Regulation of N-type Voltage-Gated Calcium Channels and Presynaptic Function by Cyclin-Dependent Kinase 5

Neuron

Volumn 75, Issue 4, 2012, Pages 675-687

  Su, Susan C ^a   Seo, Jinsoo ^a   Pan, Jen Q ^c   Samuels, Benjamin Adam ^a   Rudenko, Andrii ^a   Ericsson, Maria ^d   Neve, Rachael L ^b   Yue, David T ^e   Tsai, Li Huei ^a,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL CAV2.2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME SUBSTRATE; HIPPOCAMPAL CA1 REGION; MALE; MOLECULAR DYNAMICS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SYNAPTOSOME;

AMIODARONE; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICS; BIOTINYLATION; CALCIUM CHANNELS, N-TYPE; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE 5; ELECTRIC STIMULATION; EMBRYO, MAMMALIAN; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; IMMUNOPRECIPITATION; ION CHANNEL GATING; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MUTATION; NERVE TISSUE PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PRESYNAPTIC TERMINALS; RADIOIMMUNOASSAY; SEQUENCE ANALYSIS, PROTEIN;

EID: 84865363824     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.06.023     Document Type: Article

References (58)

1. 2+ channels. Neuron 2005, 46:891-904.
2. 2+ channels during LTP enhances low release efficacy of hippocampal CA1 perforant path synapses. Neuron 2009, 63:372-385.
3. Bach S., Knockaert M., Reinhardt J., Lozach O., Schmitt S., Baratte B., Koken M., Coburn S.P., Tang L., Jiang T., et al. Roscovitine targets, protein kinases and pyridoxal kinase. J. Biol. Chem. 2005, 280:31208-31219.
4. Bannister R.A., Mezu U., Adams S. Phosphorylation-dependent regulation of voltage-gated Ca2+ channels. Voltage-Gated Calcium Channels 2005, 168-182. Kluwer Academic/Plenum Publishers, New York. G. Zamponi (Ed.).
5. Brittain J.M., Piekarz A.D., Wang Y., Kondo T., Cummins T.R., Khanna R. An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltage-gated calcium channels. J. Biol. Chem. 2009, 284:31375-31390.
6. V2.2) deactivation by the cyclin-dependent kinase inhibitor roscovitine. Biophys. J. 2005, 89:1681-1691.
7. 2+ channels to channel-interacting slots in controlling neurotransmission at cultured hippocampal synapses. J. Neurosci. 2010, 30:4536-4546.
8. Catterall W.A., Few A.P. Calcium channel regulation and presynaptic plasticity. Neuron 2008, 59:882-901.
9. Chae T., Kwon Y.T., Bronson R., Dikkes P., Li E., Tsai L.H. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 1997, 18:29-42.
10. Cheung Z.H., Chin W.H., Chen Y., Ng Y.P., Ip N.Y. Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol. 2007, 5:e63.
11. 2+ channels, SNAP-25, and synaptotagmin. J. Biol. Chem. 2001, 276:32756-32762.
12. Dobrunz L.E., Stevens C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 1997, 18:995-1008.
13. Fu W.Y., Chen Y., Sahin M., Zhao X.S., Shi L., Bikoff J.B., Lai K.O., Yung W.H., Fu A.K., Greenberg M.E., Ip N.Y. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 2007, 10:67-76.
14. Guan J.S., Su S.C., Gao J., Joseph N., Xie Z., Zhou Y., Durak O., Zhang L., Zhu J.J., Clauser K.R., et al. Cdk5 is required for memory function and hippocampal plasticity via the cAMP signaling pathway. PLoS ONE 2011, 6:e25735.
15. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 2011, 69:304-316.
16. 2+ channels. Neuron 2002, 34:411-423.
17. Jahn R., Lang T., Südhof T.C. Membrane fusion. Cell 2003, 112:519-533.
18. 2+/calmodulin-dependent protein kinase II bound to the C-terminal domain. Proc. Natl. Acad. Sci. USA 2008, 105:341-346.
19. 2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 2011, 144:282-295.
20. 2+ channels and RIM scaffold protein covary at the presynaptic transmitter release face but are components of independent protein complexes. Neuroscience 2006, 140:1201-1208.
21. V2.2 channel-transmitter release site core complex. Eur. J. Neurosci. 2007, 26:547-559.
22. V2.2) binding partners. J. Biochem. Mol. Biol. 2007, 40:302-314.
23. Kim S.H., Ryan T.A. CDK5 serves as a major control point in neurotransmitter release. Neuron 2010, 67:797-809.
24. 2+ channels. Nat. Neurosci. 2007, 10:691-701.
25. 2+ channels in neurons. Nat. Neurosci. 2005, 8:435-442.
26. Lee M.S., Kwon Y.T., Li M., Peng J., Friedlander R.M., Tsai L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 2000, 405:360-364.
27. V2.2 channels in hippocampal neurons. J. Neurosci. 2008, 28:11333-11346.
28. Li Q., Lau A., Morris T.J., Guo L., Fordyce C.B., Stanley E.F. A syntaxin 1, Gα(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J. Neurosci. 2004, 24:4070-4081.
29. V2.2 channels modulates channel kinetics. J. Neurophysiol. 2004, 92:2820-2830.
