Formation of the full SNARE complex eliminates interactions of its individual protein components with the Kv2.1 channel

Biochemistry

Volumn 47, Issue 32, 2008, Pages 8342-8349

  Tsuk, Sharon ^a   Lvov, Anatoli ^a   Michaelevski, Izhak ^b   Chikvashvili, Dodo ^a   Lotan, Ilana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CYTOLOGY; FLOW INTERACTIONS; POTASSIUM;

CO-EXPRESSION; FUNCTIONAL INTERACTIONS; IN VITRO STUDIES; IN-VITRO; MOLECULAR EVENTS; NEUROENDOCRINE CELLS; PC12 CELLS; PHYSICAL INTERACTIONS; PLASMA MEMBRANE PROTEINS; POTASSIUM CHANNELS; POTASSIUM CURRENTS; PROTEIN COMPONENTS; SYNTAXIN; SYNTAXIN 1A; XENOPUS OOCYTES;

CHLORINE COMPOUNDS;

SHAB POTASSIUM CHANNEL; SNARE PROTEIN; SYNAPTOBREVIN 1;

ARTICLE; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUROSECRETORY CELL; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECRETION; XENOPUS;

ANIMALS; FEMALE; OOCYTES; PROTEIN BINDING; PROTEIN SUBUNITS; RATS; SHAB POTASSIUM CHANNELS; SNARE PROTEINS; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2; XENOPUS LAEVIS;

EID: 49449111603     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800512p     Document Type: Article

References (36)

