Circadian oscillation of hippocampal MAPK activity and cAMP: Implications for memory persistence

Nature Neuroscience

Volumn 11, Issue 9, 2008, Pages 1074-1082

  Eckel Mahan, Kristin L ^a   Phan, Trongha ^a   Han, Sung ^a   Wang, Hongbing ^b   Chan, Guy C K ^a   Scheiner, Zachary S ^a   Storm, Daniel R ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RAS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; LIGHT DARK CYCLE; LONG TERM MEMORY; MALE; MEMORY; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ADENYLATE CYCLASE; ANALYSIS OF VARIANCE; ANIMALS; ASSOCIATION LEARNING; BUTADIENES; CALCIUM; CIRCADIAN RHYTHM; CONDITIONING, CLASSICAL; CREB-BINDING PROTEIN; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FEAR; GENE EXPRESSION REGULATION; GTP-BINDING PROTEINS; HIPPOCAMPUS; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MOTOR ACTIVITY; NITRILES; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; TIME FACTORS;

EID: 50249187869     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2174     Document Type: Article

References (50)

1. Impey, S., Obrietan, K. & Storm, D.R. Making new connections: role of ERK/MAP kinase signaling in neuronal plasticity. Neuron 23, 11-14 (1999).
2. Sweatt, J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 14, 311-317 (2004).
3. Wang, H. & Storm, D.R. Calmodulin-regulated adenylyl cyclases: cross-talk and plasticity in the central nervous system. Mol. Pharmacol. 63, 463-468 (2003).
4. Atkins, C.M., Selcher, J.C., Petraitis, J.J., Trzaskos, J.M. & Sweatt, J.D. The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1, 602-609 (1998).
5. Schafe, G.E. et al. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J. Neurosci. 20, 8177-8187 (2000).
6. Athos, J., Impey, S., Pineda, V.V., Chen, X. & Storm, D.R. Hippocampal CRE-mediated gene expression is required for contextual memory formation. Nat. Neurosci. 5, 1119-1120 (2002).
7. Duvarci, S., Nader, K. & LeDoux, J.E. Activation of extracellular signal-regulated kinase-mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. Eur. J. Neurosci. 21, 283-289 (2005).
8. Kelly, A., Laroche, S. & Davis, S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J. Neurosci. 23, 5354-5360 (2003).
9. Silva, A.J., Kogan, J.H., Frankland, P.W. & Kida, S. CREB and memory. Annu. Rev. Neurosci. 21, 127-148 (1998).
10. Ferguson, G.D. & Storm, D.R. Why calcium-stimulated adenylyl cyclases? Physiology (Bethesda) 19, 271-276 (2004).
11. Scott, R., Bourtchuladze, R., Gossweiler, S., Dubnau, J. & Tully, T. CREB and the discovery of cognitive enhancers. J. Mol. Neurosci. 19, 171-177 (2002).
12. Kelleher, R.J. III, Govindarajan, A., Jung, H.Y., Kang, H. & Tonegawa, S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116, 467-479 (2004).
13. Bernabeu, R. et al. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc. Natl. Acad. Sci. USA 94, 7041-7046 (1997).
14. Wu, Z.L. et al. Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc. Natl. Acad. Sci. USA 92, 220-224 (1995).
15. Wong, S.T. et al. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23, 787-798 (1999).
16. 2+- stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 53, 79-89 (2007).
17. Huang, Y.Y. et al. A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83, 1211-1222 (1995).
18. Brandon, E.P. et al. Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RI beta subunit of cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 92, 8851-8855 (1995).
19. Abel, T. et al. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88, 615-626 (1997).
20. Cui, Z. et al. Inducible and reversible NR1 knockout reveals crucial role of the NMDA receptor in preserving remote memories in the brain. Neuron 41, 781-793 (2004).
21. Bekinschtein, P. et al. Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 53, 261-277 (2007).
22. Lee, A.K. & Wilson, M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183-1194 (2002).
23. Graves, L.A., Heller, E.A., Pack, A.I. & Abel, T. Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn. Mem. 10, 168-176 (2003).
