The intermediate conductance calcium-activated potassium channel KCa3.1 regulates vascular smooth muscle cell proliferation via controlling calcium-dependent signaling

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15843-15853

  Bi, Dan ^a   Toyama, Kazuyoshi ^b   Lemaître, Vincent ^a   Takai, Jun ^a   Fan, Fan ^b   Jenkins, David P ^c   Wulff, Heike ^c   Gutterman, David D ^b   Park, Frank ^b,d   Miura, Hiroto ^a,b  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPROLIFERATIVE EFFECT; CALCIUM-ACTIVATED POTASSIUM; CAMP-RESPONSE ELEMENT-BINDING PROTEINS; HUMAN CORONARY ARTERIES; PROLIFERATIVE DISEASE; TRANSCRIPTIONAL MECHANISMS; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE CELLS;

ELECTROPHYSIOLOGY; PATHOLOGY; PHOSPHORYLATION; POTASSIUM;

CALCIUM;

CALDESMON; CALPONIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLINE; NUCLEAR RECEPTOR NR4A3; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCA3.1; PROTEIN C FOS; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; ATHEROSCLEROSIS; ATTENUATION; CALCIUM CONDUCTANCE; CALCIUM SIGNALING; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VASCULAR SMOOTH MUSCLE;

ATHEROSCLEROSIS; CALCIUM; CALCIUM SIGNALING; CELL PROLIFERATION; POTASSIUM CHANNELS; VASCULAR BIOLOGY; VASCULAR SMOOTH MUSCLE CELLS;

ANGIOGENESIS INDUCING AGENTS; ATHEROSCLEROSIS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CALMODULIN-BINDING PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HUMANS; INTERMEDIATE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MEMBRANE TRANSPORT PROTEINS; MICROFILAMENT PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-SIS;

EID: 84878408383     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.427187     Document Type: Article

References (51)

