Time of day influences memory formation and dCREB2 proteins in Drosophila

Frontiers in Systems Neuroscience

Volumn 8, Issue MAR, 2014, Pages

  Fropf, Robin ^a   Zhang, Jiabin ^a   Tanenhaus, Anne K ^a   Fropf, Whitney J ^a   Siefkes, Ellen ^a   Yin, Jerry C P ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

dCREB2; Genetic; Memory formation; Sleep; Time of day; Transcription

Indexed keywords

DCREB2 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BIOLUMINESCENCE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; LUCIFERASE ASSAY; MEMORY; MOLECULAR WEIGHT; NEUROSCIENCE; NONHUMAN; PERFORMANCE; PROTEIN EXPRESSION; RADIOGRAPHY; SMELLING; TISSUE PREPARATION; TRAINING; WESTERN BLOTTING;

EID: 84897429485     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00043     Document Type: Article

References (43)

1. Belvin, M. P., Zhou, H., and Yin, J. C. (1999). The Drosophila dCREB2 gene affects the circadian clock. Neuron 22, 777-787.doi: 10.1016/S0896-6273(00)80736-9
2. Benito, E., and Barco, A. (2010). CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci. 33, 230-240.doi: 10.1016/j.tins.2010.02.001
3. Brandes, C., Plautz, J. D., Stanewsky, R., Jamison, C. F., Straume, M., Wood, K. V., et al. (1996). Novel features of Drosophila period transcription revealed by real-time luciferase reporting. Neuron 16, 687-692.doi: 10.1016/S0896-6273(00)80088-4
4. Cao, R., Butcher, G. Q., Karelina, K., Arthur, J. S., and Obrietan, K. (2013). Mitogen-and stress-activated protein kinase 1 modulates photic entrainment of the suprachiasmatic circadian clock. Eur. J. Neurosci. 37, 130-140.doi: 10. 1111/ejn.12028
5. Chen, C. C., Wu, J. K., Lin, H. W., Pai, T. P., Fu, T. F., Wu, C. L., et al. (2012). Visualizing long-term memory formation in two neurons of the Drosophila brain. Science 335, 678-685.doi: 10.1126/science.1212735
6. Davis, R. L. (2011). Traces of Drosophila memory. Neuron 70, 8-19.doi: 10.1016/j. neuron.2011.03.012
7. Decker, S., McConnaughey, S., and Page, T. L. (2007). Circadian regulation of insect olfactory learning. Proc. Natl. Acad. Sci. U S A 104, 15905-15910.doi: 10. 1073/pnas.0702082104
8. Ding, J. M., Buchanan, G. F., Tischkau, S. A., Chen, D., Kuriashkina, L., Faiman, L. E., et al. (1998). A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock. Nature 394, 381-384.doi: 10.1038/ 28639
9. Ding, J. M., Faiman, L. E., Hurst, W. J., Kuriashkina, L. R., and Gillette, M. U. (1997). Resetting the biological clock: mediation of nocturnal CREB phospho-rylation via light, glutamate, and nitric oxide. J. Neurosci. 17, 667-675.
10. Eckel-Mahan, K. L., Phan, T., Han, S., Wang, H., Chan, G. C., Scheiner, Z. S., et al. (2008). Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence. Nat. Neurosci. 11, 1074-1082.doi: 10. 1038/nn.2174
11. Fernandez, R. I., Lyons, L. C., Levenson, J., Khabour, O., and Eskin, A. (2003). Circadian modulation of long-term sensitization in Aplysia. Proc. Natl. Acad. Sci. U S A 100, 14415-14420.doi: 10.1073/pnas.2336172100
12. Fropf, R., Tubon, T. C. Jr., and Yin, J. C. (2013). Nuclear gating of a Drosophila dCREB2 activator is involved in long term memory formation. Neurobiol. Learn. Mem. 106, 258-267.doi: 10.1016/j.nlm.2013.09.006
