Estrogen prevents glutamate-induced apoptosis in C6 glioma cells by a receptor-mediated mechanism

Neuroscience

Volumn 137, Issue 1, 2006, Pages 197-209

  Sribnick, E A ^a   Ray, S K ^a   Banik, N L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Calcium; Calpain; Caspase; Estrogen receptor; Glia

Indexed keywords

1,3,5(10) ESTRATRIEN 3,17BETA DIOL 17 HEMISUCCINATE:BOVINE SERUM ALBUMIN; 17ALPHA ESTRADIOL; 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ANTIESTROGEN; BOVINE SERUM ALBUMIN; CALPAIN; CASPASE 3; CONJUGATED ESTROGEN; DNA FRAGMENT; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; FULVESTRANT; GLUTAMIC ACID; PROTEINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASSAY; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL LINE; CELL MEMBRANE; CELL PROTECTION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR CALCIUM; GLIOMA CELL; HYPOTHESIS; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CALCIUM; CALCIUM CHANNEL BLOCKERS; CELL LINE, TUMOR; CELL SURVIVAL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; GLIOMA; GLUTAMIC ACID; IN SITU NICK-END LABELING; NEUROPROTECTIVE AGENTS; RATS;

EID: 29744467003     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2005.08.074     Document Type: Article

References (79)

