Mechanisms of Activation of Voltage-Gated Potassium Channels

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Abstract

Voltage-gated potassium ion channels (Kv) play an important role in a variety of cellular processes, including the functioning of excitable cells, regulation of apoptosis, cell growth and differentiation, the release of neurotransmitters and hormones, maintenance of cardiac activity, etc. Failure in the functioning of Kv channels leads to severe genetic disorders and the development of tumors, including malignant ones. Understanding the mechanisms underlying Kv channels functioning is a key factor in determining the cause of the diseases associated with mutations in the channels, and in the search for new drugs. The mechanism of activation of the channels is a topic of ongoing debate, and a consensus on the issue has not yet been reached. This review discusses the key stages in studying the mechanisms of functioning of Kv channels and describes the basic models of their activation known to date.

About the authors

A. V. Grizel

Saint Petersburg State University

Author for correspondence.
Email: sokolova@mail.bio.msu.ru
Russian Federation

G. S. Glukhov

Moscow State MV Lomonosov University

Email: sokolova@mail.bio.msu.ru
Russian Federation

O. S. Sokolova

Moscow State MV Lomonosov University

Email: sokolova@mail.bio.msu.ru
Russian Federation

References

  1. Yu F.H., Yarov-Yarovoy V., Gutman G.A., Catterall W.A. // Pharmacol. Rev. 2005, V.57, P.387-395
  2. Gutman G.A., Chandy K.G., Grissmer S., Lazdunski M., McKinnon D., Pardo L.A., Robertson G.A., Rudy B., Sanguinetti M.C., Stühmer W., Wang X. // Pharmacol. Rev. 2005, V.57, P.473-508
  3. Hoshi T., Zagotta W.N., Aldrich R.W. // Science. 1990, V.250, P.533-538
  4. Yellen G. // Nature 2002, V.419, P.35-42
  5. Bosma M.M., Hille B. // Endocrinology. 1992, V.130, P.3411-3420
  6. Pal S.K., Takimoto K., Aizenman E., Levitan E.S. // Cell Death. Differ. 2006, V.13, P.661-667
  7. Deutsch C., Chen L.Q. // Proc. Natl. Acad. Sci. USA. 1993, V.90, P.10036-10040
  8. Singer-Lahat D., Sheinin A., Chikvashvili D., Tsuk S., Greitzer D., Friedrich R., Feinshreiber L., Ashery U., Benveniste M., Levitan E.S. // J. Neurosci. 2007, V.27, P.1651-1658
  9. MacDonald P.E., Sewing S., Wang J., Joseph J.W., Smukler S.R., Sakellaropoulos G., Saleh M.C., Chan C.B., Tsushima R.G., Salapatek A.M. // J. Biol. Chem. 2002, V.277, P.44938-44945
  10. Kim S.J., Widenmaier S.B., Choi W.S., Nian C., Ao Z., Warnock G., McIntosh C.H. // Cell Death. Differ. 2012, V.19, P.333-344
  11. Wang Q., Curran M.E., Splawski I., Burn T.C., Millholland J.M., VanRaay T.J., Shen J., Timothy K.W., Vincent G.M., de Jager T. // Nat. Genet. 1996, V.12, P.17-23
