Kv1.3 channels modulate human vascular smooth muscle cells proliferation independently of mTOR signaling pathway

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 8, 2015, Pages 1711-1722

  Cidad, Pilar ^a   Miguel Velado, Eduardo ^a   Ruiz McDavitt, Christian ^a   Alonso, Esperanza ^a   Jiménez Pérez, Laura ^a   Asuaje, Agustín ^a   Carmona, Yamila ^a   García Arribas, Daniel ^a   López, Javier ^b   Marroquín, Yngrid ^b   Fernández, Mirella ^b   Roqué, Mercè ^c   Pérez García, M Teresa ^a   López López, José Ramón ^a  

^a UNIVERSITY OF VALLADOLID   (Spain)

^b HOSPITAL CLÍNICO UNIVERSITARIO DE VALLADOLID   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cell signaling; Kv1.3 channels; Phenotypic switch; Vascular remodeling; Vascular smooth muscle cell proliferation

Indexed keywords

1 [(2 CHLOROPHENYL)DIPHENYLMETHYL] 1H PYRAZOLE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANGIOTENSIN II; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CALCIUM; CYCLIN D; EVEROLIMUS; MAMMALIAN TARGET OF RAPAMYCIN; MARGATOXIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C GAMMA; PLATELET DERIVED GROWTH FACTOR; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.5; KCNA3 PROTEIN, HUMAN; KCNA5 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; PHOSPHODIESTERASE INHIBITOR; POTASSIUM CHANNEL BLOCKING AGENT; PROTEIN KINASE INHIBITOR; TARGET OF RAPAMYCIN KINASE;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; CURRENT CLAMP TECHNIQUE; ELECTROPHYSIOLOGICAL PROCEDURES; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MEMBRANE STEADY POTENTIAL; PHENOTYPE; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR SMOOTH MUSCLE CELL; WHOLE CELL PATCH CLAMP; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; MEMBRANE POTENTIAL; METABOLISM; SMOOTH MUSCLE FIBER; TIME; VASCULAR SMOOTH MUSCLE;

CELL PROLIFERATION; CELLS, CULTURED; HUMANS; KV1.3 POTASSIUM CHANNEL; KV1.5 POTASSIUM CHANNEL; MEMBRANE POTENTIALS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; PHOSPHODIESTERASE INHIBITORS; PLATELET-DERIVED GROWTH FACTOR; POTASSIUM CHANNEL BLOCKERS; PROTEIN KINASE INHIBITORS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS; TOR SERINE-THREONINE KINASES;

EID: 84937774598     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1607-y     Document Type: Article

References (44)

