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The Journal of Neuroscience, April 1, 1999, 19(7):2455-2463

The Mitogen-Activated Protein Kinase Pathway Mediates Estrogen Neuroprotection after Glutamate Toxicity in Primary Cortical Neurons

Cherie A. Singer1, Xavier A. Figueroa-Masot3, Robert H. Batchelor1, and Daniel M. Dorsa1, 2

Departments of 1 Pharmacology and 2 Psychiatry and Behavioral Sciences and 3 Graduate Program in Neurobiology and Behavior, University of Washington, Seattle, Washington 98195

Pharmacological and biochemical approaches were used to elucidate the involvement of growth factor signaling pathways mediating estrogen neuroprotection in primary cortical neurons after glutamate excitotoxicity. We addressed the activation of mitogen-activated protein kinase (MAPK) signaling pathways, which are activated by growth factors such as nerve growth factor (NGF). Inhibition of MAPK signaling with the MAPK kinase inhibitor PD98059 blocks both NGF and estrogen neuroprotection in these neurons. These results correlate with a rapid and sustained increase in MAPK activity within 30 min of estrogen exposure. The involvement of signaling molecules upstream from MAPK was also examined to determine whether activation of MAPK by estrogen is mediated by tyrosine kinase activity. Estrogen produces a rapid, transient activation of src-family tyrosine kinases and tyrosine phosphorylation of p21ras-guanine nucleotide activating protein. Effects of estrogen on neuroprotection, as well as rapid activation of tyrosine kinase and MAPK activity, are blocked by the anti-estrogen ICI 182,780. This provides evidence that activation of the MAPK pathway by estrogen participates in mediating neuroprotection via an estrogen receptor. These results describe a novel mechanism by which cytoplasmic actions of the estrogen receptor may activate the MAPK pathway, thus broadening the understanding of effects of estrogen in neurons.

Key words: estrogen; MAPK; neuroprotection; growth factors; excitotoxicity; src; GAP

Copyright © 1999 Society for Neuroscience  0270-6474/99/1972455-09$05.00/0


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C. B. Wade, S. Robinson, R. A. Shapiro, and D. M. Dorsa
Estrogen Receptor (ER){{alpha}} and ER{beta} Exhibit Unique Pharmacologic Properties When Coupled to Activation of the Mitogen-Activated Protein Kinase Pathway
Endocrinology, June 1, 2001; 142(6): 2336 - 2342.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
P. Maher
How Protein Kinase C Activation Protects Nerve Cells from Oxidative Stress-Induced Cell Death
J. Neurosci., May 1, 2001; 21(9): 2929 - 2938.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
O. Nicole, C. Ali, F. Docagne, L. Plawinski, E. T. MacKenzie, D. Vivien, and A. Buisson
Neuroprotection Mediated by Glial Cell Line-Derived Neurotrophic Factor: Involvement of a Reduction of NMDA-Induced Calcium Influx by the Mitogen-Activated Protein Kinase Pathway
J. Neurosci., May 1, 2001; 21(9): 3024 - 3033.
[Abstract] [Full Text] [PDF]

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 Learn. Mem.Home page
R. D. Brinton
Cellular and Molecular Mechanisms of Estrogen Regulation of Memory Function and Neuroprotection Against Alzheimer's Disease: Recent Insights and Remaining Challenges
Learn. Mem., May 1, 2001; 8(3): 121 - 133.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
C. Harms, M. Lautenschlager, A. Bergk, J. Katchanov, D. Freyer, K. Kapinya, U. Herwig, D. Megow, U. Dirnagl, J. R. Weber, et al.
Differential Mechanisms of Neuroprotection by 17 {beta}-Estradiol in Apoptotic versus Necrotic Neurodegeneration
J. Neurosci., April 15, 2001; 21(8): 2600 - 2609.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
F. C. Barone, E. A. Irving, A. M. Ray, J. C. Lee, S. Kassis, S. Kumar, A. M. Badger, R. F. White, M. J. McVey, J. J. Legos, et al.
SB 239063, a Second-Generation p38 Mitogen-Activated Protein Kinase Inhibitor, Reduces Brain Injury and Neurological Deficits in Cerebral Focal Ischemia
J. Pharmacol. Exp. Ther., April 13, 2001; 296(2): 312 - 321.
[Abstract] [Full Text]

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 EndocrinologyHome page
P. M. Wise, D. B. Dubal, M. E. Wilson, S. W. Rau, and M. Bottner
Minireview: Neuroprotective Effects of Estrogen--New Insights into Mechanisms of Action
Endocrinology, March 1, 2001; 142(3): 969 - 973.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
R. Clarke, F. Leonessa, J. N. Welch, and T. C. Skaar
Cellular and Molecular Pharmacology of Antiestrogen Action and Resistance
Pharmacol. Rev., March 1, 2001; 53(1): 25 - 72.
[Abstract] [Full Text] [PDF]

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 StrokeHome page
L. D. McCullough, N. J. Alkayed, R. J. Traystman, M. J. Williams, and P. D. Hurn
Postischemic Estrogen Reduces Hypoperfusion and Secondary Ischemia After Experimental Stroke
Stroke, March 1, 2001; 32(3): 796 - 802.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
D. B. Dubal, H. Zhu, J. Yu, S. W. Rau, P. J. Shughrue, I. Merchenthaler, M. S. Kindy, and P. M. Wise
Estrogen receptor alpha , not beta , is a critical link in estradiol-mediated protection against brain injury
PNAS, February 1, 2001; (2001) 41483198.
[Abstract] [Full Text]

