CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of α-CaMKII mRNA at synapses

Neuron

Volumn 21, Issue 5, 1998, Pages 1129-1139

  Wu, Lin ^a   Wells, David ^b   Tay, Joyce ^a   Mendis, Duane ^b   Abbott, Mary Alice ^b   Barnitt, Allan ^b,c   Quinlan, Elizabeth ^b   Heynen, Arnold ^b   Fallon, Justin R ^b   Richter, Joel D ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BROWN UNIVERSITY   (United States)

^c ASSUMPTION COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CIS ACTING ELEMENT; MESSENGER RNA; PROTEIN KINASE (CALCIUM,CALMODULIN) II;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; EXPERIENCE; HIPPOCAMPUS; LONG TERM POTENTIATION; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NONHUMAN; OOCYTE; OVARY; POLYADENYLATION; PRIORITY JOURNAL; RAT; RNA TRANSLATION; SYNAPSE; VISUAL CORTEX; XENOPUS;

EID: 0032215079     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80630-3     Document Type: Article

References (64)

1. Bailey, C.H., Bartsch, D., and Kandel, E.R. (1996). Toward a molecular definition of long-term memory storage. Proc. Natl. Acad. Sci. USA 93, 13445-13452.
2. Banker, G., and Goslin, K. (1991). Culturing nerve cells. (Cambridge, MA: MIT Press).
3. Bartlett, W.P., and Banker, G.A. (1984). An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. II. synaptic relationships. J. Neurosci. 4, 1954-1965.
4. Bear, M.F., and Malenka, R.C. (1994). Synaptic plasticity: LTP and LTD. Curr. Opin. Neurobiol. 4, 389-399.
5. Bilger, A., Fox, C.A., Wahle, E., and Wickens, M. (1994). Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements. Genes Dev. 8, 1106-1116.
6. Bouvet, P., Omilli, F., Arlot-Bonnemains, Y., Legagneux, V., Roghi, C., Bassez, T., and Osborne, H.B. (1994). The deadenylation conferred by the 39untranslated region of a developmentally controlled mRNA in Xenopus embryos is switched to polyadenylation by deletion of a short sequence element. Mol. Cell. Biol. 14, 1893-1900.
7. Carlin, R.K., Grab, D.J., Cohen, R.S. and Siekevitz, P. (1980). Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 86, 831-845.
8. Carrazana, E., Pasieka, K., and Majzoub, J. (1988). The vasopressin mRNA poly(A) tract is unusually long and increases during stimulation of vasopressin gene expression in vivo. Mol. Cell. Biol. 8, 2267-2274.
9. Chen, C.Y., and Shyu, A.B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470.
10. Chicurel, M.E., Terrian, D.M., and Potter, H. (1993). mRNA at the synapse: analysis of a preparation enriched in hippocampal dendritic spines. J. Neurosci. 13, 4054-4063.
11. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
12. Crino, P.B., and Eberwine, J. (1996). Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis. Neuron 17, 1173-1187.
13. Curtis, D., Lehmann, R., and Zamore, P.D. (1995). Translational regulation in development. Cell 81, 171-178.
14. Fletcher, T.L., Cameron, P., DeCamilli, P., and Banker, G. (1991). The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11, 1617-1626.
15. Fox, C.A., and Wickens, M. (1990). Poly(A) removal during oocyte maturation: a default reaction selectively prevented by specific sequences in the 39UTR of certain maternal mRNAs. Genes Dev. 4, 2287-2298.
16. Fox, C.A., Sheets, M.D., and Wickens, M. (1989). Poly(A) addition during oocyte maturation in frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev. 3, 2151-2162.
17. Frey, U., and Morris, R.G.M. (1997). Synaptic tagging and long-term potentiation. Nature 385, 533-536.
18. Frey, U., and Morris, R.G.M. (1998). Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci. 21, 181-188.
19. Frey, U., Huang, Y.Y., and Kandel, E.R. (1993). Effects of CAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260, 1661-1664.
20. Gebauer, F., Xu, W., Cooper, G.M., and Richter, J.D. (1994). Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 13, 5712-5720.