1. Beech DJ (2007) Ion channel switching and activation in smooth-muscle cells of occlusive vascular diseases. Biochem Soc Trans 035:890–894
2. Beeton C, Wulff H, Standifer NE, Azam P, Mullen KM, Pennington MW, Kolski-Andreaco A, Wei E, Grino A, Counts DR, Wang PH et al (2006) Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc Natl Acad Sci U S A 103:17414–17419
3. Caglayan E, Vantler M, Leppänen O, Gerhardt F, Mustafov L, ten Freyhaus H, Kappert K, Odenthal M, Zimmermann WH, Tallquist MD, Rosenkranz S (2011) Disruption of platelet-derived growth factor-dependent phosphatidylinositol 3-kinase and phospholipase C γ1 activity abolishes vascular smooth muscle cell proliferation and migration and attenuates neointima formation in vivo. J Am Coll Cardiol 57:2527–2538
4. Cahalan MD, Chandy KG, DeCoursey TE, Gupta S (1985) A voltage-gated potassium channel in human T lymphocytes. J Physiol 358:197–237
5. Campbell GR, Campbell JH (1985) Smooth muscle phenotypic changes in arterial wall homeostasis: implications for the pathogenesis of atherosclerosis. Exp Mol Pathol 42:139–162
6. Chen TT, Luykenaar KD, Walsh EJ, Walsh MP, Cole WC (2006) Key role of Kv1 channels in vasoregulation. Circ Res 99:53–60
7. Cidad P, Jimenez-Perez L, Garcia-Arribas D, Miguel-Velado E, Tajada S, Ruiz-McDavitt C, Lopez-Lopez JR, Perez-Garcia MT (2012) Kv1.3 channels can modulate cell proliferation during phenotypic switch by an ion-flux independent mechanism. Arterioscler Thromb Vasc Biol 32:1299–1307
8. Cidad P, Moreno-Dominguez A, Novensa L, Roque M, Barquin L, Heras M, Perez-Garcia MT, Lopez-Lopez JR (2010) Characterization of ion channels involved in the proliferative response of femoral artery smooth muscle cells. Arterioscler Thromb Vasc Biol 30:1203–1211
9. DeCoursey TE, Chandy KG, Gupta S, Cahalan MD (1984) Voltage-gated K + channels in human lymphocyte-T—a role in mitogenesis. Nature 307:465–468
10. Eisen HJ, Tuzcu EM, Dorent R, Kobashigawa J, Mancini D, Valantine-von Kaeppler HA, Starling RC, Sörensen K, Hummel M, Lind JM, Abeywickrama KH et al (2003) Everolimus for the prevention of allograft rejection and vasculopathy in cardiac-transplant recipients. N Engl J Med 349:847–858
11. Erdogan A, Schaefer CA, Schaefer M, Luedders DW, Stockhausen F, Abdallah Y, Schaefer C, Most AK, Tillmanns H, Piper HM, Kuhlmann CR (2005) Margatoxin inhibits VEGF-induced hyperpolarization, proliferation and nitric oxide production of human endothelial cells. J Vasc Res 42:368–376
12. Formica RN Jr, Lorber KM, Friedman AL, Bia MJ, Lakkis F, Smith JD, Lorber MI (2004) The evolving experience using everolimus in clinical transplantation. Transplant Proc 36:S495–S499
13. Garcia-Calvo M, Leonard RJ, Novick J, Stevens SP, Schmalhofer W, Kaczorowski GJ, Garcia ML (1993) Purification, characterization, and biosynthesis of margatoxin, a component of Centruroides margaritatus venom that selectively inhibits voltage-dependent potassium channels. J Biol Chem 268:18866–18874
14. Hafizi S, Mordi VN, Andersson KM, Chester AH, Yacoub MH (2004) Differential effects of rapamycin, cyclosporine A, and FK506 on human coronary artery smooth muscle cell proliferation and signalling. Vasc Pharmacol 41:167–176
15. Hafizi S, Wang X, Chester AH, Yacoub MH, Proud CG (2004) ANG II activates effectors of mTOR via PI3-K signaling in human coronary smooth muscle cells. Am J Physiol Heart Circ Physiol 287:H1232–H1238
16. Hegle AP, Marble DD, Wilson GF (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
17. Heldin CH, Westermark B (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79:1283–1316
18. Hughes AD, Clunn GF, Refson J, Demoliou-Mason C (1996) Platelet-derived growth factor (PDGF): actions and mechanisms in vascular smooth muscle. Gen Pharmacol 27:1079–1089
19. Isoda K, Shiigai M, Ishigami N, Matsuki T, Horai R, Nishikawa K, Kusuhara M, Nishida Y, Iwakura Y, Ohsuzu F (2003) Deficiency of interleukin-1 receptor antagonist promotes neointimal formation after injury. Circulation 108:516–518
20. Jia L, Wang R, Tang DD (2012) Abl regulates smooth muscle cell proliferation by modulating actin dynamics and ERK1/2 activation. Am J Physiol Cell Physiol 302:C1026–C1034
21. Jones SM, Kazlauskas A (2001) Growth factor-dependent signaling and cell cycle progression. FEBS Lett 490:110–116
