 |
Previous Article | Next Article 
Volume 17, Number 2,
Issue of January 15, 1997
pp. 667-675
Copyright ©1997 Society for Neuroscience
Resetting the Biological Clock: Mediation of Nocturnal CREB
Phosphorylation via Light, Glutamate, and Nitric Oxide
Received July 7, 1996; revised Oct. 25, 1996; accepted Oct. 29, 1996.
Jian M. Ding1, 3,
Lia E. Faiman1,
William J. Hurst1,
Liana R. Kuriashkina2, and
Martha U. Gillette1, 2, 3
1 Department of Cell and Structural Biology,
2 Molecular and Integrative Physiology, and
3 The Neuroscience Program, University of Illinois, Urbana,
Illinois 61801
Synchronization between the environmental lighting cycle and the
biological clock in the suprachiasmatic nucleus (SCN) is correlated
with phosphorylation of the Ca2+/cAMP response element
binding protein (CREB) at the transcriptional activating site
Ser133. Mechanisms mediating the formation of phospho-CREB
(P-CREB) and their relation to clock resetting are unknown. To address these issues, we probed the signaling pathway between light and P-CREB.
Nocturnal light rapidly and transiently induced P-CREB-like immunoreactivity (P-CREB-lir) in the rat SCN. Glutamate (Glu) or nitric
oxide (NO) donor administration in vitro also induced P-CREB-lir in SCN neurons only during subjective night.
Clock-controlled sensitivity to phase resetting by light, Glu, and NO
is similarly restricted to subjective night. The effects of NMDA and
nitric oxide synthase (NOS) antagonists on Glu-mediated induction of P-CREB-lir paralleled their inhibition of phase shifting.
Significantly, among neurons in which P-CREB-lir was induced by light
were NADPH-diaphorase-positive neurons of the SCN's retinorecipient
area. Glu treatment increased the intensity of a 43 kDa band recognized
by anti-P-CREB antibodies in subjective night but not day, whereas
anti- CREB-lir of this band remained constant between night and day.
Inhibition of NOS during Glu stimulation diminished the anti-P-CREB-lir
of this 43 kDa band. Together, these data couple nocturnal light, Glu, NMDA receptor activation and NO signaling to CREB phosphorylation in
the transduction of brief environmental light stimulation of the retina
into molecular changes in the SCN resulting in phase resetting of the
biological clock.
Key words:
suprachiasmatic nucleus;
circadian rhythm;
glutamate;
NMDA;
nitric oxide;
CREB phosphorylation;
immunocytochemistry;
Western
blot;
nuclear protein extraction;
diaphorase;
APV;
L-NAME;
D-NAME;
SNAP
This article has been cited by other articles:

|
 |

|
 |
 
K. Bottum, E. Poon, B. Haley, S. Karmarkar, and S. A Tischkau
Suprachiasmatic nucleus neurons display endogenous resistance to excitotoxicity
Exp Biol Med,
February 1, 2010;
235(2):
237 - 246.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Duncan, A. J. Bruce-Keller, C. Conner, P. E. Knapp, R. Xu, A. Nath, and K. F. Hauser
Effects of chronic expression of the HIV-induced protein, transactivator of transcription, on circadian activity rhythms in mice, with or without morphine
Am J Physiol Regulatory Integrative Comp Physiol,
November 1, 2008;
295(5):
R1680 - R1687.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Gamble, G. C. Allen, T. Zhou, and D. G. McMahon
Gastrin-Releasing Peptide Mediates Light-Like Resetting of the Suprachiasmatic Nucleus Circadian Pacemaker through cAMP Response Element-Binding Protein and Per1 Activation
J. Neurosci.,
October 31, 2007;
27(44):
12078 - 12087.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. P. Irwin and C. N. Allen
Calcium Response to Retinohypothalamic Tract Synaptic Transmission in Suprachiasmatic Nucleus Neurons
J. Neurosci.,
October 24, 2007;
27(43):
11748 - 11757.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. V. Agostino, S. A. Plano, and D. A. Golombek
Sildenafil accelerates reentrainment of circadian rhythms after advancing light schedules
PNAS,
June 5, 2007;
104(23):
