Induction of apoptosis in macrophages via Kv1.3 and Kv1.5 potassium channels

Current Medicinal Chemistry

Volumn 19, Issue 31, 2012, Pages 5394-5404

  Leanza, L ^a   Zoratti, M ^a   Gulbins, E ^b   Szabo I ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Apoptosis; Ion channels; Kv1.3 inhibitors; Kv1.5 potassium channel; Macrophage; Mitochondria

Indexed keywords

5 (4 PHENOXYBUTOXY)PSORALEN; 5 (4 PHENYLBUTOXY)PSORALEN; CHARYBDOTOXIN; CLOFAZIMINE; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.5; PROTEIN BAK; PROTEIN BAX; SCORPION VENOM; SMALL INTERFERING RNA; STICHODACTYLA TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSFECTION; IMMUNE SYSTEM; LYMPHOCYTE; MACROPHAGE; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; ENZYME INHIBITORS; KV1.3 POTASSIUM CHANNEL; KV1.5 POTASSIUM CHANNEL; MACROPHAGES; MICE; MITOCHONDRIA; RNA INTERFERENCE; RNA, SMALL INTERFERING; STAUROSPORINE; TRANSFECTION;

EID: 84870410761     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986712803833281     Document Type: Article

References (56)

1. Cahalan, M.D.; Chandy, K.G. The functional network of ion channels in T lymphocytes. Immunol Rev., 2009, 231, 59-87.
2. Colden-Stanfield, M. Adhesion-dependent modulation of macrophage K+ channels. Adv Exp Med Biol., 2010, 674, 81-94.
3. Vicente, R.; Escalada, A.; Villalonga, N.; Texidó, L.; Roura-Ferrer, M.; Martín-Satué, M.; López-Iglesias, C.; Soler, C.; Solsona, C.; Tamkun, M.M.; Felipe, A. Association of Kv1.5 and Kv1.3 contributes to the major voltagedependent K+ channel in macrophages. J Biol Chem., 2006, 281, 37675-37685.
4. Gallin, E.K. Voltage clamp studies in macrophages from mouse spleen cultures. Science, 1981, 214, 458-460.
5. Lewis, R.S.; Cahalan, M.D. Potassium and calcium channels in lymphocytes. Annu Rev Immunol., 1995, 13, 623-653.
6. Blunck, R.; Scheel, O.; Müller, M.; Brandenburg, K.; Seitzer, U.; Seydel, U. New insights into endotoxin-induced activation of macrophages: involvement of a K+ channel in transmembrane signaling. J Immunol., 2001, 166, 1009-1015.
7. Qiu, M.R.; Campbell, T.J.; Breit, S.N. A potassium ion channel is involved in cytokine production by activated human macrophages. Clin Exp Immunol., 2002, 130, 67-74.
8. Krummel, M.F.; Cahalan, M.D. The immunological synapse: a dynamic platform for local signaling. J Clin Immunol., 2010, 30, 364-372.
9. Koni, P.A.; Khanna, R.; Chang, M.C.; Tang, M.D.; Kaczmarek, L.K.; Schlichter, L.C.; Flavell, R.A. Compensatory anion currents in Kv1.3 channel-deficient thymocytes. J Biol Chem., 2003, 278, 39443-39451.
10. Chi, V.; Pennington, M.W.; Norton, R.S.; Tarcha, E.J.; Londono, L.M.; Sims-Fahey, B.; Upadhyay, S.K.; Lakey, J.T.; Iadonato, S.; Wulff, H.; Beeton, C.; Chandy, K.G. Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases. Toxicon., 2012, 59, 529-546.
11. Wulff, H.; Castle, N.A.; Pardo, L.A. Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov., 2009, 8, 982-1001.
12. Rangaraju, S.; Chi, V.; Pennington, M.W.; Chandy, K.G. Kv1.3 potassium channels as a therapeutic target in multiple sclerosis. Expert Opin Ther Targets, 2009, 13, 909-924.
