Autonomous activity of CaMKII is only transiently increased following the induction of long-term potentiation in the rat hippocampus

European Journal of Neuroscience

Volumn 20, Issue 11, 2004, Pages 3063-3072

  Lengyel, I ^a,c   Voss, K ^b   Cammarota, M ^c   Bradshaw, K ^b   Brent, V ^c   Murphy, K P S J ^b   Giese, K P ^d   Rostas, John A P ^c   Bliss, T V P ^b  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c UNIVERSITY OF NEWCASTLE   (Australia)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

CaMKII; Long term potentiation; Protein kinases; Protein phosphatases; Protein phosphorylation

Indexed keywords

PROTEIN KINASE (CALCIUM,CALMODULIN) II; TETRYLAMMONIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; AUTOPHOSPHORYLATION; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; GENETIC MANIPULATION; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MOLECULAR MECHANICS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION;

ANIMALS; BLOTTING, WESTERN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; ELECTRIC STIMULATION; ENZYME ACTIVATION; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; PHOSPHORYLATION; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; TETRAETHYLAMMONIUM; THREONINE; TIME FACTORS;

EID: 10844270517     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03748.x     Document Type: Article

References (79)

1. + channel blocker in the hippocampus. Nature, 349, 67-69.
2. Atkins, C.M., Selcher, J.C., Petraitis, J.J., Trzaskos, J.M. & Sweatt, J.D. (1998) The MAPK cascade is required for mammalian associative learning. Nat. Neurosci., 1, 602-609.
3. Barria, A., Muller, D., Derkach, V., Griffith, L.C. & Soderling, T.R. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science, 276, 2042-2045.
4. Bayer, K.U., De Koninck, P., Leonard, A.S., Hell, J.W. & Schulman, H. (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature, 411, 801-805.
5. Bennett, M.R., Gibson, W.G. & Robinson, J. (1994) Dynamics of the CA3 pyramidal neuron autoassociative memory network in the hippocampus. Phil. Trans., 343, 167-187.
6. Bliss, T.V.B. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in hippocampus. Nature, 359, 417-420.
7. Blitzer, R.D., Connor, J.H., Brown, G.P., Wong, T., Shenolikar, S., Iyengar, R. & Landau, E.M. (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science, 280, 1940-1942.
8. Brocke, L., Chiang, L.W., Wagner, P.D. & Schulman, H. (1999) Functional implications of the subunit composition of neuronal CaM kinase II. J. Biol. Chem., 274, 22713-22722.
9. 2+-calmodulin and protein kinase Cs: a hypothetical synthesis of their conflicting convergences on shared substrate domains. Trends Neurosci., 22, 12-16.
10. Chang, B.H., Mukherji, S. & Soderling, T.R. (1998) Characterization of a calmodulin kinase II inhibitor protein in brain. Proc. Natl Acad. Sci. USA, 95, 10890-10895.
11. Chang, B.H., Mukherji, S. & Soderling, T.R. (2001) Calcium/calmodulin-dependent protein kinase II inhibitor protein: localization of isoforms in rat brain. Neuroscience, 102, 767-777.
12. Chen, H.X., Otmakhov, N., Strack, S., Colbran, R.J. & Lisman, J.E. (2001) Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? J. Neurophysiol., 85, 1368-1376.
13. 2+ oscillations. Science, 279, 227-230.
14. 2+/calmodulin-dependent protein kinase. J. Biol. Chem., 269, 31330-31333.
15. Elgersma, Y., Fedorov, N.B., Choi, E.S., Elgersma, M., Carvalho, O.M., Giese, K.P. & Silva, A.J. (2002) Inhibitory autophosphorylation of CaMKII controls PSD association. Neuron, 36, 493-505.
16. Feng, T.P. (1995) The involvement of PKC and multifunctional CaM kinase II of the postsynaptic neuron in induction and maintenance of long-term potentiation. Prog. Brain Res., 105, 55-63.
17. 2+/calmodulin-dependent protein kinase II by protein phosphatase 2C. J. Biol. Chem., 268, 133-137.
18. Fukunaga, K., Muller, D. & Miyamoto, E. (1996) CaM kinase II in long-term potentiation. Neurochem. Int., 28, 343-358.
19. Fukunaga, K., Muller, D., Ohmitsu, M., Bako, E., DePaoli-Roach, A.A. & Miyamoto, E. (2000) Decreased protein phosphatase 2A activity in hippocampal long-term potentiation. J. Neurochem., 74, 807-817.
20. 2+/calmodulin-dependent protein kinase II. J. Biol. Chem., 268, 7863-7867.
21. Gardoni, F., Caputi, A., Cimino, M., Pastorino, L., Cattabeni, F. & Di Luca, M. (1998) Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J. Neurochem., 71, 1733-1741.
22. Genoux, D., Haditsch, U., Knobloch, M., Michalon, A., Storm, D. & Mansuy, I.M. (2002) The protein phosphatase 1 is a molecular constraint on learning and memory. Nature, 418, 970-975.