9834 - 9839.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Yujnovsky, J. Hirayama, M. Doi, E. Borrelli, and P. Sassone-Corsi
Signaling mediated by the dopamine D2 receptor potentiates circadian regulation by CLOCK:BMAL1
PNAS,
April 18, 2006;
103(16):
6386 - 6391.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Hofmann, R. Feil, T. Kleppisch, and J. Schlossmann
Function of cGMP-Dependent Protein Kinases as Revealed by Gene Deletion
Physiol Rev,
January 1, 2006;
86(1):
1 - 23.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T. Barakat, B. F. O'Hara, V. H. Cao, J. E. Larkin, H. C. Heller, and N. F. Ruby
Light Pulses Do Not Induce C-Fos or Per1 in the SCN of Hamsters That Fail to Reentrain to the Photocycle
J Biol Rhythms,
August 1, 2004;
19(4):
287 - 296.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Ikeda
Calcium Dynamics and Circadian Rhythms in Suprachiasmatic Nucleus Neurons
Neuroscientist,
August 1, 2004;
10(4):
315 - 324.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Naruse, K. Oh-hashi, N. Iijima, M. Naruse, H. Yoshioka, and M. Tanaka
Circadian and Light-Induced Transcription of Clock Gene Per1 Depends on Histone Acetylation and Deacetylation
Mol. Cell. Biol.,
July 15, 2004;
24(14):
6278 - 6287.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M. Novak and H. E. Albers
Novel phase-shifting effects of GABAA receptor activation in the suprachiasmatic nucleus of a diurnal rodent
Am J Physiol Regulatory Integrative Comp Physiol,
May 1, 2004;
286(5):
R820 - R825.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Tischkau, E. T. Weber, S. M. Abbott, J. W. Mitchell, and M. U. Gillette
Circadian Clock-Controlled Regulation of cGMP-Protein Kinase G in the Nocturnal Domain
J. Neurosci.,
August 20, 2003;
23(20):
7543 - 7550.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A. Graves, K. Hellman, S. Veasey, J. A. Blendy, A. I. Pack, and T. Abel
Genetic Evidence for a Role of CREB in Sustained Cortical Arousal
J Neurophysiol,
August 1, 2003;
90(2):
1152 - 1159.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. H. Meijer and W. J. Schwartz
In Search of the Pathways for Light-Induced Pacemaker Resetting in the Suprachiasmatic Nucleus
J Biol Rhythms,
June 1, 2003;
18(3):
235 - 249.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Simonneaux and C. Ribelayga
Generation of the Melatonin Endocrine Message in Mammals: A Review of the Complex Regulation of Melatonin Synthesis by Norepinephrine, Peptides, and Other Pineal Transmitters
Pharmacol. Rev.,
June 1, 2003;
55(2):
325 - 395.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. Kuhlman, R. Silver, J. Le Sauter, A. Bult-Ito, and D. G. McMahon
Phase Resetting Light Pulses Induce Per1 and Persistent Spike Activity in a Subpopulation of Biological Clock Neurons
J. Neurosci.,
February 15, 2003;
23(4):
1441 - 1450.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Tischkau, J. W. Mitchell, S.-H. Tyan, G. F. Buchanan, and M. U. Gillette
Ca2+/cAMP Response Element-binding Protein (CREB)-dependent Activation of Per1 Is Required for Light-induced Signaling in the Suprachiasmatic Nucleus Circadian Clock
J. Biol. Chem.,
January 3, 2003;
278(2):
718 - 723.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-F. Lu and R. D. Hawkins
Ryanodine Receptors Contribute to cGMP-Induced Late-Phase LTP and CREB Phosphorylation in the Hippocampus
J Neurophysiol,
September 1, 2002;
88(3):
1270 - 1278.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Q. Butcher, H. Dziema, M. Collamore, P. W. Burgoon, and K. Obrietan
The p42/44 Mitogen-activated Protein Kinase Pathway Couples Photic Input to Circadian Clock Entrainment
J. Biol. Chem.,
August 9, 2002;
277(33):
29519 - 29525.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Stempfl, M. Vogel, G. Szabo, C. Wulbeck, J. Liu, J. C. Hall, and R. Stanewsky
Identification of Circadian-Clock-Regulated Enhancers and Genes of Drosophila melanogaster by Transposon Mobilization and Luciferase Reporting of Cyclical Gene Expression
