 |
 Previous Article | Next Article 
Volume 17, Number 16,
Issue of August 15, 1997
pp. 6189-6202
Copyright ©1997 Society for Neuroscience
Calcium Controls Gene Expression via Three Distinct Pathways That
Can Function Independently of the Ras/Mitogen-Activated Protein Kinases
(ERKs) Signaling Cascade
Received April 17, 1997; accepted May 28, 1997.
Claire M. Johnson1,
Caroline S. Hill2,
Sangeeta Chawla1,
Richard Treisman2, and
Hilmar Bading1
1 Division of Neurobiology, Medical Research Council
Laboratory of Molecular Biology, Cambridge CB2 2QH, England, and
2 Transcription Laboratory, Imperial Cancer Research Fund
Laboratories, London WC2A 3PX, England
Calcium ions are the principal second messenger in the control of
gene expression by electrical activation of neurons. However, the full
complexity of calcium-signaling pathways leading to transcriptional activation and the cellular machinery involved are not known. Using the
c-fos gene as a model system, we show here that the activity of its complex promoter is controlled by three independently operating signaling mechanisms and that their functional significance is cell type-dependent. The serum response element (SRE), which is
composed of a ternary complex factor (TCF) and a serum response factor
(SRF) binding site, integrates two calcium-signaling pathways. In PC12
cells, calcium-regulated transcription mediated by the SRE requires the
TCF site and is not inhibited by expression of the dominant-negative
Ras mutant, RasN17, nor by the MAP kinase kinase 1 inhibitor PD 98059. In contrast, TCF-dependent transcriptional regulation by nerve growth
factor or epidermal growth factor is mediated by a Ras/MAP kinases
(ERKs) pathway targeting the TCF Elk-1. In AtT20 cells and hippocampal
neurons, calcium signals can stimulate transcription via a
TCF-independent mechanism that requires the SRF binding site. The
cyclic AMP response element (CRE), which cooperates with the TCF site
in growth factor-regulated transcription, is a target of a third
calcium-regulated pathway that is little affected by the expression of
RasN17 or by PD 98059. Thus, calcium can stimulate gene expression via
a TCF-, SRF-, and CRE-linked pathway that can operate independently of
the Ras/MAP kinases (ERKs) signaling cascade in a cell type-dependent
manner.
Key words:
gene regulation;
c-fos;
calcium signaling;
cyclic AMP response element;
serum response element;
ternary complex
factor
This article has been cited by other articles:
|
|
|
|
 
Z. Yuan, S. Gong, J. Luo, Z. Zheng, B. Song, S. Ma, J. Guo, C. Hu, G. Thiel, C. Vinson, et al.
Opposing Roles for ATF2 and c-Fos in c-Jun-Mediated Neuronal Apoptosis
Mol. Cell. Biol.,
May 1, 2009;
29(9):
2431 - 2442.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. H. C. Orth, S. Lang, M. Taniguchi, and K. Aktories
Pasteurella multocida Toxin-induced Activation of RhoA Is Mediated via Two Families of G{alpha} Proteins, G{alpha}q and G{alpha}12/13
J. Biol. Chem.,
November 4, 2005;
280(44):
36701 - 36707.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. J. Knot, I. Laher, E. A. Sobie, S. Guatimosim, L. Gomez-Viquez, H. Hartmann, L.-S. Song, W.J. Lederer, W. F. Graier, R. Malli, et al.
