Molecular determinants of Kv1.3 potassium channels-induced proliferation

Journal of Biological Chemistry

Volumn 291, Issue 7, 2016, Pages 3569-3580

  Jiménez Pérez, Laura ^a   Cidad, Pilar ^a   Álvarez Miguel, Inés ^a   Santos Hipólito, Alba ^a   Torres Merino, Rebeca ^a   Alonso, Esperanza ^a   De La Fuente, Miguel Ángel ^a   López López, José Ramón ^a   Pérez García, Teresa ^a  

^a University of Valladolid   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL PROLIFERATION; ELECTROPHYSIOLOGY; PHOSPHORYLATION; PROTEINS;

ASSOCIATED SIGNALING; CONFORMATIONAL CHANGE; ELECTRO-PHYSIOLOGICAL METHODS; FUNCTIONAL EXPRESSION; MOLECULAR DETERMINANTS; OPEN CONFORMATION; POTASSIUM CHANNELS; PROLIFERATION RATE;

POTASSIUM;

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.5; SMALL INTERFERING RNA; HYBRID PROTEIN; KCNA3 PROTEIN, HUMAN; KCNA5 PROTEIN, HUMAN; MAP2K1 PROTEIN, HUMAN; MAP2K2 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PEPTIDE FRAGMENT; PHOTOPROTEIN; RECOMBINANT PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE POTENTIAL; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CLOSED CONFORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; HEK293 CELL LINE; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; OPEN CONFORMATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; TIME SERIES ANALYSIS; AGONISTS; ANTAGONISTS AND INHIBITORS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

AMINO ACID SUBSTITUTION; CELL PROLIFERATION; HEK293 CELLS; HUMANS; KV1.3 POTASSIUM CHANNEL; KV1.5 POTASSIUM CHANNEL; LUMINESCENT PROTEINS; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MAP KINASE SIGNALING SYSTEM; MUTAGENESIS, INSERTIONAL; PEPTIDE FRAGMENTS; PHOSPHORYLATION; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; RNA INTERFERENCE; TYROSINE;

EID: 84964545704     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.678995     Document Type: Article

References (36)