  12. Wray D. // Eur. Biophys. J. 2009, V.38, P.271-272
  13. Watanabe H., Nagata E., Kosakai A., Nakamura M., Yokoyama M., Tanaka K., Sasai H. // J. Neurochem. 2000, V.75, P.28-33
  14. Beekwilder J.P., O’Leary M.E., van den Broek L.P., van Kempen G.T., Ypey D.L., van den Berg R.J. // J. Pharmacol. Exp. Ther. 2003, V.304, P.531-538
  15. Camacho J. // Cancer Lett. 2006, V.233, P.1-9
  16. Milescu M., Lee H.C., Bae C.H., Kim J.I., Swartz K.J. // J. Gen. Physiol. 2013, V.141, P.203-216
  17. Thomas D., Wimmer A.B., Wu K., Hammerling B.C., Ficker E.K., Kuryshev Y.A., Kiehn J., Katus H.A., Schoels W., Karle C.A. // Naunyn Schmiedebergs Arch. Pharmacol. 2004, V.369, P.462-472
  18. Ikeda M., Tomita Y., Mouri A., Koga M., Okochi T., Yoshimura R., Yamanouchi Y., Kinoshita Y., Hashimoto R., Williams H.J. // Biological Psychiatry 2010, V.67, P.263-269
  19. Sokolova O. // FEBS Lett. 2004, V.564, P.251-256
  20. Carrington J.C., Freed D.D. // Virology Journal 1990, V.64, P.1590-1597
  21. Long S.B., Campbell E.B., Mackinnon R. // Science. 2005, V.309, P.897-903
  22. Brandt F., Etchells S.A., Ortiz J.O., Elcock A.H., Hartl F.U., Baumeister W. // Cell. 2009, V.136, P.261-271
  23. Myasnikov A.G., Afonina Z.A., Klaholz B.P. // Ultramicroscopy. 2013, V.126, P.33-39
  24. Doyle D.A., Morais Cabral J., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. // Science. 1998, V.280, P.69-77
  25. Lu Z., Klem A.M., Ramu Y. // J. Gen. Physiol. 2002, V.120, P.663-676
  26. Lu Z., Klem A.M., Ramu Y. // Nature 2001, V.413, P.809-813
  27. Labro A.J., Raes A.L., Grottesi A., van Hoorick D., Sansom M.S., Snyders D.J. // J. Gen. Physiol. 2008, V.132, P.667-680
  28. Barghaan J., Bahring R. // J. Gen. Physiol. 2009, V.133, P.205-224
  29. Batulan Z., Haddad G.A., Blunck R. // J. Biol. Chem. 2010, V.285, P.14005-14019
  30. Haddad G.A., Blunck R. // J. Gen. Physiol. 2011, V.137, P.455-472
  31. Pischalnikova A.V., Sokolova O.S. // J. Neuroimmune Pharmacol. 2009, V.4, P.71-82
  32. Leicher T., Bahring R., Isbrandt D., Pongs O. // J. Biol. Chem. 1998, V.273, P.35095-35101
  33. Shi G., Nakahira K., Hammond S., Rhodes K. J., Schechter L.E., Trimmer J.S. // Neuron. 1996, V.16, P.843-852
  34. Wray D. // Eur. Biophys. J. 2004, V.33, P.194-200
  35. Rasmusson R.L., Morales M.J., Wang S., Liu S., Campbell D.L., Brahmajothi M.V., Strauss H.C. // Circ. Res. 1998, V.82, P.739-750
  36. Sigworth F.J. // Q. Rev. Biophys. 1994, V.27, P.1-40
  37. Rettig J., Heinemann S.H., Wunder F., Lorra C., Parcej D.N., Dolly J.O., Pongs O. // Nature 1994, V.369, P.289-294
  38. Armstrong C.M., Bezanilla F. // J. Gen. Physiol. 1977, V.70, P.567-590
  39. Zagotta W.N., Hoshi T., Aldrich R.W. // Science. 1990, V.250, P.568-571