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 J. Neurosci.Home page
J. E. Cavanaugh, J. Ham, M. Hetman, S. Poser, C. Yan, and Z. Xia
Differential Regulation of Mitogen-Activated Protein Kinases ERK1/2 and ERK5 by Neurotrophins, Neuronal Activity, and cAMP in Neurons
J. Neurosci., January 15, 2001; 21(2): 434 - 443.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. B. Dubal and P. M. Wise
Neuroprotective Effects of Estradiol in Middle-Aged Female Rats
Endocrinology, January 1, 2001; 142(1): 43 - 48.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
P. S. Green, S.-H. Yang, K. R. Nilsson, A. S. Kumar, D. F. Covey, and J. W. Simpkins
The Nonfeminizing Enantiomer of 17{beta}-Estradiol Exerts Protective Effects in Neuronal Cultures and a Rat Model of Cerebral Ischemia
Endocrinology, January 1, 2001; 142(1): 400 - 406.
[Abstract] [Full Text] [PDF]

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 StrokeHome page
T. K. Toung, P. D. Hurn, R. J. Traystman, F. E. Sieber, and F. M. Faraci
Estrogen Decreases Infarct Size After Temporary Focal Ischemia in a Genetic Model of Type 1 Diabetes Mellitus Editorial Comment
Stroke, November 1, 2000; 31(11): 2701 - 2706.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A. J. Bruce-Keller, J. L. Keeling, J. N. Keller, F. F. Huang, S. Camondola, and M. P. Mattson
Antiinflammatory Effects of Estrogen on Microglial Activation
Endocrinology, October 1, 2000; 141(10): 3646 - 3656.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
P. M. Wise and D. B. Dubal
Estradiol Protects Against Ischemic Brain Injury in Middle-Aged Rats
Biol Reprod, October 1, 2000; 63(4): 982 - 985.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
M. Razandi, A. Pedram, and E. R. Levin
Plasma Membrane Estrogen Receptors Signal to Antiapoptosis in Breast Cancer
Mol. Endocrinol., September 1, 2000; 14(9): 1434 - 1447.
[Abstract] [Full Text]

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 Mol. Cell. Biol.Home page
J. Font de Mora and M. Brown
AIB1 Is a Conduit for Kinase-Mediated Growth Factor Signaling to the Estrogen Receptor
Mol. Cell. Biol., July 15, 2000; 20(14): 5041 - 5047.
[Abstract] [Full Text]

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 FASEB J.Home page
H. SAWADA, M. IBI, T. KIHARA, M. URUSHITANI, K. HONDA, M. NAKANISHI, A. AKAIKE, and S. SHIMOHAMA
Mechanisms of antiapoptotic effects of estrogens in nigral dopaminergic neurons
FASEB J, June 1, 2000; 14(9): 1202 - 1214.
[Abstract] [Full Text]

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 StrokeHome page
K. Sampei, S. Goto, N. J. Alkayed, B. J. Crain, K. S. Korach, R. J. Traystman, G. E. Demas, R. J. Nelson, P. D. Hurn, and S. Piper Duckles
Stroke in Estrogen Receptor-{alpha}-Deficient Mice • Editorial Comment
Stroke, March 1, 2000; 31(3): 738 - 744.
[Abstract] [Full Text] [PDF]

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 StrokeHome page
N. J. Alkayed, S. J. Murphy, R. J. Traystman, P. D. Hurn, and V. M. Miller
Neuroprotective Effects of Female Gonadal Steroids in Reproductively Senescent Female Rats Editorial Comment
Stroke, January 1, 2000; 31(1): 161 - 168.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
D. B. Dubal, P. J. Shughrue, M. E. Wilson, I. Merchenthaler, and P. M. Wise
Estradiol Modulates bcl-2 in Cerebral Ischemia: A Potential Role for Estrogen Receptors
J. Neurosci., August 1, 1999; 19(15): 6385 - 6393.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. de Jager, T. Pelzer, S. Muller-Botz, A. Imam, J. Muck, and L. Neyses
Mechanisms of Estrogen Receptor Action in the Myocardium. RAPID GENE ACTIVATION VIA THE ERK1/2 PATHWAY AND SERUM RESPONSE ELEMENTS
J. Biol. Chem., July 20, 2001; 276(30): 27873 - 27880.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
D. B. Dubal, H. Zhu, J. Yu, S. W. Rau, P. J. Shughrue, I. Merchenthaler, M. S. Kindy, and P. M. Wise
Estrogen receptor alpha , not beta , is a critical link in estradiol-mediated protection against brain injury
PNAS, February 13, 2001; 98(4): 1952 - 1957.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. Bi, G. Broutman, M. R. Foy, R. F. Thompson, and M. Baudry
The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus
PNAS, March 28, 2000; 97(7): 3602 - 3607.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. Bi, M. R. Foy, R.-M. Vouimba, R. F. Thompson, and M. Baudry
Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway
PNAS, November 6, 2001; 98(23): 13391 - 13395.
[Abstract] [Full Text] [PDF]


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