1. + channels: from protein complexes to function. Physiol. Rev. 90, 1437-1459
2. Wulff, H., and Castle, N. A. (2010) Therapeutic potential of KCa3.1 blockers: recent advances and promising trends. Expert Rev. Clin. Pharmacol. 3, 385-396
3. Toyama, K., Wulff, H., Chandy, K. G., Azam, P., Raman, G., Saito, T., Fujiwara, Y., Mattson, D. L., Das, S., Melvin, J. E., Pratt, P. F., Hatoum, O. A., Gutterman, D. D., Harder, D. R., and Miura, H. (2008) The intermediate-conductance calcium-activated potassium channel KCa3.1 contributes to atherogenesis in mice and humans. J. Clin. Invest. 118, 3025-3037
4. + channels regulate human airway smooth muscle proliferation. Am. J. Respir. Cell Mol. Biol. 37, 525-531
5. + channel suppresses proliferation of microvascular and macrovascular endothelial cells and angiogenesis in vivo. Arterioscler. Thromb. Vasc. Biol. 25, 704-709
6. + channel expression during B cell differentiation: implications for immunomodulation and autoimmunity. J. Immunol. 173, 776-786
7. Ghanshani, S., Wulff, H., Miller, M. J., Rohm, H., Neben, A., Gutman, G. A., Cahalan, M. D., and Chandy, K. G. (2000) Up-regulation of the IKCa1 potassium channel during T-cell activation: molecular mechanism and functional consequences. J. Biol. Chem. 275, 37137-37149 (Pubitemid 32002132)
8. Ca channel, FIK, as a prototype for the cell growth regulatory function of the IK channel family. J. Membr. Biol. 172, 249-257
9. 2+-activated potassium and volume-sensitive chloride channels in mouse mesenchymal stem cells. Am. J. Physiol. Cell Physiol 295, C1409-C1416
10. Chou, C. C., Lunn, C. A., and Murgolo, N. J. (2008) KCa3.1: target and marker for cancer, autoimmune disorder and vascular inflammation? Expert. Rev. Mol Diagn. 8, 179-187 (Pubitemid 351469437)
11. Ca channel diversity and smooth muscle cell function. Circ. Res. 85, e33-e43
12. Köhler, R., Wulff, H., Eichler, I., Kneifel, M., Neumann, D., Knorr, A., Grgic, I., Kämpfe, D., Si, H., Wibawa, J., Real, R., Borner, K., Brakemeier, S., Orzechowski, H. D., Reusch, H. P., Paul, M., Chandy, K. G., and Hoyer, J. (2003) Blockade of the intermediate-conductance calcium-activated potassium channel as a new therapeutic strategy for restenosis. Circulation 108, 1119-1125 (Pubitemid 37071524)
13. Neylon, C. B. (2002) Potassium channels and vascular proliferation. Vascul. Pharmacol. 38, 35-41
14. + channels in postischaemic heart. Clin. Exp. Pharmacol. Physiol. 29, 324-329
15. Terata, Y., Saito, T., Fujiwara, Y., Hasegawa, H., Miura, H., Watanabe, H., Chiba, Y., Kibira, S., and Miura, M. (2003) Pitavastatin inhibits upregulation of intermediate conductance calcium-activated potassium channels and coronary arteriolar remodeling induced by long-term blockade of nitric oxide synthesis. Pharmacology 68, 169-176 (Pubitemid 36831223)
16. + channel (IKCa1) mediates phenotypic modulation of coronary smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 291, H2493-H2503
17. Tharp, D. L., Wamhoff, B. R., Wulff, H., Raman, G., Cheong, A., and Bowles, D. K. (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
18. + channels in proliferating A7r5 vascular smooth muscle cells. Br. J. Pharmacol. 148, 909-917
19. Miano, J. M., Vlasic, N., Tota, R. R., and Stemerman, M. B. (1993) Localization of Fos and Jun proteins in rat aortic smooth muscle cells after vascular injury. Am. J Pathol. 142, 715-724 (Pubitemid 24063989)
20. Sylvester, A. M., Chen, D., Krasinski, K., and Andrés, V. (1998) Role of c-Fos and E2F in the induction of cyclin A transcription and vascular smooth muscle cell proliferation. J. Clin. Invest. 101, 940-948 (Pubitemid 28125270)
21. Cheong, A., Bingham, A. J., Li, J., Kumar, B., Sukumar, P., Munsch, C., Buckley, N. J., Neylon, C. B., Porter, K. E., Beech, D. J., and Wood, I. C. (2005) Downregulated REST transcription factor is a switch enabling critical potassium channel expression and cell proliferation. Mol. Cell 20, 45-52 (Pubitemid 41396561)
22. Barlow, C. A., Rose, P., Pulver-Kaste, R. A., and Lounsbury, K. M. (2006) Excitation-transcription coupling in smooth muscle. J. Physiol. 570, 59-64
23. 2+ response amplitude and duration. Nature 386, 855-858
24. McAllister, J., Ghosh, S., Berry, D., Park, M., Sadeghi, S., Wang, K. X., Parker, W. D., and Swerdlow, R. H. (2008) Effects of memantine on mitochondrial function. Biochem. Pharmacol. 75, 956-964 (Pubitemid 351174116)
25. + channel, IKCa1: a potential immunosuppressant. Proc. Natl. Acad. Sci. U.S.A. 97, 8151-8156
26. Wulff, H., Kolski-Andreaco, A., Sankaranarayanan, A., Sabatier, J. M., and Shakkottai, V. (2007) Modulators of small- and intermediate-conductance calcium-activated potassium channels and their therapeutic indications. Curr. Med. Chem. 14, 1437-1457 (Pubitemid 46902225)