  40. Blunck R., Cordero-Morales J.F., Cuello L.G., Perozo E., Bezanilla F. // J. Gen. Physiol. 2006, V.128, P.569-581
  41. Cordero-Morales J.F., Cuello L.G., Zhao Y., Jogini V., Cortes D.M., Roux B., Perozo E. // Nat. Struct. Mol. Biol. 2006, V.13, P.311-318
  42. Cordero-Morales J.F., Cuello L.G., Perozo E. // Nat. Struct. Mol. Biol. 2006, V.13, P.319-322
  43. Jiang Y., Lee A., Chen J., Ruta V., Cadene M., Chait B.T., MacKinnon R. // Nature 2003, V.423, P.33-41
  44. Long S.B., Tao X., Campbell E.B., MacKinnon R. // Nature 2007, V.450, P.376-382
  45. Laine M., Lin M.C., Bannister J.P., Silverman W.R., Mock A.F., Roux B., Papazian D.M. // Neuron. 2003, V.39, P.467-481
  46. Ruta V., Chen J., MacKinnon R. // Cell. 2005, V.123, P.463-475
  47. Posson D.J., Ge P., Miller C., Bezanilla F., Selvin P.R. // Nature 2005, V.436, P.848-851
  48. Chanda B., Asamoah O.K., Blunck R., Roux B., Bezanilla F. // Nature 2005, V.436, P.852-856
  49. Yarov-Yarovoy V., Baker D., Catterall W.A. // Proc. Natl. Acad. Sci. USA. 2006, V.103, P.7292-7297
  50. Campos F.V., Chanda B., Roux B., Bezanilla F. // Proc. Natl. Acad. Sci. USA. 2007, V.104, P.7904-7909
  51. Grabe M., Lai H.C., Jain M., Jan Y.N., Jan L.Y. // Nature 2007, V.445, P.550-553
  52. Lewis A., Jogini V., Blachowicz L., Laine M., Roux B. // J. Gen. Physiol. 2008, V.131, P.549-561
  53. Pathak M.M., Yarov-Yarovoy V., Agarwal G., Roux B., Barth P., Kohout S., Tombola F., Isacoff E.Y. // Neuron. 2007, V.56, P.124-140
  54. Khalili-Araghi F., Jogini V., Yarov-Yarovoy V., Tajkhorshid E., Roux B., Schulten K. // Biophys. J. 2010, V.98, P.2189-2198
  55. Vargas E., Bezanilla F., Roux B. // Neuron. 2011, V.72, P.713-720
  56. Jensen M.O., Jogini V., Borhani D.W., Leffler A.E., Dror R.O., Shaw D.E. // Science. 2012, V.336, P.229-233
  57. Yarov-Yarovoy V., DeCaen P.G., Westenbroek R.E., Pan C.Y., Scheuer T., Baker D., Catterall W.A. // Proc. Natl. Acad. Sci. USA. 2012, V.109, P.93-102
  58. Goldstein S.A., Miller C. // Biophys. J. 1992, V.62, P.5-7
  59. Gandhi C.S., Isacoff E.Y. // J. Gen. Physiol. 2002, V.120, P.455-463
  60. Li-Smerin Y., Hackos D.H., Swartz K.J. // Neuron. 2000, V.25, P.411-423
  61. Schonherr R., Mannuzzu L.M., Isacoff E.Y., Heinemann S.H. // Neuron. 2002, V.35, P.935-949
  62. Schoppa N.E., McCormack K., Tanouye M.A., Sigworth F.J. // Science. 1992, V.255, P.1712-1715
  63. Seoh S.A., Sigg D., Papazian D.M., Bezanilla F. // Neuron. 1996, V.16, P.1159-1167
  64. Aggarwal S.K., MacKinnon R. // Neuron. 1996, V.16, P.1169-1177
  65. Starace D.M., Stefani E., Bezanilla F. // Neuron. 1997, V.19, P.1319-1327
  66. Starace D.M., Bezanilla F. // J. Gen. Physiol. 2001, V.117, P.469-490
