17beta-estradiol protects oligodendrocytes from cytotoxicity induced cell death

Journal of Neurochemistry

Volumn 89, Issue 3, 2004, Pages 660-673

  Takao, Toshihiro ^a   Flint, Nicole ^b   Lee, Lan ^c   Ying, Xiaoyou ^d   Merrill, Jean ^c   Chandross, Karen J ^c  

^a KOCHI MEDICAL SCHOOL   (Japan)

^b Assistant Professor in the University Libraries   (United States)

^c SANOFI   (France)

^d DSE Division   (United States)

Author keywords

3 (4 morpholinyl) sydnonimine (SIN 1); CNS; Estrogen receptor; Immunocytochemistry; Nuclear hormone; RT PCR

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; LINSIDOMINE; MYELIN; PEROXYNITRITE;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL DEATH; CELL LINE; CELL MATURATION; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DEMYELINATING DISEASE; DOSE RESPONSE; IMMUNOCYTOCHEMISTRY; MYELINATION; NEUROPATHOLOGY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALIA;

EID: 2042454987     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02370.x     Document Type: Article

References (79)

1. Agrawal H. C., Clark H. B., Agrawal D., Seil F. J. and Quarles R. H. (1984) Identification of antibodies in anti-CNS and anti-PNS myelin sera by immunoblot, characterization by immunohistochemistry, and their effect in tissue culture. Brain Res. 46, 191-200.
2. Alkayed N. J., Goto S., Sugo N., Joh H. D., Klaus J., Crain B. J., Bernard O., Traystman R. J. and Hurn P. D. (2001) Estrogen and Bcl-2: gene induction and effect of transgene in experimental stroke. J. Neurosci. 21, 7543-7550.
3. Amiguet P., Fardinier M. V., Zanetta J. P. and Mattieu J. M. (1992) Purification and partial structural and functional characterization of mouse myelin/oligodendrocyte glycoprotein. J. Neurochem. 58, 1676-1682.
4. Bagasra O., Michaels F. H., Zheng Y. M., Bobroski L. E., Spitsin S. V., Fu Z. F., Tawadros R. and Koprowski H. (1995) Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc. Natl Acad. Sci. USA 92, 12041-12045.
5. Barbacanne M. A., Rami J., Michel J. B., Souchard J. P., Philippe M., Besombes J. P., Bayard F. and Arnal J. (1999) Estradiol increases rat aorta endothelium-derived relaxing factor (EDRF) activity without changes in endothelial NO synthase gene expression: possible role of decreased endothelium-derived superoxide anion production. Cardiovasc. Res. 41, 672-681.
6. Baulieu E. E. (1997) Neurosteroids: of the nervous system, by the nervous system, for the nervous system. Recent Prog. Horm. Res. 52, 1-32.
7. Behl C. and Holsboer F. (1999) The female sex hormone oestrogen as a neuroprotectant. Trends Pharmacol. Sci. 20, 441-444.
8. Behl C., Widmann M., Trapp T. and Holsboer F. (1995) 17-Estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem. Biophys. Res. Commun. 216, 473-482.
9. Beyer C., Ivanova T., Karolczak M. and Kuppers E. (2002) Cell type-specificity of nonclassical estrogen signaling in the developing midbrain. J. Steroid Biochem. Mol. Biol. 81, 319-325.
10. Burakov A., Wong C.-W., Rachez C., Cheskis B. and Freedman L. (2000) Functional interactions between the estrogen receptor and DRIP 205, a subunit of the heteromeric DRIP coactivator complex. J. Biol. Chem. 275, 20928-20934.
11. Callier S., Morissette M., Grandbois M., Pelaprat D. and Di Paolo T. (2001) Neuroprotective properties of 17beta-estradiol, progesterone, and raloxifene in MPTP C57B1/6 mice. Synapse 41, 131-138.
12. Cardona-Gómez, G. P., Mendez P., DonCarlos L. L., Azcoitia I. and Garcia-Segura L. M. (2003) Interactions of estrogen and insulin-like growth factor-1 in the brain: molecular mechanisms and functional implications. J. Steroid Biochem. Mol. Biol. 83, 211-217.
13. Carre J. L., Abalain J. H., Sarlieve L. L. and Floch H. H. (2001) Ontogeny of steroid metabolizing enzymes in rat oligodendrocytes. Steroid Biochem. Mol. Biol. 78, 89-95.
14. Chao T. C., Van Alten P. J., Greager J. A. and Walter R. J. (1995) Steroid sex hormones regulate the release of tumor necrosis factor by macrophages. Cell Immunol. 160, 43-49.
15. Compston A. and Coles A. (2002) Multiple Sclerosis. Lancet 359, 1221-1231.