13. Liu, Q.H.; Fleischmann, B.K.; Hondowicz, B.; Maier, C.C.; Turka, L.A.; Yui, K.; Kotlikoff, M.I.; Wells, A.D.; Freedman, B.D. Modulation of Kv channel expression and function by TCR and costimulatory signals during peripheral CD4(+) lymphocyte differentiation. J Exp Med., 2002, 196, 897-909.
14. Burg, E.D.; Remillard, C.V.; Yuan, J.X. K+ channels in apoptosis. J Membr Biol., 2006, 209, 3-20.
15. Szabò, I.; Zoratti, M.; Gulbins, E. Contribution of voltage-gated potassium channels to the regulation of apoptosis. FEBS Lett., 2010, 584, 2049-2056.
16. Felipe, A.; Bielanska, J.; Comes, N.; Vallejo, A.; Roig, S.; Ramón Y Cajal, S.; Condom, E.; Hernández-Losa, J.; Ferreres, J.C. Targeting the voltagedependent K(+) channels Kv1.3 and Kv1.5 as tumor biomarkers for cancer detection and prevention. Curr Med Chem., 2012, 19, 661-674.
17. Arcangeli, A.; Pillozzi, S.; Becchetti, A. Targeting ion channels in leukemias: a new challenge for treatment. Curr Med Chem., 2012, 19, 683-696.
18. Szabò, I.; Bock, J.; Jekle, A.; Soddemann, M.; Adams, C.; Lang, F.; Zoratti, M.; Gulbins, E. A novel potassium channel in lymphocyte mitochondria. J Biol Chem., 2005, 280, 12790-12798.
19. Bednarczyk, P.; Kowalczyk, J.E.; Beresewicz, M.; Dołowy, K.; Szewczyk, A.; Zabłocka, B. Identification of a voltage-gated potassium channel in gerbil hippocampal mitochondria. Biochem Biophys Res Commun., 2010, 397, 614-620.
20. Gulbins, E.; Sassi, N.; Grassmè, H.; Zoratti, M.; Szabò, I. Role of Kv1.3 mitochondrial potassium channel in apoptotic signalling in lymphocytes. Biochim Biophys Acta., 2010, 1797, 1251-1259.
21. Szabó, I.; Bock, J.; Grassmé, H.; Soddemann, M.; Wilker, B.; Lang, F.; Zoratti, M.; Gulbins, E. Mitochondrial potassium channel Kv1.3 mediates Bax-induced apoptosis in lymphocytes. Proc Natl Acad Sci U S A., 2008, 105, 14861-14866.
22. Annis, M.G.; Soucie, E.L.; Dlugosz, P.J.; Cruz-Aguado, J.A.; Penn, L.Z.; Leber, B.; Andrews, D.W. Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J., 2005, 24, 2096-2103.
23. Szabò, I.; Soddemann, M.; Leanza, L.; Zoratti, M.; Gulbins, E. Single-point mutations of a lysine residue change function of Bax and Bcl-xL expressed in Bax- and Bak-less mouse embryonic fibroblasts: novel insights into the molecular mechanisms of Bax-induced apoptosis. Cell Death Differ., 2011, 18, 427-438.
24. Leanza, L.; Henry, B.; Sassi, N.; Zoratti, M.; Chandy, K.G.; Gulbins, E.; Szabò, I. Inhibitors of mitochondrial Kv1.3 channels induce Bax/Bakindependent death of cancer cells. EMBO Mol Med., 2012, Apr 11. doi: 10.1002/emmm.201200235.
25. Koeberle, P.D.; Wang, Y.; Schlichter, L.C. Kv1.1 and Kv1.3 channels contribute to the degeneration of retinal ganglion cells after optic nerve transection in vivo. Cell Death Differ., 2010, 17: 134-144.
26. Aiyar, J.; Rizzi, J.P.; Gutman, G.A.; Chandy, K.G. The signature sequence of voltage-gated potassium channels projects into the external vestibule. J Biol Chem., 1996, 271, 31013-31016.
27. MacKinnon, R.; Cohen, S.L.; Kuo, A.; Lee, A.; Chait, B.T. Structural conservation in prokaryotic and eukaryotic potassium channels. Science, 1998, 280, 106-109.