  67. Larsson H.P., Baker O.S., Dhillon D.S., Isacoff E.Y. // Neuron. 1996, V.16, P.387-397
  68. Baker O.S., Larsson H.P., Mannuzzu L.M., Isacoff E.Y. // Neuron. 1998, V.20, P.1283-1294
  69. Papazian D.M., Shao X.M., Seoh S.A., Mock A.F., Huang Y., Wainstock D.H. // Neuron. 1995, V.14, P.1293-1301
  70. Tiwari-Woodruff S.K., Schulteis C.T., Mock A.F., Papazian D.M. // Biophys. J. 1997, V.72, P.1489-1500
  71. Tiwari-Woodruff S.K., Lin M.A., Schulteis C.T., Papazian D.M. // J. Gen. Physiol. 2000, V.115, P.123-138
  72. Li-Smerin Y., Hackos D.H., Swartz K.J. // J. Gen. Physiol. 2000, V.115, P.33-50
  73. Gandhi C.S., Clark E., Loots E., Pralle A., Isacoff E.Y. // Neuron. 2003, V.40, P.515-525
  74. Elinder F., Mannikko R., Larsson H.P. // J. Gen. Physiol. 2001, V.118, P.1-10
  75. Elinder F., Arhem P., Larsson H.P. // Biophys. J. 2001, V.80, P.1802-1809
  76. Mannuzzu L.M., Moronne M.M., Isacoff E.Y. // Science. 1996, V.271, P.213-216
  77. Yusaf S.P., Wray D., Sivaprasadarao A. // Pflugers Arch. 1996, V.433, P.91-97
  78. Cha A., Ruben P.C., George A.L., Jr. I.O., Fujimoto E., Bezanilla F. // Neuron. 1999, V.22, P.73-87
  79. Glauner K.S., Mannuzzu L.M., Gandhi C.S., Isacoff E.Y. // Nature 1999, V.402, P.813-817
  80. Bezanilla F., Perozo E., Stefani E. // Biophys. J. 1994, V.66, P.1011-1021
  81. Jiang Y., Ruta V., Chen J., Lee A., MacKinnon R. // Nature 2003, V.423, P.42-48
  82. Lee S.Y., Lee A., Chen J., MacKinnon R. // Proc. Natl. Acad. Sci. USA. 2005, V.102, P.15441-15446
  83. Yang N., George A.L., Jr. I.O., Horn R. // Neuron. 1996, V.16, P.113-122
  84. Starace D.M., Bezanilla F. // Nature 2004, V.427, P.548-553
  85. Ahern C.A., Horn R. // J. Gen. Physiol. 2004, V.123, P.205-216
  86. Gonzalez C., Rosenman E., Bezanilla F., Alvarez O., Latorre R. // Proc. Natl. Acad. Sci. USA. 2001, V.98, P.9617-9623
  87. Durell S.R., Shrivastava I.H., Guy H.R. // Biophys. J. 2004, V.87, P.2116-2130
  88. Durell S.R., Hao Y., Guy H.R. // J. Struct. Biol. 1998, V.121, P.263-284
  89. Asamoah O.K., Wuskell J.P., Loew L.M., Bezanilla F. // Neuron. 2003, V.37, P.85-97
  90. Islas L.D., Sigworth F.J. // J. Gen. Physiol. 2001, V.117, P.69-89
  91. Bezanilla F. // Physiol. Rev. 2000, V.80, P.555-592
  92. Jiang Q.X., Wang D.N., MacKinnon R. // Nature 2004, V.430, P.806-810
  93. Neale E.J., Elliott D.J., Hunter M., Sivaprasadarao A. // J. Biol. Chem. 2003, V.278, P.29079-29085
  94. Clayton G.M., Altieri S., Heginbotham L., Unger V.M., Morais-Cabral J.H. // Proc. Natl. Acad. Sci. USA. 2008, V.105, P.1511-1515
  95. Villalba-Galea C.A., Sandtner W., Starace D.M., Bezanilla F. // Proc. Natl. Acad. Sci. USA. 2008, V.105, P.17600-17607
  96. Bjelkmar P., Niemela P.S., Vattulainen I., Lindahl E. // PLoS Comput. Biol. 2009, V.5, P.e1000289
