Traffic of Kv4 K+ channels mediated by KChIP1 is via a novel post-ER vesicular pathway

Journal of Cell Biology

Volumn 171, Issue 3, 2005, Pages 459-469

  Hasdemir, Burcu ^a   Fitzgerald, Daniel J ^a   Prior, Ian A ^a   Tepikin, Alexei V ^a   Burgoyne, Robert D ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN COMPLEX I; GLYCOPROTEIN; GUANOSINE TRIPHOSPHATE; POTASSIUM; POTASSIUM CHANNEL; POTASSIUM CHANNEL INTERACTING PROTEIN 3; PROTEIN; PROTEIN SAR1; UNCLASSIFIED DRUG; VESICULAR STOMATITIS VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL MEMBRANE; CELL VACUOLE; ENDOPLASMIC RETICULUM; EXOCYTOSIS; GOLGI COMPLEX; HIPPOCAMPUS; HUMAN; HUMAN CELL; MALE; MEMBRANE TRANSPORT; MUTATION; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; RAT; SIGNAL TRANSDUCTION; TRANSPORT VESICLE;

ANIMALS; CALCIUM; CELL MEMBRANE; CELLS, CULTURED; COAT PROTEIN COMPLEX I; COP-COATED VESICLES; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HIPPOCAMPUS; HUMANS; KV CHANNEL-INTERACTING PROTEINS; MALE; MONOMERIC GTP-BINDING PROTEINS; MUTATION; NEURONS; PROTEIN TRANSPORT; RATS; RATS, WISTAR; SHAL POTASSIUM CHANNELS; VESICULAR STOMATITIS-INDIANA VIRUS; VIRAL PROTEINS;

ANIMALIA; VESICULAR STOMATITIS VIRUS;

EID: 27744482336     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200506005     Document Type: Article

References (58)