23. Gibson, W.G., Robinson, J. & Bennett, M.R. (1991) Probabilistic secretion of quanta in the central nervous system: granule cell synaptic control of pattern separation and activity regulation. Phil. Trans., 332, 199-220.
24. Giese, K.P., Fedorov, N.B., Filipkowski, R.K. & Silva, A.J. (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science, 279, 870-873.
25. Hajimohammadreza, I., Raser, K.J., Nath, R., Nadimpalli, R., Scott, M. & Wang, K.K. (1997) Neuronal nitric oxide synthase and calmodulin-dependent protein kinase IIalpha undergo neurotoxin-induced proteolysis. J. Neurochem., 69, 1006-1013.
26. 2+/calmodulin-dependent protein kinase and mutational analysis of its autoregulation. Neuron, 3, 59-70.
27. 2+/calmodulin-dependent protein kinase analyzed by site-directed mutagenesis. J. Biol. Chem., 267, 17216-17224.
28. 2+/calmodulin- dependent kinase II. Mol. Cell, 11, 1241-1251.
29. Hosokawa, T., Rusakov, D.A., Bliss, T.V. & Fine, A. (1995) Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J. Neurosci., 15, 5560-5573.
30. Huang, C.C., Liang, Y.C. & Hsu, K.S. (2001) Characterization of the mechanism underlying the reversal of long term potentiation by low frequency stimulation at hippocampal CA1 synapses. J. Biol. Chem., 276, 48108-48117.
31. 2+ channels in the induction of LTP. J. Neurosci., 13, 568-576.
32. Huber, K.M., Mauk, M.D. & Kelly, P.T. (1995a) Distinct LTP induction mechanisms: contribution of NMDA receptors and voltage-dependent calcium channels. J. Neurophysiol., 73, 270-279.
33. 2+ channels requires protein kinase activity. Neuroreport, 6, 1281-1284.
34. 2+/calmodulin-dependent protein kinase II during autophosphorylation. J. Biol. Chem., 271, 8800-8808.
35. Hudmon, A., Kim, S.A., Kolb, S.J., Stoops, J.K. & Waxham, M.N. (2001) Light scattering and transmission electron microscopy studies reveal a mechanism for calcium/calmodulin-dependent protein kinase II self association. J. Neurochem., 76, 1364-1375.
36. 2+/calmodulin- dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu. Rev. Biochem., 71, 473-510.
37. Hvalby, O., Hemmings, H.C. Jr, Paulsen, O., Czernik, A.J., Nairn, A.C., Godfraind, J.-M., Jensen, V., Raastad, M., Storm, J.F., Andersen, P. & Greengard, P. (1994) Specificity of protein kinase inhibitor peptides and induction of long-term potentiation. Proc. Natl Acad. Sci. USA, 91, 4761-4765.
38. Ishida, A., Kameshita, I., Okuno, S., Kitani, T. & Fujisawa, H. (1995) A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem. Biophys. Res. Commun., 212, 806-812.
39. Klann, E., Chen, S.J. & Sweatt, J.D. (1993) Mechanism of protein kinase C activation during the induction and maintenance of long-term potentiation probed using a selective peptide substrate. Proc. Natl Acad. Sci. USA, 90, 8337-8341.
40. 2+/ calmodulin kinase II translocates in a hippocampal slice model of ischemia. J. Neurochem., 64, 2147-2156.
41. Krucker, T., Siggins, G.R., McNamara, R.K., Lindsley, K.A., Dao, A., Allison, D.W., de Lecea, L., Lovenberg, T.W., Sutcliffe, J.G. & Gerendasy, D.D. (2002) Targeted disruption of RC3 reveals a calmodulin-based mechanism for regulating metaplasticity in the hippocampus. J. Neurosci., 22, 5525-5535.
42. Kwiatkowski, A.P. & King, M.M. (1989) Authophosphorylation of the type II calmodulin-dependent protein kinase is essential for formation of a proteolytic fragment with catalytic activity implications for long-term synaptic potentiation. Biochemistry, 28, 5380-5385.
43. Lengyel, I., Cammarota, M., Brent, V.A. & Rostas, J.A. (2001) Autonomous activity and autophosphorylation of CAMPK-II in rat hippocampal slices: effects of tissue preparation. J. Neurochem., 76, 149-154.
44. Lengyel, I., Fieuw-Makaroff, S., Hall, A.L., Sim, A.T., Rostas, J.A. & Dunkley, P.R. (2000) Modulation of the phosphorylation and activity of calcium/calmodulin-dependent protein kinase II by zinc. J. Neurochem., 75, 594-605.
45. 2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. J. Physiol. (Lond.), 532, 285.
46. Lisman, J., Schulman, H. & Cline, H. (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci., 3, 175-190.
47. Lisman, J.E. & Zhabotinsky, A.M. (2001) A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron, 31, 191-201.
48. Lledo, P.M., Hjelmstad, G.O., Mukherji, S., Soderling, T.R.X., Malenka, R.C. & 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.
49. 2+/Calmodulin-dependent kinase II autophosphorylation. J. Neurosci., 19, 2500-2510.
50. Malenka, R.C., Kauer, J.A., Perkel, D.J., Mauk, M.D., Kelly, P.T., Nicoll, R.A. & Waxham, M.N. (1989) An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature, 340, 554-557.
