A Neuronal Isoform of CPEB Regulates Local Protein Synthesis and Stabilizes Synapse-Specific Long-Term Facilitation in Aplysia

Cell

Volumn 115, Issue 7, 2003, Pages 893-904

  Si, Kausik ^a   Giustetto, Maurizio ^a   Etkin, Amit ^a   Hsu, Ruby ^a   Janisiewicz, Agnieszka M ^a   Miniaci, Maria Conchetta ^a   Kim, Joung Hun ^a   Zhu, Huixiang ^a   Kandel, Eric R ^a  

^a New York State Psychiatric Institute ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; ISOPROTEIN; RAPAMYCIN; UNCLASSIFIED DRUG;

APLYSIA; ARTICLE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SYNTHESIS REGULATION; SYNAPSE; UPREGULATION; YEAST;

APLYSIA;

EID: 0346186101     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(03)01021-3     Document Type: Article

References (43)

1. Bailey C.H., Chen M. Morphological aspects of synaptic plasticity in Aplysia. An anatomical substrate for long-term memory. Ann. NY Acad. Sci. 627:1991;181-196.
2. Bally-Cuif L., Schatz W.J., Ho R.K. Characterization of the zebrafish Orb/CPEB-related RNA binding protein and localization of maternal components in the zebrafish oocyte. Mech. Dev. 77:1998;31-47.
3. Barco A., Alarcon J.M., Kandel E.R. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell. 108:2002;689-703.
4. Bonhoeffer T., Yuste R. Spine motility. Phenomenology, mechanisms, and function. Neuron. 35:2002;1019-1027.
5. Brittis P.A., Lu Q., Flanagan J.G. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell. 110:2002;223-235.
6. Casadio A., Martin K.C., Giustetto M., Zhu H., Chen M., Bartsch D., Bailey C.H., Kandel E.R. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell. 99:1999;221-237.
7. Chang J.S., Tan L., Schedl P. The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes. Dev. Biol. 215:1999;91-106.
8. Chang J.S., Tan L., Wolf M.R., Schedl P. Functioning of the Drosophila orb gene in gurken mRNA localization and translation. Development. 128:2001;3169-3177.
9. Contractor A., Rogers C., Maron C., Henkemeyer M., Swanson G.T., Heinemann S.F. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science. 296:2002;1864-1869.
10. DesGroseillers L., Auclair D., Wickham L., Maalouf M. A novel actin cDNA is expressed in the neurons of Aplysia californica. Biochim. Biophys. Acta. 1217:1994;322-324.
11. Fox C.A., Sheets M.D., Wickens M.P. Poly(A) addition during maturation of frog oocytes. distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU Genes Dev. 3:1989;2151-2162.
12. Frey U., Morris R.G. Synaptic tagging and long-term potentiation. Nature. 385:1997;533-536.
13. Gebauer F., Richter J.D. Mouse cytoplasmic polyadenylylation element binding protein. an evolutionarily conserved protein that interacts with the cytoplasmic polyadenylylation elements of c-mos mRNA Proc. Natl. Acad. Sci. USA. 93:1996;14602-14607.
14. Gingras A.C., Raught B., Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15:2001;807-826.
15. Groisman I., Jung M.Y., Sarkissian M., Cao Q., Richter J.D. Translational control of the embryonic cell cycle. Cell. 109:2002;473-483.
16. Hake L.E., Richter J.D. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell. 79:1994;617-627.
17. Hegde A.N., Inokuchi K., Pei W., Casadio A., Ghirardi M., Chain D.G., Martin K.C., Kandel E.R., Schwartz J.H. Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell. 89:1997;115-126.
18. Henderson J.T., Georgiou J., Jia Z., Robertson J., Elowe S., Roder J.C., Pawson T. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron. 32:2001;1041-1056.
19. Huang Y.S., Jung M.Y., Sarkissian M., Richter J.D. N-methyl-D-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and alpha CaMKII mRNA polyadenylation at synapses. EMBO J. 21:2002;2139-2148.
20. Khan A., Pepio A.M., Sossin W.S. Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysia synaptosomes. J. Neurosci. 21:2001;382-391.