13. Gerstner, J. R., Lyons, L. C., Wright, K. P. Jr., Loh, D. H., Rawashdeh, O., Eckel-Mahan, K. L., et al. (2009). Cycling behavior and memory formation. J. Neurosci. 29, 12824-12830.doi: 10.1523/JNEUROSCI.3353-09.2009
14. Ginty, D. D., Kornhauser, J. M., Thompson, M. A., Bading, H., Mayo, K. E., Takahashi, J. S., et al. (1993). Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260, 238-241.doi: 10.1126/science.8097062
15. Hirano, Y., Masuda, T., Naganos, S., Matsuno, M., Ueno, K., Miyashita, T., et al. (2013). Fasting launches CRTC to facilitate long-term memory formation in Drosophila. Science 339, 443-446.doi: 10.1126/science.1227170
16. Holloway, F. A., and Wansley, R. (1973). Multiphasic retention deficits at periodic intervals after passive-avoidance learning. Science 180, 208-210.doi: 10. 1126/science.180.4082.208
17. Kandel, E. R. (2012). The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol. Brain 5:14.doi: 10.1186/1756-6606-5-14
18. Krishnan, B., Dryer, S. E., and Hardin, P. E. (1999). Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400, 375-378.doi: 10.1038/22566
19. Krishnan, B., Levine, J. D., Lynch, M. K., Dowse, H. B., Funes, P., Hall, J. C., et al. (2001). A new role for cryptochrome in a Drosophila circadian oscillator. Nature 411, 313-317.doi: 10.1038/35077094
20. Luo, J., Phan, T. X., Yang, Y., Garelick, M. G., and Storm, D. R. (2013). Increases in cAMP, MAPK activity, and CREB phosphorylation during REM sleep: implications for REM sleep and memory consolidation. J. Neurosci. 33, 6460-6468.doi: 10.1523/JNEUROSCI.5018-12.2013
21. Lyons, L. C., and Roman, G. (2008). Circadian modulation of short-term memory in Drosophila. Learn. Mem. 16, 19-27.doi: 10.1101/lm.1146009
22. Lyons, L. C., Collado, M. S., Khabour, O., Green, C. L., and Eskin, A. (2006). The circadian clock modulates core steps in long-term memory formation in Aplysia. J. Neurosci. 26, 8662-8671.doi: 10.1523/jneurosci.2307-06.2006
23. Lyons, L. C., Green, C. L., and Eskin, A. (2008). Intermediate-term memory is modulated by the circadian clock. J. Biol. Rhythms 23, 538-542.doi: 10. 1177/0748730408325359
24. Lyons, L. C., Rawashdeh, O., Katzoff, A., Susswein, A. J., and Eskin, A. (2005). Circadian modulation of complex learning in diurnal and nocturnal Aplysia. Proc. Natl. Acad. Sci. U S A 102, 12589-12594.doi: 10.1073/pnas.0503847102
25. Marshall, L., and Born, J. (2007). The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn. Sci. 11, 442-450.doi: 10.1016/j. tics.2007.09.001
26. Pai, T. P., Chen, C. C., Lin, H. H., Chin, A. L., Lai, J. S., Lee, P. T., et al. (2013). Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation. Proc. Natl. Acad. Sci. U S A 110, 7898-7903.doi: 10.1073/pnas.1216336110
27. Pitman, J. L., Huetteroth, W., Burke, C. J., Krashes, M. J., Lai, S. L., Lee, T., et al. (2011). A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body. Curr. Biol. 21, 855-861.doi: 10.1016/j.cub.2011. 03.069
28. R Development Core Team. (2013). R: a language and environment for statistical computing. Vienna, Austria. Retrieved from http://www.R-project.org/