21. Gordon, J.A., Cioffi, D., Silva, A.J., and Stryker, M.P. (1996). Deficient plasticity in the primary visual cortex of a-calcium/calmodulin-dependent protein kinase II mutant mice. Neuron 17, 491-499.
22. Hake, L.E., and Richter, J.D. (1994). CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell 79, 617-628.
23. Hake, L.E., Mendez, R., and Richter, J.D. (1998). Specificity of RNA binding by CPEB: requirement for RNA recognition motifs and a novel zinc finger. Mol. Cell. Biol. 18, 685-693.
24. Harlow, E., and Lane, D. (1988). Antibodies: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
25. Hollingsworth, E.B., McNeal, E.T., Burton, J.L., Williams, R.J., Daly, J.W., and Creveling, C.R. (1985). Biochemical characterization of a filtered synaptoneurosome preparation from guinea pig cerebral cortex: cyclic adenosine 39:59-monophosphate-generating systems, receptors, and enzymes. J. Neurosci. 5, 2240-2253.
26. Huarte, J., Stutz, A., O'Connell, M.L., Gubler, P., Belin, D., Darrow, A.L., Strickland, S., and Vassalli, J.-D. (1992). Transient translational silencing by reversible mRNA deadenylation. Cell 69, 1021-1030.
27. Hyman, L.E., and Wormington, W.M. (1988). Translational inactivation of ribosomal protein mRNAs during Xenopus oocyte maturation. Genes Dev. 2, 598-605.
28. Jacobson, A. (1996). Poly(A) metabolism and translation: the closed loop model. In Translational Control, J.W.B. Hershey, M.B. Mathews, and N. Sonenberg, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
29. Kang, H., and Schuman, E.M. (1996). A requirement for local protein synthesis in neurotrophin-induced hippocampal plasticity. Science 273, 1402-1406.
30. Kuge, H., and Richter, J.D. (1995). Cytoplasmic 39poly(A) addition induces 59cap ribose methylation: implications for translational control of maternal mRNA. EMBO J. 14, 6301-6310.
31. Liu, X.J., Sorisky, A., Zhu, L., and Pawson, T. (1995). Molecular cloning of an amphibian insulin receptor substrate 1-like cDNA and involvement of phosphatidylinositol 3-kinase in insulin-induced Xenopus oocyte maturation. Mol. Cell. Biol. 15, 3563-3570.
32. Lledo, P.M., Hjelmstad, G.O., Mukherji, S., Soderling, T.R., Malenka, R.C., and Nicoll, R.A. (1995). Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc. Natl. Acad. Sci. USA 92, 11175-11179.
33. Maller, J.L., and Koontz, J.W. (1981). A study of the induction of cell division in amphibian oocytes by insulin. Dev. Biol. 85, 309-316.
34. Maller, J.L., and Krebs, E.G. (1980). Regulation of oocyte maturation. Curr. Top. Cell. Reg. 16, 217-311.
35. Martin, K.C., Casadio, A., Zhu, H.E.Y., Rose, J.C., Chen, M., Bailey, C.H., and Kandel, E.R. (1997). Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91, 927-938.
36. Mayford, M., Baranes, D., Podsypanina, K., and Kandel, E.R. (1996). The 39-untranslated region of a-CaMKII is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc. Natl. Acad. Sci. USA 93, 13250-13255.
37. McGrew, L.L., and Richter, J.D. (1990). Translational control by cytoplasmic polyadenylation during Xenopus oocyte maturation: characterization of cis and trans elements and regulation by cyclin/MPF. EMBO J. 9, 3743-3751.
38. McGrew, L.L., Dworkin-Rastl, E., Dworkin, M.B., and Richter, J.D. (1989). Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 3, 803-815.
39. Miyashiro, K., Dichetr, M., and Eberwine, J. (1994). On the nature and differential distributon of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc. Natl Acad. Sci. USA 91, 10800-10804.
40. Muslin, A.J., Klippel, A., and Williams, L.T. (1993). Phosphatidylinositol 3-kinase activity is important for progesterone-induced Xenopus oocyte maturation. Mol. Cell. Biol. 13, 6661-6666.
