Translocation of CaMKII to dendritic microtubules supports the plasticity of local synapses

Journal of Cell Biology

Volumn 198, Issue 6, 2012, Pages 1055-1073

  Lemieux, Mado ^a   Labrecque, Simon ^a   Tardif, Christian ^a   Labrie Dion, Étienne ^a   LeBel, Éric ^a   De Koninck, Paul ^a,b  

^a CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; MUTANT PROTEIN; POSTSYNAPTIC RECEPTOR;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CALCIUM TRANSPORT; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; ENZYME LOCALIZATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; MICROTUBULE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELLS, CULTURED; DENDRITES; GLUTAMIC ACID; GLYCINE; HIPPOCAMPUS; MICROTUBULES; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RECEPTORS, AMPA; SPINE; SYNAPSES;

EID: 84869102343     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201202058     Document Type: Article

References (67)

1. Augustine, G.J., F. Santamaria, and K. Tanaka. 2003. Local calcium signaling in neurons. Neuron. 40:331-346. http://dx.doi.org/10.1016/S0896-6273 (03)00639-1
2. Baratier, J., L. Peris, J. Brocard, S. Gory-Fauré, F. Dufour, C. Bosc, A. Fourest-Lieuvin, L. Blanchoin, P. Salin, D. Job, and A. Andrieux. 2006. Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II. J. Biol. Chem. 281:19561-19569. http://dx.doi.org/10.1074/jbc.M509602200
3. Baudier, J., and R.D. Cole. 1987. Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalyzed by a calcium/calmodulindependent kinase and modulated by phospholipids. J. Biol. Chem. 262:17577-17583.
4. Bayer, K.U., P. De Koninck, A.S. Leonard, J.W. Hell, and H. Schulman. 2001. Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature. 411:801-805. http://dx.doi.org/10.1038/35081080
5. Bayer, K.U., E. LeBel, G.L. McDonald, H. O'Leary, H. Schulman, and P. De Koninck. 2006. Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J. Neurosci. 26:1164-1174. http://dx.doi.org/10.1523/JNEUROSCI.3116-05.2006
6. Bengtson, C.P., H.E. Freitag, J.M. Weislogel, and H. Bading. 2010. Nuclear calcium sensors reveal that repetition of trains of synaptic stimuli boosts nuclear calcium signaling in CA1 pyramidal neurons. Biophys. J. 99: 4066-4077. http://dx.doi.org/10.1016/j.bpj.2010.10.044
7. Branco, T., and M. Häusser. 2010. The single dendritic branch as a fundamental functional unit in the nervous system. Curr. Opin. Neurobiol. 20:494-502. http://dx.doi.org/10.1016/j.conb.2010.07.009
8. Chalifoux, J.R., and A.G. Carter. 2011. Glutamate spillover promotes the generation of NMDA spikes. J. Neurosci. 31:16435-16446. http://dx.doi.org/10.1523/JNEUROSCI.2777-11.2011
9. Colbran, R.J. 2004. Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378:1-16. http://dx.doi.org/10.1042/BJ20031547
10. Conde, C., and A. Cáceres. 2009. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 10:319-332. http://dx.doi.org/10.1038/nrn2631
11. Correia, S.S., S. Bassani, T.C. Brown, M.F. Lisé, D.S. Backos, A. El-Husseini, M. Passafaro, and J.A. Esteban. 2008. Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat. Neurosci. 11:457-466. http://dx.doi.org/10.1038/nn2063
12. Emptage, N., T.V. Bliss, and A. Fine. 1999. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron. 22:115-124. http://dx.doi.org/10.1016/S0896-6273(00)80683-2
13. Fink, C.C., K.U. Bayer, J.W. Myers, J.E. Ferrell Jr., H. Schulman, and T. Meyer. 2003. Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron. 39:283-297. http://dx.doi.org/10.1016/S0896-6273(03)00428-8
14. Frey, U., and R.G. Morris. 1998. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci. 21:181-188. http://dx.doi.org/10.1016/S0166-2236(97)01189-2
