CASK regulates CaMKII autophosphorylation in neuronal growth, calcium signaling, and learning

Frontiers in Molecular Neuroscience

Volumn 6, Issue SEP, 2013, Pages

  Gillespie, John M ^a   Hodge, James J L ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Appetitive learning; Autophosphorylation; Calcium imaging; CaMKII; CASK; Drosophila; Synaptic function

Indexed keywords

CALCIUM CALMODULIN ASSOCIATED SERINE KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; POTASSIUM CHANNEL HERG; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APPETITE; ARTICLE; AUTOPHOSPHORYLATION; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; GENE OVEREXPRESSION; LARVAL STAGE; LEARNING; MEMORY; NERVE CELL GROWTH; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NONHUMAN; NULL ALLELE; OLFACTORY DISCRIMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSPORT VESICLE; WILD TYPE;

EID: 84885077846     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2013.00027     Document Type: Article

References (56)

1. Asahina, K., Louis, M., Piccinotti, S., and Vosshall, L. B. (2009). A circuit supporting concentration-invariant odor perception in Drosophila. J. Biol. 8, 9. doi: 10.1186/jbiol108
2. Ashraf, S. I., Mcloon, A. L., Sclarsic, S. M., and Kunes, S. (2006). Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124, 191-205. doi: 10.1016/j.cell.2005.12.017
3. Atasoy, D., Schoch, S., Ho, A., Nadasy, K. A., Liu, X., Zhang, W., et al. (2007). Deletion of CASK in mice is lethal and impairs synaptic function. Proc. Natl. Acad. Sci. U.S.A. 104, 2525-2530. doi: 10.1073/pnas.0611003104
4. Butz, S., Okamoto, M., and Sudhof, T. C. (1998). A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94, 773-782. doi: 10.1016/S0092-8674(00)81736-5
5. Cattaert, D., and Birman, S. (2001). Blockade of the central generator of locomotor rhythm by noncompetitive NMDA receptor antagonists in Drosophila larvae. J. Neurobiol. 48, 58-73. doi: 10.1002/neu.1042
6. Cavaliere, S., Gillespie, J. M., and Hodge, J. J. L. (2012). KCNQ channels show conserved ethanol block and function in ethanol behaviour. PLoS ONE 7:e50279. doi: 10.1371/journal.pone.0050279
7. Chen, K., and Featherstone, D. E. (2011). Pre and postsynaptic roles for Drosophila CASK. Mol. Cell. Neurosci. 48, 171-182. doi: 10.1016/j.mcn.2011.07.009
8. Chen, Y. C., Mishra, D., Schmitt, L., Schmuker, M., and Gerber, B. (2011). A behavioral odor similarity "space" in larval Drosophila. Chem. Senses 36, 237-249. doi: 10.1093/chemse/bjq123
9. 2+/calmodulin-dependent protein kinase is highly conserved in Drosophila. Neuron 7, 439-450. doi: 10.1016/0896-6273(91)90296-C
10. 2+/calmodulin. J. Biol. Chem. 285, 17930-17937. doi: 10.1074/jbc.M109.069351
11. Donelson, N., Kim, E. Z., Slawson, J. B., Vecsey, C. G., Huber, R., and Griffith, L. C. (2012). High-resolution positional tracking for long-term analysis of Drosophila sleep and locomotion using the "tracker" program. PLoS ONE 7:e37250. doi: 10.1371/journal.pone.0037250
12. Elgersma, Y., Fedorov, N. B., Ikonen, S., Choi, E. S., Elgersma, M., Carvalho, O. M., et al. (2002). Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning. Neuron 36, 493-505. doi: 10.1016/S0896-6273(02)01007-3
13. Froyen, G., Van Esch, H., Bauters, M., Hollanders, K., Frints, S. G., Vermeesch, J. R., et al. (2007). Detection of genomic copy number changes in patients with idiopathic mental retardation by high-resolution X-array-CGH: important role for increased gene dosage of XLMR genes. Hum. Mutat. 28, 1034-1042. doi: 10.1002/humu.20564
14. Giese, K. P., Fedorov, N. B., Filipkowski, R. K., and Silva, A. J. (1998). Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279, 870-873. doi: 10.1126/science.279.5352.870
15. Griffith, L. C., Verselis, L. M., Aitken, K. M., Kyriacou, C. P., Danho, W., and Greenspan, R. J. (1993). Inhibition of calcium/calmodulin-dependent protein kinase inDrosophila disrupts behavioral plasticity. Neuron 10, 501-509. doi: 10.1016/0896-6273(93)90337-Q
16. Griffith, L. C., Wang, J., Zhong, Y., Wu, C. F., and Greenspan, R. J. (1994). Calcium/calmodulin-dependent pr-otein kinase II and potassium channel subunit eag similarly affect plasticity in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 91, 10044-10048. doi: 10.1073/pnas.91.21.10044
