. Krishnan V. (2005) Estrogen: a mitochondrial energizer that keeps on going. Mol. Pharmacol. 68, 956 958. (Pubitemid 41345786)
21. Cahill L. (2006) Why sex matters for neuroscience. Nat. Rev. Neurosci. 7, 477 484. (Pubitemid 44012287)
22. Cardona-Gomez G. P., Mendez P., DonCarlos L. L. et al. (2001) Interactions of estrogens and insulin-like growth factor-I in the brain: implications for neuroprotection. Brain Res. Rev. 37, 320 334. (Pubitemid 34020742)
23. Casadesus G., Webber K. M., Atwood C. S. et al. (2006) Lutenizing hormone modulates cognition and amyloid-beta deposition in Alzheimer APP transgenic mice. Biochim. Biophys. Acta 1762, 447 452. (Pubitemid 43344306)
24. Casadesus G., Milliken E. L., Webber K. M. et al. (2007) Increases in luteinizing hormone are associated with declines in cognitive performance. Mol. Cell. Endocrinol. 269, 107 111. (Pubitemid 46483837)
25. Chaturvedi R. K. Beal M. F. (2008) Mitochondrial approaches for neuroprotection. Ann. NY Acad. Sci. 1147, 395 412.
26. Chen H. Chan D. C. (2005) Emerging functions of mammalian mitochondrial fusion and fission. Hum. Mol. Genet. 14, R283 R289.
27. Chen H., Detmer S. A., Ewald A. J. et al. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160, 189 200. (Pubitemid 36254953)
28. Chen J. Q., Delannoy M., Cooke C. et al. (2004) Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells. Am. J. Physiol. Endocrinol. Metab. 286, E1011 E1022.
29. Chen J.-Q., Yager J. D. Russo J. (2005) Regulation of mitochondrial chain structure and function by estrogens/estrogen receptors and potential physiological/pathophysiological implications. Biochem. Biophys. Acta 1746, 1 17. (Pubitemid 41484081)
30. Chen J. Q., Russo P. A., Cooke C. et al. (2007) 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. Biochem. Biophys. Acta 1773, 1732 1746. (Pubitemid 350191975)
31. Chiueh C., Lee S., Andoh D. et al. (2003) Induction of anti-oxidative and antiapoptotic thioredoxin supports neuroprotective hypothesis of estrogen. Endocrine 21, 27 31. (Pubitemid 36677340)
32. Cyr M., Calon F., Morissette M. et al. (2000) Drugs with estrogen-like potency and brain activity: potential therapeutic application for the CNS. Curr. Pharm. Des. 6, 1287 1312. (Pubitemid 30604736)
33. Dubal D. B., Kashon M. L., Pettigrew J. M. et al. (1998) Estradiol protects against ischemic injury. J. Cereb. Blood Flow Metab. 18, 1253 1258. (Pubitemid 28509840)
34. Dubal D. B., Zhu H., Yu J. et al. (2001) Estrogen receptor alpha, not eta, is a critical link in estradiol-mediated protection against injury. Proc. Natl Acad. Sci. USA 98, 1952 1957. (Pubitemid 32165604)
35. Duckles S. P. Krause D. N. (2007) Cerebrovascular effects of oestrogen: multiplicity of action. Clin. Exp. Pharmacol. Physiol. 34, 801 808. (Pubitemid 47013501)
36. Duckles S. P., Krause D. N., Stirone C. et al. (2006) Estrogen and mitochondria: a new paradigm for vascular protection? Mol. Interv. 6, 26 35. (Pubitemid 43327520)
37. Fan L., Pandey S. C. Cohen R. S. (2008) Estrogen affects levels of Bcl-2 protein and mRNA in medial amygdala of ovariectomized rats. J. Neurosci. Res. 86, 3655 3664.
