A proteomic screen for presynaptic terminal N-type calcium channel (CaV2.2) binding partners

Journal of Biochemistry and Molecular Biology

Volumn 40, Issue 3, 2007, Pages 302-314

  Khanna, Rajesh ^a   Zougman, Alexandre ^b   Stanley, Elise F ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b Protana Analytical Services   (Canada)

Author keywords

Active zone; Cytoplasmic matrix; Particle web; Scaffold; Synaptosome; Transmitter release site

Indexed keywords

RATTUS;

EID: 34249711444     PISSN: 12258687     EISSN: 02191024     Source Type: Journal    
DOI: 10.5483/bmbrep.2007.40.3.302     Document Type: Article

References (41)

1. Atlas, D. (2001) Functional and physical coupling of voltage-sensitive calcium channels with exocytotic proteins: ramifications for the secretion mechanism. J. Neurochem. 77, 972-985.
2. Bennett, M. K., Calakos, N. and Scheller, R. H. (1992) Syntaxin: A synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Sci. 257, 255-259.
3. Blackstone, C. D., Moss, S. J., Martin, L. J., Levey, A. I., Price, D. L. and Huganir, R. L. (1992) Biochemical characterization and localization of a non-N-methyl-D-aspartate glutamate receptor in rat brain. J. Neurochem. 58, 1118-1126.
4. Calakos, N., Schoch, S., Sudhof, T. C. and Malenka, R. C. (2004) Multiple roles for the active zone protein RIM1alpha in late stages of neurotransmitter release. Neuron 42, 889-896.
5. Dieck T. S., Altrock, W. D., Kessels, M. M., Qualmann, B., Regus, H., Brauner, D., Fejtova, A., Bracko, O., Gundelfinger, E. D. and Brandstatter, J. H. (2005) Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 168, 825-836.
6. Dresbach, T., Qualmann, B., Kessels, M. M., Garner, C. C. and Gundelfinger, E. D. (2001) The presynaptic cytomatrix of brain synapses. Cell Mol. Life Sci. 58, 94-116.
7. El Far, O., Charvin, N., Leveque, C., Martin-Moutot, N., Takahashi, M. and Seagar, M. J. (1995) Interaction of a synaptobrevin (VAMP)-syntaxin complex with presynaptic calcium channels. FEBS Letters, 361, 101-105.
8. Fried, R. C. and Blaustein, M. P. (1978) Retrieval and recycling of synaptic vesicle membrane in pinched-off nerve terminals (synaptosomes). J. Cell Biol. 78, 685-700.
9. Geppert, M., Goda, Y., Stevens, C. F. and Südhof, T. C. (1997) The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature (Lond.) 387, 810-814.
10. Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P. and Grant, S. G. (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3, 661-669.
11. Ishikawa, H., Shimada, O., Murakami, T., Saisu, H. and Abe, T. (1993) Immunohistochemical localization of the proteins associated with brain N-type calcium channels. Ann. N.Y. Acad. Sci. 707, 376-378.
12. Jones, O. T., Bernstein, G. M., Jones, E. J., Jugloff, D. G., Law, M., Wong, W. and Mills, L. R. (1997) N-Type calcium channels in the developing rat hippocampus: subunit, complex, and regional expression. J. Neurosci. 17, 6152-6164.
13. Khanna, R., Li, Q., Sun, L., Collins, T. J. and Stanley, E. F. (2006) N type Ca(2+) channels and RIM scaffold protein covary at the presynaptic transmitter release face but are components of independent protein complexes. Neurosci. 140, 1201-1208
14. Khanna, R., Sun, L., Li, Q., Guo, L. and Stanley, E. F. (2006) Long splice variant N type calcium channels are clustered at presynaptic transmitter release sites without modular adaptor proteins. Neurosci. 138, 1115-1125.
15. Koh, T. W., Verstreken, P. and Bellen, H. J. (2004) Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43, 193-205.
16. Lau, L. F., Mammen, A., Ehlers, M. D., Kindler, S., Chung, W. J., Garner, C. C. and Huganir, R. L. (1996) Interaction of the N-methyl-D-aspartate receptor complex with a novel synapse-associated protein, SAP102. J. Biol. Chem. 271, 21622-21628.
17. Li, D., Wang, F., Lai, M., Chen, Y. and Zhang, J. F. (2005) A protein phosphatase 2calpha-Ca2+ channel complex for dephosphorylation of neuronal Ca2+ channels phosphorylated by protein kinase C. J .Neurosci. 25, 1914-1923.
18. Li, K. W., Hornshaw, M. P., Van der Schors, R. C., Watson, R., Tate, S., Casetta, B., Jimenez, C. R., Gouwenberg, Y., Gundelfinger, E. D., Smalla, K. and Smit, A. B. (2004a) Proteomics analysis of rat brain postsynaptic density. Implications of the diverse protein functional groups for the integration of synaptic physiology. J. Biol. Chem. 279, 987-1002.