1. Amberg, G.C., S.D. Koh, W.J. Hatton, K.J. Murray, K. Monaghan, B. Horowitz, and K.M. Sanders. 2002. Contribution of Kv4 channels toward the A-type potassium current in murine colonic myocytes. J. Physiol. 544:403-415.
2. An, W.F., M.R. Bowlby, M. Betty, J. Cao, H.P. Ling, G. Mendoza, J.W. Hinson, K.I. Mattsson, B.W. Strassle, J.S. Trimmer, and K.J. Rhodes. 2000. Modulation of A-type potassium channels by a family of calcium sensors. Nature. 403:553-556.
3. Aridor, M., S.I. Bannykh, T. Rowe, and W.E. Balch. 1995. Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131:875-893.
4. Aridor, M., K.N. Fish, S. Bannykh, J. Weissman, T.H. Roberts, J. Lippincott-Schwartz, and W.E. Balch. 2001. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152:213-229.
5. Aridor, M., A.K. Guzik, A. Bielli, and K.N. Fish. 2004. Endoplasmic reticulum export site formation and function in dendrites. J. Neurosci. 24:3770-3776.
6. Bahring, R., J. Dannenberg, H.C. Peters, T. Leicher, O. Pongs, and D. Isbrandt. 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.
7. Barnard, R.J., A. Morgan, and R.D. Burgoyne. 1997. Stimulation of NSF ATPase activity by alpha-SNAP is required for SNARE complex disassembly and exocytosis. J. Cell Biol. 139:875-883.
8. Beckers, C.J., D.S. Keller, and W.E. Balch. 1987. Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the Golgi complex. Cell. 50:523-534.
9. Bednarek, S.Y., M. Ravazzola, M. Hosobuchi, M. Amherdt, A. Perrelet, R. Schekman, and L. Orci. 1995. COPI- and COPII-coated vesicles bud directly from the endoplasmic reticulum in yeast. Cell. 83:1183-1196.
10. Bergmann, J.E. 1989. Using temperature-sensitive mutants of VSV to study membrane protein biogenesis. Methods Cell Biol. 32:85-110.
11. Bernard, C., A. Anderson, A. Becker, N.P. Poolos, H. Beck, and D. Johnston. 2004. Acquired dendritic channelopathy in temporal lobe epilepsy. Science. 305:532-535.
12. Birnbaum, S.G., A.W. Varga, L.L. Yuan, A.E. Anderson, J.D. Sweatt, and L.A. Schrader. 2004. Structure and function of Kv4-family transient potassium channels. Physiol. Rev. 84:803-833.
13. Blum, R., F. Pfeiffer, P. Feick, W. Nastainczyk, B. Kohler, K.H. Schafer, and I. Schulz. 1999. Intracellular localization and in vivo trafficking of p24A and p23. J. Cell Sci. 112:537-548.
14. 2+-binding proteins. Biochem. J. 353:1-12.
15. 2+-sensor proteins: multitalented regulators of neuronal function. Trends Neurosci. 27:203-209.
16. Christoforidis, S., H.M. McBride, R.D. Burgoyne, and M. Zerial. 1999. The Rab5 effector EEA1 is a core component of endosome docking. Nature. 397:621-625.
17. Dascher, C., and W.E. Balch. 1994. Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J. Biol. Chem. 269:1437-1448.
18. Dilks, D., H.P. Ling, M. Cockett, P. Sokol, and R. Numann. 1999. Cloning and expression of the human kv4.3 potassium channel. J. Neurophysiol. 81:1974-1977.
19. Griffiths, G., S. Pfeiffer, K. Simons, and K. Matlin. 1985. Exit of newly synthesized membrane proteins from the trans cisterna of the Golgi complex to the plasma membrane. J. Cell Biol. 101:949-964.
20. Hatano, N., S. Ohya, and Y. Imaizumi. 2002. Functional interaction between KChIP1 and GFP-fused Kv4.3L co-expressed in HEK293 cells. Pflugers Arch. 444:80-88.
21. Haynes, L.P., G.M.H. Thomas, and R.D. Burgoyne. 2005. Interaction of neuronal calcium sensor-1 and ARF1 allows bidirectional control of PI(4) kinase and TGN-plasma membrane traffic. J. Biol. Chem. 280:6047-6054.
22. Holmqvist, M.H., J. Cao, R. Hernandez-Pineda, M.D. Jacobson, K.I. Carroll, M.A. Sung, M. Betty, P. Ge, K.J. Gilbride, M.E. Brown, et al. 2002.Elimination of fast inactivation in Kv4 A-type potassium channels by an auxiliary subunit domain. Proc. Natl. Acad. Sci. USA. 99:1035-1040.
23. Horton, A.C., and M.D. Ehlers. 2003. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23:6188-6199.
24. 2+-dependent binding partners for the neuronal calcium sensor protein neurocalcin delta: interaction with actin, clathrin and tubulin. Biochem. J. 363:599-608.
25. Kuge, O., C. Dascher, L. Orci, T. Rowe, M. Amherdt, H. Plutner, M. Ravazzola, G. Tanigawa, J.E. Rothman, and W.E. Balch. 1994. Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments. J. Cell Biol. 125:51-65.
26. Kunjilwar, K., C. Strang, D. DeRubeis, and P.J. Pfaffinger. 2004. kCHIP3 rescues the functional expression of Shal channel tetramerization mutants. J. Biol. Chem. 279:54542-54551.
27. Lanoix, J., J. Ouwendijk, C.-C. Lin, A. Stark, H.D. Love, J. Ostermann, and T. Nilsson. 1999. GTP hydrolysis by arf-1 mediates sorting and concentration of Golgi resident enzymes into functional COP1 vesicles. EMBO J. 18:4935-4948.
28. Liou, W., H.J. Geuze, and J.W. Slot. 1996. Improving structural integrity of cryosections for immunogold labeling. Histochem. Cell Biol. 106:41-58.