38. Felty Q. Roy D. (2005) Estrogen, mitochondria, and growth of cancer and non-cancer cells. J. Carciogenesis 4, 1 18.
39. Felty Q., Xiong W. C., Sun D. et al. (2005) Estrogen-induced mitochondrial reactive oxygen species as signal-transduction messenger. Biochemistry 44, 6900 6909. (Pubitemid 40632408)
40. Flynn J. M., Dimitrijevich S. D., Younes M. et al. (2008) Role of wild-type estrogen receptor-beta in mitochondrial cytoprotection of cultured normal male and female human lens epithelial cells. Am. J. Physiol. Endocrinol. Metab. 295, E637 E647.
41. Fried G., Andersson E., Csöregh L. et al. (2004) Estrogen receptor beta is expressed in human embryonic brain cells and is regulated by 17beta-estradiol. Eur. J. Neurosci. 20, 2345 2354. (Pubitemid 39472397)
42. Fukui H. Moraes C. T. (2008) The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci. 31, 251 256.
43. Galea L. A. (2008) Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res. Rev. 57, 332 341.
44. Gillies G. E., Murray H. E., Dexter D. et al. (2004) Sex dimorphisms in the neuroprotective effects of estrogen in an animal model of Parkinson's disease. Pharmacol. Biochem. Behav. 78, 513 522. (Pubitemid 38906665)
45. Gonzalez Deniselle M. C., Gonzalez S. L. De Nicola A. F. (2001) Cellular basis of steroid neuroprotection in the wobber mouse, a genetic model of motoneuron disease. Cell. Mol. Neurobiol. 21, 237 254. (Pubitemid 32852778)
46. Gordon K. B., Macrae I. M. Carswell V. O. (2005) Effects of 17β-oestradiol on cerebral ischemic damage and lipid peroxidation. Brain Res. 108, 155 162. (Pubitemid 40255855)
47. Grossman A., Oppenheim J., Grondin G. et al. (1989) Immunocytochemical localization of the [3H]estradiol-binding protein in rat pancreatic acinar cells. Endocrinology 124, 2857 2866. (Pubitemid 19154119)
48. Hajszan T., Milner T. A. Leranth C. (2007) Sex steroids and the dentate gyrus. Prog. Brain Res. 163, 399 415.
49. Härtig S., Beyer C. Arnold S. (2006) Effect of hypoxia upon the transcription pattern of subunit isoforms and kinetics of cytochrome c oxidase in astrocytes and neurons. J. Neurochem. 99, 937 951. (Pubitemid 44583451)
50. Hatzoglou E. Sekeris C. E. (1997) The detection of nucleotide sequences with strong similarity to hormone responsive elements in the genome of eubacteria and archaebacteria and their possible relation to similar sequences present in the mitochondrial genome. J. Theor. Biol. 184, 339 344. (Pubitemid 27096276)
51. Herrick S. P., Waters E. M., Drake C. T. et al. (2006) Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Res. 1121, 46 58. (Pubitemid 44708881)
