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Volume 17, Number 4,
Issue of February 15, 1997
pp. 1291-1301
Copyright ©1997 Society for Neuroscience
Neurotransmitter- and Growth Factor-Induced cAMP Response Element
Binding Protein Phosphorylation in Glial Cell Progenitors: Role of
Calcium Ions, Protein Kinase C, and Mitogen-Activated Protein
Kinase/Ribosomal S6 Kinase Pathway
Received Sept. 18, 1996; revised Nov. 8, 1996; accepted Dec. 4, 1996.
Mario Pende1,
Tracey L. Fisher2,
Peter B. Simpson1,
James T. Russell1,
John Blenis2, and
Vittorio Gallo1
1 Laboratory of Cellular and Molecular Neurophysiology,
National Institute of Child Health and Human Development, National
Institutes of Health, Bethesda, Maryland 20892, and
2 Department of Cell Biology, Harvard Medical School,
Boston, Massachusetts 02115
To understand how extracellular signals may produce long-term
effects in neural cells, we have analyzed the mechanism by which neurotransmitters and growth factors induce phosphorylation of the
transcription factor cAMP response element binding protein (CREB) in
cortical oligodendrocyte progenitor (OP) cells. Activation of glutamate
receptor channels by kainate, as well as stimulation of
G-protein-coupled cholinergic receptors by carbachol and tyrosine kinase receptors by basic fibroblast growth factor (bFGF), rapidly leads to mitogen-activated protein kinase (MAPK) phosphorylation and
ribosomal S6 kinase (RSK) activation. Kainate and carbachol activation
of the MAPK pathway requires extracellular calcium influx and is
accompanied by protein kinase C (PKC) induction, with no significant
increase in GTP binding to Ras. Conversely, growth factor-stimulated
MAPK phosphorylation is independent of extracellular calcium and is
accompanied by Ras activation. Both basal and stimulated MAPK activity
in OP cells are influenced by cytoplasmic calcium levels, as shown by
their sensitivity to the calcium chelator
bis(2-aminophenoxy)ethane-N,N,N ,N-tetra-acetic acid.
The kinetics of CREB phosphorylation in response to the various
agonists corresponds to that of MAPK activation. Moreover, CREB
phosphorylation and MAPK activation are similarly affected by calcium
ions. The MEK inhibitor PD 098059, which selectively prevents
activation of the MAPK pathway, strongly reduces induction of CREB
phosphorylation by kainate, carbachol, bFGF, and the phorbol ester TPA.
We propose that in OPs the MAPK/RSK pathway mediates CREB
phosphorylation in response to calcium influx, PKC activation, and
growth factor stimulation.
Key words:
non-NMDA receptors;
muscarinic receptors;
basic
fibroblast growth factor;
ribosomal S6 kinase;
transcription factor;
oligodendrocytes
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|
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274(6):
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[PDF]
|
|
|
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|
|
|
|
|
|
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[Abstract]
[PDF]
|
|
|
|
|
|
|
S. M. Rodems and D. H. Spector
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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[Full Text]
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|
|
|
|
|
|
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[Full Text]
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|
|
|
|
|
|
|
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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January 1, 1998;
78(1):
99 - 141.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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275(31):
23549 - 23558.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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276(8):
5892 - 5899.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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276(17):
13858 - 13866.
[Abstract]
[Full Text]
[PDF]
|
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|
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