15. Govindarajan, A., R.J. Kelleher, and S. Tonegawa. 2006. A clustered plasticity model of long-term memory engrams. Nat. Rev. Neurosci. 7:575-583. http://dx.doi.org/10.1038/nrn1937
16. Govindarajan, A., I. Israely, S.Y. Huang, and S. Tonegawa. 2011. The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron. 69:132-146. http://dx.doi.org/10.1016/j.neuron.2010.12.008
17. Guillaud, L., R. Wong, and N. Hirokawa. 2008. Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat. Cell Biol. 10:19-29. http://dx.doi.org/10.1038/ncb1665
18. Hanson, P.I., and H. Schulman. 1992. Neuronal Ca2+/calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61:559-601. http://dx.doi.org/10.1146/annurev.bi.61.070192.003015
19. Hanson, P.I., T. Meyer, L. Stryer, and H. Schulman. 1994. Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals. Neuron. 12:943-956. http://dx.doi.org/10.1016/0896-6273(94)90306-9
20. Hardie, J., and N. Spruston. 2009. Synaptic depolarization is more effective than back-propagating action potentials during induction of associative long-term potentiation in hippocampal pyramidal neurons. J. Neurosci. 29:3233-3241. http://dx.doi.org/10.1523/JNEUROSCI.6000-08.2009
21. Harvey, C.D., and K. Svoboda. 2007. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature. 450:1195-1200. http://dx.doi.org/10.1038/nature06416
22. Hayashi, Y., S.H. Shi, J.A. Esteban, A. Piccini, J.C. Poncer, and R. Malinow. 2000. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science. 287:2262-2267. http://dx.doi.org/10.1126/science.287.5461.2262
23. Higley, M.J., and B.L. Sabatini. 2008. Calcium signaling in dendrites and spines: practical and functional considerations. Neuron. 59:902-913. http://dx.doi.org/10.1016/j.neuron.2008.08.020
24. Hudmon, A., E. Lebel, H. Roy, A. Sik, H. Schulman, M.N. Waxham, and P. De Koninck. 2005. A mechanism for Ca2+/calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association. J. Neurosci. 25:6971-6983. http://dx.doi.org/10.1523/JNEUROSCI.4698-04.2005
25. Jaskolski, F., C. Mulle, and O.J. Manzoni. 2005. An automated method to quantify and visualize colocalized fluorescent signals. J. Neurosci. Methods. 146:42-49. http://dx.doi.org/10.1016/j.jneumeth.2005.01.012
26. Jourdain, P., K. Fukunaga, and D. Muller. 2003. Calcium/calmodulin-dependent protein kinase II contributes to activity-dependent filopodia growth and spine formation. J. Neurosci. 23:10645-10649.
27. Karcher, R.L., J.T. Roland, F. Zappacosta, M.J. Huddleston, R.S. Annan, S.A. Carr, and V.I. Gelfand. 2001. Cell cycle regulation of myosin-V by calcium/calmodulin-dependent protein kinase II. Science. 293:1317-1320. http://dx.doi.org/10.1126/science.1061086
28. Kleindienst, T., J. Winnubst, C. Roth-Alpermann, T. Bonhoeffer, and C. Lohmann. 2011. Activity-dependent clustering of functional synaptic inputs on developing hippocampal dendrites. Neuron. 72:1012-1024. http://dx.doi.org/10.1016/j.neuron.2011.10.015
29. Korkotian, E., and M. Segal. 2007. Morphological constraints on calcium dependent glutamate receptor trafficking into individual dendritic spine. Cell Calcium. 42:41-57. http://dx.doi.org/10.1016/j.ceca.2006.11.006
30. Lee, S.J., Y. Escobedo-Lozoya, E.M. Szatmari, and R. Yasuda. 2009. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature. 458:299-304. http://dx.doi.org/10.1038/nature07842
31. Li, Q., A. Lau, T.J. Morris, L. Guo, C.B. Fordyce, and E.F. Stanley. 2004. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J. Neurosci. 24:4070-4081. http://dx.doi.org/10.1523/JNEUROSCI.0346-04.2004
32. Lisman, J., R. Yasuda, and S. Raghavachari. 2012. Mechanisms of CaMKII action in long-term potentiation. Nat. Rev. Neurosci. 13:169-182.
33. Lohmann, C., and T. Bonhoeffer. 2008. A role for local calcium signaling in rapid synaptic partner selection by dendritic filopodia. Neuron. 59:253-260. http://dx.doi.org/10.1016/j.neuron.2008.05.025
