Kv1.5 in the immune system: The good, the bad, or the ugly?

Frontiers in Physiology

Volumn 1 NOV, Issue , 2010, Pages

  Felipe, Antonio ^a   Soler, Concepció ^a   Comes, Núria ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Association; Channelosome; Heterotetramers; Leukocytes; Potassium channels

Indexed keywords

EID: 84857709781     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2010.00152     Document Type: Article

References (96)

1. Abi-Char, J., El-Haou, S., Balse, E., Neyroud, N., Vranckx, R., Coulombe, A., and Hatem, S. N. (2008). The anchoring protein SAP97 retains Kv1.5 channels in the plasma membrane of cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 294, H1851-H1861.
2. Agarwal, J. R., Griesinger, F., Stühmer, W., and Pardo, L. A. (2010). The potassium channel Ether à go-go is a novel prognostic factor with functional relevance in acute myeloid leukemia. Mol. Cancer 9, 18.
3. Ashcroft, F. M. (2000). Ion Channels and Disease: Channelopathies. San Diego: Academic Press.
4. + channels in human T lymphocytes. J. Biol. Chem. 267, 8650-8657.
5. Autieri, M. V., Belkowski, S. M., Constantinescu, C. S., Cohen, J. A., and Prystowsky, M. B. (1997). Lymphocyte-specific inducible expression of potassium channel beta subunits. J. Neuroimmunol. 77, 8-16.
6. Beeton, C., and Chandy, K. G. (2005). Potassium channels, memory T cells, and multiple sclerosis. Neuroscientist 11, 550-562.
7. Bielanska, J., Hernandez-Losa, J., Perez-Verdaguer, M., Moline, T., Somoza, R., Ramon, Y. C. S., Condom, E., Ferreres, J. C., and Felipe, A. (2009). Voltage-dependent potassium channels Kv1.3 and Kv1.5 in human cancer. Curr. Cancer Drug Targets 9, 904-914.
8. Cahalan, M. D., and Chandy, K. G. (1997). Ion channels in the immune system as targets for immunosuppression. Curr. Opin. Biotechnol. 8, 749-756.
9. Cahalan, M. D., and Chandy, K. G. (2009). The functional network of ion channels in T lymphocytes. Immunol. Rev. 231, 59-87.
10. Cahalan, M. D., Chandy, K. G., DeCoursey, T. E., and Gupta, S. (1985) A voltagegated potassium channel in human T lymphocytes. J. Physiol. 358, 197-237.
11. Cayabyab, F. S., Khanna, R., Jones, O. T., and Schlichter, L. C. (2000). Suppression of the rat microglia Kv1.3 current by src-family tyrosine kinases and oxygen/glucose deprivation. Eur. J. Neurosci. 12, 1949-1960.
12. + channels in rat microglia. Neurosci. Lett. 300, 67-70.
13. Decoursey, T. E., Chandy, K. G., Gupta, S., and Cahalan, M. D. (1987). Two types of potassium channels in murine T lymphocytes. J. Gen. Physiol. 89, 379-404.
14. + channels. J. Biol. Chem. 279, 394-400.
15. Du, Y. M., Zhang, X. X., Tu, D. N., Zhao, N., Liu, Y. J., Xiao, H., Sanguinetti, M. C., Zou, A., and Liao, Y. H. (2010). Molecular determinants of Kv1.5 channel block by diphenyl phosphine oxide-1. J. Mol. Cell Cardiol. 48, 1111-1120.
16. Eder, C. (1998). Ion channels in microglia (brain macrophages). Am. J. Physiol. 275, C327-C342.
17. + currents of bone marrow-derived macro-phages. Naunyn Schmiedebergs Arch. Pharmacol. 355, 198-202.
18. Eder, C., Fischer, H. G., Hadding, U., and Heinemann, U. (1995). Properties of voltage-gated currents of microglia developed using macrophage colony-stimulating factor. Pflugers Arch. 430, 526-533.