52. Hertzig S. Martinou J. C. (2008) Mitochondrial dynamics: to be in good shape to survive. Curr. Mol. Med. 8, 131 137.
53. Hirai K., Aliev G., Nunomura A. et al. (2001) Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci. 21, 3017 3023. (Pubitemid 32323483)
54. Honda K., Shimohama S., Sawada H. et al. (2001) Nongenomic antiapoptotic signal transduction by estrogen in cultured cortical neurons. J. Neurosci. Res. 64, 466 475. (Pubitemid 32521766)
55. Hurn P. D. Macrae I. M. (2000) Estrogen as neuroprotectant in stroke. J. Cereb. Blood Flow Metab. 20, 631 652. (Pubitemid 30217502)
56. Irwin R. W., Yao J., Hamilton R. T. et al. (2008) Progesterone and estrogen regulate oxidative metabolism in brain mitochondria. Endocrinology 149, 3167 3175. (Pubitemid 351724522)
57. Ivanova I., Mendez P., Garcia-Segura L. M. et al. (2002) Rapid stimulation of the PI3-kinase/Akt signalling pathway in developing midbrain neurones by oestrogen. J. Neuroendocrinol. 14, 73 79. (Pubitemid 34083073)
58. Kajta M., Trotter A., Lason W. et al. (2006) Impact of 17beta-estradiol on cytokine-mediated apoptotic effects in primary hippocampal and neocortical cell cultures. Brain Res. 1116, 64 74. (Pubitemid 44488596)
59. Karakaya S., Kipp M. Beyer C. (2007) Estrogen regulates the expression and activity of the dopamine transporter (DAT) in astrocytes of the nigrostriatal system. J. Neuroendocrinol. 19, 682 690. (Pubitemid 47386542)
60. Karbowski M., Norris K. L., Cleland M. M. et al. (2006) Role of Bax and Bak in mitochondrial morphogenesis. Nature 44, 658 662. (Pubitemid 44564703)
61. Kipp K., Karakaya S., Pawlak J. et al. (2006) 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, 376 390. (Pubitemid 44738014)
62. Kipp M., Karakaya S., Johann S. et al. (2007) Oestrogen and progesterone reduce expression of LPS-stimulated TNF-alpha and interleukin-18 in mesencephalic and cortical astrocytes. J. Neuroendocrinol. 19, 819 822. (Pubitemid 47386883)
63. Klinge C. M. (2008) Estrogenic control of mitochondrial function and biogenesis. J. Cell. Biochem. 105, 1342 1351.
64. Knott A. B., Perkins G., Schwarzenbacher R. et al. (2008) Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 9, 505 518. (Pubitemid 351873464)
65. Küppers E., Ivanova T. Karolczak M. (2001) Classical and non-classical estrogen action in the developing midbrain. Horm. Behav. 40, 196 202. (Pubitemid 32846352)
66. Langston J. W., Ballard P., Tetrud J. W. et al. (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219, 979 980. (Pubitemid 13189531)
67. Lee S. Y., Andoh T., Murphy D. L. et al. (2003) 17beta-estradiol activates ICI 182,780-sensitive estrogen receptors and cyclic GMP-dependent thioredoxin expression for neuroprotection. FASEB J. 17, 947 948.
68. Lee Y. L., Jeong S. Y., Marbowski M. et al. (2004) Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and OPA1 in apoptosis. Mol. Cell. Biol. 2004, 5001 5011.
69. Lobaton C. D., Vay L., Hernandez-Sanmigual E. et al. (2005) Modulation of mitochondrial Ca(2+) uptake by estrogen receptor agonists and antagonists. Br. J. Pharmacol. 145, 862 871. (Pubitemid 41129007)
70. Mahad D., Lassmann H. Turnbull D. (2008) Review: Mitochondria and disease progression in multiple sclerosis. Neuropathol. Appl. Neurobiol. 34, 577 589.
71. Mahesh V. B., Dhandapani K. M. Brann D. W. (2006) Role of astrocytes in reproduction and neuroprotection. Mol. Cell. Endocrinol. 246, 1 9. (Pubitemid 43238391)
72. Mancuso M., Orsucci D., Siciliano G. Murri L. (2008) Mitochondria, mitochondrial DNA and Alzheimer's disease. What comes first? Curr. Alzheimer Res. 5, 457 468.
73. Mattingly K. A., Ivanova M. M., Riggs K. A. et al. (2008) Estradiol stimulates transcription of nuclear regulatory factor-1 and increases mitochondrial biogenesis. Mol. Endocrinol. 22, 609 622.