19. Li, Q., Lau, A., Morris, T. J., Guo, L., Fordyce, C. B. and Stanley, E. F. (2004b) 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.
20. Marie, B., Sweeney, S. T., Poskanzer, K. E., Roos, J., Kelly, R. B. and Davis, G. W. (2004) Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron 43, 207-219.
21. Maximov, A. and Bezprozvanny, I. (2002) Synaptic targeting of N-type calcium channels in hippocampal neurons. J. Neurosci. 22, 6939-6952.
22. Maximov, A., Sudhof, T. C. and Bezprozvanny, I. (1999) Association of neuronal calcium channels with modular adaptor proteins. J. Biol. Chem. 274, 24453-24456.
23. Mirotznik, R. R., Zheng, X. and Stanley, E. F. (2000) G-Protein types involved in calcium channel inhibition at a presynaptic nerve terminal. J. Neurosci. 20, 7614-7621.
24. Peng, J., Kim, M. J., Cheng, D., Duong, D. M., Gygi, S. P. and Sheng, M. (2004) Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J. Biol. Chem. 279, 21003-21011.
25. Perkins, D. N., Pappin, D. J., Creasy, D. M. and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567.
26. Phillips, G. R., Florens, L., Tanaka, H., Khaing, Z. Z., Fidler, L., Yates, J. R., III and Colman, D. R. (2005) Proteomic comparison of two fractions derived from the transsynaptic scaffold. J. Neurosci. Res. 81, 762-775
27. Phillips, G. R., Huang, J. K., Wang, Y., Tanaka, H., Shapiro, L., Zhang, W. et al. (2001) The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 32, 63-77.
28. 2+ entry. J. Neurosci. 17, 8169-8177.
29. Saisu, H., Ibaraki, K., Yamaguchi, T., Sekine, Y. and Abe, T. (1991) Monoclonal antibodies immunoprecipitating omega-conotoxin-sensitive calcium channel molecules recognize two novel proteins localized in the nervous system. Biochem. Biophys. Res. Commun. 181, 59-66.
30. Schmitt-Ulms, G., Hansen, K., Liu, J., Cowdrey, C., Yang, J., DeArmond, S. J., Cohen, F. E., Prusiner, S. B. and Baldwin, M. A. (2004) Time-controlled transcardiac perfusion cross-linking for the study of protein interactions in complex tissues. Nat. Biotechnol. 22, 724-731.
31. Schrimpf, S. P., Meskenaite, V., Brunner, E., Rutishauser, D., Walther, P., Eng, J., Aebersold, R. and Sonderegger, P. (2005) Proteomic analysis of synaptosomes using isotope-coded affinity tags and mass spectrometry. Proteomics 5, 2531-2541.
32. Sheng, Z. H., Westenbroek, R. E. and Catterall, W. A. (1998) Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery. J. Bioenerg. Biomembr. 30, 335-345.
33. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal.Chem. 68, 850-858.
34. 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. (2003) Calcium channel structural determinants of synaptic transmission between identified invertebrate neurons. J. Biol. Chem. 278, 4258-4267
35. Stanley, E. F. (1997) The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci. 20, 404-409.
36. Sun, L., Li, Q., Khanna, R., Chan, A. W., Wong, F. and Stanley, E. F. (2006) Transmitter release face Ca channel clusters persist at isolated presynaptic terminals. Eur. J. Neurosci. 23, 1391-1396.
37. Sunderland, W. J., Son, Y. J., Miner, J. H., Sanes, J. R. and Carlson, S. S. (2000) The presynaptic calcium channel is part of a transmembrane complex linking a synaptic laminin (alpha4beta2gamma1) with non-erythroid spectrin. J. Neurosci. 20, 1009-1019.
38. Takao-Rikitsu, E., Mochida, S., Inoue, E., guchi-Tawarada, M., Inoue, M., Ohtsuka, T. and Takai, Y. (2004) Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release. J. Cell Biol. 164, 301-311.
39. Vigers, A. J. and Pfenninger, K. H. (1991) N-type and L-type calcium channels are present in nerve growth cones. Numbers increase on synaptogenesis. Brain Res. Dev. Brain Res. 60, 197-203.
40. Witzmann, F. A., Arnold, R. J., Bai, F., Hrncirova, P., Kimpel, M. W., Mechref, Y. S., McBride, W. J., Novotny, M. V., Pedrick, N. M., Ringham, H. N. and Simon, J. R. (2005) A proteomic survey of rat cerebral cortical synaptosomes. Proteomics 5, 2177-2201.
41. Ziv, N. E. and Garner, C. C. (2004) Cellular and molecular mechanisms of presynaptic assembly. Nat. Rev. Neurosci. 5, 385-399.