19. Eldstrom, J., Choi, W. S., Steele, D. F., and Fedida, D. (2003). SAP97 increases Kv1.5 currents through an indirect N-terminal mechanism. FEBS Lett. 547, 205-211.
20. Eldstrom, J., Van Wagoner, D. R., Moore, E. D., and Fedida, D. (2006). Localization of Kv1.5 channels in rat and canine myocyte sarcolemma. FEBS Lett. 580, 6039-6046.
21. + currents of mouse dendritic cells. FEBS Lett. 373, 127-130.
22. + uptake, and cell volume. Am. J. Physiol. 265, C1230-C1238.
23. Folco, E. J., Liu, G. X., and Koren, G. (2004). Caveolin-3 and SAP97 form a scaffolding protein complex that regulates the voltage-gated potassium channel Kv1.5. Am. J. Physiol. Heart Circ. Physiol. 287, H681-H690.
24. Fordyce, C. B., Jagasia, R., Zhu, X., and Schlichter, L. C. (2005). Microglia Kv1.3 channels contribute to their ability to kill neurons. J. Neurosci. 25, 7139-7149.
25. Freedman, B. D., Price, M. A., and Deutsch, C. J. (1992). Evidence for voltage modulation of IL-2 production in mitogen-stimulated human peripheral blood lymphocytes. J. Immunol. 149, 3784-3794.
26. Gallin, E. K. (1981). Voltage clamp studies in macrophages from mouse spleen cultures. Science 214, 458-460.
27. Gallin, E. K. (1984). Electrophysiological properties of macrophages. Fed. Proc. 43, 2385-2389.
28. Gallin, E. K., and Gallin, J. I. (1977). Interaction of chemotactic factors with human macrophages. Induction of transmembrane potential changes. J. Cell Biol. 75, 277-289.
29. Gallin, E. K., and Livengood, D. R. (1980). Nonlinear current-voltage relationships in cultured macrophages. J. Cell Biol. 85, 160-165.
30. Gallin, E. K., Wiederhold, M. L., Lipsky, P. E., and Rosenthal, A. S. (1975). Spontaneous and induced membrane hyperpolarizations in macrophages. J. Cell. Physiol. 86(Suppl. 2), 653-661.
31. + channel in T cells. J. Biol. Chem. 267, 20971-20979.
32. + channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 45, 1227-1234.
33. Gutman, G. A., Chandy, K. G., Grissmer, S., Lazdunski, M., McKinnon, D., Pardo, L. A., Robertson, G. A., Rudy, B., Sanguinetti, M. C., Stuhmer, W., and Wang, X. (2005). International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol. Rev. 57, 473-508.
34. Hille, B. (2001). Ion Channels of Excitable Membranes, 3rd Edn. Sunderland, MA: Sinauer.
35. + channels in activated microglia in vivo. Glia 24, 408-414.
36. Judge, S. I., Lee, J. M., Bever, C. T. Jr., and Hoffman, P. M. (2006). Voltage-gated potassium channels in multiple sclerosis: Overview and new implications for treatment of central nervous system inflammation and degeneration. J. Rehabil. Res. Dev. 43, 111-122.
37. Jurkat-Rott, K., Lerche, H., and Lehmann-Horn, F. (2002). Hereditary channelopathies in neurology. J. Neurol. 249, 1493-1502.
38. Jurkat-Rott, K., Lerche, H., Weber, Y., and Lehmann-Horn, F. (2010). Hereditary channelopathies in neurology. Adv. Exp. Med. Biol. 686, 305-334
39. + channels and the microglial respiratory burst. Am. J. Physiol., Cell Physiol. 280, C796-C806.
40. Kim, S. Y., Silver, M. R., and DeCoursey, T. E. (1996). Ion channels in human THP-1 monocytes. J. Membr. Biol. 152, 117-130.
41. Koni, P. A., Khanna, R., Chang, M. C., Tang, M. D., Kaczmarek, L. K., Schlichter, L. C., and Flavella, R. A. (2003). Compensatory anion currents in Kv1.3 channel-deficient thymocytes. J. Biol. Chem. 278, 39443-39451.
