On the Mechanism of Synaptic Depression Induced by CaMKIIN, an Endogenous Inhibitor of CaMKII

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Gouet, Camilo ^a   Aburto, Belen ^a   Vergara, Cecilia ^a   Sanhueza, Magdalena ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM DEPRESSION; NERVE EXCITABILITY; NEUROMODULATION; NEWBORN; NONHUMAN; POSTSYNAPTIC POTENTIAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS INHIBITION; RAT; RESPONSE TIME; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CARRIER PROTEINS; HIPPOCAMPUS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER;

RATTUS;

EID: 84869046072     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049293     Document Type: Article

References (51)

1. Colbran RJ, Brown AM, (2004) Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr Opin Neurobiol 14: 318-327.
2. Elgersma Y, Sweatt JD, Giese KP, (2004) Mouse genetic approaches to investigating calcium/calmodulin-dependent protein kinase II function in plasticity and cognition. J Neurosci 24: 8410-8415.
3. Strack S, Choi S, Lovinger DM, Colbran RJ, (1997) Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density. J Biol Chem 272: 13467-13470.
4. Shen K, Meyer T, (1999) Dynamic control of CaMKII translocation and localization. Science 284: 162-166.
5. Otmakhov N, Tao-Cheng J-H, Carpenter S, Asrican B, Dosemeci A, et al. (2004) Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. J Neurosci 24: 9324-9331.
6. Strack S, Colbran RJ, (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.
7. Bayer KU, De Koninck P, Leonard AS, Hell JW, Schulman H, (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411: 801-805.
8. Lisman J, Yasuda R, Raghavachari S, (2012) Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13: 169-182.
9. Malinow R, Schulman H, Tsien RW, (1989) Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245: 862-866.
10. Silva AJ, Stevens CF, Tonegawa S, Wang Y, (1992) Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257: 201-206.
11. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ, (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279: 870-873.
12. Barria A, Malinow R, (2005) NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48: 289-301.
13. Zhou Y, Takahashi E, Li W, Halt A, Wiltgen B, et al. (2007) Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. J Neurosci 27: 13843-13853.
14. Halt AR, Dallapiazza RF, Zhou Y, Stein IS, Qian H, et al. (2012) CaMKII binding to GluN2B is critical during memory consolidation. EMBO J 31: 1203-1216.
15. Lucchesi W, Mizuno K, Giese KP, (2011) Novel insights into CaMKII function and regulation during memory formation. Brain Res Bull 85: 2-8.
16. Asrican B, Lisman J, Otmakhov N, (2007) Synaptic strength of individual spines correlates with bound Ca2+-calmodulin-dependent kinase II. J Neurosci 27: 14007-14011.
17. Petralia RS, Sans N, Wang Y-xian, Wenthold RJ, (2005) Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 29: 436-452.
18. Swulius MT, Kubota Y, Forest A, Waxham MN, (2010) Structure and composition of the postsynaptic density during development. J Comp Neurol 518: 4243-4260.
19. Merrill MA, Chen Y, Strack S, Hell JW, (2005) Activity-driven postsynaptic translocation of CaMKII. Trends Pharmacol Sci 26: 645-653.
20. Okabe S, (2007) Molecular anatomy of the postsynaptic density. Mol Cell Neurosci 34: 503-518.
21. Chang BH, Mukherji S, Soderling TR, (1998) Characterization of a calmodulin kinase II inhibitor protein in brain. Proc Natl Acad Sci U S A 95: 10890-10895.
22. Vest RS, Davies KD, Leary HO, Port JD, Bayer KU, (2007) Dual mechanism of a natural CaMKII inhibitor. Mol Biol Cell 18: 5024-5033.
23. Chang BH, Mukherji S, Soderling TR, (2001) Calcium/calmodulin-dependent protein kinase II inhibitor protein: localization of isoforms in rat brain. Neuroscience 102: 767-777.
24. Radwańska K, Tudor-Jones AA, Mizuno K, Pereira GS, Lucchesi W, et al. (2010) Differential regulation of CaMKII inhibitor beta protein expression after exposure to a novel context and during contextual fear memory formation. Genes Brain Behav 9: 648-657.
25. Saha S, Datta K, Rangarajan P, (2007) Characterization of mouse neuronal Ca2+/calmodulin kinase II inhibitor alpha. Brain Res 1148: 38-42.
