Cdk5 Promotes Synaptogenesis by Regulating the Subcellular Distribution of the MAGUK Family Member CASK

Neuron

Volumn 56, Issue 5, 2007, Pages 823-837

  Samuels, Benjamin Adam ^a,b   Hsueh, Yi Ping ^c   Shu, Tianzhi ^a   Liang, Haoya ^d   Tseng, Huang Chun ^a   Hong, Chen Jei ^c   Su, Susan C ^a   Volker, Janet ^b   Neve, Rachael L ^e   Yue, David T ^d   Tsai, Li Huei ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MCLEAN HOSPITAL   (United States)

Author keywords

CELLBIO; MOLNEURO; SIGNALING

Indexed keywords

CYCLIN DEPENDENT KINASE 5; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; NEUREXIN; NEUROLIGIN;

ARTICLE; CALCIUM TRANSPORT; CELLULAR DISTRIBUTION; ENZYME PHOSPHORYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; AUTISTIC DISORDER; CALCIUM CHANNELS; CYCLIN-DEPENDENT KINASE 5; GUANYLATE KINASE; IMMUNOGLOBULINS; ION CHANNEL GATING; MEMBRANE PROTEINS; MICE; PHOSPHORYLATION; PRESYNAPTIC TERMINALS; PROTEINS; RECEPTOR CROSS-TALK; SUBCELLULAR FRACTIONS; SYNAPSES;

EID: 36549085044     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.09.035     Document Type: Article

References (70)