27. Sankaranarayanan, A., Raman, G., Busch, C., Schultz, T., Zimin, P. I., Hoyer, J., Köhler, R., and Wulff, H. (2009) Naphtho[1,2-d]thiazol-2-ylamine (SKA-31), a new activator of KCa2 and KCa3.1 potassium channels, potentiates the endothelium-derived hyperpolarizing factor response and lowers blood pressure. Mol. Pharmacol. 75, 281-295
28. + channels by NS309 (6,7-dichloro-1H-indole-2,3-dione 3-oxime). Biochim. Biophys. Acta 1665, 1-5
29. Tolić-Nørrelykke, I. M., and Wang, N. (2005) Traction in smooth muscle cells varies with cell spreading. J. Biomech. 38, 1405-1412 (Pubitemid 40744897)
30. Park, F., Ohashi, K., Chiu, W., Naldini, L., and Kay, M. A. (2000) Efficient lentiviral transduction of liver requires cell cycling in vivo. Nat. Genet. 24, 49-52 (Pubitemid 30041419)
31. Hollenbeck, S. T., Nelson, P. R., Yamamura, S., Faries, P. L., Liu, B., and Kent, K. C. (2004) Intracellular calcium transients are necessary for platelet-derived growth factor but not extracellular matrix protein-induced vascular smooth muscle cell migration. J. Vasc. Surg. 40, 351-358 (Pubitemid 39055902)
32. Martínez-González, J., Rius, J., Castelló, A., Cases-Langhoff, C., and Badimon, L. (2003) Neuron-derived orphan receptor-1 (NOR-1) modulates vascular smooth muscle cell proliferation. Circ. Res. 92, 96-103 (Pubitemid 36105612)
33. Pulver, R. A., Rose-Curtis, P., Roe, M. W., Wellman, G. C., and Lounsbury, K. M. (2004) Store-operated Ca2+ entry activates the CREB transcription factor in vascular smooth muscle. Circ. Res. 94, 1351-1358 (Pubitemid 38724481)
34. Rothman, A., Wolner, B., Button, D., and Taylor, P. (1994) Immediate-early gene expression in response to hypertrophic and proliferative stimuli in pulmonary arterial smooth muscle cells. J. Biol. Chem. 269, 6399-6404 (Pubitemid 24191011)
35. Mayr, B., and Montminy, M. (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609 (Pubitemid 33674011)
36. Kaplan-Albuquerque, N., Van Putten, V., Weiser-Evans, M. C., and Nemenoff, R. A. (2005) Depletion of serum response factor by RNA interference mimics the mitogenic effects of platelet derived growth factor-BB in vascular smooth muscle cells. Circ. Res. 97, 427-433 (Pubitemid 41298172)
37. Sirois, M. G., Simons, M., and Edelman, E. R. (1997) Antisense oligonucleotide inhibition of PDGFR-β receptor subunit expression directs suppression of intimal thickening. Circulation 95, 669-676 (Pubitemid 27063045)
38. Feske, S. (2007) Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 7, 690-702
39. Raicu, M., Florea, S., Costache, G., Popov, D., and Simionescu, M. (2000) Clotrimazole inhibits smooth muscle cell proliferation and has a vasodilator effect on resistance arteries. Fundam. Clin. Pharmacol. 14, 477-485
40. Sun, D., Gong, Y., Kojima, H., Wang, G., Ravinsky, E., Zhang, M., and Minuk, G. Y. (2003) Increasing cell membrane potential and GABAergic activity inhibits malignant hepatocyte growth. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G12-G19 (Pubitemid 36736383)
41. + transport and electrical membrane properties during the cell cycle. J. Cell Physiol. 107, 75-83
42. + channel by its opener 1-ethyl-2-benzimidazolinone in HaCaT keratinocytes. Inverse effects on cell growth and proliferation. J. Biol. Chem. 278, 3323-3330
43. 2+ channels modulate expression of smooth muscle differentiation marker genes via a Rho kinase/myocardin/SRF-dependent mechanism. Circ. Res. 95, 406-414
44. 2+, calmodulin, and cyclins in vascular smooth muscle cell cycle. Circ. Res. 98, 1240-1243
45. Berridge, M. J. (1995) Calcium signalling and cell proliferation. Bioessays. 17, 491-500
46. 2+-sensitive G1/S transitions in vascular smooth muscle cells. Circ. Res. 98, 1273-1281
47. Desdouets, C., Matesic, G., Molina, C. A., Foulkes, N. S., Sassone-Corsi, P., Brechot, C., and Sobczak-Thepot, J. (1995) Cell cycle regulation of cyclin A gene expression by the cyclic AMP-responsive transcription factors CREB and CREM. Mol. Cell. Biol. 15, 3301-3309
48. Brugnara, C., Gee, B., Armsby, C. C., Kurth, S., Sakamoto, M., Rifai, N., Alper, S. L., and Platt, O. S. (1996) Therapy with oral clotrimazole induces inhibition of the Gardos channel and reduction of erythrocyte dehydration in patients with sickle cell disease. J. Clin. Invest. 97, 1227-1234 (Pubitemid 26085478)
49. Rouzaire-Dubois, B., Milandri, J. B., Bostel, S., and Dubois, J. M. (2000) Control of cell proliferation by cell volume alterations in rat C6 glioma cells. Pflugers Arch. 440, 881-888
50. + channels. EMBO J. 18, 5540-5547
51. 2+ release. FEBS J. 273, 3585-3597