A VAMP7/Vti1a SNARE complex distinguishes a non-conventional traffic route to the cell surface used by KChIP1 and Kv4 potassium channels

Biochemical Journal

Volumn 418, Issue 3, 2009, Pages 529-540

  Flowerdew, Sarah E ^a   Burgoyne, Robert D ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Calcium binding protein; K+ channel interacting protein (KChIP); Neuronal calcium sensor (NCS) protein; Potassium channel; Soluble N ethylmaleimide sensitive fusion protein attachment protein receptor (SNARE)

Indexed keywords

CALCIUM-BINDING PROTEIN; K+ CHANNEL-INTERACTING PROTEIN (KCHIP); NEURONAL CALCIUM SENSOR (NCS) PROTEIN; POTASSIUM CHANNEL; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FUSION PROTEIN ATTACHMENT PROTEIN RECEPTOR (SNARE);

CALCIUM; CALCIUM ALLOYS; NUCLEIC ACIDS; PLASMAS; POTASSIUM; PROTEINS; RNA; SENSORS;

CELL MEMBRANES;

CELL PROTEIN; KV CHANNEL INTERACTING PROTEIN; RAB PROTEIN; SHAL POTASSIUM CHANNEL; SMALL INTERFERING RNA; SNARE PROTEIN; SYNAPTOBREVIN; SYNAPTOBREVIN 7; UNCLASSIFIED DRUG; VESICLE ASSOCIATED MEMBRANE PROTEIN 7; VESICULAR STOMATITIS VIRUS G PROTEIN; G PROTEIN, VESICULAR STOMATITIS VIRUS; MEMBRANE PROTEIN; QB SNARE PROTEIN; VAMP7 PROTEIN, HUMAN; VIRUS ENVELOPE PROTEIN; VTI1A PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; ANIMAL; GENETICS; HELA CELL; METABOLISM; MOUSE; NEUROBLASTOMA; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; HELA CELLS; HUMANS; KV CHANNEL-INTERACTING PROTEINS; MEMBRANE GLYCOPROTEINS; MICE; NEUROBLASTOMA; PROTEIN TRANSPORT; QB-SNARE PROTEINS; R-SNARE PROTEINS; RAB1 GTP-BINDING PROTEINS; SHAL POTASSIUM CHANNELS; SNARE PROTEINS; VIRAL ENVELOPE PROTEINS;

EID: 62149148157     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081736     Document Type: Article

References (50)