Twenty Years of Calcium Imaging: Cell Physiology to Dye For
Mol. Interv.,
April 1, 2005;
5(2):
112 - 127.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Puri, B. S. Magenheimer, R. L. Maser, E. M. Ryan, C. A. Zien, D. D. Walker, D. P. Wallace, S. J. Hempson, and J. P. Calvet
Polycystin-1 Activates the Calcineurin/NFAT (Nuclear Factor of Activated T-cells) Signaling Pathway
J. Biol. Chem.,
December 31, 2004;
279(53):
55455 - 55464.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Rose, P. Froment, V. Perrot, M. J. Quon, D. LeRoith, and J. Dupont
The Luteinizing Hormone-releasing Hormone Inhibits the Anti-apoptotic Activity of Insulin-like Growth Factor-1 in Pituitary {alpha}T3 Cells by Protein Kinase C{alpha}-mediated Negative Regulation of Akt
J. Biol. Chem.,
December 10, 2004;
279(50):
52500 - 52516.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Yamaguchi, D. P. Wallace, B. S. Magenheimer, S. J. Hempson, J. J. Grantham, and J. P. Calvet
Calcium Restriction Allows cAMP Activation of the B-Raf/ERK Pathway, Switching Cells to a cAMP-dependent Growth-stimulated Phenotype
J. Biol. Chem.,
September 24, 2004;
279(39):
40419 - 40430.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. W. Landsberg and J. X.-J. Yuan
Calcium and TRP Channels in Pulmonary Vascular Smooth Muscle Cell Proliferation
Physiology,
April 1, 2004;
19(2):
44 - 50.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. H. Chang, S. Poser, and Z. Xia
A Novel Role For Serum Response Factor in Neuronal Survival
J. Neurosci.,
March 3, 2004;
24(9):
2277 - 2285.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. H. Nashat and R. Langer
Temporal Characteristics of Activation, Deactivation, and Restimulation of Signal Transduction following Depolarization in the Pheochromocytoma Cell Line PC12
Mol. Cell. Biol.,
July 15, 2003;
23(14):
4788 - 4795.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. J. Haisenleder, H. A. Ferris, and M. A. Shupnik
The Calcium Component of Gonadotropin-Releasing Hormone-Stimulated Luteinizing Hormone Subunit Gene Transcription Is Mediated by Calcium/Calmodulin-Dependent Protein Kinase Type II
Endocrinology,
June 1, 2003;
144(6):
2409 - 2416.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Apati, J. Janossy, A. Brozik, P. I. Bauer, and M. Magocsi
Calcium Induces Cell Survival and Proliferation through the Activation of the MAPK Pathway in a Human Hormone-dependent Leukemia Cell Line, TF-1
J. Biol. Chem.,
March 7, 2003;
278(11):
9235 - 9243.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. L. Allen and L. A. Leinwand
Intracellular Calcium and Myosin Isoform Transitions. CALCINEURIN AND CALCIUM-CALMODULIN KINASE PATHWAYS REGULATE PREFERENTIAL ACTIVATION OF THE IIa MYOSIN HEAVY CHAIN PROMOTER
J. Biol. Chem.,
November 15, 2002;
277(47):
45323 - 45330.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Lin, D. Wang, and W. Sadee
Serum Response Factor Activation by Muscarinic Receptors via RhoA. NOVEL PATHWAY SPECIFIC TO M1 SUBTYPE INVOLVING CALMODULIN, CALCINEURIN, AND Pyk2
J. Biol. Chem.,
October 18, 2002;
277(43):
40789 - 40798.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Maturana, G. Van Haasteren, I. Piuz, C. Castelbou, N. Demaurex, and W. Schlegel
Spontaneous Calcium Oscillations Control c-fos Transcription via the Serum Response Element in Neuroendocrine Cells
J. Biol. Chem.,
October 11, 2002;
277(42):
39713 - 39721.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. V. Vasilyev, M. A. Lawson, D. Dipaolo, N. J. G. Webster, and P. L. Mellon
Different Signaling Pathways Control Acute Induction versus Long-Term Repression of LH{beta} Transcription by GnRH
Endocrinology,
September 1, 2002;
143(9):
3414 - 3426.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Mao and J. Q. Wang
Glutamate Cascade to cAMP Response Element-Binding Protein Phosphorylation in Cultured Striatal Neurons through Calcium-Coupled Group I Metabotropic Glutamate Receptors
Mol. Pharmacol.,
September 1, 2002;
62(3):
473 - 484.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Levkovitz and J. M. Baraban
A Dominant Negative Egr Inhibitor Blocks Nerve Growth Factor-Induced Neurite Outgrowth by Suppressing c-Jun Activation: Role of an Egr/c-Jun Complex
J. Neurosci.,
May 15, 2002;
22(10):
3845 - 3854.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Guo, J. Krucken, W. P. M. Benten, and F. Wunderlich
Estradiol-induced Nongenomic Calcium Signaling Regulates Genotropic Signaling in Macrophages
J. Biol. Chem.,
February 22, 2002;
277(9):
7044 - 7050.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Schratt, B. Weinhold, A. S. Lundberg, S. Schuck, J. Berger, H. Schwarz, R. A. Weinberg, U. Rüther, and A. Nordheim
Serum Response Factor Is Required for Immediate-Early Gene Activation yet Is Dispensable for Proliferation of Embryonic Stem Cells
Mol. Cell. Biol.,
April 15, 2001;
21(8):
2933 - 2943.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
Y. Levkovitz, K. J. O'Donovan, and J. M. Baraban
Blockade of NGF-Induced Neurite Outgrowth by a Dominant-Negative Inhibitor of the Egr Family of Transcription Regulatory Factors
J. Neurosci.,
January 1, 2001;
21(1):
45 - 52.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. Platoshyn, V. A. Golovina, C. L. Bailey, A. Limsuwan, S. Krick, M. Juhaszova, J. E. Seiden, L. J. Rubin, and J. X.-J. Yuan
Sustained membrane depolarization and pulmonary artery smooth muscle cell proliferation
Am J Physiol Cell Physiol,
November 1, 2000;
279(5):
C1540 - C1549.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Khammanivong and D. E. Nelson
Light Pulses Suppress Responsiveness within the Mouse Photic Entrainment Pathway
J Biol Rhythms,
October 1, 2000;
15(5):
393 - 405.