29. Ruby, N. F., Fernandez, F., Garrett, A., Klima, J., Zhang, P., Sapolsky, R., et al. (2013). Spatial memory and long-term object recognition are impaired by circadian arrhythmia and restored by the GABAA antagonist pentylenetetrazole. PLoS One 8:e72433. doi: 10.1371/journal.pone.00
30. Ruby, N. F., Hwang, C. E., Wessells, C., Fernandez, F., Zhang, P., Sapolsky, R., et al. (2008). Hippocampal-dependent learning requires a functional circadian system. Proc. Natl. Acad. Sci. U S A 105, 15593-15598.doi: 10.1073/pnas.0808259105
31. Stanewsky, R., Jamison, C. F., Plautz, J. D., Kay, S. A., and Hall, J. C. (1997). Multiple circadian-regulated elements contribute to cycling period gene expression in Drosophila. EMBO J. 16, 5006-5018.doi: 10.1093/emboj/16.16.5006
32. Tanenhaus, A. K., Zhang, J., and Yin, J. C. (2012). In vivo circadian oscillation of dCREB2 and NF-B activity in the Drosophila nervous system. PLoS One 7:e45130.doi: 10.1371/journal.pone.0045130
33. Tischkau, S. A., Gallman, E. A., Buchanan, G. F., and Gillette, M. U. (2000). Differential cAMP gating of glutamatergic signaling regulates long-term state changes in the suprachiasmatic circadian clock. J. Neurosci. 20, 7830-7837.
34. Tischkau, S. A., Weber, E. T., Abbott, S. M., Mitchell, J. W., and Gillette, M. U. (2003). Circadian clock-controlled regulation of cGMP-protein kinase G in the nocturnal domain. J. Neurosci. 23, 7543-7550.
35. Tubon, T. C. Jr., Zhang, J., Friedman, E. L., Jin, H., Gonzales, E. D., Zhou, H., et al. (2013). dCREB2-mediated enhancement of memory formation. J. Neurosci. 33, 7475-7487.doi: 10.1523/JNEUROSCI.4387-12.2013
36. van Alphen, B., Yap, M. H., Kirszenblat, L., Kottler, B., and van Swinderen, B. (2013). A dynamic deep sleep stage in Drosophila. J. Neurosci. 33, 6917-6927.doi: 10.1523/JNEUROSCI.0061-13.2013
37. van Swinderen, B., Nitz, D. A., and Greenspan, R. J. (2004). Uncoupling of brain activity from movement defines arousal states in Drosophila. Curr. Biol. 14, 81-87.doi: 10.1016/j.cub.2003.12.057
38. Walker, M. P., and Stickgold, R. (2004). Sleep-dependent learning and memory consolidation. Neuron 44, 121-133.doi: 10.1016/j.neuron.2004.08.031
39. Wu, C. L., Shih, M. F., Lai, J. S., Yang, H. T., Turner, G. C., Chen, L., et al. (2011). Heterotypic gap junctions between two neurons in the drosophila brain are critical for memory. Curr. Biol. 21, 848-854.doi: 10.1016/j.cub.2011.02.041
40. Yin, J. C., Del Vecchio, M., Zhou, H., and Tully, T. (1995a). CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81, 107-115.doi: 10.1016/0092-8674(95)90375-5
41. Yin, J. C., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G., et al. (1994). Induction of a dominant negative CREB transgene specifically blocks long term memory in Drosophila. Cell 79, 49-58.doi: 10.1016/0092-8674(94)90399-9
42. Yin, J. C., Wallach, J. S., Wilder, E. L., Klingensmith, J., Dang, D., Perrimon, N., et al. (1995b). A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist. Mol. Cell. Biol. 15, 5123-5130.
43. Zhang, J., Little, C. J., Tremmel, D. M., Yin, J. C., and Wesley, C. S. (2013). Notch-inducible hyperphosphorylated CREB and its ultradian oscillation in long-term memory formation. J. Neurosci. 33, 12825-12834.doi: 10.1523/JNEUROSCI. 0783-13.2013