1. Agler H.L., Evans J., Tay L.H., Anderson M.J., Colecraft H.M., and Yue D.T. G protein-gated inhibitory module of N-type (ca(v)2.2) ca2+ channels. Neuron 46 (2005) 891-904
2. Atasoy D., Schoch S., Ho A., Nadasy K.A., Liu X., Zhang W., Mukherjee K., Nosyreva E.D., Fernandez-Chacon R., Missler M., et al. Deletion of CASK in mice is lethal and impairs synaptic function. Proc. Natl. Acad. Sci. USA 104 (2007) 2525-2530
3. Barclay J.W., Aldea M., Craig T.J., Morgan A., and Burgoyne R.D. Regulation of the fusion pore conductance during exocytosis by cyclin-dependent kinase 5. J. Biol. Chem. 279 (2004) 41495-41503
4. Biederer T., and Scheiffele P. Mixed-culture assays for analyzing neuronal synapse formation. Nat. Protoc. 2 (2007) 670-676
5. Biederer T., Sara Y., Mozhayeva M., Atasoy D., Liu X., Kavalali E.T., and Sudhof T.C. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297 (2002) 1525-1531
6. Butz S., Okamoto M., and Sudhof T.C. A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94 (1998) 773-782
7. Chih B., Engelman H., and Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307 (2005) 1324-1328
8. Cruz J.C., Tseng H.C., Goldman J.A., Shih H., and Tsai L.H. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 40 (2003) 471-483
9. Dai Y., Taru H., Deken S.L., Grill B., Ackley B., Nonet M.L., and Jin Y. SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 9 (2006) 1479-1487
10. Dean C., Scholl F.G., Choih J., DeMaria S., Berger J., Isacoff E., and Scheiffele P. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6 (2003) 708-716
11. Elias G.M., Funke L., Stein V., Grant S.G., Bredt D.S., and Nicoll R.A. Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52 (2006) 307-320
12. Fischer A., Sananbenesi F., Pang P.T., Lu B., and Tsai L.H. Opposing roles of transient and prolonged expression of p25 in synaptic plasticity and hippocampus-dependent memory. Neuron 48 (2005) 825-838
13. Fletcher A.I., Shuang R., Giovannucci D.R., Zhang L., Bittner M.A., and Stuenkel E.L. Regulation of exocytosis by cyclin-dependent kinase 5 via phosphorylation of Munc18. J. Biol. Chem. 274 (1999) 4027-4035
14. Floyd S.R., Porro E.B., Slepnev V.I., Ochoa G.C., Tsai L.H., and De Camilli P. Amphiphysin 1 binds the cyclin-dependent kinase (cdk) 5 regulatory subunit p35 and is phosphorylated by cdk5 and cdc2. J. Biol. Chem. 276 (2001) 8104-8110
15. Froyen G., Van Esch H., Bauters M., Hollanders K., Frints S.G., Vermeesch J.R., Devriendt K., Fryns J.P., and Marynen P. 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 (2007) 1034-1042
16. Geppert M., Goda Y., Stevens C.F., and Sudhof T.C. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature 387 (1997) 810-814
17. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., and Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119 (2004) 1013-1026
18. Hata Y., Butz S., and Sudhof T.C. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16 (1996) 2488-2494
19. Ho A., Morishita W., Hammer R.E., Malenka R.C., and Sudhof T.C. A role for Mints in transmitter release: Mint 1 knockout mice exhibit impaired GABAergic synaptic transmission. Proc. Natl. Acad. Sci. USA 100 (2003) 1409-1414
20. Hong C.J., and Hsueh Y.P. CASK associates with glutamate receptor interacting protein and signaling molecules. Biochem. Biophys. Res. Commun. 351 (2006) 771-776
21. Hoogenraad C.C., Feliu-Mojer M.I., Spangler S.A., Milstein A.D., Dunah A.W., Hung A.Y., and Sheng M. Liprinalpha1 degradation by calcium/calmodulin-dependent protein kinase II regulates LAR receptor tyrosine phosphatase distribution and dendrite development. Dev. Cell 12 (2007) 587-602
22. Hsueh Y.P. The role of the MAGUK protein CASK in neural development and synaptic function. Curr. Med. Chem. 13 (2006) 1915-1927
23. Hsueh Y.P., and Sheng M. Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J. Neurosci. 19 (1999) 7415-7425
24. Hsueh Y.P., Yang F.C., Kharazia V., Naisbitt S., Cohen A.R., Weinberg R.J., and Sheng M. Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J. Cell Biol. 142 (1998) 139-151
