Differential synaptic distribution of the scaffold proteins cask and caskin1 in the bovine retina

Molecular and Cellular Neuroscience

Volumn 62, Issue , 2014, Pages 19-29

  Anjum, Rizwana ^a   Ayoubian, Hiresh ^a   Schmitz, Frank ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Cask; Caskin1; Retina; Ribbon synapse; RIMs; Rod and cone photoreceptor; Synapse

Indexed keywords

CALCIUM CALMODULIN DEPENDENT SERINE PROTEIN KINASE; CASKIN1 PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; CASK PROTEIN; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; PROTEIN ANTIBODY; RIBEYE PROTEIN; RIM1 PROTEIN; RIM2 PROTEIN; CASK KINASES; GUANYLATE KINASE; NERVE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANTIBODY LABELING; ARTICLE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; RETINA; RIBBON SYNAPSE; SYNAPSE; SYNAPTOSOME; WESTERN BLOTTING; ANIMAL TISSUE; CATTLE; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CONVENTIONAL SYNAPSE; IMMUNODETECTION; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; PROTEIN EXPRESSION; RETINA BIPOLAR GANGLION CELL; VISUAL INFORMATION; ANIMAL; BOVINE; CYTOSKELETON; METABOLISM; RETINA ROD;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CATTLE; CYTOSKELETON; GUANYLATE KINASE; NERVE TISSUE PROTEINS; PRESYNAPTIC TERMINALS; RETINA; RETINAL ROD PHOTORECEPTOR CELLS; SYNAPSES;

EID: 84906227147     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.08.004     Document Type: Article

References (87)