28. Gao, Y.D.; Garcia, M.L. Interaction of agitoxin2, charybdotoxin, and iberiotoxin with potassium channels: selectivity between voltage-gated and Maxi-K channels. Proteins, 2003, 52, 146-154.
29. Kalman, K.; Pennington, M.W.; Lanigan, M.D.; Nguyen, A.; Rauer, H.; Mahnir, V.; Paschetto, K.; Kem, W.R.; Grissmer, S.; Gutman, G.A.; Christian, E.P.; Cahalan, M.D.; Norton, R.S.; Chandy, K.G. ShK-Dap22, a potent Kv1.3-specific immunosuppressive polypeptide. J Biol Chem., 1998, 273, 32697-32707.
30. Hu, C.L.; Zeng, X.M.; Zhou, M.H.; Shi, Y.T.; Cao, H.; Mei, Y.A. Kv1.1 is associated with neuronal apoptosis and modulated by protein kinase C in the rat cerebellar granule cell. J Neurochem., 2008, 106, 1125-1137.
31. Vennekamp, J.; Wulff, H.; Beeton, C.; Calabresi, P.A.; Grissmer, S.; Hänsel, W.; Chandy, K.G. Kv1.3 blocking 5-phenylalkoxypsoralens: a new class of immunomodulators. Mol Pharmacol., 2004, 65, 1364-1374.
32. Schmitz, A.; Sankaranarayanan, A.; Azam, P.; Schmidt-Lassen, K.; Homerick, D.; Hänsel, W.; Wulff, H. Design of PAP-1, a selective small molecule Kv1.3 blocker, for the suppression of effector memory T cells in autoimmune diseases. Mol Pharmacol., 2005, 68, 1254-1270.
33. Zimin, P.I.; Garic, B.; Bodendiek, S.B.; Mahieux, C.; Wulff, H.; Zhorov, B.S. Potassium channel block by a tripartite complex of two cationophilic ligands and a potassium ion. Mol Pharmacol., 2010, 78, 588-99.
34. Ren, Y.R.; Pan, F.; Parvez, S.; Fleig, A.; Chong, C.R.; Xu, J.; Dang, Y.; Zhang, J.; Jiang, H.; Penner, R.; Liu, J.O. Clofazimine inhibits human Kv1.3 potassium channel by perturbing calcium oscillation in T lymphocytes. PLoS One, 2008, 3, e4009.
35. Lagrutta, A.; Wang, J.; Fermini, B.; Salata, J.J. Novel, potent inhibitors of human Kv1.5 K+ channels and ultrarapidly activating delayed rectifier potassium current. J Pharmacol Exp Ther., 2006, 317, 1054-1063.
36. Rauer, H.; Pennington, M.; Cahalan, M.; Chandy, K.G. Structural conservation of the pores of calcium-activated and voltage-gated potassium channels determined by a sea anemone toxin. J Biol Chem., 1999, 274, 21885-21892.
37. Villalonga, N.; David, M.; Bielanska, J.; Vicente, R.; Comes, N.; Valenzuela, C.; Felipe, A. Immunomodulation of voltage-dependent K+ channels in macrophages: molecular and biophysical consequences. J Gen Physiol., 2010, 135, 135-147.
38. Bonnet, S., Archer, S.L., Allalunis-Turner, J., Haromy, A., Beaulieu, C., Thompson R et al. (2006) A mitochondria-K+-channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell, 11, 37-51.
39. Szabò, I.; Leanza, L.; Gulbins, E.; Zoratti, M. Physiology of potassium channels in the inner membrane of mitochondria. Pflugers Arch., 2012, 463, 231-246.
40. Zoratti, M.; De Marchi, U.; Gulbins, E.; Szabò, I. Novel channels of the inner mitochondrial membrane. Biochim Biophys Acta., 2009, 1787, 351-363.
41. Xu, W.; Liu, Y.; Wang, S.; McDonald, T.; Van Eyk, J.E.; Sidor, A.; O'Rourke, B. Cytoprotective role of Ca2+- activated K+ channels in the cardiac inner mitochondrial membrane. Science, 2002, 298, 1029-1033.