17. 2+/calmodulin-dependent protein kinase analysed by site-directed mutagenesis. J. Biol. Chem. 267, 17216-17224.
18. Hardingham, N., Glazewski, S., Pakhotin, P., Mizuno, K., Chapman, P. F., Giese, K. P., et al. (2003). Neocortical long-term potentiation and experience-dependent synaptic plasticity require alpha-calcium/calmodulin-dependent protein kinase II autophosphorylation. J. Neurosci. 23, 4428-4436.
19. Hoang, B., and Chiba, A. (2001). Single-cell analysis of Drosophila larval neuromuscular synapses. Dev. Biol. 229, 55-70. doi: 10.1006/dbio.2000.9983
20. Hodge, J. J., Mullasseril, P., and Griffith, L. C. (2006). Activity-dependent gating of CaMKII autonomous activity by Drosophila CASK. Neuron 51, 327-337. doi: 10.1016/j.neuron.2006.06.020
21. Holahan, M. R., Rekart, J. L., Sandoval, J., and Routtenberg, A. (2006). Spatial learning induces presynaptic structural remodeling in the hippocampal mossy fiber system of two rat strains. Hippocampus 16, 560-570. doi: 10.1002/hipo.20185
22. Hsueh, Y. P. (2006). The role of the MAGUK protein CASK in neural development and synaptic function. Curr. Med. Chem. 13, 1915-1927. doi: 10.2174/092986706777585040
23. 2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 284, 28146-28155. doi: 10.1074/jbc.M109.005900
24. Jan, L. Y., and Jan, Y. N. (1982). Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc. Natl. Acad. Sci. U.S.A. 79, 2700-2704. doi: 10.1073/pnas.79.8.2700
25. Kawasaki, F., Zou, B., Xu, X., and Ordway, R. W. (2004). Active zone localisation of presynaptic calcium channels encoded by the cacophony locus of Drosophila. J. Neurosci. 24, 282-285. doi: 10.1523/JNEUROSCI.3553-03.2004
26. Koh, Y. H., Popova, E., Thomas, U., Griffith, L. C., and Budnik, V. (1999). Regulation of DLG localization at synapses by CaMKII-dependent phosphorylation. Cell 98, 353-363. doi: 10.1016/S0092-8674(00)81964-9
27. Lisman, J., Schulman, H., and Cline, H. (2002). The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3, 175-190. doi: 10.1038/nrn753
28. 2+/CaM-responsive pool of CaMKII by scaffold-dependent autophosphorylation. Neuron 40, 1185-1197. doi: 10.1016/S0896-6273(03)00786-4
29. Macleod, G. T., Marin, L., Charlton, M. P., and Atwood, H. L. (2004). Synaptic vesicles: test for a role in presynaptic calcium regulation. J. Neurosci. 24, 2496-2505. doi: 10.1523/JNEUROSCI.5372-03.2004
30. Mahr, A., and Aberle, H. (2006). The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr. Patterns 6, 299-309. doi: 10.1016/j.modgep.2005.07.006
31. Malik, J. J., Gillespie, J. M., and Hodge, J. J. L. (2013). CASK and CaMKII function in the mushroom body α'/β' neurons during Drosophila memory formation. Front. Neural Cicuits 7:52. doi: 10.3389/fncir.2013.00052
32. Marble, D. D., Hegle, A. P., Snyder, E. D. 2nd., Dimitratos, S., Bryant, P. J., and Wilson, G. F. (2005). Camguk/CASK enhances Ether-a-go-go potassium current by a phosphorylation-dependent mechanism. J. Neurosci. 25, 4898-4907. doi: 10.1523/JNEUROSCI.4566-04.2005
33. Mehren, J. E., and Griffith, L. C. (2004). Calcium-independent calcium/calmodulin-dependent protein kinase II in the adult Drosophila CNS enhances the training of pheromonal cues. J. Neurosci. 24, 10584-10593. doi: 10.1523/JNEUROSCI.3560-04.2004
34. + channel gene BEC1/KCNH3 enhances cognitive function. J. Neurosci. 29, 14637-14645. doi: 10.1523/JNEUROSCI.0901-09.2009
35. Najm, J., Horn, D., Wimplinger, I., Golden, J. A., Chizhikov, V. V., Sudi, J., et al. (2008). Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum. Nat. Genet. 40, 1065-1067. doi: 10.1038/ng.194
36. Park, D., Coleman, M. J., Hodge, J. J., Budnik, V., and Griffith, L. C. (2002). Regulation of neuronal excitability in Drosophila by constitutively active CaMKII. J. Neurobiol. 52, 24-42. doi: 10.1002/neu.10066
37. Pauls, D., Selcho, M., Gendre, N., Stocker, R. F., and Thum, A. S. (2010). Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. J. Neurosci. 30, 10655-10666. doi: 10.1523/JNEUROSCI.1281-10.2010