1. Pardo, L. A. (2004) Voltage-gated potassium channels in cell proliferation. Physiology 19, 285-292.
2. Wulff, H., Castle, N. A., and Pardo, L. A. (2009) Voltage-gated potassium channels as therapeutic targets. Nat. Rev. Drug. Discov. 8, 982-1001.
3. Chandy, K. G., Wulff, H., Beeton, C., Pennington, M., Gutman, G. A., and Cahalan, M. D. (2004) K+ channels as targets for specific immunomodulation. Trends Pharmacol. Sci. 25, 280-289.
4. Coetzee, W. A., Amarillo, Y., Chiu, J., Chow, A., Lau, D., McCormack, T., Moreno, H., Nadal, M. S., Ozaita, A., Pountney, D., Saganich, M., Vega- Saenz de Miera, E., and Rudy, B. (1999) Molecular diversity of K+ channels. Ann. N.Y. Acad. Sci. 868, 233-285.
5. DeCoursey, T. E., Chandy, K. G., Gupta, S., and Cahalan, M. D. (1984) Voltage-gated K+ channels in human lymphocyte-T: A role in mitogenesis. Nature 307, 465-468.
6. Erdogan, A., Schaefer, C. A., Schaefer, M., Luedders, D. W., Stockhausen, F., Abdallah, Y., Schaefer, C., Most, A. K., Tillmanns, H., Piper, H. M., and Kuhlmann, C. R. (2005) Margatoxin inhibits VEGF-induced hyperpolarization, proliferation, and nitric oxide production of human endothelial cells. J. Vasc. Res. 42, 368-376.
7. Miguel-Velado, E., Moreno-Domínguez, A., Colinas, O., Cidad, P., Heras, M., Pérez-García, M. T., and López-López, J. R. (2005) Contribution of Kv channels to phenotypic remodeling of human uterine artery smooth muscle cells. Circ. Res. 97, 1280-1287.
8. Cidad, P., Moreno-Domínguez, A., Novensá, L., Roqué, M., Barquín, L., Heras, M., Pérez-García, M. T., and López-López, J. R. (2010) Characterization of ion channels involved in the proliferative response of femoral artery smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 30, 1203-1211.
9. Beeton, C., Wulff, H., Standifer, N. E., Azam, P., Mullen, K. M., Pennington, M. W., Kolski-Andreaco, A., Wei, E., Grino, A., Counts, D. R., Wang, P. H., LeeHealey, C. J., S Andrews, B., Sankaranarayanan, A., Homerick, D., Roeck, W. W., Tehranzadeh, J., Stanhope, K. L., Zimin, P., Havel, P. J., Griffey, S., Knaus, H. G., Nepom, G. T., Gutman, G. A., Calabresi, P. A., and Chandy, K. G. (2006) Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc. Natl. Acad. Sci. U.S.A. 103, 17414-17419.
10. Kotecha, S. A., and Schlichter, L. C. (1999) Switch in endogenous hippocampal microglia and a role in proliferation. J. Neurosci. 19, 10680-10693.
11. Chittajallu, R., Chen, Y., Wang, H., Yuan, X., Ghiani, C. A., Heckman, T., McBain, C. J., and Gallo, V. (2002) Regulation of Kv1 subunit expression in oligodendrocyte progenitor cells and their role in G1/S phase progression of the cell cycle. Proc. Natl. Acad. Sci. U.S.A. 99, 2350-2355.
12. Villalonga, N., David, M., Bielanska, J., Vicente, R., Comes, N., Valenzuela, C., and Felipe, A. (2010) Immunomodulation of voltage-dependent K+ channels in macrophages: molecular and biophysical consequences. J. Gen. Physiol. 135, 135-147.
13. Cidad, P., Jiménez-Pérez, L., García-Arribas, D., Miguel-Velado, E., Tajada, S., Ruiz-McDavitt, C., López-López, J. R., and Pérez-García, M. T. (2012) Kv1.3 channels can modulate cell proliferation during phenotypic switch by an ion-flux independent mechanism. Arterioscler. Thromb. Vasc. Biol. 32, 1299-1307.
14. Levite, M., Cahalon, L., Peretz, A., Hershkoviz, R., Sobko, A., Ariel, A., Desai, R., Attali, B., and Lider, O. (2000) Extracellular K+ and opening of voltage-gated potassium channels activate T cell integrin function: physical and functional association between Kv1.3 channels and β1 integrins. J. Exp. Med. 191, 1167-1176.
15. Artym, V. V., and Petty, H. R. (2002) Molecular proximity of Kv1.3 voltage- gated potassium channels and β1-integrins on the plasma membrane of melanoma cells: Effects of cell adherence and channel blockers. J. Gen. Physiol. 120, 29-37.
16. Welschoff, J., Matthey, M., and Wenzel, D. (2014) RGD peptides induce relaxation of pulmonary arteries and airways via β3-integrins. FASEB J. 28, 2281-2292.
17. Hu, L., Gocke, A. R., Knapp, E., Rosenzweig, J. M., Grishkan, I. V., Baxi, E. G., Zhang, H., Margolick, J. B., Whartenby, K. A., and Calabresi, P. A. (2012) Functional blockade of the voltage-gated potassium channel Kv1.3 mediates reversion of t effector to central memory lymphocytes through SMAD3/p21cip1 signaling. J. Biol. Chem. 287, 1261-1268.