16. Confavreux C., Hutchinson M., Hours M. M., Cotinovis-Tourniare P. and Moreau T. (1998) Rate of pregnancy-relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N. Engl. J. Med. 339, 285-291.
17. Curry J. J. and Heim L. M. (1966) Brain myelination after neonatal administration of oestradiol. Nature 209, 915-916.
18. Dashiell S. M., Tanner S. L., Pant H. C. and Quarles R. H. (2002) Myelin-associated glycoprotein modulates expression and phosphorylation of neuronal cytoskeletal elements and their associated kinases. J. Neurochem. 81, 1263-1272.
19. Dhandapani K. and Brann D. (2003) Neuroprotective effects of estrogen and tamoxifen in vitro: a facilitative role for glia? Endocrine 21, 59-66.
20. Duquette P., Pleines J., Girard M., Charest L., Senecal-Quevillon M. and Masse C. (1992) The increased susceptibility of women to multiple sclerosis. Can. J. Neurol. Sci. 19, 466-471.
21. Eisenbarth G. S., Walsh F. S. and Nirenberg M. (1979) Monoclonal antibody to a plasma membrane antigen of neurons. Proc. Natl Acad. Sci. USA 76, 4913-4917.
22. Fitzpatrick S. L., Funkhouser J. M., Sindoni D. M., Stevis P. E., Deecher D. C., Bapat A. R., Merchenthaler I. and Frail D. E. (1999) Expression of estrogen receptor-β protein in rodent ovary. Endocrinology 140, 2581-2591.
23. Friend K. E., Ang L. W. and Shupnik M. A. (1995) Estrogen regulates the expression of several different estrogen receptor mRNA isoforms in rat pituitary. Proc. Natl Acad. Sci. USA 92, 4367-4371.
24. Garcia-Segura L. M., Duenas M., Fernandez-Galaz M. C., Chowen J. A., Argente J., Naftolin F. and Torres-Aleman I. (1996) Interaction of the signalling pathways of insulin-like growth factor-I and sex steroids in the neuroendocrine hypothalamus. Horm. Res. 46, 160-164.
25. Garcia-Segura L. M., Azcoitia I. and DonCarlos L. L. (2001) Neuroprotection by estradiol. Prog. In Neurobiol. 63, 29-60.
26. Gibson U. E., Heid C. A. and Williams P. M. (1996) A novel method for real time quantitative RT-PCR. Genome Res. 6, 995-1001.
27. Goodman Y., Bruce A. J., Cheng B. and Mattson M. P. (1996) Estrogens attenuate and corticosterone exacerbates excytotoxicity, oxidative injury and amyloid-peptide toxicity in hippocampal neurons. J. Neurochem. 66, 1836-1844.
28. Green P. S., Bishop J. and Simpkins J. W. (1997) 17-Estradiol exerts neuroprotective effects on SK-N-SH cells. J. Neurosci. 17, 511-515.
29. Hu S. K., Mitcho Y. L. and Rath N. C. (1988) Effects oestradiol interleukin 1 synthesis by macrophages. Int. Immunol. 10, 247-252.
30. Ito A., Buenafe A. C., Matejuk A., Zamora A., Silverman M., Dwyer J., Vandenbark A. A. and Offner H. (2002) Estrogen inhibits systemic T cell expression of TNF-alpha and recruitment of TNF-alpha (+) T cells and macrophages into the CNS of mice developing experimental encephalomyelitis. Clin. Immunol. 102, 275-282.
31. Kakinoki R., Bishop A. T., Tu Y.-K. and Matsui N. (2002) Detection of the proliferated donor cells in bone grafts in rats, using PCR for a Y-chromosome-specific gene. J. Orthop. Sci. 7, 252-257.
32. Katzenellenbogen J. A., O'Malley B. W. and Katzenellenbogen B. S. (1996) Tripartite steroid hormone receptor pharmacology: interaction with multiple effector sites as a basis for the cell- and promoter specific action of these hormones. Mol. Endocrinol. 10, 119-131.
33. Kim S., Liva S. M., Dalal M. A., Verity M. A. and Voskuhl R. R. (1999) Estriol ameliorates autoimmune demyelinating disease: implications for Multiple Sclerosis. Neurology 52, 1230-1238.
34. Kousteni S., Bellido T., Plotkin L. I. et al. (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104, 719-730.
35. Kuiper G. G. J. M., Enmark E., Pelto-Huikko M., Nilsson S. and Gustafsson J.-A. (1996) Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl Acad. Sci. USA 93, 5925-5930.
36. Kuiper G. G. J. M., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S. and Gustafsson J.-A. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863-870.