1. Birnbaum, S. G., Varga, A. W., Yuan, L.-L., Anderson, A. E., Sweatt, J. D. and Schrader, L. A. (2004) Structure and function of Kv4-family transient potassium channels. Physiol. Rev. 84, 803-833
2. Isbrandt, D., Leicher, T., Waldschutz, R., Zhu, X., Luhmann, U., Michel, U., Sauter, K. and Pongs, O. (2000) Gene structures and expression profiles of three human KCND (Kv4) potassium channels mediating A-type currents I(TO) and I(SA). Genomics 64, 144-154
3. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869-875
4. Cai, X., Liang, C. W., Muralidharan, S., Kao, J. P., Tang, C. M. and Thompson, S. M. (2004) Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44, 351-364
5. Bernard, C., Anderson, A., Becker, A., Poolos, N. P., Beck, H. and Johnston, D. (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305, 532-535
6. An, W. F., Bowlby, M. R., Bett, M., Cao, J., Ling, H. P., Mendoza, G., Hinson, J. W., Mattsson, K. I., Strassle, B. W., Trimmer, J. S. and Rhodes, K. J. (2000) Modulation of A-type potassium channels by a family of calcium sensors. Nature 403, 553-556
7. 2+-binding proteins. Biochem. J. 353, 1-12
8. Burgoyne, R. D. (2007) Neuronal calcium sensor proteins: generating diversity in neuronal Ca(2+) signalling. Nat. Rev. Neurosci. 8, 182-193
9. Pioletti, M., Findeisen, F., Hura, G. L. and Minor, D. L. (2006) Three-dimensional structure of the KChIP1-Kv4.3 T1 complex reveals a cross-shaped octamer. Nat. Struct. Mol. Biol. 13, 987-995
10. Wang, H., Yan, Y., Liu, Q., Huang, Y., Shen, Y., Chen, L., Chen, Y., Yang, Q., Hao, Q., Wang, K. and Chai, J. (2007) Structural basis for modulation of Kv4 K(+) channels by auxiliary KChIP subunits. Nat. Neurosci. 10, 32-39
11. + channels. J. Cell Sci. 116, 4833-4845
12. + channels mediated by KChIP1 is via a novel post-ER vesicular pathway. J. Cell Biol. 171, 459-469
13. Shibata, R., Misonou, H., Campomanes, C. R., Anderson, A. E., Schrader, L. A., Doliveira, L. C., Carroll, K. I., Sweatt, J. D., Rhodes, K. J. and Trimmer, J. S. (2003) A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J. Biol. Chem. 278, 36445-36454
14. Bahring, R., Dannenberg, J., Peters, H. C., Leicher, T., Pongs, O. and Isbrandt, D. (2001) Conserved Kv4 N-terminal domain critical for effects of Kv channel interacting protein 2.2 on channel expression and gating. J. Biol. Chem. 276, 23888-23894
15. Takimoto, K., Yang, E.-K. and Conforti, L. (2002) Palmitoylation of KChIP splicing variants is required for efficient cell surface expression of Kv4.3 channels. J. Biol. Chem. 277, 26904-26911
16. Beckers, C. J. M. and Balch, W. E. (1989) Calcium and GTP: essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus. J. Cell Biol. 108, 1245-1256
17. Presley, J. F., Cole, N. B., Schroer, T. A., Hirschberg, K., Zaal, K. J. M. and Lippincott-Schwartz, J. (1997) ER-to-Golgi transport visualized in living cells. Nature 389, 81-85
18. Kuge, O., Dascher, C., Orci, L., Rowe, T., Amherdt, M., Plutner, H., Ravazzola, M., Tanigawa, G., Rothman, J. E. and Balch, W. E. (1994) Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments. J. Cell Biol. 125, 51-65
19. Gurkan, C., Koulov, A. V. and Balch, W. E. (2007) An evolutionary perspective on eukaryotic membrane trafficking. Adv. Exp. Med. Biol. 607, 73-83
20. Bannykh, S. I. and Balch, W. E. (1997) Membrane dynamics at the endoplasmic reticulum-Golgi interface. J. Cell Biol. 138, 1-4
21. Bednarek, S. Y., Ravazzola, M., Hosobuchi, M., Amherdt, M., Perrelet, A., Schekman, R. and Orci, L. (1995) COPI- and COPII-coated vesicles bud directly from the endoplasmic reticulum in yeast. Cell 29, 1183-1196
22. Takida, S., Maeda, Y. and Kinoshita, T. (2008) Mammalian GPI-anchored proteins require p24 proteins for their efficient transport from the ER to the plasma membrane. Biochem. J. 409, 555-562
23. Muniz, M., Morsomme, P. and Riezman, H. (2001) Protein sorting upon exit from the endoplasmic reticulum. Cell 104, 313-320
24. Stephens, D. J. and Pepperkok, R. (2002) Imaging of procollagen transport reveals COPI-dependent cargo sorting during ER-to-Golgi transport in mammalian cells. J. Cell Sci. 115, 1149-1160
25. Starkuviene, V. and Pepperkok, R. (2007) Differential requirements for ts-O45-G and procollagen biosynthetic transport. Traffic 8, 1035-1051
26. Siddiqi, S. A., Gorelick, F. S., Mahan, J. T. and Mansbach, C. M. (2003) COPII proteins are required for Golgi fusion but not for endoplasmic reticulum budding of the pre-chylomicron transport vesicle. J. Cell Sci. 116, 415-427
27. Wu, G., Zhao, G. and He, Y. (2003) Distinct pathways for the trafficking of angiotensin II and adrenergic receptors from the endoplasmic reticulum to the cell surface: Rab1-independent transport of a G protein-coupled receptor. J. Biol. Chem. 278, 47062-47069