34. Lu, W., H. Man, W. Ju, W.S. Trimble, J.F. MacDonald, and Y.T. Wang. 2001. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron. 29:243-254. http://dx.doi.org/10.1016/S0896-6273(01)00194-5
35. Maas, C., D. Belgardt, H.K. Lee, F.F. Heisler, C. Lappe-Siefke, M.M. Magiera, J. van Dijk, T.J. Hausrat, C. Janke, and M. Kneussel. 2009. Synaptic activation modifies microtubules underlying transport of postsynaptic cargo. Proc. Natl. Acad. Sci. USA. 106:8731-8736. http://dx.doi.org/10.1073/pnas.0812391106
36. Makino, H., and R. Malinow. 2009. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron. 64:381-390. http://dx.doi.org/10.1016/j.neuron.2009.08.035
37. Maletic-Savatic, M., T. Koothan, and R. Malinow. 1998. Calcium-evoked dendritic exocytosis in cultured hippocampal neurons. Part II: mediation by calcium/calmodulin-dependent protein kinase II. J. Neurosci. 18:6814-6821.
38. Marsden, K.C., A. Shemesh, K.U. Bayer, and R.C. Carroll. 2010. Selective translocation of Ca2+/calmodulin protein kinase IIalpha (CaMKIIalpha) to inhibitory synapses. Proc. Natl. Acad. Sci. USA. 107:20559-20564. http://dx.doi.org/10.1073/pnas.1010346107
39. Matsuzaki, M., N. Honkura, G.C. Ellis-Davies, and H. Kasai. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature. 429:761-766. http://dx.doi.org/10.1038/nature02617
40. Nault, F., and P. De Koninck. 2010. Dissociated hippocampal neurons. In Protocols in Neural Cell Cultures. Springer Protocols Handbooks. 137-160.
41. Opazo, P., S. Labrecque, C.M. Tigaret, A. Frouin, P.W. Wiseman, P. De Koninck, and D. Choquet. 2010. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron. 67:239-252. http://dx.doi.org/10.1016/j.neuron.2010.06.007
42. Otmakhov, N., J.H. Tao-Cheng, S. Carpenter, B. Asrican, A. Dosemeci, T.S. Reese, and J. Lisman. 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. http://dx.doi.org/10.1523/JNEUROSCI.2350-04.2004
43. Park, M., J.M. Salgado, L. Ostroff, T.D. Helton, C.G. Robinson, K.M. Harris, and M.D. Ehlers. 2006. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron. 52:817-830. http://dx.doi.org/10.1016/j.neuron.2006.09.040
44. Patterson, M.A., E.M. Szatmari, and R. Yasuda. 2010. AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc. Natl. Acad. Sci. USA. 107: 15951-15956. http://dx.doi.org/10.1073/pnas.0913875107
45. Pi, H.J., N. Otmakhov, F. El Gaamouch, D. Lemelin, P. De Koninck, and J. Lisman. 2010. CaMKII control of spine size and synaptic strength: role of phosphorylation states and nonenzymatic action. Proc. Natl. Acad. Sci. USA. 107:14437-14442. http://dx.doi.org/10.1073/pnas .1009268107
46. Redondo, R.L., and R.G. Morris. 2011. Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 12:17-30. http://dx.doi.org/10.1038/nrn2963
47. Rich, R.C., and H. Schulman. 1998. Substrate-directed function of calmodulin in autophosphorylation of Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 273:28424-28429. http://dx.doi.org/10.1074/jbc.273.43.28424
48. Robison, A.J., M.A. Bass, Y. Jiao, L.B. MacMillan, L.C. Carmody, R.K. Bartlett, and R.J. Colbran. 2005. Multivalent interactions of calcium/calmodulindependent protein kinase II with the postsynaptic density proteins NR2B, densin-180, and alpha-actinin-2. J. Biol. Chem. 280:35329-35336. http://dx.doi.org/10.1074/jbc.M502191200
49. Rodriguez, A., D.B. Ehlenberger, D.L. Dickstein, P.R. Hof, and S.L. Wearne. 2008. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One. 3:e1997.
50. Rose, J., S.X. Jin, and A.M. Craig. 2009. Heterosynaptic molecular dynamics: locally induced propagating synaptic accumulation of CaM kinase II. Neuron. 61:351-358. http://dx.doi.org/10.1016/j.neuron.2008.12.030
