CAMP Response Element-binding Protein 1 Feedback Loop is Necessary for Consolidation of Long-term Synaptic Facilitation in Aplysia

Overview

Journal J Neurosci

Specialty Neurology

Date 2008 Feb 22

PMID 18287513

Citations 44

Authors

Rong-Yu Liu

Diasinou Fioravante

Shreyansh Shah

John H Byrne

Affiliations

Soon will be listed here.

Abstract

The transcription factor cAMP response element (CRE)-binding protein (CREB) plays an essential role in the induction of many forms of long-term synaptic plasticity. Levels of CREB1, the Aplysia homolog of CREB, show sustained elevations for several hours after the induction of long-term synaptic facilitation (LTF). Furthermore, CREB1 binds to the promoter of its own gene. These results suggest the existence of a CREB1-positive feedback loop that contributes to the consolidation of LTF. In the present study, we provide a detailed, quantitative characterization of the dynamics of CREB1 mRNA and protein as well as CREB1 phosphorylation after LTF induction. Injections of CRE oligonucleotides prevented the increase in CREB1 in response to 5-HT, corroborating the existence of the CREB1 feedback loop. This loop probably sustains CRE-dependent gene transcription, which remains elevated for at least 12 h after LTF induction. LTF is blocked by injection of CREB1 antibody after the induction phase, suggesting that the CREB1-positive feedback is required for consolidation of LTF.

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References

OLeary F, Byrne J, Cleary L . Long-term structural remodeling in Aplysia sensory neurons requires de novo protein synthesis during a critical time period. J Neurosci. 1995; 15(5 Pt 1):3519-25. PMC: 6578244. View

Mohamed H, Yao W, Fioravante D, Smolen P, Byrne J . cAMP-response elements in Aplysia creb1, creb2, and Ap-uch promoters: implications for feedback loops modulating long term memory. J Biol Chem. 2005; 280(29):27035-43. DOI: 10.1074/jbc.M502541200. View

Dash P, Hochner B, Kandel E . Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature. 1990; 345(6277):718-21. DOI: 10.1038/345718a0. View

Kaang B, Kandel E, Grant S . Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron. 1993; 10(3):427-35. DOI: 10.1016/0896-6273(93)90331-k. View

Antzoulatos E, Cleary L, Eskin A, Baxter D, Byrne J . Desensitization of postsynaptic glutamate receptors contributes to high-frequency homosynaptic depression of aplysia sensorimotor connections. Learn Mem. 2003; 10(5):309-13. DOI: 10.1101/lm.61403. View

Chin J, Angers A, Cleary L, Eskin A, Byrne J . Transforming growth factor beta1 alters synapsin distribution and modulates synaptic depression in Aplysia. J Neurosci. 2002; 22(9):RC220. PMC: 6758346. DOI: 20026363. View

Angers A, Fioravante D, Chin J, Cleary L, Bean A, Byrne J . Serotonin stimulates phosphorylation of Aplysia synapsin and alters its subcellular distribution in sensory neurons. J Neurosci. 2002; 22(13):5412-22. PMC: 6758201. DOI: 20026555. View

Zhang F, Endo S, Cleary L, Eskin A, Byrne J . Role of transforming growth factor-beta in long-term synaptic facilitation in Aplysia. Science. 1997; 275(5304):1318-20. DOI: 10.1126/science.275.5304.1318. View

Montarolo P, Goelet P, Castellucci V, Morgan J, Kandel E, Schacher S . A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science. 1986; 234(4781):1249-54. DOI: 10.1126/science.3775383. View

10.

Chin J, Angers A, Cleary L, Eskin A, Byrne J . TGF-beta1 in Aplysia: role in long-term changes in the excitability of sensory neurons and distribution of TbetaR-II-like immunoreactivity. Learn Mem. 1999; 6(3):317-30. PMC: 311291. View

11.

Lonze B, Ginty D . Function and regulation of CREB family transcription factors in the nervous system. Neuron. 2002; 35(4):605-23. DOI: 10.1016/s0896-6273(02)00828-0. View

12.

Ohno M, Fornerod M, Mattaj I . Nucleocytoplasmic transport: the last 200 nanometers. Cell. 1998; 92(3):327-36. DOI: 10.1016/s0092-8674(00)80926-5. View

13.

Frost W, Castellucci V, Hawkins R, Kandel E . Monosynaptic connections made by the sensory neurons of the gill- and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization. Proc Natl Acad Sci U S A. 1985; 82(23):8266-9. PMC: 391484. DOI: 10.1073/pnas.82.23.8266. View

14.

Schacher S, Proshansky E . Neurite regeneration by Aplysia neurons in dissociated cell culture: modulation by Aplysia hemolymph and the presence of the initial axonal segment. J Neurosci. 1983; 3(12):2403-13. PMC: 6564656. View

15.

Wainwright M, Zhang H, Byrne J, Cleary L . Localized neuronal outgrowth induced by long-term sensitization training in aplysia. J Neurosci. 2002; 22(10):4132-41. PMC: 6757634. DOI: 20026347. View

16.

Marinesco S, Carew T . Serotonin release evoked by tail nerve stimulation in the CNS of aplysia: characterization and relationship to heterosynaptic plasticity. J Neurosci. 2002; 22(6):2299-312. PMC: 6758260. View

17.

Muller U, Carew T . Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons. Neuron. 1999; 21(6):1423-34. DOI: 10.1016/s0896-6273(00)80660-1. View

18.

Casadio A, Martin K, Giustetto M, Zhu H, Chen M, Bartsch D . A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell. 1999; 99(2):221-37. DOI: 10.1016/s0092-8674(00)81653-0. View

19.

Levenson J, Byrne J, Eskin A . Levels of serotonin in the hemolymph of Aplysia are modulated by light/dark cycles and sensitization training. J Neurosci. 1999; 19(18):8094-103. PMC: 6782455. View

20.

Zhao Y, Hegde A, Martin K . The ubiquitin proteasome system functions as an inhibitory constraint on synaptic strengthening. Curr Biol. 2003; 13(11):887-98. DOI: 10.1016/s0960-9822(03)00332-4. View