29. Ma, D., and L.Y. Jan. 2002. ER transport signals and trafficking of potassium channels and receptors. Curr. Opin. Neurobiol. 12:287-292.
30. + channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J. Neurosci. 15:3840-3851.
31. Mironov, A.A., A.A. Mironov Jr., G.V. Beznoussenko, A. Trucco, P. Lupetti, J.D. Smith, W.J. Geerts, A.J. Koster, K.N. Burger, M.E. Martone, et al. 2003. ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev. Cell. 5:583-594.
32. Morohashi, Y., N. Hatano, S. Ohya, R. Takikawa, T. Watabiki, N. Takasugi, Y. Imaizumi, T. Tomita, and T. Iwatsubo. 2002. Molecular cloning and characterization of CALP/KChIP4, a novel EF-hand protein interacting with presenilin 2 and voltage-gated potassium channel subunit Kv4. J. Biol. Chem. 277:14965-14975.
33. (2+)/myristoyl switch in neuronal calcium sensor-1. J. Biol. Chem. 279:14347-14354.
34. 2+ signal transduction. J. Biol. Chem. 277:14227-14237.
35. + channels. J. Cell Sci. 116:4833-4845.
36. 2+/myristoyl switch protein hippocalcin in living cells. J. Cell Biol. 163:715-721.
37. Oka, T., and A. Nakano. 1994. Inhibition of GTP hydrolysis by Sar1p causes accumulation of vesicles that are a functional intermediate of the ER-to-Golgi transport in yeast. J. Cell Biol. 124:425-434.
38. + channel cloned from mammalian brain. Proc. Natl. Acad. Sci. USA. 88:4386-4390.
39. Pierce, J.P., T. Mayer, and J.B. McCarthy. 2001. Evidence for a satellite secretory pathway in neuronal dendritic spines. Curr. Biol. 11:351-355.
40. Presley, J.F., N.B. Cole, T.A. Schroer, K. Hirschberg, K.J. Zaal, and J. Lippincott-Schwartz. 1997. ER-to-Golgi transport visualized in living cells. Nature. 389:81-85.
41. Rhodes, K.J., K.I. Carroll, M.A. Sung, L.C. Doliveira, M.M. Monaghan, S.L. Burke, B.W. Strassle, L. Buchwalder, M. Menegola, J. Cao, et al. 2004. KChIPs and Kv4α subunits as integral components of A-type potassium channels in mammalian brain. J. Neurosci. 24:7903-7915.
42. Rowe, T., M. Aridor, J.M. McCaffery, H. Plutner, C. Nuoffer, and W.E. Balch. 1996. COPII vesicles derived from mammalian endoplasmic reticulum microsomes recruit COPI. J. Cell Biol. 135:895-911.
43. 2+ ions in dendritic spines. Neuron. 33:439-452.
44. Scannevin, R.H., K. Wang, F. Jow, J. Megules, D.C. Kopsco, W. Edris, K.C. Carroll, Q. Lu, W. Xu, Z. Xu, et al. 2004. Two N-terminal domains of Kv4 K(+) channels regulate binding to and modulation by KChIP1. Neuron. 41:587-598.
45. Serodio, P., C. Kentros, and B. Rudy. 1994. Identification of molecular components of A-type channels activating at subthreshold potentials. J. Neurophysiol. 72:1516-1529.
46. + channel proteins in rat central neurons. Neuron. 9:271-284.
47. Shibasaki, K., K. Nakahira, J.S. Trimmer, R. Shibata, M. Akita, S. Watanabe, and K. Ikenaka. 2004. Mossy fibre contact triggers the targeting of Kv4.2 potassium channels to dendrites and synapses in developing cerebellar granule neurons. J. Neurochem. 89:897-907.
48. Shibata, R., H. Misonou, C.R. Campomanes, A.E. Anderson, L.A. Schrader, L.C. Doliveira, K.I. Carroll, J.D. Sweatt, K.J. Rhodes, and J.S. Trimmer. 2003. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J. Biol. Chem. 278:36445-36454.
49. Spilker, C., and K.H. Braunewell. 2003. Calcium-myristoyl switch, subcellular localization, and calcium-dependent translocation of the neuronal calcium sensor protein VILIP-3, and comparison with VILIP-1 in hippocampal neurons. Mol. Cell. Neurosci. 24:766-778.
50. Stephens, D.J., and R. Pepperkok. 2001. Illuminating the secretory pathway: when do we need vesicles? J. Cell Sci. 114:1053-1059.
51. Stephens, D.J., and R. Pepperkok. 2002. Imaging of procollagen transport reveals COPI-dependent cargo sorting during ER-to-Golgi transport mammalian cells. J. Cell Sci. 115:1149-1160.
52. Stephens, D.J., and R. Pepperkok. 2004. Differential effects of a GTP-restricted mutant of Sar1p on segregation of cargo during export from the endoplasmic reticulum. J. Cell Sci. 117:3635-3644.
53. Stephens, D.J., N. Lin-Marq, A. Pagano, R. Pepperkok, and J.P. Paccaud. 2000. COPI-coated ER-to-Golgi transport complexes segregate from COPII close proximity to ER exit sites. J. Cell Sci. 113:2177-2185.
54. Takimoto, K., E.K. Yang, and L. Conforti. 2002. Palmitoylation of KChIP splicing variants is required for efficient cell surface expression of Kv4.3 channels. J. Biol. Chem. 277:26904-26911.
55. Tanaka, T., J.B. Ames, T.S. Harvey, L. Stryer, and M. Ikura. 1995. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature. 376:444-447.
56. Zhang, C.J., A.G. Rosenwald, M.C. Willingham, S. Skuntz, J. Clark, and R. Kahn. 1994. Expression of a dominant allele of human ARF1 inhibits membrane traffic in vivo. J. Cell Biol. 124:289-300.
57. +) channels. Neuron. 41:573-586.
58. Zozulya, S., and L. Stryer. 1992. Calcium-myristoyl protein switch. Proc. Natl. Acad. Sci. USA. 89:11569-11573.