37. Langer-Gould A., Garren H., Slansky A., Ruiz P. J. and Steinman L. (2002) Later pregnancy suppresses relapse in experimental autoimmune encehphalomyelitis: evidence for a suppressive pregnancy-related serum factor. J. Immunol. 169, 1084-1091.
38. Leclercq G. (2002) Molecular forms of the estrogen receptor in breast cancer. J. Steroid Biochem. Mol. Biol. 80, 259-272.
39. Lee S. J. and McEwen B. S. (2001) Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications. Annu. Rev. Pharmacol. Toxicol. 41, 569-591.
40. Liu J. S., Zhao M. L., Brosnan C. F. and Lee S. C. (2001) Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am. J. Pathol. 158, 2057-2066.
41. Mangelsdorf D., Thummel C., Beato M., Herrlich P., Schutz G., Umezono K., Blumberg B., Kastner P., Mark M. and Chambon P. (1995) The nuclear receptor superfamily: the second decade. Cell 83, 835-839.
42. Manthorpe P., Fagnani R., Skaper S. D. and Varon S. (1986) An automated colorimetric microassay for neuronotrophic factors. Dev. Brain Res. 25, 191-198.
43. McCarthy K. D. and de Veliis J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902.
44. Miranda R. C. and Toran-Allerand C. D. (1992) Developmental expression of estrogen receptor mRNA in the rat cerebral cortex: a nonisotopic in situ hybridization histochemistry study. Cereb. Cortex 2, 1-15.
45. Mitra S. W., Hoskin E., Yudkovitz J. et al. (2003) Immunolocalization of Estrogen Receptor beta in the Mouse Brain: Comparison with Estrogen Receptor alpha. Endocrinology 144, 2055-2067.
46. Mosselman S., Polman J. and Dijkema R. (1996) ERβ: identification and characterization of a novel human estrogen receptor. FEBS Lett. 392, 49-53.
47. Nathan L. and Chaudhuri G. (1997) Estrogens and atherosclerosis. Annu. Rev. Pharmacol. Toxicol. 37, 477-515.
48. Olsen N. J. and Kovacs W. J. (2002) Hormones, pregnancy, and rheumatoid arthritis. J. Gend. Specif. Med. 5, 28-37.
49. Orikasa C., Kondo Y., Hayashi S., McEwen B. S. and Sakuma Y. (2002) Sexually dimorphic expression of estrogen receptor β in the anteroventral periventricular nucleus of the rat preoptic area: Implication in luteinizing hormone surge. Proc. Natl Acad. Sci. USA 99, 3306-3311.
50. Perez-Martin M., Azcoitia I., Trejo J. L., Sierra A. and Garcia-Segura L. M. (2003) An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat. Eur. J. Neurosci. 18, 923-930.
51. Pi X., Zhang B., Li J. and Voogt J. L. (2003) Promoter usage and estrogen regulation of prolactin receptor gene in the brain of the female rat. Neuroendocrinology 77, 187-197.
52. Platania P., Laureanti F., Bellomo M., Giuffrida R., Giuffrida-Stella A. M., Catania M. V. and Sortino M. A. (2003) Differential expression of estrogen receptors alpha and beta in the spinal cord during postnatal development: localization in glial cells. Neuroendocrinology 77, 334-340.
53. Saji S., Sakaguchi H., Andersson S., Warner M. and Gustafsson J. A. (2001) Quantitative Analysis of Estrogen Receptor Proteins in Rat Mammary Gland. Endocrinology 142, 3177-3186.
54. Santagati S., Melcangi R. C., Celotti F., Martini L. and Maggi A. (1994) Estrogen receptor is expressed in different types of glial cells in culture. J. Neurochem. 63, 2058-2064.
55. Santeusanio G., Mauriello A., Ventura L., Liberati F., Colantoni A., Lasorella R. and Spagnoli L. G. (2000) Immunohistochemical analysis of estrogen receptors in breast carcinomas using monoclonal antibodies that recognize different domains of the receptor molecule. Appl. Immunohistochem. Mol. Morph. 8, 275-284.
56. Sar M. and Welsch F. (1999) Differential expression of estrogen receptor-beta and estrogen receptor-alpha in the rat ovary. Endocrinology 140, 963-971.
57. Scherer S. S., Braun P., Grinspan J., Collarini E., Wang D.-y. and Kamholz J. (1994) Differential regulation of the 2′,3′-cyclic nucleotide 3′-phosphodiesterase gene during oligodendrocyte development. Neuron 12, 1363-1375.
58. Schomberg D. W., Couse J. F., Mukherjee A., Lubahn D. B., Sar M., Mayo K. E. and Korach K. S. (1999) Targeted disruption of the estrogen receptor-alpha gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology 140, 2733-2744.