[Abstract]
[PDF]
|
|
|
|
|
|
|
F. Sun, M. J. Hug, N. A. Bradbury, and R. A. Frizzell
Protein Kinase A Associates with Cystic Fibrosis Transmembrane Conductance Regulator via an Interaction with Ezrin
J. Biol. Chem.,
May 5, 2000;
275(19):
14360 - 14366.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. A. Krueger, E. A. Warner, and D. R. Dowd
Involvement of Thyrotroph Embryonic Factor in Calcium-mediated Regulation of Gene Expression
J. Biol. Chem.,
May 5, 2000;
275(19):
14524 - 14531.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Wang, H. Zheng, and H.-R. Berthoud
Functional vagal input to chemically identified neurons in pancreatic ganglia as revealed by Fos expression
Am J Physiol Endocrinol Metab,
November 1, 1999;
277(5):
E958 - E964.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Kumahara, T. Ebihara, and D. Saffen
Protein Kinase Inhibitor H7 Blocks the Induction of Immediate-Early Genes zif268 and c-fos by a Mechanism Unrelated to Inhibition of Protein Kinase C but Possibly Related to Inhibition of Phosphorylation of RNA Polymerase II
J. Biol. Chem.,
April 9, 1999;
274(15):
10430 - 10438.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Beltman, J. R. Erickson, G. A. Martin, J. F. Lyons, and S. J. Cook
C3 Toxin Activates the Stress Signaling Pathways, JNK and p38, but Antagonizes the Activation of AP-1 in Rat-1 Cells
J. Biol. Chem.,
February 5, 1999;
274(6):
3772 - 3780.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. D. Best, E. S. Maywood, K. L. Smith, and M. H. Hastings
Rapid Resetting of the Mammalian Circadian Clock
J. Neurosci.,
January 15, 1999;
19(2):
828 - 835.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Vanhoutte, J.-V. Barnier, B. Guibert, C. Pages, M.-J. Besson, R. A. Hipskind, and J. Caboche
Glutamate Induces Phosphorylation of Elk-1 and CREB, Along with c-fos Activation, via an Extracellular Signal-Regulated Kinase-Dependent Pathway in Brain Slices
Mol. Cell. Biol.,
January 1, 1999;
19(1):
136 - 146.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. J. Cook, N. Aziz, and M. McMahon
The Repertoire of Fos and Jun Proteins Expressed during the G1 Phase of the Cell Cycle Is Determined by the Duration of Mitogen-Activated Protein Kinase Activation
Mol. Cell. Biol.,
January 1, 1999;
19(1):
330 - 341.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Sgambato, C. Pages, M. Rogard, M.-J. Besson, and J. Caboche
Extracellular Signal-Regulated Kinase (ERK) Controls Immediate Early Gene Induction on Corticostriatal Stimulation
J. Neurosci.,
November 1, 1998;
18(21):
8814 - 8825.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Chawla, G. E. Hardingham, D. R. Quinn, and H. Bading
CBP: A Signal-Regulated Transcriptional Coactivator Controlled by Nuclear Calcium and CaM Kinase IV
Science,
September 4, 1998;
281(5382):
1505 - 1509.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
P. Vanhoutte, J. L. Nissen, B. Brugg, B. D. Gaspera, M.-J. Besson, R. A. Hipskind, and J. Caboche
Opposing Roles of Elk-1 and Its Brain-specific Isoform, Short Elk-1, in Nerve Growth Factor-induced PC12 Differentiation
J. Biol. Chem.,
February 9, 2001;
276(7):
5189 - 5196.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Tabuchi, R. Nakaoka, K. Amano, M. Yukimine, T. Andoh, Y. Kuraishi, and M. Tsuda
Differential Activation of Brain-derived Neurotrophic Factor Gene Promoters I and III by Ca2+ Signals Evoked via L-type Voltage-dependent and N-Methyl-D-aspartate Receptor Ca2+ Channels
J. Biol. Chem.,
June 2, 2000;
275(23):
17269 - 17275.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