74. Milner T. A., Ayoola K., Drake C. T. et al. (2005) Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 491, 81 95. (Pubitemid 41263413)
75. Milner T. A., Lubbers L. S., Alves S. E. et al. (2008) Nuclear and extranuclear estrogen binding sites in the rat forebrain and autonomic medullary areas. Endocrinology 149, 3306 3312. (Pubitemid 351919599)
76. Moats R. K. Ramirez V. D. (1998) Rapid uptake and binding of estradiol-17beta6-(O-carboxymethyl)oxime:125-labeled BSA by female rat liver. Biol. Reprod. 58, 531 538. (Pubitemid 28099121)
77. Monje P. Bolard R. (2001) Subcellular distribution of native estrogen receptor alpha and beta isoforms in rabbit uterus and ovary. J. Cell. Biochem. 82, 467 479. (Pubitemid 32729410)
78. Morale M. C., Serra P. A., L′Episcopo F. et al. (2006) Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience 138, 869 878. (Pubitemid 43306827)
79. Nilsen J. (2008) Estradiol and neurodegenerative oxidative stress. Front. Neuroendocrinol. 29, 463 475.
80. Nilsen J. Brinton D. W. (2004) Mitochondria as therapeutic targets of estrogen action in the central nervous system. Curr. Drug Targets CNS Neurol. Disord. 3, 297 313. (Pubitemid 39242916)
81. Pawlak J., Karolczak M., Krust A. et al. (2005) Estrogen receptor-alpha is associated with the plasma membrane of astrocytes and coupled to the MAP/Src-kinase pathway. Glia 50, 270 275. (Pubitemid 40769856)
82. Peri A. Serio M. (2008) Neuroprotective effects of the Alzheimer's disease-related gene seladin-1. J. Mol. Endocrinol. 41, 251 261.
83. Pozzi S., Benedusi V., Maggi A. et al. (2006) Estrogen action in neuroprotection and brain inflammation. Ann. NY Acad. Sci. 1089, 302 323. (Pubitemid 47092090)
84. Raz L., Khan M. M., Mahesh V. B. et al. (2008) Rapid estrogen signaling in the brain. Neurosignals 16, 140 153. (Pubitemid 351263221)
85. Razmara A., Duckles S. P., Krause D. N. et al. (2007) Estrogen suppresses brain mitochondrial oxidative stress in female and male rats. Brain Res. 1176, 71 81. (Pubitemid 47553127)
86. Razmara A., Sunday L., Stirone C. et al. (2008) Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain endothelial cells. J. Pharmacol. Exp. Ther. 352, 782 790. (Pubitemid 351724313)
87. Reddy P. H. Beal M. F. (2005) Are mitochondria critical in the pathogenesis of Alzheimer's disease? Brain Res. Rev. 49, 618 632. (Pubitemid 41546661)
88. Reddy P. H. Beal M. F. (2008) Amyloid beta, mitochondrial dysfunction and synaptic damage: implication for cognitive decline in aging and Alzheimer's disease. Trends Mol. Med. 14, 45 53.
89. Rodríguez-Navarro J. A., Solano R. M., Casarejos M. J. et al. (2008) Gender differences and estrogen effects in parkin null mice. J. Neurochem. 106, 2143 2157.
90. Santel A. Fuller M. T. (2001) Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114, 2763 2774.
91. Sayre L. M., Smith M. A. Perry G. (2001) Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr. Med. Chem. 8, 721 738. (Pubitemid 32427903)
92. Schapira A. H. (2008) Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol. 7, 97 109. (Pubitemid 350251942)
93. Schmidt A. J., Krieg J. C. Vedder H. (2002) Differential effects of glucocorticoids and gonadal steroids on glutathione levels in neuronal and glial systems. J. Neurosci. Res. 67, 544 550. (Pubitemid 34117124)
94. Schreiber S. N., Emter R., Hock M. B. et al. (2004) The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc. Natl Acad. Sci. USA 101, 6472 6477. (Pubitemid 38585998)
95. Schumacher M., Guennoun R., Stein D. G. De Nicola A. F. (2007) Progesterone: therapeutic opportunities for neuroprotection and myelin repair. Pharmacol. Ther. 116, 77 106. (Pubitemid 47398920)
96. Sharma K. Mehra R. D. (2008) Long-term administration of estrogen or tamoxifen to ovariectomized rats affords neuroprotection to hippocampal neurons by modulating the expression of Bcl-2 and Bax. Brain Res. 14, 1204.