1. Alpadi K., Magupalli V.G., Käppel S., Köblitz L., Schwarz K., Seigel G.M., Sung C.H., Schmitz F. RIBEYE recruits Munc119, a mammalian ortholog of the Caenorhabditis elegans protein unc119, to synaptic ribbons of photoreceptor synapses. J. Biol. Chem. 2008, 283:26461-26467.
2. Atasoy D., Schoch S., Ho A., Nadasy K.A., Liu X., Zhang W., Mukherjee K., Nosyreva E.D., Fernendez-Chacon R., Missler M., Kavalali E.T., Südhof T.C. Deletion of Cask in mice is lethal and impairs synaptic function. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2525-2530.
3. Balázs A., Csizmok V., Buday L., Rakács M., Kiss R., Bokor M., Udupa R., Tompa K., Tompa P. High levels of structural disorder in scaffold proteins as exemplified by a novel neuronal protein, CASK-interactive protein 1. FEBS J. 2009, 276:3744-3756.
4. Biederer T., Südhof T.C. Mints as adapters. Direct binding to neurexins and recruitment of munc18. J. Biol. Chem. 2000, 275:39803-39806.
5. Biederer T., Südhof T.C. CASK and protein 4.1 support F-actin nucleation on neurexins. J. Biol. Chem. 2001, 276:47869-47876.
6. Biederer T., Sara Y., Mozhayeva M., Atasoy D., Liu X., Kavalali E.T., Südhof T.C. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 2002, 297:1525-1531.
7. Borg J.P., LÕpez-Figueroa M.O., da Taddèo-Borg M., Kroon D.E., Turner R.S., Watson S.J., Margolis B. Molecular analysis of the X11-mLin-2/Cask complex in brain. J. Neurosci. 1999, 19:1307-1316.
8. Buday L., Wunderlich L., Tamas P. The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell. Signal. 2002, 14:723-731.
9. Butz S., Okamoto M., Südhof T.C. A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 1998, 94:773-782.
10. Chen K., Featherstone D.E. Pre- and postsynaptic roles for Drosophila CASK. Mol. Cell. Neurosci. 2011, 48:171-182.
11. Cohen A.R., Woods D.F., Marfatia S.M., Walther Z., Chishti A.H., Anderson J.M. Human Cask/Lin2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J. Cell Biol. 1998, 142:129-138.
12. Dai Y., Taru H., Deken S.L., Grill B., Ackley B., Nonet M.L., Jin Y. SYD-2 liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 2006, 9:1479-1487.
13. Dean C., Dresbach T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci. 2006, 29:21-29.
14. Dudanova I., Klein R. The axon's balancing act: cis- and trans-interactions between Ephs and ephrins. Neuron 2011, 71:1-3.
15. Egea J., Klein R. Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol. 2007, 17:230-238.
16. Fawcett J.P., Georgiou J., Ruston J., Bladt F., Sherman A., Warner N., Saab B.J., Scott R., Roder J.C., Pawson T. Nck adapter proteins control the organization of neuronal circuits important for walking. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20973-20978.
17. Garrity P.A., Rao Y., Salecker I., McGlade J., Pawson T., Zipursky S.L. Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter proteins. Cell 1996, 85:639-650.
18. Gillespie J.M., Hodge J.J. CASK regulates CaMKII autophosphorylation in neuronal growth, calcium signaling, and learning. Front. Mol. Neurosci. 2013, 6:27.
19. Gosh K.K., Bujan S., Haverkamp S., Feigenspan A., Wässle H. Types of bipolar cells in the mouse retina. J. Comp. Neurol. 2004, 469:70-82.
20. Hata Y., Butz S., Südhof T.C. CASK, a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 1996, 16:2488-2494.
21. Hayashi S., Mizuno S., Migita O., Okuyama T., Makita Y., Hata A., Imoto I., Inazawa J. The CASK gene harbored in a deletion detected by array-CGH as a potential candidate for a gene causative of X-linked dominant mental retardation. Am. J. Med. Genet. A 2008, 146A:2145-2151.
22. Heidelberger R., Thoreson W.B., Witkovsky P. Synaptic transmission at retinal ribbon synapses. Prog. Retin. Eye Res. 2005, 24:682-720.
23. Helmstaedter M., Briggman K.L., Turaga S.C., Jain V., Seung H.S., Denk W. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 2013, 500:168-174.
24. Hsueh Y.P. The role of the MAGUK protein CASK in neural development and synaptic function. Curr. Med. Chem. 2006, 13:1915-1927.
25. Hsueh Y.P. Calcium/calmodulin-dependent serine protein kinase and mental retardation. Ann. Neurol. 2009, 66:438-443.
26. Hsueh Y.P., Yang F.C., Kharazia V., Naisbitt S., Cohen A.R., Weinberg R.J., Sheng M. Direct interaction of CASK/LIN2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J. Cell Biol. 1998, 142:140-151.
27. Hsueh Y.P., Wang T.F., Yang F.C., Sheng M. Nuclear translocation and transcription regulation by the membrane-associated guanylate kinase CASK/Lin-2. Nature 2000, 404:298-302.