21. Kim C.H., Lisman J.E. A role of actin filament in synaptic transmission and long-term potentiation. J. Neurosci. 19:1999;4314-4324.
22. Kim J.H., Udo H., Li H.L., Youn T.Y., Chen M., Kandel E.R., Bailey C.H. Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron. 40:2003;151-165.
23. Lantz V., Ambrosio L., Schedl P. The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos. Development. 115:1992;75-88.
24. Liu J., Schwartz J.H. The cytoplasmic polyadenylation element binding protein and polyadenylation of messenger RNA in Aplysia neurons. Brain Res. 959:2003;68-76.
25. Liu Q.R., Hattar S., Endo S., MacPhee K., Zhang H., Cleary L.J., Byrne J.H., Eskin A. A developmental gene (Tolloid/BMP-1) is regulated in Aplysia neurons by treatments that induce long-term sensitization. J. Neurosci. 17:1997;755-764.
26. Loreni F., Thomas G., Amaldi F. Transcription inhibitors stimulate translation of 5′ TOP mRNAs through activation of S6 kinase and the mTOR/FRAP signalling pathway. Eur. J. Biochem. 267:2000;6594-6601.
27. Martin K.C., Casadio A., Zhu H., Yapping E., Rose J.C., Chen M., Bailey C.H., Kandel E.R. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses. a function for local protein synthesis in memory storage Cell. 91:1997;927-938.
28. McGrew L.L., Dworkin-Rastl E., Dworkin M.B., Richter J.D. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 3:1989;803-815.
29. Mendez R., Richter J.D. Translational control by CPEB. a means to the end Nat. Rev. Mol. Cell Biol. 2:2001;521-529.
30. Mendez R., Hake L.E., Andresson T., Littlepage L.E., Ruderman J.V., Richter J.D. Phosphorylation of CPE binding factor by Eg2 regulates translation of c-mos mRNA. Nature. 404:2000;302-307. a.
31. Mendez R., Murthy K.G., Ryan K., Manley J.L., Richter J.D. Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Mol. Cell. 6:2000;1253-1259. b.
32. Moccia R., Chen D., Lyles V., Kapuya E., Yapping E., Kalachikov S., Spahn C.M., Frank J., Kandel E.R., Barad M., Martin K.C. An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J. Neurosci. 23:2003;9409-9417.
33. Montarolo P.G., Goelet P., Castellucci V.F., Morgan J., Kandel E.R., Schacher S. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science. 234:1986;1249-1254.
34. Reverte C.G., Yuan L., Keady B.T., Lacza C., Attfield K.R., Mahon G.M., Freeman B., Whitehead I.P., Hake L.E. XGef is a CPEB-interacting protein involved in Xenopus oocyte maturation. Dev. Biol. 255:2003;383-398.
35. Salles F.J., Strickland S. Analysis of poly(A) tail lengths by PCR. the PAT assay Methods Mol. Biol. 118:1999;441-448.
36. Schroeder K.E., Condic M.L., Eisenberg L.M., Yost H.J. Spatially regulated translation in embryos. asymmetric expression of maternal Wnt-11 along the dorsal-ventral axis in Xenopus Dev. Biol. 214:1999;288-297.
37. Schwarze S.R., Dowdy S.F. In vivo protein transduction. Intracellular delivery of biologically active proteins, compounds and DNA Trends Pharmacol. Sci. 21:2000;45-48.
38. Si K., Lindquist S., Kandel E.R. A neuronal isoform of the Aplysia CPEB has prion-like properties. Cell. 115:2003;879-891. , this issue.
39. Stebbins-Boaz B., Hake L.E., Richter J.D. CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 15:1996;2582-2592.
40. Stebbins-Boaz B., Cao Q., de Moor C.H., Mendez R., Richter J.D. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol. Cell. 4:1999;1017-1027.
41. Tan L., Chang J.S., Costa A., Schedl P. An autoregulatory feedback loop directs the localized expression of the Drosophila CPEB protein Orb in the developing oocyte. Development. 128:2001;1159-1169.
42. Theis M., Si K., Kandel E.R. Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proc. Natl. Acad. Sci. USA. 100:2003;9602-9607.
43. Wu L., Wells D., Tay J., Mendis D., Abbott M.A., Barnitt A., Quinlan E., Heynen A., Fallon J.R., Richter J.D. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron. 21:1998;1129-1139.