1. T. Amano, T. Yamakuni, N. Okabe, R. Kuwahara, F. Ozawa, F. Hishinuma Regulation of nerve growth factor and nerve growth factor receptor production by NMDA in C6 glioma cells Mol Brain Res 14 1992 35 42
2. 2+ channel modulation in the neuroprotective actions of estrogen in beta-amyloid protein and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) cytotoxic models Neurochem Int 45 2004 31 38
3. S. Bansil, H.J. Lee, S. Jindal, C.R. Holtz, S.D. Cook Correlation between sex hormones and magnetic resonance imaging lesions in multiple sclerosis Acta Neurologica Scandinavica 99 1999 91 94
4. H. Bayir, D.W. Marion, A.M. Puccio, S.R. Wisniewski, K.L. Janesko, R.S. Clark, P.M. Kochanek Marked gender effect on lipid peroxidation after severe traumatic brain injury in adult patients J Neurotrauma 21 2004 1 8
5. C. Behl, T. Skutella, F. Lezoualch, A. Post, M. Widmann, C.J. Newton, F. Holsboer Neuroprotection against oxidative stress by estrogens structure-activity relationship Mol Pharmacol 51 1997 535 541
6. P. Benda, J. Lightbody, G. Sato, L. Levine, W. Sweet Differentiated rat glial cell strain in tissue culture Science 161 1968 370 371
7. 2+-permeable AMPA receptors in delayed neurodegeneration Cold Spring Harb Symp Quant Biol 61 1996 373 384
8. J. Bishop, J.W. Simpkins Estradiol treatment increases viability of glioma and neuroblastoma cells in vitro Mol Cell Neurosci 5 1994 303 308
9. K. Blomgren, C. Zhu, X. Wang, J.O. Karlsson, A.L. Leverin, B.A. Bahr, C. Mallard, H. Hagberg Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia a mechanism of "pathological apoptosis"? J Biol Chem 276 2001 10191 10198
10. M. Bresjanac, G. Antauer Reactive astrocytes of the quinolinic acid-lesioned rat striatum express GFRα1 as well as GDNF in vivo Exp Neurol 164 2000 53 59
11. P.S. Brookes, Y. Yoon, J.L. Robotham, M.W. Anders, S.S. Sheu Calcium, ATP, and ROS a mitochondrial love-hate triangle Am J Physiol Cell Physiol 287 2004 C817 C833
12. A.J. Bruce-Keller, J.L. Keeling, J.N. Keller, F.F. Huang, S. Camondola, M.P. Mattson Antiinflammatory effects of estrogen on microglial activation Endocrinology 141 2000 3646 3656
13. V.V. Chaban, E.A. Mayer, H.S. Ennes, P.E. Micevych Estradiol inhibits ATP-induced intracellular calcium concentration increase in dorsal root ganglia neurons Neuroscience 118 2003 941 948
14. A.C. Charles, E.R. Dirksen, J.E. Merrill, M.J. Sanderson Mechanisms of intercellular calcium signaling in glial cells studied with dantrolene and thapsigargin Glia 7 1993 134 145
15. J. Chen, N. Adachi, K. Liu, T. Arai The effects of 17β-estradiol on ischemia-induced neuronal damage in the gerbil hippocampus Neuroscience 87 1998 817 822
16. H. Cheng, J.P. Wu, S.F. Tzeng Neuroprotection of glial cell line-derived neurotrophic factor in damaged spinal cords following contusive injury J Neurosci Res 69 2002 397 405
17. P. Claes, K. Van Kolen, D. Roymans, D. Blero, K. Vissenberg, C. Erneux, J.P. Verbelen, E.L. Esmans, H. Slegers Reactive blue 2 inhibition of cyclic AMP-dependent differentiation of rat C6 glioma cells by purinergic receptor-independent inactivation of phosphatidylinositol 3-kinase Biochem Pharmacol 67 2004 1489 1498
18. R.S. Cotran Robbins pathologic basis of disease 1999 Saunders Philadelphia
19. 2+ exchanger increases susceptibility to ischemia/reperfusion injury in male, but not female, transgenic mice Circ Res 83 1998 1215 1223
20. + in NMDA excitotoxicity in glucose-deprived and depolarized cerebellar granule cells J Neurochem 81 2002 379 389
21. S. Desagher, J. Glowinski, J. Premont Astrocytes protect neurons from hydrogen peroxide toxicity J Neurosci 16 1996 2553 2562
22. D.B. Dubal, H. Zhu, J. Yu, S.W. Rau, P.J. Shughrue, I. Merchenthaler, M.S. Kindy, 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
23. R.J. Dumont, D.O. Okonkwo, S. Verma, R.J. Hurlbert, P.T. Boulos, D.B. Ellegala, A.S. Dumont Acute spinal cord injury, part I pathophysiologic mechanisms Clin Neuropharmacol 24 2001 254 264
24. M. Enari, H. Sakahira, H. Yokoyama, K. Okawa, A. Iwamatsu, S. Nagata A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD Nature 391 1998 43 50
25. J.R. Faulkner, J.E. Herrmann, M.J. Woo, K.E. Tansey, N.B. Doan, M.V. Sofroniew Reactive astrocytes protect tissue and preserve function after spinal cord injury J Neurosci 24 2004 2143 2155
26. J.L. Fitzpatrick, A.L. Mize, C.B. Wade, J.A. Harris, R.A. Shapiro, D.M. Dorsa Estrogen-mediated neuroprotection against β-amyloid toxicity requires expression of estrogen receptor α or β and activation of the MAPK pathway J Neurochem 82 2002 674 682