28. Hu H.T., Hsueh Y.P. Calcium influx and postsynaptic proteins coordinate the dendritic filopodium-spine transition. Dev. Neurobiol. 2014, 10.1002/dneu.22181.
29. Jahn R., Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature 2012, 490:201-207.
30. Jeyifous O., Waites C.L., Specht C.G., Fujisawa S., Schubert M., Lin E.I., Marshall J., Aoki C., de Silva T., Montgomery J.M., Garner C.C., Green W.N. SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway. Nat. Neurosci. 2009, 12:1011-1019.
31. Kao T.J., Kania A. Ephrin-mediated cis-attenuation of Eph receptor signaling is essential for spinal motor axon guidance. Neuron 2011, 71:76-91.
32. Kittelmann M., Hegermann J., Goncharov A., Taru H., Ellisman M.H., Richmond J.E., Jin Y., Eimer S. Liprin-alpha/SYD-2 determines the size of dense projections in presynaptic active zones in C. elegans. J. Cell Biol. 2013, 203:849-863.
33. Klein R. Axon guidance: opposing EPHects in the growth cone. Cell 2005, 121:4-6.
34. Klein R., Kania A. Ephrin signalling in the developing nervous system. Curr. Opin. Neurobiol. 2014, 27:16-24.
35. Ko J., Na M., Kim S., Lee J.R., Kim E. Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins. J. Biol. Chem. 2003, 278:42377-42385.
36. LaConte L., Mukherjee K. Structural constraints and functional divergences in CASK evolution. Biochem. Soc. Trans. 2013, 41:1017-1022.
37. Landgraf P., Mikhaylova M., Macharadze T., Borutzki C., Zenclussen A.C., Wahle P., Kreutz M.R. Binding of Y-P30 to syndecan 2/3 regulates the nuclear localization of CASK. PLoS One 2014, 9:e85924.
38. Lee B.B., Martin P.R., Grünert U. Retinal connectivity and primate vision. Prog. Retin. Eye Res. 2010, 29:622-639.
39. Li W., Fan J., Woodley D.T. Nck/Dock: an adapter between cell surface receptors and the actin cytoskeleton. Oncogene 2001, 20:6403-6417.
40. Lin E.I., Jeyifous O., Green W.N. CASK regulates SAP97 conformation and its interactions with AMPA and NMDA receptors. J. Neurosci. 2013, 33:12067-12076.
41. Malik B.R., Gillespie J.M., Hodge J.J. CASK and CaMKII function in the mushroom body α'/β' neurons during Drosophila memory formation. Front. Neural Circ. 2013, 7:52.
42. Marc R.E., Jones B.W., Watt C.B., Anderson J.R., Sigulinsky C., Lauritzen S. Retinal connectomics: towards complete, accurate networks. Prog. Retin. Eye Res. 2013, 37:141-162.
43. Marquardt T., Shirasaki R., Gosh S., Andrews S.E., Carter N., Hunter T., Pfaff S.C. Coexpressed EphA receptors and ephrin-A ligands mediate opposing actions on growth cone navigation from distinct membrane domains. Cell 2005, 121:127-139.
44. Martinez-Estrada O.M., Villa A., Breviario F., Orsenigo F., Dejana E., Bazzoni G. Association of junctional adhesion molecule with calcium/calmodulin-dependent serine-protein kinase (CASK/LIN2) in human epithelial Caco-2 cells. J. Biol. Chem. 2001, 276:9291-9296.
45. Maximov A., Bezprozvanny I. Synaptic targeting of N-type calcium channels in hippocampal neurons. J. Neurosci. 2002, 22:6939-6952.
46. Maximov A., Südhof T.C., Bezprozvanny I. Association of neuronal calcium channels with modular adapter proteins. J. Biol. Chem. 1999, 274:24453-24456.
47. Mercer A.J., Thoreson W.B. The dynamic architecture of photoreceptor ribbon synapses: cytoskeletal, extracellular matrix, and intramembrane proteins. Vis. Neurosci. 2011, 28:453-471.
48. Missler M., Südhof T.C. Neurexins: three genes and 1001 products. Trends Genet. 1998, 14:20-26.
49. Missler M., Fernandez-Chacon R., Südhof T.C. The making of neurexins. J. Neurochem. 1998, 71:1339-1347.
50. Missler M., Südhof T.C., Biederer T. Synaptic cell adhesion. Cold Spring Harb. Perspect. Biol. 2012, 4(4):a005694.
51. Montgomery J.M., Zamorano P.L., Garner C.C. MAGUKs in synapse assembly and function: an emerging view. Cell. Mol. Life Sci. 2004, 61:911-924.
52. Morgans C.W., Kensel-Hammes P., Hurley J.B., Burton K., Idzerda R., McKnight G.S., Bajjalieh S.M. Loss of the synaptic vesicle protein SV2B results in reduced neurotransmission and altered synaptic vesicle protein expression in the retina. PLoS One 2009, e5230.
53. 2+-independent neurexin kinase. Cell 2008, 133:328-339.
54. 2+-sensitive kinase. Sci. Signal. 2010, 3(119):ra33.
55. Najm J., Horn D., Wimplinger I., Golden J.A., Chizhikov V.V., Sudi J., Christian S.L., Ullmann R., Kuechler A., Haas C.A., Flubacher A., Charnas L.R., Uyanik G., Frank U., Klopocki E., Dobyns W.B., Kutsche K. Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum. Nat. Genet. 2008, 40:1065-1067.
56. Pesti S., Bálazs A., Udupa R., Szabo B., Fekete A., Bogel G., Buday L. Complex formation of EphB1/Nck/Caskin1 leads to tyrosine phosphorylation and structural changes of the Caskin1 SH3 domain. Cell Commun. Signal. 2012, 10:36.