51. Malgaroli, A., Malinow, R., Schulman, H. & Tsien, R.W. (1992) Persistent signalling and changes in presynaptic function in long-term potentiation. CIBA Found. Symp, 164, 176-191.
52. Malinow, R., Schulman, H. & Tsien, R.W. (1989) Inhibition of postsynaptic PKC or CAMK-II blocks induction but not expression of LTP. Science, 245, 862-866.
53. Martin, K.C., Michael, D., Rose, J.C., Barad, M., Casadio, A., Zhu, H. & 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.
54. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D. & Kandel, E.R. (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science, 274, 1678-1683.
55. 2+/calmodulin-dependent protein kinase II with neuronal cytoskeletal proteins. Characterization of binding to a 190-kDa postsynaptic density protein. J. Biol. Chem., 270, 10043-10049.
56. Meyer, T., Hanson, P.I., Stryer, L. & Schulman, H. (1992) Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science, 256, 1199-1202.
57. 2+-triggered molecular switch. Cell, 44, 861-870.
58. 2+/calmodulin-dependent protein kinase II phosphorylation of the presynaptic protein synapsin I is persistently increased during long-term potentiation. Proc. Natl Acad. Sci. USA, 93, 15451-15456.
59. + current of rat hippocampal neurones in vitro. J. Physiol. (Lond.), 457, 575-590.
60. 2+/calmodulin-activated protein kinase II to syntaxin 1A. J. Neurosci., 22, 3342-3351.
61. Otmakhov, N., Griffith, L.C. & Lisman, J.E. (1997) Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J. Neurosci., 17, 5357-5365.
62. Otmakhova, N.A., Otmakhov, N., Mortenson, L.H. & Lisman, J.E. (2000) Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J. Neurosci., 20, 4446-4451.
63. Ouyang, Y., Kantor, D., Harris, K.M., Schuman, E.M. & 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.
64. Ouyang, Y., Rosenstein, A., Kreiman, G., Schuman, E.M. & Kennedy, M.B. (1999) Tetanic stimulation leads to increased accumulation of Ca (2+) /Calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J. Neurosci., 19, 7823-7833.
65. Patton, B.L., Molloy, S.S. & Kennedy, M.B. (1993) Autophosphorylation of type II CaM kinase in hippocampal neurons: localization of phospho- and dephosphokinase with complementary phosphorylation site-specific antibodies. Mol. Biol. Cell, 4, 159-172.
66. Pettit, D.L., Perlman, S. & Malinow, R. (1994) Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science, 266, 1881-1885.
67. Shen, K. & Meyer, T. (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science, 284, 162-166.
68. Silva, A.J., Wang, Y., Paylor, R., Wehner, J.M., Stevens, C.F. & Tonegawa, S. (1992) Alpha calcium/calmodulin kinase II mutant mice: deficient long-term potentiation and impaired spatial learning. CSHS Quantit. Biol., 57, 527-539.
69. 2+/calmodulin-dependent protein kinase II by protein phosphatases 1 and 2A. J. Neurochem., 68, 2119-2128.
70. Strack, S., Choi, S., Lovinger, D.M. & Colbran, R.J. (1997b) Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density. J. Biol. Chem., 272, 13467-13470.
71. Strack, S. & Colbran, R.J. (1998) Autophosphorylation-dependent targeting of calcium/calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem., 273, 20689-20692.
72. Strack, S., Robison, A.J., Bass, M.A. & Colbran, R.J. (2000) Association of calcium/calmodulin-dependent kinase II with developmentally regulated splice variants of the postsynaptic density protein densin-180. J. Biol. Chem., 275, 25061-25064.
73. 2+/calmodulin-dependent protein kinase II into postsynaptic density after decapitation. J. Neurochem., 63, 1529-1537.
74. Tan, S.E. & Chen, S.S. (1997) The activation of calcium/calmodulin- dependent protein kinase II after glutamate or potassium stimulation in hippocampal slices. Brain Res. Bull., 43, 269-273.
75. Tompa, P. & Friedrich, P. (1998) Synaptic metaplasticity and the local charge effect in postsynaptic densities. Trends. Neurosci., 21, 97-102.
76. 2+/CaM induces synaptic potentiation requiring CaMKII and PKC activity. Neuron, 15, 443-452.
77. Wang, J.H. & Kelly, P.T. (1996) The balance between postsynaptic Ca (2+)-dependent protein kinase and phosphatase activities controlling synaptic strength. Learn. Mem., 3, 170-181.
78. Yang, H.W., Hu, X.D., Zhang, H.M., Xin, W.J., Li, M.T., Zhang, T., Zhou, L.J. & Liu, X.G. (2004) Roles of CaMKII, PKA, and PKC in the induction and maintenance of LTP of C-fiber-evoked field potentials in rat spinal dorsal horn. J. Neurophysiol., 91, 1122-1133.
79. 2+/calmodulin-dependent protein kinase II from postsynaptic densities. FEBS Lett., 446, 239-242.