30. Luebke J.I., Dunlap K., Turner T.J. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron 1993, 11:895-902.
31. Maximov A., Bezprozvanny I. Synaptic targeting of N-type calcium channels in hippocampal neurons. J. Neurosci. 2002, 22:6939-6952.
32. Mitra A., Mitra S.S., Tsien R.W. Heterogeneous reallocation of presynaptic efficacy in recurrent excitatory circuits adapting to inactivity. Nat. Neurosci. 2011, 15:250-257.
33. Murthy V.N., Sejnowski T.J., Stevens C.F. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 1997, 18:599-612.
34. Neve R.L., Neve K.A., Nestler E.J., Carlezon W.A. Use of herpes virus amplicon vectors to study brain disorders. Biotechniques 2005, 39:381-391.
35. Ohshima T., Ward J.M., Huh C.G., Longenecker G., Veeranna, Pant H.C., Brady R.O., Martin L.J., Kulkarni A.B. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. USA 1996, 93:11173-11178.
36. Patrick G.N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P., Tsai L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999, 402:615-622.
37. Poncer J.C., McKinney R.A., Gähwiler B.H., Thompson S.M. Either N- or P-type calcium channels mediate GABA release at distinct hippocampal inhibitory synapses. Neuron 1997, 18:463-472.
38. Rakić S., Yanagawa Y., Obata K., Faux C., Parnavelas J.G., Nikolić M. Cortical interneurons require p35/Cdk5 for their migration and laminar organization. Cereb. Cortex 2009, 19:1857-1869.
39. Samuels B.A., Hsueh Y.P., Shu T., Liang H., Tseng H.C., Hong C.J., Su S.C., Volker J., Neve R.L., Yue D.T., Tsai L.H. Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK. Neuron 2007, 56:823-837.
40. Seeburg D.P., Feliu-Mojer M., Gaiottino J., Pak D.T., Sheng M. Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron 2008, 58:571-583.
41. Sheng Z.H., Rettig J., Takahashi M., Catterall W.A. Identification of a syntaxin-binding site on N-type calcium channels. Neuron 1994, 13:1303-1313.
42. Sheng Z.H., Westenbroek R.E., Catterall W.A. Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery. J. Bioenerg. Biomembr. 1998, 30:335-345.
43. Snutch T.P. Targeting chronic and neuropathic pain: the N-type calcium channel comes of age. NeuroRx 2005, 2:662-670.
44. Su S.C., Tsai L.H. Cyclin-dependent kinases in brain development and disease. Annu. Rev. Cell Dev. Biol. 2011, 27:465-491.
45. 2+ channels and synaptic transmission. Nature 1993, 361:165-168.
46. Tan T.C., Valova V.A., Malladi C.S., Graham M.E., Berven L.A., Jupp O.J., Hansra G., McClure S.J., Sarcevic B., Boadle R.A., et al. Cdk5 is essential for synaptic vesicle endocytosis. Nat. Cell Biol. 2003, 5:701-710.
47. Tomizawa K., Ohta J., Matsushita M., Moriwaki A., Li S.T., Takei K., Matsui H. Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity. J. Neurosci. 2002, 22:2590-2597.
48. Tsai L.H., Delalle I., Caviness V.S., Chae T., Harlow E. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 1994, 371:419-423.
49. Viard P., Butcher A.J., Halet G., Davies A., Nürnberg B., Heblich F., Dolphin A.C. PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane. Nat. Neurosci. 2004, 7:939-946.
50. Weiss N., Sandoval A., Kyonaka S., Felix R., Mori Y., De Waard M. Rim1 modulates direct G-protein regulation of Ca(v)2.2 channels. Pflugers Arch. 2011, 461:447-459.
51. Westenbroek R.E., Hell J.W., Warner C., Dubel S.J., Snutch T.P., Catterall W.A. Biochemical properties and subcellular distribution of an N-type calcium channel α 1 subunit. Neuron 1992, 9:1099-1115.
52. 2+ channels in supporting hippocampal synaptic transmission. Science 1994, 264:107-111.
53. Yan Z., Chi P., Bibb J.A., Ryan T.A., Greengard P. Roscovitine: a novel regulator of P/Q-type calcium channels and transmitter release in central neurons. J. Physiol. 2002, 540:761-770.
54. Yarotskyy V., Elmslie K.S. Roscovitine, a cyclin-dependent kinase inhibitor, affects several gating mechanisms to inhibit cardiac L-type (Ca(V)1.2) calcium channels. Br. J. Pharmacol. 2007, 152:386-395.
55. Yokoyama C.T., Sheng Z.H., Catterall W.A. Phosphorylation of the synaptic protein interaction site on N-type calcium channels inhibits interactions with SNARE proteins. J. Neurosci. 1997, 17:6929-6938.
56. Zamponi G.W., Bourinet E., Nelson D., Nargeot J., Snutch T.P. Crosstalk between G proteins and protein kinase C mediated by the calcium channel α1 subunit. Nature 1997, 385:442-446.
57. Zhu L.Q., Liu D., Hu J., Cheng J., Wang S.H., Wang Q., Wang F., Chen J.G., Wang J.Z. GSK-3 β inhibits presynaptic vesicle exocytosis by phosphorylating P/Q-type calcium channel and interrupting SNARE complex formation. J. Neurosci. 2010, 30:3624-3633.
58. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 2002, 64:355-405.