59. Scott G. S., Virag L., Szabo C. and Hooper D. C. (2003) Peroxynitrite-induced oligodendrocyte toxicity is not dependent on poly (ADP-ribose) polymerase activation. Glia 41, 105-116.
60. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J. C. and Weiss S. (2003) Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299, 117-120.
61. Sicotte N. L., Liva S. M., Klutch R., Pfieffer P., Bouvier S., Odesa S., Wu T. C. J. and Voskuhl R. R. (2002) Treatment of Multiple Sclerosis with pregnancy hormone estriol. Ann. Neurol. 52, 421-428.
62. Singer C. A., Rogers K. L., Strickland T. M. and Dorsa D. M. (1996) Estrogen protects primary cortical neurons from glutamate toxicity. Neurosci. Lett. 212, 13-16.
63. Singer C. A., Rogers K. L. and Dorsa D. M. (1998) Modulation of Bcl-2 expression: a potential component of estrogen protection in NT2 neurons. Neuroreport 9, 2565-2568.
64. Singer C. A., Figueroa-Masot X. A., Batchelor R. H. and Dorsa D. M. (1999) The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J. Neurosci. 19, 2455-2463.
65. Singh M., Setalo G., Guan X., Warren M. and Toran-Allerand C. D. (1999) Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: Convergence of estrogen and neurotrophin signaling pathways. J. Neurosci. 19, 1179-1188.
66. Stefano G. B., Prevot V., Beauvillain J. C., Fimiani C., Welters I., Cadet P., Breton C., Pestel J., Salzet M. and Bilfinger T. V. (1999) Estradiol coupling to human monocyte nitric oxide release is dependent on intracellular calcium transients: evidence for an estrogen surface receptor. J. Immunol. 163, 3758.
67. Thi A. D., Jung-Testas I. and Baulieu E.-E. (1998) Neuronal signals are required for estrogen-mediated induction of progesterone receptor in cultured rat Schwann cells. J. Steroid Biochem. Mol. Biol. 67, 201-211.
68. Toran-Allerand C. D., Guan X., MacLusky N. J., Horvath T. L., Diano S., Singh M., Connolly E. S. Jr, Nethrapalli I. S. and Tinnikov A. A. (2002) ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J. Neurosci. 22, 8391-8401.
69. Torreilles F., Salman-Tabcheh S., Guerin M. and Torreilles J. (1999) Neurodegenerative disorders: the role of peroxynitrite. Brain Res. Brain Res. Rev. 30, 153-163.
70. Tostes R. C., Nigro D., Fortes Z. B. and Carvalho M. H. (2003) Effects of estrogen on the vascular system. BraZ. J. Med. Biol. Res. 36, 1143-1158.
71. Touil T., Deloire-Grassin M. S. A., Vital C., Petry K. G. and Brochet B. (2001) In vivo damage of CNS myelin and axons induced by peroxynitrite. Neuroreport 12, 3637-3644.
72. Trackey J. L., Uliasz T. F. and Hewett S. J. (2001) Sin-1 induced cytotoxicity in mixed cortical cell culture: peroxynitrite-dependent and -independent induction of excitotoxic cell death. J. Neurochem. 79, 445-455.
73. van der Veen R. C. and Roberts L. J. (1999) Contrasting roles for nitric oxide and peroxynitrite in the peroxidation of myelin lipids. J. Neuroimmunol. 95, 1-7.
74. Wang L., Andersson S., Warner M. and Gustafsson J. A. (2003) Estrogen receptor (ER) beta knockout mice reveal a role for ERbeta in migration of cortical neurons in the developing brain. Proc. Natl Acad. Sci. USA 100, 703-708.
75. Watters J. J. and Dorsa D. M. (1998) Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms. J. Neurosci. 18, 6672-6680.
76. Weaver C. E., Park-Chung M., Gibbs T. T. and Farb D. H. (1997) 17beta-estradiol protects against NMDA-induced excitoxicity by direct inhibition of NMDA receptors. Brain Res. 761, 338-341.
77. Williams S., Leventhal C., Lemmon V., Nedgergaard M. and Goldman S. A. (1999) Estrogen Promotes the initial migration and inception of NgCAM-dependent calcium signaling by new neurons of the adult songbird brain. Mol. Cell Neurosci. 13, 41-55.
78. Xia S., Cai Z. Y., Thio L. L., Kim-Han J. S., Dugan L. L., Covey D. F. and Rothman S. M. (2002) The estrogen receptor is not essential for all estrogen neuroprotection: new evidence from a new analog. Neurobiol. Dis. 9, 282-293.
79. Zwain I. H. and Yen S. S. C. (1999) Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140, 3843-3852.