18. Robbins, J. R., Lee, S. M., Filipovich, A. H., Szigligeti, P., Neumeier, L., Petrovic, M., and Conforti, L. (2005) Hypoxia modulates early events in T cell receptor-mediated activation in human T lymphocytes via Kv1.3 channels. J. Physiol. 564, 131-143.
19. Colley, B. S., Biju, K. C., Visegrady, A., Campbell, S., and Fadool, D. A. (2007) Neurotrophin B receptor kinase increases Kv subfamily member 1.3 (Kv1.3) ion channel half-life and surface expression. Neuroscience 144, 531-546.
20. Lang, F., and Shumilina, E. (2013) Regulation of ion channels by the serum- And glucocorticoid-inducible kinase SGK1. FASEB J. 27, 3-12.
21. Vautier, F., Belachew, S., Chittajallu, R., and Gallo, V. (2004) Shaker-type potassium channel subunits differentially control oligodendrocyte pro-genitor proliferation. Glia 48, 337-345.
22. Cidad, P., Miguel-Velado, E., Ruiz-McDavitt, C., Alonso, E., Jiménez- Pérez, L., Asuaje, A., Carmona, Y., García-Arribas, D., López, J., Marroquín, Y., Fernández, M., Roqué, M., Pérez-García, M. T., and López- López, J. R. (2015) Kv1.3 channels modulate human vascular smooth muscle cells proliferation independently of mTOR signaling pathway. Pflugers Arch. 467, 1711-1722.
23. Hegle, A. P., Marble, D. D., and Wilson, G. F. (2006) A voltage-driven switch for ion-independent signaling by ether-a-go-go K+ channels. Proc. Natl. Acad. Sci. U.S.A. 103, 2886-2891.
24. Millership, J. E., Devor, D. C., Hamilton, K. L., Balut, C. M., Bruce, J. I., and Fearon, I. M. (2011) Calcium-activated K+ channels increase cell proliferation independent of K+ conductance. Am. J. Physiol. Cell Physiol. 300, C792-C802.
25. Uebele, V. N., England, S. K., Chaudhary, A., Tamkun, M. M., and Snyders, D. J. (1996) Functional differences in Kv1.5 currents expressed in mammalian cell lines are due to the presence of endogenous Kv - 2.1 subunits. J. Biol. Chem. 271, 2406-2412.
26. McCormack, T., McCormack, K., Nadal, M. S., Vieira, E., Ozaita, A., and Rudy, B. (1999) The effects of Shaker β-subunits on the human lymphocyte K+ channel Kv1.3. J. Biol. Chem. 274, 20123-20126.
27. Bowlby, M. R., Fadool, D. A., Holmes, T. C., and Levitan, I. B. (1997) Modulation of the Kv1, 3 potassium channel by receptor tyrosine kinases. J. Gen. Physiol. 110, 601-610.
28. Martínez-Mármol, R., Pérez-Verdaguer, M., Roig, S. R., Vallejo-Gracia, A., Gotsi, P., Serrano-Albarrás, A., Bahamonde, M. I., Ferrer-Montiel, A., Fernández-Ballester, G., Comes, N., and Felipe, A. (2013)Anon-canonical di-acidic signal at the C-terminus of Kv1.3 determines anterograde trafficking and surface expression. J. Cell Sci. 126, 5681-5691.
29. Hoshi, T., Zagotta, W. N., and Aldrich, R. W. (1990) Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250, 533-538.
30. Barros, F., Domínguez, P., and de la Peña, P. (2012) Cytoplasmic domains and voltage-dependent potassium channel gating. Front. Pharmacol. 3, 49.
31. Becchetti, A. (2011) Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer. Am. J. Physiol. Cell Physiol. 301, C255-C265.
32. Urrego, D., Tomczak, A. P., Zahed, F., Stühmer, W., and Pardo, L. A. (2014) Potassium channels in cell cycle and cell proliferation. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369, 20130094.
33. Lee, A., Fakler, B., Kaczmarek, L. K., and Isom, L. L. (2014) More than a pore: ion channel signaling complexes. J. Neurosci. 34, 15159-15169.
34. Kaczmarek, L. K. (2006) Non-conducting functions of voltage-gated ion channels. Nat. Rev. Neurosci. 7, 761-771.
35. Fadool, D. A., Tucker, K., Perkins, R., Fasciani, G., Thompson, R. N., Parsons, A. D., Overton, J. M., Koni, P. A., Flavell, R. A., and Kaczmarek, L. K. (2004) Kv1.3 channel gene-targeted deletion produces "Super-Smeller Mice" with altered glomeruli, interacting scaffolding proteins, and biophysics. Neuron 41, 389-404.
36. Hajdu, P., Martin, G. V., Chimote, A. A., Szilagyi, O., Takimoto, K., and Conforti, L. (2015) The C terminus SH3-binding domain of Kv1.3 is required for the actin-mediated immobilization of the channel via cortactin. Mol. Biol. Cell 26, 1640-1651.