25. Hsueh Y.P., Wang T.F., Yang F.C., and Sheng M. Nuclear translocation and transcription regulation by the membrane-associated guanylate kinase CASK/LIN-2. Nature 404 (2000) 298-302
26. Ichtchenko K., Hata Y., Nguyen T., Ullrich B., Missler M., Moomaw C., and Sudhof T.C. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 81 (1995) 435-443
27. Jamain S., Quach H., Betancur C., Rastam M., Colineaux C., Gillberg I.C., Soderstrom H., Giros B., Leboyer M., Gillberg C., and Bourgeron T. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 34 (2003) 27-29
28. Kaech S.M., Whitfield C.W., and Kim S.K. The LIN-2/LIN-7/LIN-10 complex mediates basolateral membrane localization of the C. elegans EGF receptor LET-23 in vulval epithelial cells. Cell 94 (1998) 761-771
29. Kaufmann N., DeProto J., Ranjan R., Wan H., and Van Vactor D. Drosophila liprin-α and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34 (2002) 27-38
30. Khanna R., Sun L., Li Q., Guo L., and Stanley E.F. Long splice variant N type calcium channels are clustered at presynaptic transmitter release sites without modular adaptor proteins. Neuroscience 138 (2006) 1115-1125
31. Lee S.Y., Wenk M.R., Kim Y., Nairn A.C., and De Camilli P. Regulation of synaptojanin 1 by cyclin-dependent kinase 5 at synapses. Proc. Natl. Acad. Sci. USA 101 (2004) 546-551
32. Levinson J.N., and El-Husseini A. Building excitatory and inhibitory synapses: Balancing neuroligin partnerships. Neuron 48 (2005) 171-174
33. Lin Y., McDonough S.I., and Lipscombe D. Alternative splicing in the voltage-sensing region of N-Type CaV2.2 channels modulates channel kinetics. J. Neurophysiol. 92 (2004) 2820-2830
34. Lin Y.L., Lei Y.T., Hong C.J., and Hsueh Y.P. Syndecan-2 induces filopodia and dendritic spine formation via the neurofibromin-PKA-Ena/VASP pathway. J. Cell Biol. 177 (2007) 829-841
35. Matsubara M., Kusubata M., Ishiguro K., Uchida T., Titani K., and Taniguchi H. Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J. Biol. Chem. 271 (1996) 21108-21113
36. Maximov A., and Bezprozvanny I. Synaptic targeting of N-type calcium channels in hippocampal neurons. J. Neurosci. 22 (2002) 6939-6952
37. Maximov A., Sudhof T.C., and Bezprozvanny I. Association of neuronal calcium channels with modular adaptor proteins. J. Biol. Chem. 274 (1999) 24453-24456
38. Miller K.E., DeProto J., Kaufmann N., Patel B.N., Duckworth A., and Van Vactor D. Direct observation demonstrates that Liprin-alpha is required for trafficking of synaptic vesicles. Curr. Biol. 15 (2005) 684-689
39. Nguyen T., and Sudhof T.C. Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell-adhesion molecules. J. Biol. Chem. 272 (1997) 26032-26039
40. Okamoto M., and Sudhof T.C. Mints, Munc18-interacting proteins in synaptic vesicle exocytosis. J. Biol. Chem. 272 (1997) 31459-31464
41. Olsen O., Moore K.A., Fukata M., Kazuta T., Trinidad J.C., Kauer F.W., Streuli M., Misawa H., Burlingame A.L., Nicoll R.A., and Bredt D.S. Neurotransmitter release regulated by a MALS-liprin-alpha presynaptic complex. J. Cell Biol. 170 (2005) 1127-1134
42. Olsen O., Moore K.A., Nicoll R.A., and Bredt D.S. Synaptic transmission regulated by a presynaptic MALS/Liprin-alpha protein complex. Curr. Opin. Cell Biol. 18 (2006) 223-227
43. Patel M.R., Lehrman E.K., Poon V.Y., Crump J.G., Zhen M., Bargmann C.I., and Shen K. Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 9 (2006) 1488-1498
44. Rosales C.R., Osborne K.D., Zuccarino G.V., Scheiffele P., and Silverman M.A. A cytoplasmic motif targets neuroligin-1 exclusively to dendrites of cultured hippocampal neurons. Eur. J. Neurosci. 22 (2005) 2381-2386
45. Sara Y., Biederer T., Atasoy D., Chubykin A., Mozhayeva M.G., Sudhof T.C., and Kavalali E.T. Selective capability of SynCAM and neuroligin for functional synapse assembly. J. Neurosci. 25 (2005) 260-270
46. Scheiffele P., Fan J., Choih J., Fetter R., and Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101 (2000) 657-669
47. Serra-Pages C., Medley Q.G., Tang M., Hart A., and Streuli M. Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins. J. Biol. Chem. 273 (1998) 15611-15620