57. Rao Y. Dissecting Nck/Dock signaling pathways in Drosophila visual system. Int. J. Biol. Sci. 2005, 1:80-86.
58. Schmitz F. The making of synaptic ribbons: how they are built and what they do. Neuroscientist 2009, 15:611-624.
59. 2+] and GCAPs: aspects on the structure and function of photoreceptor ribbon synapses. Front. Mol. Neurosci. 2014, 7:3.
60. Schmitz F., Königstorfer A., Südhof T.C. RIBEYE, a component of ribbon synapses: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 2000, 28:857-872.
61. Schoch S., Castillo P.E., Jo T., Mukherjee K., Geppert M., Wang Y., Schmitz F., Malenka R.C., Südhof T.C. RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 2002, 415:321-326.
62. 2+-triggered neurotransmitter release. EMBO J. 2006, 25:5825-5852.
63. Sheffler-Collins S.I., Dalva M.B. EphBs: an integral link between synaptic functions and synaptopathies. Trends Neurosci. 2012, 35:293-304.
64. Spangler S.A., Hoogenraad C.C. Liprin-alpha proteins: scaffold molecules for synapse maturation. Biochem. Soc. Trans. 2007, 35:1278-1282.
65. Spangler S.A., Schmitz S.K., Kevenaar J.T., de Graaff E., de Wit H., Demmers J., Toonen R.F., Hoogenraad C.C. Liprin-α2 promotes the presynaptic recruitment and turnover of RIM1/Cask to facilitate synaptic transmission. J. Cell Biol. 2013, 201:915-928.
66. Srivastava N., Rabichaux M.A., Chenaux G., Henkemeyer M., Cowan C.W. EphB2 receptor forward signalling controls cortical growth cone collapse via Nck and Pak. Mol. Cell. Neurosci. 2013, 52:106-116.
67. Stafford R.L., Ear J., Knight M.J., Bowie J.U. The molecular basis of the Caskin1 and Mint1 interaction with Cask. J. Mol. Biol. 2011, 412:3-13.
68. Stafford R.L., Hinde E., Knight M.J., Pennella M.A., Ear J., Digman M.A., Gratton E., Bowie J.U. Tandem SAM domain structure of human Caskin1: a presynaptic, self-assembling scaffold for Cask. Structure 2011, 19:1826-1836.
69. Stein E., Huynh-Do U., Lane A.A., Cerretti D.P., Daniel T.O. Nck recruitment to Eph receptor, EphB1/ELK, couples ligand activation to c-Jun kinase. J. Biol. Chem. 1998, 273:1303-1308.
70. Stryker E., Johnson K.G. LAR, liprin alpha and the regulation of active zone morphogenesis. J. Cell Sci. 2007, 120:3723-3728.
71. Südhof T.C. The presynaptic active zone. Neuron 2012, 75:11-25.
72. Südhof T.C. Calcium control of neurotransmitter release. Cold Spring Harb. Perspect. Biol. 2012, 4(1):a011353.
73. Südhof T.C. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 2013, 80:675-690.
74. Südhof T.C. A molecular machine for neurotransmitter release: synaptotagmin and beyond. Nat. Med. 2013, 19:1227-1231.
75. Südhof T.C., Rizo J. Synaptic vesicle exocytosis. Cold Spring Harb. Perspect. Biol. 2011, 3(12):a005637. (pii).
76. Südhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
77. Tabuchi K., Biederer T., Butz S., Südhof T.C. CASK participates in alternative tripartite complexes in which Mint1 competes for binding with Caskin1, a novel CASK-binding protein. J. Neurosci. 2002, 22:4264-4273.
78. 2+ sensor protein GCAP2 to photoreceptor synaptic ribbons. J. Neurosci. 2010, 30:6559-6576.
79. Wahl S., Katiyar R., Schmitz F. A local, periactive zone endocytic machinery at photoreceptor synapses in close vicinity to synaptic ribbons. J. Neurosci. 2013, 33:10278-10300.
80. Wan Q.F., Heidelberger R. Synaptic release at mammalian bipolar cell terminals. Vis. Neurosci. 2011, 28:109-119.
81. Wang Y., Okamoto M., Schmitz F., Hofmann K., Südhof T.C. RIM is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 1997, 388:593-598.
82. Wang M.M., Janz R., Belizaire R., Frishman L.J., Sherry D.M. Differential distribution and developmental expression of synaptic vesicle protein 2 isoforms in the mouse retina. J. Comp. Neurol. 2003, 460:106-122.
83. Wässle H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 2004, 5:747-757.
84. Wei Z., Zheng S., Spangler S.A., Yu C., Hogenraad C.C., Zhang M. Liprin-mediated large signaling complex organization revealed by the liprin-α/Cask and liprin-α/liprin-β complex structures. Mol. Cell 2011, 43:586-598.
85. Weng Y.L., Liu N., DiAntonio A., Broihier H.T. The cytoplasmic adaptor protein Cask mediates Lar signal transduction during Drosophila motor axon guidance. J. Neurosci. 2011, 31:4421-4433.
86. Wu S.M. Synaptic organization of the vertebrate retina: general principles and species-specific variations. Invest. Ophthalmol. Vis. Sci. 2010, 51:1263-1274.
87. Zamponi G.W. Regulation of presynaptic calcium channels by synaptic proteins. J. Pharmacol. Sci. 2003, 92:79-83.