42. Kotecha, S. A., and Schlichter, L. C. (1999). A Kv1.5 to Kv1.3 switch in endogenous hippocampal microglia and a role in proliferation. J. Neurosci. 19, 10680-10693.
43. Krummel, M. F., and Cahalan, M. D. (2010). The immunological synapse: a dynamic platform for local signaling. J. Clin. Immunol. 30, 364-372.
44. Lehmann-Horn, F., and Jurkat-Rott K. (1999). Voltage-gated ion channels and hereditary disease. Physiol. Rev. 79, 1317-1372.
45. + channels. J. Mol. Cell Cardiol. 39, 121-132.
46. + lymphocyte differentiation. J. Exp. Med. 196, 897-909.
47. Mackenzie, A. B., Chirakkal, H., and North, R. A. (2003). Kv1.3 potassium channels in human alveolar macrophages. Am. J. Physiol. Lung Cell Mol. Physiol. 285, L862-L868.
48. Martens, J. R., Kwak, Y. G., and Tamkun, M. M. (1999). Modulation of Kv channel alpha/beta subunit interactions. Trends Cardiovasc. Med. 9, 253-258.
49. + channels to distinct lipid raft populations. Targeting of Kv1.5 to caveolae. J. Biol. Chem. 276, 8409-8414.
50. Martinez-Marmol, R., Villalonga, N., Sole, L., Vicente, R., Tamkun, M. M., Soler, C., and Felipe, A. (2008). Multiple Kv1.5 targeting to membrane surface microdomains. J. Cell Physiol. 217, 667-673.
51. Matzner, N., Zemtsova, I. M., Nguyen, T. X., Duszenko, M., Shumilina, E., and Lang, F. (2008). Ion channels modulating mouse dendritic cell functions. J. Immunol. 181, 6803-6809.
52. McEwen, D. P., Li, Q., Jackson, S., Jenkins, P. M., and Martens, J. R. (2008). Caveolin regulates kv1.5 trafficking to cholesterol-rich membrane microdomains. Mol. Pharmacol. 73, 678-685.
53. Mello de Queiroz, F., Ponte, C. G., Bonomo, A., Vianna-Jorge, R., and Suarez-Kurtz, G. (2008). Study of membrane potential in T lymphocytes subpopulations using flow cytometry. BMC Immunol. 9, 63. doi: 10.1186/1471-2172-9-63.
54. Menteyne, A., Levavasseur, F., Audinat, E., and Avignone, E. (2009). Predominant functional expression of Kv1.3 by activated microglia of the hippocampus after Status epilepticus. PLoS One. 4, e6770. doi: 10.1371/journal.pone.0006770.
55. Mullen, K. M., Rozycka, M., Rus, H., Hu, L., Cudrici, C., Zafranskaia, E., Pennington, M. W., Johns, D. C., Judge, S. I., and Calabresi, P. A. (2006). Potassium channels Kv1.3 and Kv1.5 are expressed on blood-derived dendritic cells in the central nervous system. Ann. Neurol. 60, 118-127.
56. Murata, M., Buckett, P. D., Zhou, J., Brunner, M., Folco, E., and Koren, G. (2001). SAP97 interacts with Kv1.5 in heterologous expression systems. Am. J. Physiol. Heart Circ. Physiol. 281, H2575-H2584.
57. Nelson, D. J., Jow, B., and Jow, F. (1992). Lipopolysaccharide induction of outward potassium current expression in human monocyte-derived macro-phages: lack of correlation with secretion. J. Membr. Biol. 125, 207-218.
58. Nelson, D. J., Jow, B., and Popovich, K. J. (1990) Whole-cell currents in macrophages: II. Alveolar macrophages. J. Membr. Biol. 117, 45-55.
59. 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.
60. Pannasch, U., Farber, K., Nolte, C., Blonski, M., Yan Chiu, S., Messing, A., and Kettenmann, H. (2006). The potassium channels Kv1.5 and Kv1.3 modulate distinct functions of microglia. Mol. Cell. Neurosci. 33, 401-411.