48. Setou M., Nakagawa T., Seog D.H., and Hirokawa N. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288 (2000) 1796-1802
49. Shin H., Wyszynski M., Huh K.H., Valtschanoff J.G., Lee J.R., Ko J., Streuli M., Weinberg R.J., Sheng M., and Kim E. Association of the kinesin motor KIF1A with the multimodular protein liprin-alpha. J. Biol. Chem. 278 (2003) 11393-11401
50. Shuang R., Zhang L., Fletcher A., Groblewski G.E., Pevsner J., and Stuenkel E.L. Regulation of Munc-18/syntaxin 1A interaction by cyclin-dependent kinase 5 in nerve endings. J. Biol. Chem. 273 (1998) 4957-4966
51. Simske J.S., Kaech S.M., Harp S.A., and Kim S.K. LET-23 receptor localization by the cell junction protein LIN-7 during C. elegans vulval induction. Cell 85 (1996) 195-204
52. Song J.Y., Ichtchenko K., Sudhof T.C., and Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. USA 96 (1999) 1100-1105
53. Spafford J.D., and Zamponi G.W. Functional interactions between presynaptic calcium channels and the neurotransmitter release machinery. Curr. Opin. Neurobiol. 13 (2003) 308-314
54. Spafford J.D., Munno D.W., Van Nierop P., Feng Z.P., Jarvis S.E., Gallin W.J., Smit A.B., Zamponi G.W., and Syed N.I. Calcium channel structural determinants of synaptic transmission between identified invertebrate neurons. J. Biol. Chem. 278 (2003) 4258-4267
55. Szatmari P., Paterson A.D., Zwaigenbaum L., Roberts W., Brian J., Liu X.Q., Vincent J.B., Skaug J.L., Thompson A.P., Senman L., et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat. Genet. 39 (2007) 319-328
56. Tabuchi K., Blundell J., Etherton M.R., Hammer R.E., Liu X., Powell C.M., and Sudhof T.C. A Neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318 (2007) 71-76
57. 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. 5 (2003) 701-710
58. Tomizawa K., Sunada S., Lu Y.F., Oda Y., Kinuta M., Ohshima T., Saito T., Wei F.Y., Matsushita M., Li S.T., et al. Cophosphorylation of amphiphysin I and dynamin I by Cdk5 regulates clathrin-mediated endocytosis of synaptic vesicles. J. Cell Biol. 163 (2003) 813-824
59. Tsai L.H., Delalle I., Caviness Jr. V.S., Chae T., and Harlow E. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371 (1994) 419-423
60. Ullrich B., Ushkaryov Y.A., and Sudhof T.C. Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron 14 (1995) 497-507
61. Ushkaryov Y.A., Petrenko A.G., Geppert M., and Sudhof T.C. Neurexins: synaptic cell-surface proteins related to the alpha-latrotoxin receptor and laminin. Science 257 (1992) 50-56
62. Varoqueaux F., Aramuni G., Rawson R.L., Mohrmann R., Missler M., Gottmann K., Zhang W., Sudhof T.C., and Brose N. Neuroligins determine synapse maturation and function. Neuron 51 (2006) 741-754
63. Venturin M., Moncini S., Villa V., Russo S., Bonati M.T., Larizza L., and Riva P. Mutations and novel polymorphisms in coding regions and UTRs of CDK5R1 and OMG genes in patients with non-syndromic mental retardation. Neurogenetics 7 (2006) 59-66
64. Wang G.S., Hong C.J., Yen T.Y., Huang H.Y., Ou Y., Huang T.N., Jung W.G., Kuo T.Y., Sheng M., Wang T.F., and Hsueh Y.P. Transcriptional modification by a CASK-interacting nucleosome assembly protein. Neuron 42 (2004) 113-128
65. Wang T.F., Ding C.N., Wang G.S., Luo S.C., Lin Y.L., Ruan Y., Hevner R., Rubenstein J.L., and Hsueh Y.P. Identification of Tbr-1/CASK complex target genes in neurons. J. Neurochem. 91 (2004) 1483-1492
66. Xie Z., Sanada K., Samuels B.A., Shih H., and Tsai L.H. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114 (2003) 469-482
67. Yu H., Saura C.A., Choi S.Y., Sun L.D., Yang X., Handler M., Kawarabayashi T., Younkin L., Fedeles B., Wilson M.A., et al. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron 31 (2001) 713-726
68. Zamponi G.W. Regulation of presynaptic calcium channels by synaptic proteins. J. Pharmacol. Sci. 92 (2003) 79-83
69. Zhang Y., Luan Z., Liu A., and Hu G. The scaffolding protein CASK mediates the interaction between rabphilin3a and beta-neurexins. FEBS Lett. 497 (2001) 99-102
70. Zhen M., and Jin Y. The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401 (1999) 371-375