27. L.M. Garcia-Segura, A. Wozniak, I. Azcoitia, J.R. Rodriguez, R.E. Hutchison, J.B. Hutchison Aromatase expression by astrocytes after brain injury implications for local estrogen formation in brain repair Neuroscience 89 1999 567 578
28. L. Gollapudi, M.M. Oblinger Estrogen and NGF synergistically protect terminally differentiated, ERα-transfected PC12 cells from apoptosis J Neurosci Res 56 1999 471 481
29. 2+ indicators with greatly improved fluorescence properties J Biol Chem 260 1985 3440 3450
30. J.A. Gustafsson Estrogen receptor β a new dimension in estrogen mechanism of action J Endocrinol 163 1999 379 383
31. C. Hermenegildo, A. Cano Pure anti-oestrogens Hum Reprod Update 6 2000 237 243
32. C.E. Ihionkhan, K.L. Chambliss, L.L. Gibson, L.D. Hahner, M.E. Mendelsohn, P.W. Shaul Estrogen causes dynamic alterations in endothelial estrogen receptor expression Circ Res 91 2002 814 820
33. C. Kawas, S. Resnick, A. Morrison, R. Brookmeyer, M. Corrada, A. Zonderman, C. Bacal, D.D. Lingle, E. Metter A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease the Baltimore Longitudinal Study of Aging Neurology 48 1997 1517 1521
34. G.G. Kuiper, B. Carlsson, K. Grandien, E. Enmark, J. Haggblad, S. Nilsson, J.A. Gustafsson Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β Endocrinology 138 1997 863 870
35. N.C. Kupina, M.R. Detloff, W.F. Bobrowski, B.J. Snyder, E.D. Hall Cytoskeletal protein degradation and neurodegeneration evolves differently in males and females following experimental head injury Exp Neurol 180 2003 55 73
36. S. Lankiewicz, C. Marc Luetjens, N. Truc Bui, A.J. Krohn, M. Poppe, G.M. Cole, T.C. Saido, J.H. Prehn Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death J Biol Chem 275 2000 17064 17071
37. Y.J. Lee, E. Shacter Hydrogen peroxide inhibits activation, not activity, of cellular caspase-3 in vivo Free Radic Biol Med 29 2000 684 692
38. Y. Liang, S. Belford, F. Tang, L. Prokai, J.W. Simpkins, J.A. Hughes Membrane fluidity effects of estratrienes Brain Res Bull 54 2001 661 668
39. N.J. Linford, D.M. Dorsa 17beta-Estradiol and the phytoestrogen genistein attenuate neuronal apoptosis induced by the endoplasmic reticulum calcium-ATPase inhibitor thapsigargin Steroids 67 2002 1029 1040
40. C. Matute, E. Alberdi, G. Ibarretxe, M.V. Sanchez-Gomez Excitotoxicity in glial cells Eur J Pharmacol 447 2002 239 246
41. K.M. McGinnis, M.M. Whitton, M.E. Gnegy, K.K. Wang Calcium/calmodulin- dependent protein kinase IV is cleaved by caspase-3 and calpain in SH-SY5Y human neuroblastoma cells undergoing apoptosis J Biol Chem 273 1998 19993 20000
42. C. Mead, V.W. Pentreath Evaluation of toxicity indicators in rat primary astrocytes, C6 glioma and human 1321N1 astrocytoma cells can gliotoxicity be distinguished from cytotoxicity? Arch Toxicol 72 1998 372 380
43. A. Mendelowitsch, M.F. Ritz, J. Ros, H. Langemann, O. Gratzl 17β-Estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate a new neuroprotective pathway Brain Res 901 2001 230 236
44. A. Menuet, Y. Le Page, O. Torres, L. Kern, O. Kah, F. Pakdel Analysis of the estrogen regulation of the zebrafish estrogen receptor (ER) reveals distinct effects of ERα, ERβ1 and ERβ2 J Mol Endocrinol 32 2004 975 986
45. E.K. Michaelis Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging Prog Neurobiol 54 1998 369 415
46. S. Mosselman, J. Polman, R. Dijkema ERβ identification and characterization of a novel human estrogen receptor FEBS Lett 392 1996 49 53
47. A. Murayama, F. Fukai, T. Murachi Action of calpain on the basic estrogen receptor molecule of porcine uterus J Biochem 95 1984 1697 1704
48. J. Nilsen, S.H. Chen, R.D. Brinton Dual action of estrogen on glutamate-induced calcium signaling mechanisms requiring interaction between estrogen receptors and src/mitogen activated protein kinase pathway Brain Res 930 2002 216 234
49. S. Okada, M. Nakamura, Y. Mikami, T. Shimazaki, M. Mihara, Y. Ohsugi, Y. Iwamoto, K. Yoshizaki, T. Kishimoto, Y. Toyama, H. Okano Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury J Neurosci Res 76 2004 265 276
50. Z. Pang, V. Bondada, T. Sengoku, R. Siman, J.W. Geddes Calpain facilitates the neuron death induced by 3-nitropropionic acid and contributes to the necrotic morphology J Neuropathol Exp Neurol 62 2003 633 643
51. T.C. Pappas, B. Gametchu, C.S. Watson Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding FASEB J 9 1995 404 410
52. I. Pita, A.M. Jelaso, C.F. Ide IL-1β increases intracellular calcium through an IL-1 type 1 receptor mediated mechanism in C6 astrocytic cells Int J Dev Neurosci 17 1999 813 820
53. L. Prokai, K. Prokai-Tatrai, P. Perjesi, A.D. Zharikova, E.J. Perez, R. Liu, J.W. Simpkins Quinol-based cyclic antioxidant mechanism in estrogen neuroprotection Proc Natl Acad Sci USA 100 2003 11741 11746
