Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin

Cell

Volumn 92, Issue 1, 1998, Pages 25-37

  Winder, Danny G ^a   Mansuy, Isabelle M ^a   Osman, Mona ^a   Moallem, Theodore M ^a   Kandel, Eric R ^a  

^a New York Stt Psychiat Inst ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; PHOSPHATASE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE OVEREXPRESSION; HIPPOCAMPUS; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS; MUS MUSCULUS;

EID: 0032498272     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80896-X     Document Type: Article

References (44)

1. Abel, T., Nguyen, P.V., Barad, M., Deuel, T.A.S., Kandel, E.R., and Bourtchouladze, R. (1997). Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampal-based long-term memory. Cell 88, 1-11.
2. Bartsch, D., Ghirardi, M., Skehel, P.A., Karl, K.A., Herder, S.P., Chen, M., Bailey, C.M., and Kandel, E.R. (1995). Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83, 979-992.
3. Bear, M.F., and Abraham, W.C. (1996). Long-term depression in hippocampus. Annu. Rev. Neurosci. 19, 437-462.
4. 2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87, 1203-1214.
5. Blitzer, R.D., Wong, T., Nouranifar, R., Iyengar, R., and Landau, E.M. (1995). Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15, 1403-1414.
6. Bolshakov, V.Y., Golan, H., Kandel, E.R., and Siegelbaum, S.A. (1997). Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19, 635-651.
7. Choi, T., Huang, M., Gorman C., and Jaenisch, R. (1991). A generic intron increases gene expression in transgenic mice. Mol. Cell. Biol. 11, 3070-3074.
8. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid gnanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
9. Gustafson, E.L., Girault, J.A., Hemmings, H.C., Jr., Nairn, A.C., and Greengard, P. (1991) Immunocytochemical localization of phosphatase inhibitor-1 in rat brain. J. Comp. Neurol. 310, 170-188.
10. Figurov, A., Boddeke, H., and Muller, D. (1993). Enhancement of AMPA-mediated synaptic transmission by the protein phosphatase inhibitor calyculin A in rat hippocampal slices. Eur. J. Neurosci. 5, 1035-1041.
11. 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.
12. Helekar, S.A., and Patrick, J. (1997). Peptidyl prolyl cis-trans isomerase activity of cyclophilin Ain functional homo-oligomeric receptor expression. Proc. Natl. Acad. Sci. USA 94, 5432-5437.
13. Hogan, B., Beddington, R., Constantini, F., and Lacy, E. (1994). Manipulating the Mouse Embryo, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory).
14. Huang, Y.-Y., Nguyen, P.V., Abel, T., and Kandel, E.R. (1996). Longlasting forms of synaptic potentiation in the mammalian hippocampus. Learn. Mem. 3, 74-85.
15. Hubbard, M.J., and Klee, C.B. (1991). Exogenous kinases and phosphatases as probes of intracellular modulation. In Molecular Neurobiology, A Practical Approach, J. Chad and H. Wheal, eds. (London: Oxford), pp. 135-157.
16. Klee, C.B. (1991). Concerted regulation of protein phosphorylation and dephosphorylation by calmodulin. Neurochem. Res. 16, 1059-1065.
17. Klee, C.B., Krinks, M.H., Manalan, A.S., Cohen, P., and Stewart, A.A. (1983). Isolation and characterization of bovine brain calcineurin: a calmodulin-stimulated protein phosphatase. Meth. Enzymol. 102, 227-244.
18. Kuno, T., Mukai, H., Ito, A., Chang, C.-D., Kishima, K., Saito, N., and Tanaka, C. (1992). Distinct cellular expression of calcineurin Aα and Aβ in rat brain. J. Neurochem. 58, 1643-1651.
19. Lisman, J. (1994). The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci. 17, 406-412.
20. Lu, Y.-F., Tomizawa, K., Morikawa, A., Hayashi, Y., Tokuda, M., Itano, T., Hatase, O., and Matsui, H. (1996). Calcineurin inhibitors, FK506 and cyclosporin A, suppress the NMDA receptor-mediated potentials and LTP, but not depotentiation in the rat hippocampus. Brain Res. 729, 142-146.
