A non-canonical di-acidic signal at the C-terminus of Kv1.3 determines anterograde trafficking and surface expression

Journal of Cell Science

Volumn 126, Issue 24, 2013, Pages 5681-5691

  Marti'nez Mármol, Ramón ^a   Pérez Verdaguer, Mireia ^a   Roig, Sara R ^a   Vallejo Gracia, Albert ^a   Gotsi, Pelagia ^a   Serrano Albarrás, Antonio ^a   Bahamonde, María Isabel ^b   Ferrer Montiel, Antonio ^c   Fernández Ballester, Gregorio ^c   Comes, Núria ^a   Felipe, Antonio ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^c MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

Forward traffic motifs; Lymphocytes; Neurons; Plasma membrane; Voltage dependent K+ channels

Indexed keywords

COAT PROTEIN COMPLEX II; POTASSIUM CHANNEL KV1.3; SHAKER POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CHEMICAL ANALYSIS; CONFOCAL MICROSCOPY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RAT; SECRETORY PATHWAY; SURFACE PROPERTY;

FORWARD-TRAFFIC MOTIFS; LYMPHOCYTES; NEURONS; PLASMA MEMBRANE; VOLTAGE-DEPENDENT K+ CHANNELS;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ANIMALS; CELL MEMBRANE; COATOMER PROTEIN; HEK293 CELLS; HUMANS; KV1.3 POTASSIUM CHANNEL; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RATS; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS;

EID: 84890536081     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.134825     Document Type: Article

References (54)