97. Shulman L. M. (2007) Gender differences in Parkinson's disease. Gend. Med. 4, 8 18. (Pubitemid 46917063)
98. Sicotte N. L., Liva S. M., Klutch R. et al. (2002) Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann. Neurol. 52, 421 428.
99. Simpkins J. W. Dykens J. A. (2008) Mitochondrial mechanisms of estrogen neuroprotection. Brain Res. Rev. 57, 421 430.
100. Simpkins J. W. Singh M. (2008) More than a decade of estrogen neuroprotection. Alzheimers Dement. 4, S131 S136.
101. Simpkins J. W., Rajakumar G., Zhang Y. Q. et al. (1997) Estrogen may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J. Neurosurg. 87, 724 730. (Pubitemid 27454591)
102. Simpkins J. W., Wang J., Wang X. et al. (2005) Mitochondria play a central role in estrogen-induced neuroprotection. Curr. Drug Tragets CNS Neurol. Disord. 4, 69 83. (Pubitemid 41403316)
103. Simpkins J. W., Yang S. H., Sarkar S. N. et al. (2008) Estrogen actions on mitochondria-physiological and pathological implications. Mol. Cell. Endocrinol. 290, 51 59.
104. Singh M., Dykens J. A. Simpkins J. W. (2006) Novel mechanisms for estrogen-induced neuroprotection. Exp. Biol. Med. 231, 514 521.
105. Singh S., Misiak M., Beyer C. et al. (2009) Cytochrome c oxidase isoform IV-2 is involved in 3-nitroproprionic acid-induced toxicity in striatal astrocytes. Glia (in press).
106. Sojanowski D., Koutsopoulos O. S., Okamoto K. et al. (2004) Levels of human Fis1 at the mitochondrial outer membrane regulates mitochondrial morphology. J. Cell Sci. 117, 1201 1210. (Pubitemid 38456101)
107. Stirone C., Duckles S. P., Krause D. N. et al. (2005) Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol. Pharmacol. 68, 956 959.
108. Sugioka R., Shimizu S. Tsujimoto Y. (2004) Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J. Biol. Chem. 279, 52726 52734. (Pubitemid 39656648)
109. Sullivan P. G., Rabchevsky A. G., Waldmeier P. C. et al. (2005) Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J. Neurosci. Res. 79, 231 239. (Pubitemid 40116440)
110. Swerdlow R. H. Khan S. M. (2004) A "mitochondrial cascade hypothesis" for sporadic Alzheimer's disease. Med. Hypotheses 63, 8 20. (Pubitemid 38887104)
111. Szewczyk A. Wojtczak L. (2002) Mitochondria as a pharmacological target. Pharmacol. Rev. 54, 101 127. (Pubitemid 34211027)
112. Tresguerres J. A., Kireev R., Tresguerres A. F. et al. (2008) Molecular mechanism involved in the hormonal prevention of aging in rat. J. Steroid Biochem. Mol. Biol. 108, 318 326. (Pubitemid 351179643)
113. Trotter A., Bokelmann B., Sorgo W. et al. (2001) Follow-up examination at the age of 15 months of extremely preterm infants after postnatal estradiol and progesterone replacement. J. Clin. Endocrinol. Metab. 86, 601 603. (Pubitemid 32207465)
114. Trotter A., Ebsen M., Kiossis E. et al. (2006) Prenatal estrogen and progesterone deprivation impairs alveolar formation and fluid clearance. Pediatric Res. 60, 60 64. (Pubitemid 44297614)
115. Van Itallie C. M. Dannies P. S. (1988) Estrogen induces accumulation of the mitochondrial ribonucleic acid for subunit II of cytochrome oxidase in pituitary tumor cells. Mol. Endocrinol. 2, 332 337. (Pubitemid 18125027)
116. Vanlangenakker N., Berghe T. R. V., Krysko D. V. et al. (2008) Molecular mechanisms and pathophysiology of necrotic cell death. Curr. Mol. Med. 8, 207 220. (Pubitemid 351982539)
117. Vedder H., Anthes N., Stumm G. et al. (1999) Estrogen hormones reduce lipid peroxidation in cells and tissues of the central nervous system. J. Neurochem. 72, 2531 2538. (Pubitemid 29242205)
118. Vegeto E., Benedusi V. Maggi A. (2008) Estrogen-anti-inflammatory activity in brain: a therapeutic opportunity for menopause and neurodegenerative diseases. Front. Neuroendocrinol. 29, 507 519.