26. Lepicard EM, Mizuno K, Antunes-Martins A, von Hertzen LSJ, Giese KP, (2006) An endogenous inhibitor of calcium/calmodulin-dependent kinase II is up-regulated during consolidation of fear memory. Eur J Neurosci 23: 3063-3070.
27. Sanhueza M, McIntyre CC, Lisman JE, (2007) Reversal of synaptic memory by Ca2+/calmodulin-dependent protein kinase II inhibitor. J Neurosci 27: 5190-5199.
28. Sanhueza M, Fernandez-Villalobos G, Stein IS, Kasumova G, Zhang P, et al. (2011) Role of the CaMKII/NMDA receptor complex in the maintenance of synaptic strength. J Neurosci 31: 9170-9178.
29. Waung MW, Huber KM, (2010) Protein translation in synaptic plasticity: mGluR-LTD, Fragile X. Curr Opin Neurobiol. 19: 319-326.
30. Malenka RC, Bear MF, (2004) LTP and LTD: an embarrassment of riches. Neuron 44: 5-21.
31. Oliet SH, Malenka RC, Nicoll RA, (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18: 969-982.
32. Hudmon A, Schulman H, Kim J, Maltez JM, Tsien RW, et al. (2005) CaMKII tethers to L-type Ca2+ channels, establishing a local and dedicated integrator of Ca2+ signals for facilitation. J Cell Biol 171: 537-547.
33. Abiria SA, Colbran RJ, (2010) CaMKII associates with CaV1.2 L-type calcium channels via selected β subunits to enhance regulatory phosphorylation. J Neurochem 112: 150-161.
34. Karpova A, Mikhaylova M, Thomas U, Knöpfel T, Behnisch T, (2006) Involvement of protein synthesis and degradation in long-term potentiation of Schaffer collateral CA1 synapses. J Neurosci 26: 4949-4955.
35. Fonseca R, Vabulas RM, Hartl FU, Bonhoeffer T, Nägerl UV, (2006) A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52: 239-245.
36. Huber KM, Kayser MS, Bear MF, (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288: 1254-1256.
37. Hou L, Antion MD, Hu D, Spencer CM, Paylor R, et al. (2006) Dynamic translational and proteasomal regulation of Fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 51: 441-454.
38. Xiao M-Y, Wasling P, Hanse E, Gustafsson B, (2004) Creation of AMPA-silent synapses in the neonatal hippocampus. Nat Neurosci 7: 236-243.
39. Carlier E, Dargent B, De Waard M, Couraud F, (2000) Na(+) channel regulation by calmodulin kinase II in rat cerebellar granule cells. Biochem Biophys Res Commun 274: 394-399.
40. Nelson AB, Gittis AH, du Lac S, (2005) Decreases in CaMKII activity trigger persistent potentiation of intrinsic excitability in spontaneously firing vestibular nucleus neurons. Neuron 46: 623-631.
41. Fitzjohn SM, Collingridge GL, (2002) Calcium stores and synaptic plasticity. Cell Calcium 32: 405-411.
42. Palm-Apergi C, Lorents A, Padari K, Pooga M, Hällbrink M, (2009) The membrane repair response masks membrane disturbances caused by cell-penetrating peptide uptake. FASEB J 23: 214-223.
43. Duchardt F, Fotin-Mleczek M, Schwarz H, Fischer R, Brock R, (2007) A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8: 848-866.
44. Newpher TM, Ehlers MD, (2008) Glutamate receptor dynamics in dendritic microdomains. Neuron 58: 472-497.
45. Choquet D, (2010) Fast AMPAR trafficking for a high-frequency synaptic transmission. Eur J Neurosci 32: 250-260.
46. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, et al. (2010) CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67: 239-252.
47. Lee S-JR, Escobedo-Lozoya Y, Szatmari EM, Yasuda R, (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458: 299-304.
48. Lengyel I, Voss K, Cammarota M, Bradshaw K, Brent V, et al. (2004) Autonomous activity of CaMKII is only transiently increased following the induction of long-term potentiation in the rat hippocampus. Eur J Neurosci 20: 3063-3072.
49. Feng B, Raghavachari S, Lisman J, (2011) Quantitative estimates of the cytoplasmic, PSD, and NMDAR-bound pools of CaMKII in dendritic spines. Brain Res 1419: 46-52.
50. Cheriyan J, Kumar P, Mayadevi M, Surolia A, Omkumar RV, (2011) Calcium/calmodulin dependent protein kinase II bound to NMDA receptor 2B subunit exhibits increased ATP affinity and attenuated dephosphorylation. PLoS One 6: e16495.
51. Mullasseril P, Dosemeci A, Lisman JE, Griffith LC, (2007) A structural mechanism for maintaining the "on-state" of the CaMKII memory switch in the post-synaptic density. J Neurochem 103: 357-364.