 |
Previous Article | Next Article 
The Journal of Neuroscience, July 1, 1999, 19(13):5301-5310
Voltage-Dependent Neuromodulation of Na+ Channels by
D1-Like Dopamine Receptors in Rat Hippocampal Neurons
Angela R.
Cantrell,
Todd
Scheuer, and
William A.
Catterall
Department of Pharmacology, University of Washington, Seattle,
Washington 98195-7280
Activation of D1-like dopamine (DA) receptors reduces peak
Na+ current in acutely isolated hippocampal neurons
through phosphorylation of the subunit of the
Na+ channel by cAMP-dependent protein kinase (PKA).
Here we report that neuromodulation of Na+ currents
by DA receptors via PKA is voltage-dependent in the range of 110 to
70 mV and is also sensitive to concurrent activation of protein
kinase C (PKC). Depolarization enhanced the ability of D1-like DA
receptors to reduce peak Na+ currents via the PKA
pathway. Similar voltage-dependent modulation was observed when PKA was
activated directly with the membrane-permeant PKA activator DCl-cBIMPS
(cBIMPS; 20 µM), indicating that the membrane potential
dependence occurs downstream of PKA. PKA activation caused only a small
( 2.9 mV) shift in the voltage dependence of steady-state inactivation
and had no effect on slow inactivation or on the rates of entry into
the fast or slow inactivated states, suggesting that another mechanism
is responsible for coupling of membrane potential changes to PKA
modulation. Activation of PKC with a low concentration of the
membrane-permeant diacylglycerol analog oleylacetyl glycerol also
potentiated modulation by SKF 81297 or cBIMPS, and these effects were
most striking at hyperpolarized membrane potentials where PKA
modulation was not stimulated by membrane depolarization. Thus,
activation of D1-like DA receptors causes a strong reduction in
Na+ current via the PKA pathway, but it is effective
primarily when it is combined with depolarization or activation of PKC.
The convergence of these three distinct signaling modalities on the
Na+ channel provides an intriguing mechanism for
integration of information from multiple signaling pathways in the
hippocampus and CNS.
Key words:
Na+ current; neuromodulation; cAMP-dependent protein kinase; protein kinase C; hippocampus; dopamine
receptors; phosphorylation
Copyright © 1999 Society for Neuroscience 0270-6474/99/19135301-10$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
C. Copel, N. Osorio, M. Crest, M. Gola, P. Delmas, and N. Clerc
Activation of neurokinin 3 receptor increases Nav1.9 current in enteric neurons
J. Physiol.,
April 1, 2009;
587(7):
1461 - 1479.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Dai, L. M. Jordan, and B. Fedirchuk
Modulation of Transient and Persistent Inward Currents by Activation of Protein Kinase C in Spinal Ventral Neurons of the Neonatal Rat
J Neurophysiol,
January 1, 2009;
101(1):
112 - 128.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Rosenkranz and D. Johnston
State-Dependent Modulation of Amygdala Inputs by Dopamine-Induced Enhancement of Sodium Currents in Layer V Entorhinal Cortex
J. Neurosci.,
June 27, 2007;
27(26):
7054 - 7069.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. C. Rotaru, D. A. Lewis, and G. Gonzalez-Burgos
Dopamine D1 receptor activation regulates sodium channel-dependent EPSP amplification in rat prefrontal cortex pyramidal neurons
J. Physiol.,
June 15, 2007;
581(3):
981 - 1000.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. P. Few, T. Scheuer, and W. A. Catterall
Dopamine modulation of neuronal Na+ channels requires binding of A kinase-anchoring protein 15and PKA by a modified leucine zipper motif
PNAS,
March 20, 2007;
104(12):
5187 - 5192.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Chen, J. D. Bohanick, M. Nishihara, J. K. Seamans, and C. R. Yang
Dopamine D1/5 Receptor-Mediated Long-Term Potentiation of Intrinsic Excitability in Rat Prefrontal Cortical Neurons: Ca2+-Dependent Intracellular Signaling
J Neurophysiol,
March 1, 2007;
97(3):
2448 - 2464.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Lavialle-Defaix, H. Gautier, A. Defaix, B. Lapied, and F. Grolleau
Differential Regulation of Two Distinct Voltage-Dependent Sodium Currents by Group III Metabotropic Glutamate Receptor Activation in Insect Pacemaker Neurons
J Neurophysiol,
November 1, 2006;
96(5):
2437 - 2450.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Peterson, M. E. Wolf, and F. J. White
Repeated amphetamine administration decreases D1 dopamine receptor-mediated inhibition of voltage-gated sodium currents in the prefrontal cortex.