24. Gais, S., Plihal, W., Wagner, U. & Born, J. Early sleep triggers memory for early visual discrimination skills. Nat. Neurosci. 3, 1335-1339 (2000).
25. Huber, R., Ghilardi, M.F., Massimini, M. & Tononi, G. Local sleep and learning. Nature 430, 78-81 (2004).
26. Devan, B.D. et al. Circadian phase-shifted rats show normal acquisition, but impaired long-term retention of place information in the water task. Neurobiol. Learn. Mem. 75, 51-62 (2001).
27. Tapp, W.N. & Holloway, F.A. Phase shifting circadian rhythms produces retrograde amnesia. Science 211, 1056-1058 (1981).
28. Stephan, F.K. & Kovacevic, N.S.Multiple retention deficit in passive avoidance in rats is eliminated by suprachiasmatic lesions. Behav. Biol. 22, 456-462 (1978).
29. Fernandez, R.I., Lyons, L.C., Levenson, J., Khabour, O. & Eskin, A. Circadian modulation of long-term sensitization in Aplysia. Proc. Natl. Acad. Sci. USA 100, 14415-14420 (2003).
30. Leirer, V.O., Tanke, E.D. & Morrow, D.G. Time of day and naturalistic prospective memory. Exp. Aging Res. 20, 127-134 (1994).
31. Maury, P. & Queinnec, Y. Influence of time of 24-hour day on depth of processing in recall memory. Br. J. Psychol. 83, 249-260 (1992).
32. Folkard, S., Wever, R.A. & Wildgruber, C.M. Multi-oscillatory control of circadian rhythms in human performance. Nature 305, 223-226 (1983).
33. Chaudhury, D. & Colwell, C.S. Circadian modulation of learning and memory in fear-conditioned mice. Behav. Brain Res. 133, 95-108 (2002).
34. Hauber, W. & Bareiss, A. Facilitative effects of an adenosine A1/A2 receptor blockade on spatial memory performance of rats: selective enhancement of reference memory retention during the light period. Behav. Brain Res. 118, 43-52 (2001).
35. Holloway, F.A. & Wansley, R.A. Multiple retention deficits at periodic intervals after active and passive avoidance learning. Behav. Biol. 9, 1-14 (1973).
36. Obrietan, K., Impey, S. & Storm, D.R. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat. Neurosci. 1, 693-700 (1998).
37. Selcher, J.C., Atkins, C.M., Trzaskos, J.M., Paylor, R. & Sweatt, J.D. A necessity for MAP kinase activation in mammalian spatial learning. Learn. Mem. 6, 478-490 (1999).
38. Shalin, S.C. et al. Neuronal MEK is important for normal fear conditioning in mice. J. Neurosci. Res. 75, 760-770 (2004).
39. Valentinuzzi, V.S. et al. Locomotor response to an open field during C57BL/6J active and inactive phases: differences dependent on conditions of illumination. Physiol. Behav. 69, 269-275 (2000).
40. Granados-Fuentes, D., Prolo, L.M., Abraham, U. & Herzog, E.D. The suprachiasmatic nucleus entrains, but does not sustain, circadian rhythmicity in the olfactory bulb. J. Neurosci. 24, 615-619 (2004).
41. Ohta, H., Yamazaki, S. & McMahon, D.G. Constant light desynchronizes mammalian clock neurons. Nat. Neurosci. 8, 267-269 (2005).
42. Aschoff, J. Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Z. Tierpsychol. 49, 225-249 (1979).
43. Keiper, M. et al. Epac- and Ca2+-controlled activation of Ras and extracellular signal-regulated kinases by Gs-coupled receptors. J. Biol. Chem. 279, 46497-46508 (2004).
44. Sharma, S.K. & Carew, T.J. The roles of MAPK cascades in synaptic plasticity and memory in Aplysia: facilitatory effects and inhibitory constraints. Learn. Mem. 11, 373-378 (2004).
45. Hetman, M. & Gozdz, A. Role of extracellular signal-regulated kinases 1 and 2 in neuronal survival. Eur. J. Biochem. 271, 2050-2055 (2004).
46. Shimizu, E., Tang, Y.P., Rampon, C. & Tsien, J.Z. NMDA receptor-dependent synaptic reinforcement as a crucial process formemory consolidation. Science 290, 1170-1174 (2000).
47. Peigneux, P. et al. Are spatialmemories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535-545 (2004).
48. Mednick, S., Nakayama, K. & Stickgold, R. Sleep-dependent learning: a nap is as good as a night. Nat. Neurosci. 6, 697-698 (2003).
49. Marshall, L., Helgadottir, H., Molle, M. & Born, J. Boosting slow oscillations during sleep potentiates memory. Nature 444, 610-613 (2006).
50. Born, J., Rasch, B. & Gais, S. Sleep to remember. Neuroscientist 12, 410-424 (2006).