51. Schiller, J., Y. Schiller, and D.E. Clapham. 1998. NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat. Neurosci. 1:114-118. http://dx.doi.org/10.1038/693
52. Schiller, J., G. Major, H.J. Koester, and Y. Schiller. 2000. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature. 404:285-289. http://dx.doi.org/10.1038/35005094
53. Schulman, H. 1984. Phosphorylation of microtubule-associated proteins by a Ca2+/calmodulin-dependent protein kinase. J. Cell Biol. 99:11-19. http://dx.doi.org/10.1083/jcb.99.1.11
54. Shen, K., and T. Meyer. 1999. Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science. 284:162-166. http://dx.doi.org/10.1126/science.284.5411.162
55. Sobczyk, A., V. Scheuss, and K. Svoboda. 2005. NMDA receptor subunit-dependent [Ca2+] signaling in individual hippocampal dendritic spines. J. Neurosci. 25:6037-6046. http://dx.doi.org/10.1523/JNEUROSCI.1221-05.2005
56. Steward, O., and S. Halpain. 1999. Lamina-specific synaptic activation causes domain-specific alterations in dendritic immunostaining for MAP2 and CAM kinase II. J. Neurosci. 19:7834-7845.
57. Sutton, M.A., and E.M. Schuman. 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell. 127:49-58. http://dx.doi.org/10.1016/j.cell.2006.09.014
58. Takahashi, N., K. Kitamura, N. Matsuo, M. Mayford, M. Kano, N. Matsuki, and Y. Ikegaya. 2012. Locally synchronized synaptic inputs. Science. 335:353-356. http://dx.doi.org/10.1126/science.1210362
59. Tallini, Y.N., M. Ohkura, B.R. Choi, G. Ji, K. Imoto, R. Doran, J. Lee, P. Plan, J. Wilson, H.B. Xin, et al. 2006. Imaging cellular signals in the heart in vivo: Cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc. Natl. Acad. Sci. USA. 103:4753-4758. http://dx.doi org/10.1073/pnas.0509378103
60. Toni, N., P.A. Buchs, I. Nikonenko, C.R. Bron, and D. Muller. 1999. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature. 402:421-425. http://dx.doi.org/10.1038/46574
61. Vallano, M.L., J.R. Goldenring, R.S. Lasher, and R.J. Delorenzo. 1986. Association of calcium/calmodulin-dependent kinase with cytoskeletal preparations: phosphorylation of tubulin, neurofilament, and microtubule-associated proteins. Ann. N. Y. Acad. Sci. 466:357-374. http://dx.doi org/10.1111/j.1749-6632.1986.tb38406.x
62. Wang, Z., J.G. Edwards, N. Riley, D.W. Provance Jr., R. Karcher, X.D. Li, I.G. Davison, M. Ikebe, J.A. Mercer, J.A. Kauer, and M.D. Ehlers. 2008. Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell. 135:535-548. http://dx.doi.org/10.1016/j.cell.2008.09.057
63. Witte, H., D. Neukirchen, and F. Bradke. 2008. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180:619-632. http://dx.doi.org/10.1083/jcb.200707042
64. Xie, Z., D.P. Srivastava, H. Photowala, L. Kai, M.E. Cahill, K.M. Woolfrey, C.Y. Shum, D.J. Surmeier, and P. Penzes. 2007. Kalirin-7 controls activitydependent structural and functional plasticity of dendritic spines. Neuron. 56:640-656. http://dx.doi.org/10.1016/j.neuron.2007.10.005
65. Yamagata, Y., S. Kobayashi, T. Umeda, A. Inoue, H. Sakagami, M. Fukaya, M. Watanabe, N. Hatanaka, M. Totsuka, T. Yagi, et al. 2009. Kinasedead knock-in mouse reveals an essential role of kinase activity of Ca2+/calmodulin-dependent protein kinase IIalpha in dendritic spine enlargement, long-term potentiation, and learning. J. Neurosci. 29:7607-7618. http://dx.doi.org/10.1523/JNEUROSCI.0707-09.2009
66. Yang, E., and H. Schulman. 1999. Structural examination of autoregulation of multifunctional calcium/calmodulin-dependent protein kinase II. J. Biol. Chem. 274:26199-26208. http://dx.doi.org/10.1074/jbc.274.37.26199
67. Zacharias, D.A., J.D. Violin, A.C. Newton, and R.Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 296:913-916. http://dx.doi.org/10.1126/science.1068539