61. Panyi, G., Bagdany, M., Bodnar, A., Vamosi, G., Szentesi, G., Jenei, A., Matyus, L., Varga, S., Waldmann, T. A., Gaspar, R., and Damjanovich, S. (2003). Colocalization and nonrandom distribution of Kv1.3 potassium channels and CD3 molecules in the plasma membrane of human T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 100, 2592-2597.
62. Panyi, G., Vamosi, G., Bacso, Z., Bagdany, M., Bodnar, A., Varga, Z., Gaspar, R., Matyus, 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. U.S.A. 101, 1285-1290.
63. Panyi, G., Varga, Z., and Gaspar, R. (2004). Ion channels and lymphocyte activation. Immunol. Lett. 92, 55-66.
64. Park, S. A., Lee, Y. C., Ma, T. Z., Park, J. A., Han, M. K., Lee, H. H., Kim, H. G., and Kwak, Y. G. (2006). hKv1.5 channels play a pivotal role in the functions of human alveolar macrophages. Biochem. Biophys. Res. Commun. 346, 567-571.
65. Pillozzi, S., Brizzi, M. F., Balzi, M., Crociani, O., Cherubini, A., Guasti, L., Bartolozzi, B., Becchetti, A., Wanke, E., Bernabei, P. A., Olivotto, M., Pegoraro, L., and Arcangeli, A. (2002). HERG potassium channels are constitutively expressed in primary human acute myeloid leukemias and regulate cell proliferation of normal and leukemic hemopoietic progenitors. Leukemia 16, 1791-1798.
66. Pottosin, II, Valencia-Cruz, G., Bonales-Alatorre, E., Shabala, S. N., and Dobrovinskaya, O. R. (2007). Methyl-beta-cyclodextrin reversibly alters the gating of lipid rafts-associated Kv1.3 channels in Jurkat T lymphocytes. Pflugers Arch. 454, 235-244.
67. + channels induced by lipopolysaccharide in microglia. Mol. Cells 7, 610-614.
68. Rangaraju, S., Chi, V., Pennington, M. W., and Chandy, K. G. (2009). Kv1.3 potassium channels as a therapeutic target in multiple sclerosis. Expert Opin. Ther. Targets. 13, 909-924.
69. Rink, T. J., Montecucco, C., Hesketh, T. R., and Tsien, R. Y. (1980). Lymphocyte membrane potential assessed with fluorescent probes. Biochim. Biophys. Acta 595, 15-30.
70. Roden, D. M., Balser, J. R., George, A. L., Jr., and Anderson, M. E. (2002). Cardiac ion channels. Annu. Rev. Physiol. 64, 431-475.
71. Roepke, T. K., Kontogeorgis, A., Ovanez, C., Xu, X., Young, J. B., Purtell, K., Goldstein, P. A., Christini, D. J., Peters, N. S., Akar, F. G., Gutstein, D. E., Lerner, D. J., and Abbott, G. W. (2008). Targeted deletion of kcne2 impairs ventricular repolarization via disruption of I (K,slow1) and I (to,f). FASEB J. 22, 3648-3660.
72. Sanguinetti, M. C., and Tristani-Firouzi, M. (2006). hERG potassium channels and cardiac arrhythmia. Nature 440, 463-469.
73. Schilling, T., Quandt, F. N., Cherny, V. V., Zhou, W., Heinemann, U., Decoursey, T. E., and Eder, C. (2000). Upregulation of Kv1.3 K(+) channels in microglia deactivated by TGF-beta. Am. J. Physiol. Cell Physiol. 279, C1123-C1134.
74. 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.
75. + channels in neoplastic hematopoietic cells. J. Biol. Chem. 277, 18528-18534.
76. Sole, L., and Felipe, A. (2010). Does a physiological role for KCNE subunits exist in the immune system? Commun. Integr. Biol. 3, 166-168.
77. Sole, L., Roura-Ferrer, M., Perez-Verdaguer, M., Oliveras, A., Calvo, M., Fernandez-Fernandez, J. M., and Felipe, A. (2009). KCNE4 suppresses Kv1.3 currents by modulating trafficking, surface expression and channel gating. J. Cell Sci. 122, 3738-3748.