38. Pi, H. J., Otmakhov, N., Lemelin, D., De Koninck, P., and Lisman, J. (2010). Autonomous CaMKII can promote either long-term potentiation or long-term depression, depending on the state of T305/T306 phosphorylation. J. Neurosci. 30, 8704-8709. doi: 10.1523/JNEUROSCI.0133-10.2010
39. Piluso, G., D'amico, F., Saccone, V., Bismuto, E., Rotundo, I. L., Di Domenico, M., et al. (2009). A missense mutation in CASK causes FG syndrome in an Italian family. Am. J. Hum. Genet. 84, 162-177. doi: 10.1016/j.ajhg.2008.12.018
40. Pulver, S. R., Pashkovski, S. L., Hornstein, N. J., Garrity, P. A., and Griffith, L. C. (2009). Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J. Neurophysiol. 101, 3075-3088. doi: 10.1152/jn.00071.2009
41. Ranganayakulu, G., Schulz, R. A., and Olson, E. N. (1996). Wingless signaling induces nautilus expression in the ventral mesoderm of the Drosophila embryo. Dev. Biol. 176, 143-148. doi: 10.1006/dbio.1996.9987
42. Samuels, B. A., Hsueh, Y. P., Shu, T., Liang, H., Tseng, H. C., Hong, C. J., et al. (2007). Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK. Neuron 56, 823-837. doi: 10.1016/j.neuron.2007.09.035
43. Sanhueza, M., Fernandez-Villalobos, G., Stein, I. S., Kasumova, G., Zhang, P., Bayer, K. U., et al. (2011). Role of the CaMKII/NMDA receptor complex in the maintenance of synaptic strength. J. Neurosci. 31, 9170-9178. doi: 10.1523/JNEUROSCI.1250-11.2011
44. Schuster, C. M., Davis, G. W., Fetter, R. D., and Goodman, C. S. (1996). Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17, 655-667. doi: 10.1016/S0896-6273(00)80198-1
45. Sherwood, N. T., Sun, Q., Xue, M., Zhang, B., and Zinn, K. (2004). Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2:e429. doi: 10.1371/journal.pbio.0020429
46. Slawson, J. B., Kuklin, E. A., Ejima, A., Mukherjee, K., Ostrovsky, L., and Griffith, L. C. (2011). Central regulation of locomotor behavior of Drosophila melanogaster depends on a CASK isoform containing CaMK-like and L27 domains. Genetics 187, 171-184. doi: 10.1534/genetics.110.123406
47. Spangler, S. A., Schmitz, S. K., Kevenaar, J. T., de Graaff, E., de Wit, H., Demmers, J., et al. (2013). Liprin-α2 promotes the presynaptic recruitment and turnover of RIM1/CASK to facilitate synaptic transmission. J. Cell Biol. 201, 915-928. doi: 10.1083/jcb.201301011
48. Sun, M., Liu, L., Zeng, X., Xu, M., Fang, M., and Xie, W. (2009). Genetic interaction between Neurexin and CAKI/CMG is important for synaptic function in Drosophilaneuromuscular junction. Neurosci. Res. 64, 362-371. doi: 10.1016/j.neures.2009.04.009
49. Sun, X. X., Hodge, J. J., Zhou, Y., Nguyen, M., and Griffith, L. C. (2004). The eag potassium channel binds and locally activates calcium/calmodulin-dependent protein kinase II. J. Biol. Chem. 279, 10206-10214. doi: 10.1074/jbc.M310728200
50. Tarpey, P. S., Smith, R., Pleasance, E., Whibley, A., Edkins, S., Hardy, C., et al. (2009). A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation. Nat. Genet. 41, 535-543. doi: 10.1038/ng.367
51. Thum, A. S., Jenett, A., Ito, K., Heisenberg, M., and Tanimoto, H. (2007). Multiple memory traces for olfactory reward learning in Drosophila. J. Neurosci. 27, 11132-11138. doi: 10.1523/JNEUROSCI.2712-07.2007
52. Tian, L., Hires, S. A., Mao, T., Huber, D., Chiappe, M. E., Chalasani, S. H., et al. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881. doi: 10.1038/nmeth.1398
53. Tully, T., and Quinn, W. G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A 157, 263-277. doi: 10.1007/BF01350033
54. Unni, V. K., Zakharenko, S. S., Zablow, L., Decostanzo, A. J., and Siegelbaum, S. A. (2004). Calcium release from presynaptic ryanodine-sensitive stores is required for long-term depression at hippocampal CA3-CA3 pyramidal neuron synapses. J. Neurosci. 24, 9612-9622. doi: 10.1523/JNEUROSCI.5583-03.2004
55. Wang, Z., Wilson, G. F., and Griffith, L. C. (2002). Calcium/calmodulin-dependent protein kinase II phosphorylates and regulates the Drosophila eag potassium channel. J. Biol. Chem. 277, 24022-24029. doi: 10.1074/jbc.M201949200
56. Zordan, M. A., Massironi, M., Ducato, M. G., Te Kronnie, G., Costa, R., Reggiani, C., et al. (2005). Drosophila CAKI/CMG protein, a homolog of human CASK, is essential for regulation of neurotransmitter vesicle release. J. Neurophysiol. 94, 1074-1083. doi: 10.1152/jn.00954.2004