28. Ye, B., Zhang, Y., Song, W., Younger, S. H., Jan, L. Y. and Jan, Y. N. (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130, 717-729
29. Kloepper, T. H., Kienle, C. N. and Fasshauer, D. (2007) An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell 18, 3463-3471
30. Dascher, C., Matteson, J. and Balch, W. E. (1994) Syntaxin 5 regulates endoplasmic reticulum to Golgi transport. J. Biol. Chem. 269, 29363-29366
31. Xu, D., Joglekar, A. P., Williams, A. L. and Hay, J. C. (2000) Subunit structure of a mammalian ER/Golgi SNARE complex. J. Biol. Chem. 275, 39631-39639
32. Zhang, T. and Hong, W. (2001) Ykt6 forms a SNARE complex with syntaxin 5, GS28, and Bet1 and participates in a late stage in endoplasmic reticulum-Golgi transport. J. Biol. Chem. 276, 27480-27487
33. Siddiqi, S. A., Siddiqi, S., Mahan, J., Peggs, K., Gorelick, F. S. and Mansbach, C. M. (2006) The identification of a novel ER to Golgi SNARE complex used by the pre-chylomicron transport vesicle. J. Biol. Chem. 281, 20974-20982
34. Venn, N., Haynes, L. P. and Burgoyne, R. D. (2008) Specific effects of KChIP3/calsenilin/DREAM but not KChIPs1, 2 and 4 on calcium signalling and regulated secretion in PC12 cells. Biochem. J. 413, 71-80
35. Handley, M. T. W., Haynes, L. P. and Burgoyne, R. D. (2007) Differential dynamics of Rab3A and Rab27A on secretory granules. J. Cell Sci. 120, 973-984
36. Hasegawa, H., Zinsser, S., Rhee, Y., Vik-Mo, E. O., Davanger, S. and Hay, J. C. (2003) Mammalian ykt6 is a neuronal SNARE targeted to a specialized compartment by its profilin-like amino terminal domain. Mol. Biol. Cell. 14, 698-720
37. ΔΔCT method. Methods 25, 402-408
38. Haas, A. K., Yoshimura, S., Stephens, D. J., Preisinger, C., Fuchs, E. and Barr, F. A. (2007) Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. J. Cell Sci. 120, 2997-3010
39. Galli, T., Zahraoui, A., Vaidyanathan, V. V., Raposo, G., Tian, J. M., Karin, M., Niemann, H. and Louvard, D. (1998) A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol. Biol. Cell 9, 1437-1448
40. Pryor, P. R., Mullock, B. M., Bright, N. A., Lindsay, M. R., Gray, S. R., Richardson, S. C., Stewart, A., James, D. E., Piper, R. C. and Luzio, J. P. (2004) Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 5, 590-595
41. Advani, R. J., Yang, B., Prekeris, R., Lee, K. C., Klumperman, J. and Scheller, R. H. (1999) VAMP-7 mediates vesicular transport from endosomes to lysosomes. J. Cell Biol. 146, 765-776
42. Rossi, V., Banfield, D. K., Vacca, M., Dietrich, L. E., Ungermann, C., D'Esposito, M., Galli, T. and Filippini, F. (2004) Longins and their longin domains: regulated SNAREs and multifunctional SNARE regulators. Trends Biochem. Sci. 29, 682-688
43. Ward, D. M., Pevsner, J., Scullion, M. A., Vaughn, M. and Kaplan, J. (2000) Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol. Biol. Cell 11, 2327-2333
44. Coco, S., Raposo, G., Martinez, S., Fontaine, J. J., Takamori, S., Zahraoui, A., Jahn, R., Matteoli, M., Louvard, D. and Galli, T. (1999) Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: evidence for a novel membrane compartment. J. Neurosci. 19, 9803-9812
45. Martinez-Arca, S., Coco, S., Mainguy, G., Schenk, U., Alberts, P., Bouille, P., Mezzina, M., Prochiantz, A., Matteoli, M., Louvard, D. and Galli, T. (2001) A common exocytotic mechanism mediates axonal and dendritic outgrowth. J. Neurosci. 21, 3830-3838
46. Greaves, J., Salaun, C., Fukata, Y., Fukata, M. and Chamberlain, L. H. (2008) Palmitoylation and membrane interactions of the neuroprotective chaperone cysteine-string protein. J. Biol. Chem. 283, 25014-25026
47. Pruunsild, P. and Timmusk, T. (2005) Structure, alternative splicing, and expression of the human and mouse KCNIP gene family. Genomics 86, 581-593
48. Kuo, H.-C., Cheng, C.-F., Clark, R. B., Lin, J. J.-C., Lin, J. L.-C., Hoshijima, M., Nguyen-Tran, V. T. B., Gu, Y., Ikeda, Y., Chu, P.-H. et al. (2001) A defect in the Kv channel-interacting protein 2 (KChIp2) gene leads to a complete loss of Ito and confers susceptibility to ventricular tachycardia. Cell 107, 801-813
49. Advani, R. J., Bae, H. R., Bock, J. B., Chao, D. S., Doung, Y. C., Prekeris, R., Yoo, J. S. and Scheller, R. H. (1998) Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J. Biol. Chem. 273, 10317-10324
50. Xu, Y., Wong, S. H., Tang, B. L., Subramaniam, V. N., Zhang, T. and Hong, W. (1998) A 29-kilodalton Golgi soluble N-ethylmaleimide-sensitive factor attachment protein receptor (Vti1-rp2) implicated in protein trafficking in the secretory pathway. J. Biol. Chem. 273, 21783-21789