1. Sudhof, T. C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
2. Bennett, M. K. (1995) SNAREs and the specificity of transport vesicle targeting. Curr. Opin. Cell Biol. 7, 581-586.
3. Zamponi, G. W. (2003) Regulation of presynaptic calcium channels by synaptic proteins. J. Pharmacol. Sci. 92, 79-83.
4. MacDonald, P. E., Sewing, S., Wang, J., Joseph, J. W., Smukler, S. R., Sakellaropoulos, G., Saleh, M. C., Chan, C. B., Tsushima, R. G., Salapatek, A. M., and Wheeler, M. B. (2002) Inhibition of Kv2.1 voltage-dependent K+ channels in pancreatic beta-cells enhances glucose-dependent insulin secretion. J. Biol. Chem. 277, 44938-44945.
5. Murakoshi, H., and Trimmer, J. S. (1999) Identification of the Kv2.1 K+ channel as a major component of the delayed rectifier K+ current in rat hippocampal neurons. J. Neurosci. 19, 1728-1735.
6. Singer-Lahat, D., Chikvashvili, D., and Lotan, I. (2008) Direct interaction of endogenous Kv channels with Syntaxin enhances exocytosis by neuroendocrine cells. PLoS ONE 3, e1381.
7. Singer-Lahat, D., Sheinin, A., Chikvashvili, D., Tsuk, S., Greitzer, D., Friedrich, R., Feinshreiber, L., Ashery, U., Benveniste, M., Levitan, E. S., and Lotan, I. (2007) K+ channel facilitation of exocytosis by dynamic interaction with syntaxin. J. Neurosci. 27, 1651-1658.
8. MacDonald, P. E., Wang, G., Tsuk, S., Dodo, C., Kang, Y., Tang, L., Wheeler, M. B., Cattral, M. S., Lakey, J. R., Salapatek, A. M., Lotan, I., and Gaisano, H. Y. (2002) Synaptosome-associated protein of 25 kilodaltons modulates Kv2.1 voltage-dependent K(+) channels in neuroendocrine islet beta-cells through an interaction with the channel N terminus. Mol. Endocrinol. 16, 2452-2461.
9. Wolf-Goldberg, T., Michaelevski, I., Tsuk, S., Chikvashvili, D., and Lotan, I. (2006) Regulation by t-SNAREs of Kv2.2 activation and inactivation gating is different from that of Kv2.1; implications to underlying protein-protein interactions.
10. Leung, Y. M., Kang, Y., Gao, X., Xia, F., Xie, H., Sheu, L., Tsuk, S., Lotan, I., Tsushima, R. G., and Gaisano, H. Y. (2003) Syntaxin 1A binds to the cytoplasmic C terminus of Kv2.1 to regulate channel gating and trafficking. J. Biol. Chem. 278, 17532-17538.
11. Michaelevski, I., Chikvashvili, D., Tsuk, S., Singer-Lahat, D., Kang, Y., Linial, M., Gaisano, H. Y., Fili, O., and Lotan, I. (2003) Direct interaction of target SNAREs with the Kv2.1 channel. Modal regulation of channel activation and inactivation gating. J. Biol. Chem. 278, 34320-34330.
12. Tsuk, S., Michaelevski, I., Bentley, G. N., Joho, R. H., Chikvashvili, D., and Lotan, I. (2005) Kv2.1 channel activation and inactivation is influenced by physical interactions of both syntaxin 1A and the syntaxin 1A/soluble N-ethylmaleimide-sensitive factor-25 (t-SNARE) complex with the C terminus of the channel. Mol. Pharmacol. 67, 480-488.
13. Leung, Y. M., Kwan, E. P., Ng, B., Kang, Y., and Gaisano, H. Y. (2007) SNAREing voltage-gated K+ and ATP-sensitive K+ channels: tuning beta-cell excitability with syntaxin-1A and other exocytotic proteins. Endocr. Rev. 28, 653-663.
14. Lvov, A., Chikvashvili, D., Michaelevski, I., and Lotan, I. (2008) VAMP2 interacts directly with the N terminus of Kv2.1 to enhance channel inactivation. Pfluegers Arch.
15. Levin, G., Chikvashvili, D., Singer-Lahat, D., Peretz, T., Thornhill, W. B., and Lotan, I. (1996) Phosphorylation of a K+ channel alpha subunit modulates the inactivation conferred by a beta subunit. Involvement of cytoskeleton. J. Biol. Chem. 271, 29321-29328.
16. Levin, G., Keren, T., Peretz, T., Chikvashvili, D., Thornhill, W. B., and Lotan, I. (1995) Regulation of RCK1 currents with a cAMP analog via enhanced protein synthesis and direct channel phosphorylation. J. Biol. Chem. 270, 14611-14618.
17. Fili, O., Michaelevski, I., Bledi, Y., Chikvashvili, D., Singer-Lahat, D., Boshwitz, H., Linial, M., and Lotan, I. (2001) Direct interaction of a brain voltage-gated K+ channel with syntaxin 1A: functional impact on channel gating. J. Neurosci. 21, 1964-1974.
18. Jing, J., Chikvashvili, D., Singer-Lahat, D., Thornhill, W. B., Reuveny, E., and Lotan, I. (1999) Fast inactivation of a brain K+ channel composed of Kv1.1 and Kvbeta1.1 subunits modulated by G protein beta gamma subunits. EMBO J. 18, 1245-1256.
19. Kobrinsky, E., Stevens, L., Kazmi, Y., Wray, D., and Soldatov, N. M. (2006) Molecular rearrangements of the Kv2.1 potassium channel termini associated with voltage gating. J. Biol. Chem. 281, 19233-19240.
20. Rhodes, K. J., Keilbaugh, S. A., Barrezueta, N. X., Lopez, K. L., and Trimmer, J. S. (1995) Association and colocalization of K+ channel alpha- and beta-subunit polypeptides in rat brain. J. Neurosci. 15, 5360-5371.
21. Trimmer, J. S. (1993) Expression of Kv2.1 delayed rectifier K+ channel isoforms in the developing rat brain. FEBS Lett. 324, 205-210.
22. Hwang, P. M., Fotuhi, M., Bredt, D. S., Cunningham, A. M., and Snyder, S. H. (1993) Contrasting immunohistochemical localizations in rat brain of two novel K+ channels of the Shab subfamily. J. Neurosci. 13, 1569-1576.
23. MacDonald, P. E., Ha, X. F., Wang, J., Smukler, S. R., Sun, A. M., Gaisano, H. Y., Salapatek, A. M., Backx, P. H., and Wheeler, M. B. (2001) Members of the Kv1 and Kv2 voltage-dependent K(+) channel families regulate insulin secretion. Mol. Endocrinol. 15, 1423-1435.
24. Colman, A., and Morser, J. (1979) Export of proteins from oocytes of Xenopus laevis. Cell 17, 517-526.
25. Cavalli, A., Eder-Colli, L., Dunant, Y., Loctin, F., and Morel, N. (1991) Release of acetylcholine by Xenopus oocytes injected with mRNAs from cholinergic neurons. EMBO J. 10, 1671-1675.
26. Aleu, J., Martin-Satue, M., Navarro, P., Perez de Lara, I., Bahima, L., Marsal, J., and Solsona, C. (2003) Release of ATP induced by hypertonic solutions in Xenopus oocytes. J. Physiol. 547, 209-219.
27. El-Jouni, W., Haun, S., Hodeify, R., Hosein Walker, A., and Machaca, K. (2007) Vesicular traffic at the cell membrane regulates oocyte meiotic arrest. Development 134, 3307-3315.
28. Cohen, R., Schmitt, B. M., and Atlas, D. (2008) Reconstitution of depolarization and Ca2+-evoked secretion in Xenopus oocytes monitored by membrane capacitance. Methods Mol. Biol. 440, 269-282.
29. Shah, M. M., Anderson, A. E., Leung, V., Lin, X., and Johnston, D. (2004) Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44, 495-508.
30. Leung, Y. M., Kang, Y., Xia, F., Sheu, L., Gao, X., Xie, H., Tsushima, R. G., and Gaisano, H. Y. (2005) Open form of syntaxin-1A is a more potent inhibitor than wild-type syntaxin-1A of Kv2.1 channels. Biochem. J. 387, 195-202.
31. Sorensen, J. B. (2005) SNARE complexes prepare for membrane fusion. Trends Neurosci. 28, 453-455.
32. Kerschensteiner, D., Soto, F., and Stocker, M. (2005) Fluorescence measurements reveal stoichiometry of K+ channels formed by modulatory and delayed rectifier alpha-subunits. Proc. Natl. Acad. Sci. U.S.A. 102, 6160-6165.
33. Kurata, H. T., Soon, G. S., Eldstrom, J. R., Lu, G. W., Steele, D. F., and Fedida, D. (2002) Amino-terminal determinants of U-type inactivation of voltage-gated K+ channels. J. Biol. Chem. 277, 29045-29053.
34. Ju, M., Stevens, L., Leadbitter, E., and Wray, D. (2003) The Roles of N- and C-terminal determinants in the activation of the Kv2.1 potassium channel. J. Biol. Chem. 278, 12769-12778.
35. VanDongen, A. M., Frech, G. C., Drewe, J. A., Joho, R. H., and Brown, A. M. (1990) Alteration and restoration of K+ channel function by deletions at the N- and C-termini. Neuron 5, 433-443.
36. Vaidyanathan, V. V., Yoshino, K., Jahnz, M., Dorries, C., Bade, S., Nauenburg, S., Niemann, H., and Binz, T. (1999) Proteolysis of SNAP-25 isoforms by botulinum neurotoxin types A, C, and E: domains and amino acid residues controlling the formation of enzyme-substrate complexes and cleavage. J. Neurochem. 72, 327-337.