78. Stuhmer, W., Ruppersberg, J. P., Schroter, K. H., Sakmann, B., Stocker, M., Giese, K. P., Perschke, A., Baumann, A., and Pongs, O. (1989). Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J. 8, 3235-3244.
79. Swanson, R., Marshall, J., Smith, J. S., Williams, J. B., Boyle, M. B., Folander, K., Luneau, C. J., Antanavage, J., Oliva, C., Buhrow, S. A., Bennet, C., Stein, R. B., and Kaczmarek, L. K. (1990). Cloning and expression of cDNA and genomic clones encoding three delayed rectifier potassium channels in rat brain. Neuron 4, 929-939.
80. Toth, A., Szilagyi, O., Krasznai, Z., Panyi, G., and Hajdu, P. (2009). Functional consequences of Kv1.3 ion channel rearrangement into the immunological synapse. Immunol. Lett. 125, 15-21.
81. Vacher, H., Mohapatra, D. P., and Trimmer, J. S. (2008). Localization and targeting of voltage-dependent ion channels in mammalian central neurons. Physiol. Rev. 88, 1407-1447.
82. Varga, Z., Hajdu, P., and Panyi, G. (2010). Ion channels in T lymphocytes: an update on facts, mechanisms and therapeutic targeting in autoimmune diseases. Immunol. Lett. 130, 19-25.
83. Vennekamp, J., Wulff, H., Beeton, C., Calabresi, P. A., Grissmer, S., Hansel, W., and Chandy, K. G. (2004). Kv1.3-blocking 5-phenylalkoxypsoralens: a new class of immunomodulators. Mol. Pharmacol. 65, 1364-1374.
84. + channels. J. Physiol. (Lond.) 503, 317-331.
85. + channel responses during proliferation and activation in macrophages. J. Biol. Chem. 278, 46307-46320.
86. Vicente, R., Escalada, A., Soler, C., Grande, M., Celada, A., Tamkun, M. M., Solsona, C., and Felipe, A. (2005a). Pattern of Kv beta subunit expression in macrophages depends upon proliferation and the mode of activation. J. Immunol. 174, 4736-4744.
87. + current in macrophages? J. Physiol. Biochem. 61, 61-62.
88. + channel in macrophages. J. Biol. Chem. 281, 37675-37685.
89. 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.
90. + channels in macrophages: molecular and biophysical consequences. J. Gen Physiol. 135, 135-147.
91. Villalonga, N., David, M., Bielańska, J., González, T., Parra, D., Soler, C., Comes, N., Valenzuela, C., and Felipe, A. (2010b). Immunomodulatory effects of diclofenac in leukocytes through the targeting of Kv1.3 voltage-dependent potassium channels. Biochem. Pharmacol. 80, 858-866.
92. Villalonga, N., Escalada, A., Vicente, R., Sanchez-Tillo, E., Celada, A., Solsona, C., and Felipe, A. (2007). Kv1.3/Kv1.5 heteromeric channels compromise pharmacological responses in macrophages. Biochem. Biophys. Res. Commun. 352, 913-918.
93. Villalonga, N., Martinez-Marmol, R., Roura-Ferrer, M., David, M., Valenzuela, C., Soler, C., and Felipe, A. (2008). Cell cycle-dependent expression of Kv1.5 is involved in myoblast proliferation. Biochim. Biophys. Acta. 1783, 728-736.
94. 2+-dependent functions in peptidog-lycan-stimulated mouse dendritic cells. Cell. Physiol. Biochem. 24, 167-176.
95. + conductance in cultured mouse peritoneal macrophages. Proc. Natl. Acad. Sci. U.S.A. 81, 3083-3087.
96. Zsiros, E., Kis-Toth, K., Hajdu, P., Gaspar, R., Bielanska, J., Felipe, A., Rajnavolgyi, E., and Panyi, G. (2009). Developmental switch of the expression of ion channels in human dendritic cells. J. Immunol. 183, 4483-4492.