1. Biervert, C., Schroeder, B. C., Kubisch, C., Berkovic, S. F., Propping, P., Jentsch, T. J. and Steinlein, O. K. (1998). A potassium channel mutation in neonatal human epilepsy. Science 279, 403-406.
2. Cahalan, M. D. and Chandy, K. G. (2009). The functional network of ion channels in T lymphocytes. Immunol. Rev. 231, 59-87.
3. Cavallin, M. A., Powell, K., Biju, K. C. and Fadool, D. A. (2010). State-dependent sculpting of olfactory sensory neurons is attributed to sensory enrichment, odor deprivation, and aging. Neurosci. Lett. 483, 90-95.
4. Conforti, L. (2012). The ion channel network in T lymphocytes, a target for immunotherapy. Clin. Immunol. 142, 105-106.
5. Curran, M. E., Splawski, I., Timothy, K. W., Vincent, G. M., Green, E. D. and Keating, M. T. (1995). A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell 80, 795-803.
6. Delisle, B. P., Underkofler, H. A., Moungey, B. M., Slind, J. K., Kilby, J. A., Best, J. M., Foell, J. D., Balijepalli, R. C., Kamp, T. J. and January, C. T. (2009). Small GTPase determinants for the Golgi processing and plasmalemmal expression of human ether-a-go-go related (hERG) K+ channels. J. Biol. Chem. 284, 2844-2853.
7. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T. et al. (2003). A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24, 1999-2012.
8. Farhan, H., Reiterer, V., Kriz, A., Hauri, H. P., Pavelka, M., Sitte, H. H. and Freissmuth, M. (2008). Signal-dependent export of GABA transporter 1 from the ER-Golgi intermediate compartment is specified by a C-terminal motif. J. Cell Sci. 121, 753-761.
9. Gazula, V. R., Strumbos, J. G., Mei, X., Chen, H., Rahner, C. and Kaczmarek, L. K. (2010). Localization of Kv1.3 channels in presynaptic terminals of brainstem auditory neurons. J. Comp. Neurol. 518, 3205-3220.
10. Guerois, R., Nielsen, J. E. and Serrano, L. (2002). Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J. Mol. Biol. 320, 369-387.
11. Guex, N. and Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723.
12. Hasdemir, B., Fitzgerald, D. J., Prior, I. A., Tepikin, A. V. and Burgoyne, R. D. (2005). Traffic of Kv4 K+ channels mediated by KChIP1 is via a novel post-ER vesicular pathway. J. Cell Biol. 171, 459-469.
13. Hille, B. (2001). Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer.
14. Hoshi, T., Zagotta, W. N. and Aldrich, R. W. (1990). Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250, 533-538.
15. Kartner, N., Augustinas, O., Jensen, T. J., Naismith, A. L. and Riordan, J. R. (1992). Mislocalization of delta F508 CFTR in cystic fibrosis sweat gland. Nat. Genet. 1, 321- 327.
16. Koeberle, P. D. and Schlichter, L. C. (2010). Targeting K(V) channels rescues retinal ganglion cells in vivo directly and by reducing inflammation. Channels (Austin) 4, 337-346.
17. Krieger, E., Koraimann, G. and Vriend, G. (2002). Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Proteins 47, 393-402.
18. Lai, H. C. and Jan, L. Y. (2006). The distribution and targeting of neuronal voltagegated ion channels. Nat. Rev. Neurosci. 7, 548-562.
19. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996). AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486.
20. Li, D., Takimoto, K. and Levitan, E. S. (2000). Surface expression of Kv1 channels is governed by a C-terminal motif. J. Biol. Chem. 275, 11597-11602.
21. Ma, D., Zerangue, N., Raab-Graham, K., Fried, S. R., Jan, Y. N. and Jan, L. Y. (2002). Diverse trafficking patterns due to multiple traffic motifs in G proteinactivated inwardly rectifying potassium channels from brain and heart. Neuron 33, 715-729.
22. Mancias, J. D. and Goldberg, J. (2008). Structural basis of cargo membrane protein discrimination by the human COPII coat machinery. EMBO J. 27, 2918-2928.
23. Manganas, L. N. and Trimmer, J. S. (2000). Subunit composition determines Kv1 potassium channel surface expression. J. Biol. Chem. 275, 29685-29693.
24. Manganas, L. N., Akhtar, S., Antonucci, D. E., Campomanes, C. R., Dolly, J. O. and Trimmer, J. S. (2001a). Episodic ataxia type-1 mutations in the Kv1.1 potassium channel display distinct folding and intracellular trafficking properties. J. Biol. Chem. 276, 49427-49434.
25. Manganas, L. N., Wang, Q., Scannevin, R. H., Antonucci, D. E., Rhodes, K. J. and Trimmer, J. S. (2001b). Identification of a trafficking determinant localized to the Kv1 potassium channel pore. Proc. Natl. Acad. Sci. USA 98, 14055-14059.
26. Marks, D. R., Tucker, K., Cavallin, M. A., Mast, T. G. and Fadool, D. A. (2009). Awake intranasal insulin delivery modifies protein complexes and alters memory, anxiety, and olfactory behaviors. J. Neurosci. 29, 6734-6751.
27. Misonou, H. and Trimmer, J. S. (2004). Determinants of voltage-gated potassium channel surface expression and localization in Mammalian neurons. Crit. Rev. Biochem. Mol. Biol. 39, 125-145.
28. Morris, G. M., Huey, R. and Olson, A. J. (2008). Using AutoDock for ligand-receptor docking. Curr. Protoc. Bioinformatics 24, 8.14.1-8.14.40.
29. Neyroud, N., Tesson, F., Denjoy, I., Leibovici, M., Donger, C., Barhanin, J., Fauré, S., Gary, F., Coumel, P., Petit, C. et al. (1997). A novel mutation in the potassium channel gene KVLQT1 causes the Jervell and Lange-Nielsen cardioauditory syndrome. Nat. Genet. 15, 186-189.