Genetics,
February 1, 2002;
160(2):
571 - 593.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. P. Pando and P. Sassone-Corsi
Signaling to the Mammalian Circadian Clocks: In Pursuit of the Primary Mammalian Circadian Photoreceptor
Sci. Signal.,
November 6, 2001;
2001(107):
re16 - re16.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Prosser
Glutamate Blocks Serotonergic Phase Advances of the Mammalian Circadian Pacemaker through AMPA and NMDA Receptors
J. Neurosci.,
October 1, 2001;
21(19):
7815 - 7822.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. J. Kriegsfeld, D. L. Drazen, and R. J. Nelson
Circadian Organization in Male Mice Lacking the Gene for Endothelial Nitric Oxide Synthase (eNOS-/-)
J Biol Rhythms,
April 1, 2001;
16(2):
142 - 148.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M A Pennartz, R. Hamstra, and A. M S Geurtsen
Enhanced NMDA receptor activity in retinal inputs to the rat suprachiasmatic nucleus during the subjective night
J. Physiol.,
April 1, 2001;
532(1):
181 - 194.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Tischkau, E. A. Gallman, G. F. Buchanan, and M. U. Gillette
Differential cAMP Gating of Glutamatergic Signaling Regulates Long-Term State Changes in the Suprachiasmatic Circadian Clock
J. Neurosci.,
October 15, 2000;
20(20):
7830 - 7837.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Horikawa, S.-i. Yokota, K. Fuji, M. Akiyama, T. Moriya, H. Okamura, and S. Shibata
Nonphotic Entrainment by 5-HT1A/7 Receptor Agonists Accompanied by Reduced Per1 and Per2 mRNA Levels in the Suprachiasmatic Nuclei
J. Neurosci.,
August 1, 2000;
20(15):
5867 - 5873.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-F. Lu, E. R. Kandel, and R. D. Hawkins
Nitric Oxide Signaling Contributes to Late-Phase LTP and CREB Phosphorylation in the Hippocampus
J. Neurosci.,
December 1, 1999;
19(23):
10250 - 10261.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Obrietan, S. Impey, D. Smith, J. Athos, and D. R. Storm
Circadian Regulation of cAMP Response Element-mediated Gene Expression in the Suprachiasmatic Nuclei
J. Biol. Chem.,
June 18, 1999;
274(25):
17748 - 17756.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. J. Kriegsfeld, G. E. Demas, S. E. Lee Jr., T. M. Dawson, V. L. Dawson, and R. J. Nelson
Circadian Locomotor Analysis of Male Mice Lacking the Gene for Neuronal Nitric Oxide Synthase (nNOS-/-)
J Biol Rhythms,
February 1, 1999;
14(1):
20 - 27.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. D. A. Kopp, C. Schomerus, F. Dehghani, H.-W. Korf, and H. Meissl
Pituitary Adenylate Cyclase-Activating Polypeptide and Melatonin in the Suprachiasmatic Nucleus: Effects on the Calcium Signal Transduction Cascade
J. Neurosci.,
January 1, 1999;
19(1):
206 - 219.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. von Gall, G. E. Duffield, M. H. Hastings, M. D. A. Kopp, F. Dehghani, H.-W. Korf, and J. H. Stehle
CREB in the Mouse SCN: A Molecular Interface Coding the Phase-Adjusting Stimuli Light, Glutamate, PACAP, and Melatonin for Clockwork Access
J. Neurosci.,
December 15, 1998;
18(24):
10389 - 10397.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. S. Reiss and T. Komatsu
Does Nitric Oxide Play a Critical Role in Viral Infections?
J. Virol.,
June 1, 1998;
72(6):
4547 - 4551.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A. Scheving and W. Gardner
Circadian regulation of CREB transcription factor in mouse esophagus
Am J Physiol Cell Physiol,
April 1, 1998;
274(4):
C1011 - C1016.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Tischkau, J. A. Barnes, F.-J. Lin, E. M. Myers, J. W. Soucy, E. L. Meyer-Bernstein, W. J. Hurst, P. W. Burgoon, D. Chen, A. Sehgal, et al.
Oscillation and Light Induction of timeless mRNA in the Mammalian Circadian Clock
J. Neurosci.,
June 15, 1999;
19(12):
RC15 - RC15.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|