J. Neurosci.,
March 22, 2006;
26(12):
3164 - 3168.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Rosenkranz and D. Johnston
Dopaminergic regulation of neuronal excitability through modulation of Ih in layer V entorhinal cortex.
J. Neurosci.,
March 22, 2006;
26(12):
3229 - 3244.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Hayashida and A. T. Ishida
Dopamine Receptor Activation Can Reduce Voltage-Gated Na+ Current by Modulating Both Entry Into and Recovery From Inactivation
J Neurophysiol,
November 1, 2004;
92(5):
3134 - 3141.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. C. Cooper, S. J. Moore, N. P. Staff, and N. Spruston
Psychostimulant-Induced Plasticity of Intrinsic Neuronal Excitability in Ventral Subiculum
J. Neurosci.,
October 29, 2003;
23(30):
9937 - 9946.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Dong and F. J. White
Dopamine D1-Class Receptors Selectively Modulate a Slowly Inactivating Potassium Current in Rat Medial Prefrontal Cortex Pyramidal Neurons
J. Neurosci.,
April 1, 2003;
23(7):
2686 - 2695.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-j. Liu, S. D. Dib-Hajj, M. Renganathan, T. R. Cummins, and S. G. Waxman
Modulation of the Cardiac Sodium Channel Nav1.5 by Fibroblast Growth Factor Homologous Factor 1B
J. Biol. Chem.,
January 3, 2003;
278(2):
1029 - 1036.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. M. Grieco, F. S. Afshari, and I. M. Raman
A Role for Phosphorylation in the Maintenance of Resurgent Sodium Current in Cerebellar Purkinje Neurons
J. Neurosci.,
April 15, 2002;
22(8):
3100 - 3107.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Lezcano and C. Bergson
D1/D5 Dopamine Receptors Stimulate Intracellular Calcium Release in Primary Cultures of Neocortical and Hippocampal Neurons
J Neurophysiol,
April 1, 2002;
87(4):
2167 - 2175.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Wicher
Peptidergic Modulation of Insect Voltage-Gated Ca2+ Currents: Role of Resting Ca2+ Current and Protein Kinases A and C
J Neurophysiol,
November 1, 2001;
86(5):
2353 - 2362.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. T. Gulledge and D. B. Jaffe
Multiple Effects of Dopamine on Layer V Pyramidal Cell Excitability in Rat Prefrontal Cortex
J Neurophysiol,
August 1, 2001;
86(2):
586 - 595.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. F. Lopreato, Y. Lu, A. Southwell, N. S. Atkinson, D. M. Hillis, T. P. Wilcox, and H. H. Zakon
Evolution and divergence of sodium channel genes in vertebrates
PNAS,
June 19, 2001;
98(13):
7588 - 7592.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Maurice, T. Tkatch, M. Meisler, L. K. Sprunger, and D. J. Surmeier
D1/D5 Dopamine Receptor Activation Differentially Modulates Rapidly Inactivating and Persistent Sodium Currents in Prefrontal Cortex Pyramidal Neurons
J. Neurosci.,
April 1, 2001;
21(7):
2268 - 2277.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Wicher
Peptidergic Modulation of an Insect Na+ Current: Role of Protein Kinase A and Protein Kinase C
J Neurophysiol,
January 1, 2001;
85(1):
374 - 383.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. A. Gorelova and C. R. Yang
Dopamine D1/D5 Receptor Activation Modulates a Persistent Sodium Current in Rat Prefrontal Cortical Neurons In Vitro
J Neurophysiol,
July 1, 2000;
84(1):
75 - 87.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. K. Park, S. A. Sedore, C. Cronmiller, and J. Hirsh
Type II cAMP-dependent Protein Kinase-deficient Drosophila Are Viable but Show Developmental, Circadian, and Drug Response Phenotypes
J. Biol. Chem.,
June 30, 2000;
275(27):
20588 - 20596.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-j. Liu, S. D. Dib-Hajj, and S. G. Waxman
Fibroblast Growth Factor Homologous Factor 1B Binds to the C Terminus of the Tetrodotoxin-resistant Sodium Channel rNav1.9a (NaN)
J. Biol. Chem.,
May 25, 2001;
276(22):
18925 - 18933.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|