42. Gu, X.Q.; Siemen, D.; Parvez, S.; Cheng, Y.; Xue, J.; Zhou, D.; Sun, X.; Jonas, E.A.; Haddad, G.G. Hypoxia increases BK channel activity in the inner mitochondrial membrane. Biochem Biophys Res Commun., 2007, 358, 311-316.
43. Siemen, D.; Loupatatzis, C.; Borecky, J.; Gulbins, E.; Lang, F. Ca2+-activated K channel of the BK-type in the inner mitochondrial membrane of a human glioma cell line. Biochem Biophys Res Commun., 1999, 257, 549-554.
44. Cheng, Y.; Gulbins, E.; Siemen, D. Activation of the permeability transition pore by Bax via inhibition of the mitochondrial BK channel. Cell Physiol Biochem., 2011, 27, 191-200.
45. De Marchi, U.; Sassi, N.; Fioretti, B.; Catacuzzeno, L.; Cereghetti, G.M.; Szabò, I.; Zoratti, M. Intermediate conductance Ca2+-activated potassium channel (KCa3.1) in the inner mitochondrial membrane of human colon cancer cells. Cell Calcium., 2009, 45, 509-516.
46. Ardehali H, O'Rourke B (2005) Mitochondrial K(ATP) channels in cell survival and death. J Mol Cell Cardiol. 39: 7-16.
47. Vicente, R.; Villalonga, N.; Calvo, M.; Escalada, A.; Solsona, C.; Soler, C.; Tamkun, M.M.; Felipe, A. Kv1.5 association modifies Kv1.3 traffic and membrane localization. J Biol Chem., 2008, 283, 8756-8764.
48. Zsiros, E.; Kis-Toth, K.; Hajdu, P.; Gaspar, R.; Bielanska, J.; Felipe, A.; Rajnavolgyi, E.; Panyi, G. Developmental switch of the expression of ion channels in human dendritic cells. J Immunol., 2009, 183, 4483-4492.
49. Vicente, R.; Escalada, A.; Coma, M.; Fuster, G.; Sánchez- Tilló, E.; López-Iglesias, C.; Soler, C.; Solsona, C.; Celada, A.; Felipe, A. Differential voltage-dependent K+ channel responses during proliferation and activation in macrophages. J Biol Chem., 2003, 278, 46307-46320.
50. Hanley, P.J.; Kronlage, M.; Kirschning, C.; Del Rey, A.; Di Virgilio, F.; Leipziger, J.; Chessell, I.P.; Sargin, S.; Filippov, M.A.; Lindemann, O.; Mohr, S.; Königs, V.; Schillers, H.; Bähler, M.; Schwab, A. Transient P2X7 receptor activation triggers macrophage death independent of Toll-like receptors 2 and 4, caspase-1, and pannexin-1 proteins. J Biol Chem., 2012, 287: 10650-10663.
51. Yuan, X.J., Wang, J., Juhaszova, M., Gaine, S.P. and Rubin, L.J. (1998) Attenuated K+ channel gene transcription in primary pulmonary hypertension. Lancet. 351, 726 -727.
52. Brevnova, E.E., Platoshyn, O., Zhang, S. and Yuan, JX.-J. (2004) Overexpression of human KCNA5 increases IK(V) and enhances apoptosis. Am J Physiol Cell Physiol 287, C715-C722.
53. Fukuda, K.; Kobayashi, A.; Watabe, K. The role of tumor-associated macrophage in tumor progression. Front Biosci (Schol Ed)., 2012, 4, 787-798.
54. Allavena, P.; Mantovani, A. Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol., 2012, 167, 195-205.
55. Grunnet, M.; Rasmussen, HB.; Hay-Schmidt,A.; Rosenstierne,M.; Kalerke, DA.; Olesen,SP.; Jespersen,T. KCNE4 Is an Inhibitory Subunit to Kv1.1 and Kv1.3 Potassium Channels. Biophysical J. 2003, 85: 1525-1537.
56. Sutachan, JJ.; Watanabe, I.; Zhu, J.; Gottschalk, A.; Recio-Pinto, E.; Thornhill, WB. Effects of Kv1.1 channel glycosylation on C-type inactivation and simulated action potentials. Brain Res. 20051058:30-43.