41. Ouyang, Y., Kantor, D., Harris, K.M., Schuman, E.M., and Kennedy, M.B. (1997). Visualization of the distribution of autophosphorylated calcium/calmodulin-dependent protein kinase II after tetanic stimulation in the CA1 area of the hippocampus. J. Neurosci. 17, 5416-5427.
42. cdc2 and phosphorylation of a 58-kDa CPE-binding protein. Genes Dev. 5, 1697-1708.
43. Pettit, D.L., Perlman, S., and Malinow, R. (1994). Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science 266, 1881-1885.
44. Richter, J.D. (1996). Dynamics of poly(A) addition and removal during development. In Translational Control, M. Mathews, J.W.B. Hershey, and N. Sonenberg, eds. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
45. Salles, F.J., Darrow, F.J., O'Connell, M.L., and Strickland, S. (1992). Isolation of novel murine maternal mRNAs regulated by cytoplasmic polyadenylation. Genes Dev. 6, 1202-1212.
46. Schuman, E.M. (1997). Synapse specificity and long-term information storage. Neuron 18, 339-342.
47. Sheets, M.D., Wu, M., and Wickens, M. (1995). Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature 374, 511-516.
48. Silva, A.J., Stevens, C.F., Tonegawa, S., and Wang, Y. (1992). Deficient hippocampal long term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 201-206.
49. Simon, R., and Richter, J.D. (1994). Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryonic cytoplasmic polyadenylation element-binding proteins. Mol. Cell. Biol. 14, 7867-7875.
50. Simon, R., Tassan, J.P., and Richter, J.D. (1992). Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev. 6, 2580-2591.
51. Simon, R., Wu, L., and Richter, J.D. (1996). Cytoplasmic polyadenylation of activin receptor mRNA and the control of pattern formation in Xenopus development. Dev. Biol. 179, 239-250.
52. Sossin, W.S. (1996). Mechanisms for the generation of synapse specificity in long-term memory: the implications for a requirement for transcription. Trends Neurosci. 19, 215-218.
53. Stebbins-Boaz, B., and Richter, J.D. (1994). Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early Xenopus development. Mol. Cell. Biol. 14, 5870-5880.
54. Stebbins-Boaz, B., and Richter, J.D. (1997). Translational control during early development. Crit. Rev. Eukar. Gene Expr. 71, 73-94.
55. Stebbins-Boaz, B., Hake, L.E., and Richter, J.D. (1996). CPEB controls the cytoplasmic polyadenylation of cyclin, cdk2, and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 15, 2582-2592.
56. Steward, O. (1997). mRNA localization in neurons: a multipurpose mechanism? Neuron 18, 9-12.
57. Steward, O., and Falk, P.M. (1986). Protein synthetic machinery at postsynaptic sires during synaptogenesis: a quantitative study of the association between polyribosomes and developing synapses. J. Neurosci. 6, 412-423.
58. Steward, O., and Levy, W.B. (1982). Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 2, 284-291.
59. Strickland, S., Huarte, J., Belin, D., Vassalli, A., Rickles, R.J., and Vassalli, J.-D. (1988). Antisense RNA directed against the 39noncoding region prevents dormant mRNA activation in mouse oocytes. Science 241, 680-684.
60. Tiedge, H., and Brosius, J. (1996). Translational machinery in dendrites of hippocampal neurons in culture. J. Neurosci. 16, 7171-7181.
61. Varnum, S.M., and Wormington, W.M. (1990). Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. Genes Dev. 4, 2278-2286.
62. Vassalli, J.-D., Huarte, J., Belin, D., Gubler, P., Vassalli, A., O'Connell, M.L., Parton, L.A., Ricklens, R.J., and Strickland, S. (1989). Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev. 3, 2163-2171.
63. Wu, G.Y, and Cline, H.T. (1998). Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279, 222-226.
64. Wu, L., Good, P.J., and Richter, J.D. (1997). The 36-kilodalton embryonic-type cytoplasmic polyadenylation element binding protein in Xenopus laevis is ElrA, a member of the ELAV family of RNA-binding proteins. Mol. Cell. Biol. 17, 6402-6409.