22. Jones SM, Kazlauskas A (2001) Growth-factor-dependent mitogenesis requires two distinct phases of signalling. Nat Cell Biol 3:165–172
23. Jurek A, Heldin CH, Lennartsson J (2011) Platelet-derived growth factor-induced signaling pathways interconnect to regulate the temporal pattern of Erk1/2 phosphorylation. Cell Signal 23:280–287
24. Kohler R, Wulff H, Eichler I, Kneifel M, Neumann D, Knorr A, Grgic I, Kampfe D, Si H, Wibawa J, Real R et al (2003) Blockade of the intermediate-conductance calcium-activated potassium channel as a new therapeutic strategy for restenosis. Circulation 108:1119–1125
25. Liou SF, Yeh JL, Liang JC, Chiu CC, Lin YT, Chen IJ (2004) Inhibition of mitogen-mediated proliferation of rat vascular smooth muscle cells by labedipinedilol-A through PKC and ERK 1/2 pathway. J Cardiovasc Pharmacol 44:539–551
26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
27. Miguel-Velado E, Moreno-Dominguez A, Colinas O, Cidad P, Heras M, Perez-Garcia MT, López-López JR (2005) Contribution of Kv channels to phenotypic remodeling of human uterine artery smooth muscle cells. Circ Res 97:1280–1287
28. Millership JE, Devor DC, Hamilton KL, Balut CM, Bruce JIE, Fearon IM (2011) Calcium-activated K + channels increase cell proliferation independent of K + conductance. Am J Physiol Cell Physiol 300:C792–C802
29. Millette E, Rauch BH, Kenagy RD, Daum G, Clowes AW (2006) Platelet-derived growth factor-BB transactivates the fibroblast growth factor receptor to induce proliferation in human smooth muscle cells. Trends Cardiovasc Med 16:25–28
30. Moreno-Dominguez A, Cidad P, Miguel-Velado E, Lopez-Lopez JR, Perez-Garcia MT (2009) De novo expression of Kv6.3 contributes to changes in vascular smooth muscle cell excitability in a hypertensive mice strain. J Physiol 587:625–640
31. Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767–801
32. Pardo LA (2004) Voltage-gated potassium channels in cell proliferation. Physiology 19:285–292
33. Roche S, Koegl M, Courtneidge SA (1994) The phosphatidylinositol 3-kinase alpha is required for DNA synthesis induced by some, but not all, growth factors. Proc Natl Acad Sci U S A 91:9185–9189
34. Roovers K, Assoian RK (2000) Integrating the MAP kinase signal into the G1 phase cell cycle machinery. Bioessays 22:818–826
35. Sabri A, Govindarajan G, Griffin TM, Byron KL, Samarel AM, Lucchesi PA (1998) Calcium- and protein kinase -dependent activation of the tyrosine kinase PYK2 by angiotensin II in vascular smooth muscle. Circ Res 83:841–851
36. Schmitz A, Sankaranarayanan A, Azam P, Schmidt-Lassen K, Homerick D, Hansel W, Wulff H (2005) Design of PAP-1, a selective small molecule Kv1.3 blocker, for the suppression of effector memory T cells in autoimmune diseases. Mol Pharmacol 68:1254–1270
37. Si H, Grgic I, Heyken WT, Maier T, Hoyer J, Reusch HP, Köhler R (2006) Mitogenic modulation of Ca2+-activated K+ channels in proliferating A7r5 vascular smooth muscle cells. Br J Pharmacol 148:909–917
38. Stehlik J, Edwards LB, Kucheryavaya AY, Benden C, Christie JD, Dipchand AI, Dobbels F, Kirk R, Rahmel AO, Hertz MI (2012) The registry of the international society for heart and lung transplantation: 29th official adult heart transplant report—2012. J Heart Lung Transplant 31:1052–1064
39. + channels in mice mesenteric vascular smooth muscle cells. J Physiol 590:6075–6091
40. Tallquist M, Kazlauskas A (2004) PDGF signaling in cells and mice. Cytokine Growth Factor Rev 15:205–213
41. Tharp DL, Bowles DK (2009) The intermediate-conductance Ca2+-activated K+ channel (KCa3.1) in vascular disease. Cardiovasc Hematol Agents Med Chem 7:1–11
42. Tharp DL, Wamhoff BR, Wulff H, Raman G, Cheong A, Bowles DK (2008) Local delivery of the KCa3.1 blocker, TRAM-34, prevents acute angioplasty-induced coronary smooth muscle phenotypic modulation and limits stenosis. Arterioscler Thromb Vasc Biol 28:1084–1089
43. Wulff H, Castle NA, Pardo LA (2009) Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov 8:982–1001
44. Zhan Y, Kim S, Yasumoto H, Namba M, Miyazaki H, Iwao H (2002) Effects of dominant-negative c-Jun on platelet-derived growth factor-induced vascular smooth muscle cell proliferation. Arterioscler Thromb Vasc Biol 22:82–88