30. Nicolaou, S. A., Szigligeti, P., Neumeier, L., Lee, S. M., Duncan, H. J., Kant, S. K., Mongey, A. B., Filipovich, A. H. and Conforti, L. (2007). Altered dynamics of Kv1.3 channel compartmentalization in the immunological synapse in systemic lupus erythematosus. J. Immunol. 179, 346-356.
31. Nishimura, N. and Balch, W. E. (1997). A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277, 556-558.
32. Panyi, G., Vámosi, G., Bacsó, Z., Bagdány, M., Bodnár, A., Varga, Z., Gáspár, R., Mátyus, L. and Damjanovich, S. (2004). Kv1.3 potassium channels are localized in the immunological synapse formed between cytotoxic and target cells. Proc. Natl. Acad. Sci. USA 101, 1285-1290.
33. Rea, R., Spauschus, A., Eunson, L. H., Hanna, M. G. and Kullmann, D. M. (2002). Variable K(+) channel subunit dysfunction in inherited mutations of KCNA1. J. Physiol. 538, 5-23.
34. Rivera, J. F., Chu, P. J. and Arnold, D. B. (2005). The T1 domain of Kv1.3 mediates intracellular targeting to axons. Eur. J. Neurosci. 22, 1853-1862.
35. Schwede, T., Kopp, J., Guex, N. and Peitsch, M. C. (2003). SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385.
36. Schwegmann-Wessels, C., Al-Falah, M., Escors, D., Wang, Z., Zimmer, G., Deng, H., Enjuanes, L., Naim, H. Y. and Herrler, G. (2004). A novel sorting signal for intracellular localization is present in the S protein of a porcine coronavirus but absent from severe acute respiratory syndrome-associated coronavirus. J. Biol. Chem. 279, 43661-43666.
37. Schymkowitz, J., Borg, J., Stricher, F., Nys, R., Rousseau, F. and Serrano, L. (2005). The FoldX web server: an online force field. Nucleic Acids Res. 33, W382-W388.
38. Sevier, C. S., Weisz, O. A., Davis, M. and Machamer, C. E. (2000). Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol. Biol. Cell 11, 13-22.
39. Sivaprasadarao, A., Taneja, T. K., Mankouri, J. and Smith, A. J. (2007). Trafficking of ATP-sensitive potassium channels in health and disease. Biochem. Soc. Trans. 35, 1055-1059.
40. Sokolova, O., Kolmakova-Partensky, L. and Grigorieff, N. (2001). Threedimensional structure of a voltage-gated potassium channel at 2.5 nm resolution. Structure 9, 215-220.
41. Sokolova, O., Accardi, A., Gutierrez, D., Lau, A., Rigney, M. and Grigorieff, N. (2003). Conformational changes in the C terminus of Shaker K+ channel bound to the rat Kvbeta2-subunit. Proc. Natl. Acad. Sci. USA 100, 12607-12612.
42. Steele, D. F., Zadeh, A. D., Loewen, M. E. and Fedida, D. (2007). Localization and trafficking of cardiac voltage-gated potassium channels. Biochem. Soc. Trans. 35, 1069-1073.
43. Taneja, T. K., Mankouri, J., Karnik, R., Kannan, S., Smith, A. J., Munsey, T., Christesen, H. B., Beech, D. J. and Sivaprasadarao, A. (2009). Sar1-GTPasedependent ER exit of KATP channels revealed by a mutation causing congenital hyperinsulinism. Hum. Mol. Genet. 18, 2400-2413.
44. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
45. Tóth, A., Szilágyi, O., Krasznai, Z., Panyi, G. and Hajdú, P. (2009). Functional consequences of Kv1.3 ion channel rearrangement into the immunological synapse. Immunol. Lett. 125, 15-21.
46. Tsigelny, I., Hotchko, M., Yuan, J. X. and Keller, S. H. (2005). Identification of molecular determinants that modulate trafficking of DeltaF508 CFTR, the mutant ABC transporter associated with cystic fibrosis. Cell Biochem. Biophys. 42, 41-53.
47. Vicente, R., Escalada, A., Coma, M., Fuster, G., Sánchez-Tilló, E., López-Iglesias, C., Soler, C., Solsona, C., Celada, A. and Felipe, A. (2003). Differential voltagedependent K+ channel responses during proliferation and activation in macrophages. J. Biol. Chem. 278, 46307-46320.
48. Vicente, R., Villalonga, N., Calvo, M., Escalada, A., Solsona, C., Soler, C., Tamkun, M. M. and Felipe, A. (2008). Kv1.5 association modifies Kv1.3 traffic and membrane localization. J. Biol. Chem. 283, 8756-8764.
49. Villalonga, N., David, M., Bielańska, J., González, T., Parra, D., Soler, C., Comes, N., Valenzuela, C. and Felipe, A. (2010). Immunomodulatory effects of diclofenac in leukocytes through the targeting of Kv1.3 voltage-dependent potassium channels. Biochem. Pharmacol. 80, 858-866.
50. Wang, X., Matteson, J., An, Y., Moyer, B., Yoo, J. S., Bannykh, S., Wilson, I. A., Riordan, J. R. and Balch, W. E. (2004). COPII-dependent export of cystic fibrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J. Cell Biol. 167, 65-74.
51. Ward, T. H., Polishchuk, R. S., Caplan, S., Hirschberg, K. and Lippincott-Schwartz, J. (2001). Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557-570.
52. Zanetti, G., Pahuja, K. B., Studer, S., Shim, S. and Schekman, R. (2012). COPII and the regulation of protein sorting in mammals. Nat. Cell Biol. 14, 20-28.
53. Zhu, J., Watanabe, I., Gomez, B. and Thornhill, W. B. (2001). Determinants involved in Kv1 potassium channel folding in the endoplasmic reticulum, glycosylation in the Golgi, and cell surface expression. J. Biol. Chem. 276, 39419-39427.
54. Zhu, J., Watanabe, I., Gomez, B. and Thornhill, W. B. (2003). Trafficking of Kv1.4 potassium channels: interdependence of a pore region determinant and a cytoplasmic C-terminal VXXSL determinant in regulating cell-surface trafficking. Biochem. J. 375, 761-768.