21. Mansuy, I.M., Mayford, M., Jacob, B., Kandel, E.R., and Bach, M.E. (1998). Restricted and regulated overexpression reveals calcineurin as a regulator of the transition between hippocampal-dependent short- and long-term memory. Cell 92, this issue, 39-49.
22. Martin, K.C., Michael, D., Rose, J.C., Barad, M., Casadio, A., Zhu, H., and Kandel, E.R. (1997). MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18, 899-912.
23. Mayford, M., Mansuy, I.M., Muller, R.U., and Kandel, E.R. (1997). Memory and behavior: a second generation of genetically modified mice. Curr. Biol. 7, R580-R589.
24. Mulkey, R.M., Endo, S., Shenolikar, S., and Malenka, R.C. (1994). Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486-488.
25. Muller, D., Hefft, S., and Figurov, A. (1995). Heterosynaptic interactions between LTP and LTD in CA1 hippocampal slices. Neuron 14, 599-605.
26. O'Keefe, S.J., Tamura, J., Kincaid, R., Tocci, M.J., and O'Neill, E.A. (1992). FK-506 and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357, 692-694.
27. Osten, P., Valsamis, L., Harris, A., and Sacktor, T.C. (1996). Protein synthesis-dependent formation of protein kinase Mζ in long-term potentiation. J. Neurosci. 16, 2444-2451.
28. Parsons, J.N., Wiederrecht, G.J., Salowe, S., Burbaum, J.J., Rokosz, L.L., Kincaid, R.L., and O'Keefe, S.J. (1994). Regulation of calcineurin phosphatase activity and interaction with the FK-506-FK-506 binding protein complex. J. Biol. Chem. 269, 19610-19616.
29. Paterson, J.M., Smith, S.M., Harmar, A.J., and Antoni, F.A. (1995). Control of a novel adenylyl cyclase by calcineurin. Biochem. Biophys. Res. Comm. 214, 1000-1008.
30. Raman, I.M., Tong, G., and Jahr, C.E. (1996). β-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase. Neuron 16, 415-421.
31. Roberson, E.D., English, J.D., and Sweatt, J.D. (1996). A biochemist's view of long-term potentiation. Learn. Mem. 3, 1-24.
32. Sakagami, H., Ebina, K. and Kondo, H. (1994). Localization of phosphatase inhibitor-1 mRNA in the developing and adult rat brain in comparison with that of protein phosphatase-1 mRNAs. Mouse Brain Res. 25, 7-18.
33. 2+-dependent phosphatase calcineurin in gene transcription that is stimulated by cAMP through cAMP response elements. J. Biol. Chem. 270, 8860-8866.
34. Stanton, P.K., and Sarvey, J.M. (1984). Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J. Neurosci. 4, 3080-3088.
35. Thomas, M.J., Moody, T.D., Makhinson, M., and O'Dell, T.J. (1996). Activity-dependent β-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17, 475-482.
36. Tong, G., Shepherd, D., and Jahr, C.E. (1995). Synaptic desensitization of NMDA receptors by calcineurin. Science 267, 1510-1512.
37. Traynelis, S.F., and Wahl, P. (1997). Control of rat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J. Physiol. 503, 513-531.
38. 2+-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn. Mem. 3, 170-181.
39. 2+ signaling mechanisms in hippocampal CA1 neurons. J. Neurosci. 17, 4600-4611.
40. Wang, J.-H., and Stelzer, A. (1994). Inhibition of phosphatase 2B prevents expression of hippocampal long-term potentiation. Neuroreport 5, 2377-2380.
41. Yakel, J.L. (1997). Calcineurin regulation of synaptic function: from ion channels to transmitter release and gene transcription. Trends Neurosci. 18, 124-134.
42. Yin, J.C.P., Wallach, J.S., Del Vecchio, M., Wilder, E.L., Zhou, M., Quinn, W.G., and Tully, T. (1994). Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49-58.
43. Yin, J.C.P., Del Vecchio, M., Zhou, M., Quinn, W.G., and Tully, T. (1995). CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81, 107-115.
44. Zucker, R.S. (1989). Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13-31.