54. K.L. Purnanam, R.M. Boustany Assessment of cell viability and histochemical methods in apoptosis Y.A. Hannun R.M. Boustany Apoptosis in neurobiology 1999 CRC Press New York 133
55. S.K. Ray, N.L. Banik Calpain and its involvement in the pathophysiology of CNS injuries and diseases therapeutic potential of calpain inhibitors for prevention of neurodegeneration Curr Drug Targets CNS Neurol Disord 2 2003 173 189
56. S.K. Ray, G.G. Wilford, C.V. Crosby, E.L. Hogan, N.L. Banik Diverse stimuli induce calpain overexpression and apoptosis in C6 glioma cells Brain Res 829 1999 18 27
57. M. Razandi, A. Pedram, G.L. Greene, E.R. Levin Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript studies of ERα and ERβ expressed in Chinese hamster ovary cells Mol Endocrinol 13 1999 307 319
58. R.L. Roof, E.D. Hall Estrogen-related gender difference in survival rate and cortical blood flow after impact-acceleration head injury in rats J Neurotrauma 17 2000 1155 1169
59. R. Sattler, Z. Xiong, W.Y. Lu, M. Hafner, J.F. MacDonald, M. Tymianski Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein Science 284 1999 1845 1848
60. K.M. Sharrow, A. Kumar, T.C. Foster Calcineurin as a potential contributor in estradiol regulation of hippocampal synaptic function Neuroscience 113 2002 89 97
61. S.A. Shumaker, C. Legault, S.R. Rapp, L. Thal, R.B. Wallace, J.K. Ockene, S.L. Hendrix, B.N. Jones 3rd, A.R. Assaf, R.D. Jackson, J.M. Kotchen, S. Wassertheil-Smoller, J. Wactawski-Wende, W. Investigators Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial JAMA 289 2003 2651 2662
62. H. Shy, L. Malaiyandi, P.S. Timiras Protective action of 17β-estradiol and tamoxifen on glutamate toxicity in glial cells Int J Dev Neurosci 18 2000 289 297
63. J.W. Simpkins, G. Rajakumar, Y.Q. Zhang, C.E. Simpkins, D. Greenwald, C.J. Yu, N. Bodor, A.L. Day Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat J Neurosurg 87 1997 724 730
64. C.A. Singer, X.A. Figueroa-Masot, R.H. Batchelor, D.M. Dorsa The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons J Neurosci 19 1999 2455 2463
65. E.A. Sribnick, S.K. Ray, M.W. Nowak, L. Li, N.L. Banik 17β-Estradiol attenuates glutamate-induced apoptosis and preserves electrophysiologic function in primary cortical neurons J Neurosci Res 76 2004 688 696
66. E.A. Sribnick, J.M. Wingrave, D.D. Matzelle, S.K. Ray, N.L. Banik Estrogen as a neuroprotective agent in the treatment of spinal cord injury Ann N Y Acad Sci 993 2003 125 133
67. P.E. Stevis, D.C. Deecher, L. Suhadolnik, L.M. Mallis, D.E. Frail Differential effects of estradiol and estradiol-BSA conjugates Endocrinology 140 1999 5455 5458
68. +](o) Am J Physiol Cell Physiol 279 2000 C1710 C1721
69. P. Sur, E.A. Sribnick, J.M. Wingrave, M.W. Nowak, S.K. Ray, N.L. Banik Estrogen attenuates oxidative stress-induced apoptosis in C6 glial cells Brain Res 971 2003 178 188
70. P.M. Tiidus, D. Holden, E. Bombardier, S. Zajchowski, D. Enns, A. Belcastro Estrogen effect on post-exercise skeletal muscle neutrophil infiltration and calpain activity Can J Physiol Pharmacol 79 2001 400 406
71. A.C. Towle, P.Y. Sze Steroid binding to synaptic plasma membrane differential binding of glucocorticoids and gonadal steroids J Steroid Biochem 18 1983 135 143
72. C.B. Wade, S. Robinson, R.A. Shapiro, D.M. Dorsa Estrogen receptor (ER)α and ERβ exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway Endocrinology 142 2001 2336 2342
73. K.K. Wang, R. Posmantur, R. Nath, K. McGinnis, M. Whitton, R.V. Talanian, S.B. Glantz, J.S. Morrow Simultaneous degradation of αII- and βII-spectrin by caspase 3 (CPP32) in apoptotic cells J Biol Chem 273 1998 22490 22497
74. M.E. Wilson, Y. Liu, P.M. Wise Estradiol enhances Akt activation in cortical explant cultures following neuronal injury Mol Brain Res 102 2002 48 54
75. D.E. Wood, A. Thomas, L.A. Devi, Y. Berman, R.C. Beavis, J.C. Reed, E.W. Newcomb Bax cleavage is mediated by calpain during drug-induced apoptosis Oncogene 17 1998 1069 1078
76. H.Y. Wu, K. Tomizawa, Y. Oda, F.Y. Wei, Y.F. Lu, M. Matsushita, S.T. Li, A. Moriwaki, H. Matsui Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration J Biol Chem 279 2004 4929 4940
77. B. Xue, M. Hay 17β-Estradiol inhibits excitatory amino acid-induced activity of neurons of the nucleus tractus solitarius Brain Res 976 2003 41 52
78. 2+/calmodulin-dependent protein kinase IV in amygdala Neuroreport 12 2001 2987 2990
79. U.J. Zimmerman, L. Boring, J.H. Pak, N. Mukerjee, K.K. Wang The calpain small subunit gene is essential its inactivation results in embryonic lethality IUBMB Life 50 2000 63 68