119. Vic P., Vignon F., Derocq D. Rochefort H. (1982) Effect of estradiol on the ultrastructure of the MCF7 human breast cancer cells in culture. Cancer Res. 42, 667 673. (Pubitemid 12173611)
120. Wang L., Andersson S., Warner M. et al. (2001) Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc. Natl Acad. Sci. USA 98, 2792 2796. (Pubitemid 32209562)
121. Wang X., Su B., Fujioka H. Zhu X. (2008a) Dynamin-like protein 1 reduction underlies mitochondrial morphology and distribution abnormalities in fibroblasts from sporadic Alzheimer's disease patients. Am. J. Pathol. 173, 470 482.
122. Wang X., Su B., Siedlak S. L., Moreira P. I., Fujioka H., Wang Y., Casadesus G. Zhu X. (2008b) Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fusion/fission proteins. Proc. Natl Acad. Sci. USA 105, 19318 19323.
123. Watanabe T., Inoue S., Hiroi H. et al. (1998) Isolation of estrogen-responsive genes with a CpG island library. Mol. Cell. Biol. 18, 442 449. (Pubitemid 28021055)
124. Webber K. M., Casadesus G., Marlatt M. W. et al. (2005) Estrogen bows to a new master: the role of gonadotropins in Alzheimer's pathogenesis. Ann. N.Y. Acad. Sci. USA 1052, 201 209. (Pubitemid 41338970)
125. Woolley C. S. (2007) Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 47, 657 680. (Pubitemid 46272142)
126. Yaffe M. P. (1999) The machinery of mitochondrial inheritance and behavior. Science 283, 1493 1497.
127. Yang S. H., Shi J., Day A. L. et al. (2000) Estradiol exerts neuroprotective effects when administered after ischemic insult. Stroke 31, 745 749.
128. Yang S. H., Liu R., Perez E. J. et al. (2004) Mitochondrial localization of estrogen receptor beta. Proc. Natl Acad. Sci. USA 101, 4130 4135. (Pubitemid 38410620)
129. Yang S. H., Sarkar S. N., Liu R. et al. (2009) Estrogen receptor beta as mitochondrial vulnerability factor. J. Biol. Chem. 284, 9540 9548.
130. Yune T. Y., Park H. G., Lee J. Y. et al. (2008) Estrogen-induced Bcl-2 expression after spinal cord injury is mediated through phosphoinositide-3- kinase/Akt-dependent CREB activation. J. Neurotrauma 25, 1121 1131.
131. Zeviani M. Carelli V. (2007) Mitochondrial disorders. Curr. Opin. Neurol. 20, 564 571. (Pubitemid 47462287)
132. Zhang Y. Bhavnani B. R. (2005) Glutamate-induced apoptosis in primary cortical neurons is inhibited by equine estrogens via down-regulation of caspase-3 and prevention of cytochrome c release. BMC Neurosci. 6, 13.
133. Zheng J. Ramirez V. D. (1999) Purification and identification of an estrogen binding protein from rat brain: oligomycin sensitive-conferring protein (OSCP), a subunit of mitochondrial FoF1-ATP synthase/ATPase. J. Steroid Biochem. Mol. Biol. 68, 65 75. (Pubitemid 29130387)
134. Zuchner S., Zappia I. V., Muglia M. et al. (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nature 36, 449 451. (Pubitemid 38620027)