  97. Vieira-Pires R.S., Morais-Cabral J.H. // J. Gen. Physiol. 2010, V.136, P.585-592
  98. Broomand A., Elinder F. // Neuron. 2008, V.59, P.770-777
  99. Chen X., Wang Q., Ni F., Ma J. // Proc. Natl. Acad. Sci. USA. 2010, V.107, P.11352-11357
  100. Tombola F., Pathak M.M., Gorostiza P., Isacoff E.Y. // Nature 2007, V.445, P.546-549
  101. Ramsey I.S., Mokrab Y., Carvacho I., Sands Z.A., Sansom M.S., Clapham D.E. // Nat. Struct. Mol. Biol. 2010, V.17, P.869-875
  102. Wood M.L., Schow E.V., Freites J.A., White S.H., Tombola F., Tobias D.J. // Biochim. Biophys. Acta. 2012, V.1818, P.286-293
  103. Horn R., Ding S., Gruber H.J. // J. Gen. Physiol. 2000, V.116, P.461-476
  104. del Camino D., Kanevsky M., Yellen G. // J. Gen. Physiol. 2005, V.126, P.419-428
  105. Pathak M., Kurtz L., Tombola F., Isacoff E. // J. Gen. Physiol. 2005, V.125, P.57-69
  106. Zagotta W.N., Hoshi T., Aldrich R.W. // J. Gen. Physiol. 1994, V.103, P.321-362
  107. Schmidt D., Jiang Q.X., MacKinnon R. // Nature 2006, V.444, P.775-779
  108. Guy H.R., Seetharamulu P. // Proc. Natl. Acad. Sci. USA. 1986, V.83, P.508-512
  109. Khalili-Araghi F., Jogini V., Yarov-Yarovoy V., Tajkhorshid E., Roux B., Schulten K. // Biophys. J. 2010, V.98, P.2189-2198
  110. Ahern C.A., Horn R. // Neuron. 2005, V.48, P.25-29
  111. Freites J.A., Tobias D.J., White S.H. // Biophys. J. 2006, V.91, №90, P.92
  112. Sands Z.A., Sansom M.S. // Structure. 2007, V.15, P.235-244
  113. Jogini V., Roux B. // Biophys. J. 2007, V.93, P.3070-3082
  114. Tao X., Lee A., Limapichat W., Dougherty D.A., MacKinnon R. // Science. 2010, V.328, P.67-73
  115. Delemotte L., Tarek M., Klein M.L., Amaral C., Treptow W. // Proc. Natl. Acad. Sci. USA. 2011, V.108, P.6109-6114
  116. Henrion U., Zumhagen S., Steinke K., Strutz-Seebohm N., Stallmeyer B., Lang F., Schulze-Bahr E., Seebohm G. // Cell Physiol. Biochem. 2012, V.29, P.809-818
  117. Cole K.S., Moore J.W. // Biophys. J. 1960, V.1, P.1-14
  118. Lin M.C., Hsieh J.Y., Mock A.F., Papazian D.M. // J. Gen. Physiol. 2011, V.138, P.155-163
  119. Tao X., MacKinnon R. // J. Mol. Biol. 2008, V.382, P.24-33
  120. Madin K., Sawasaki T., Kamura N., Takai K., Ogasawara T., Yazaki K., Takei T., Miura K. I., Endo Y. // FEBS Lett. 2004, V.562, P.155-159
  121. Jensen M.O., Borhani D.W., Lindorff-Larsen K., Maragakis P., Jogini V., Eastwood M.P., Dror R.O., Shaw D.E. // Proc. Natl. Acad. Sci. USA. 2010, V.107, P.5833-5838
  122. Schwarz T.L., Tempel B.L., Papazian D.M., Jan Y.N., Jan L.Y. // Nature 1988, V.331, P.137-142
  123. Zhou Y., Morais-Cabral J.H., Kaufman A., MacKinnon R. // Nature 2001, V.414, P.43-48
  124. Berneche S., Roux B. // Proc. Natl. Acad. Sci. USA. 2003, V.100, P.8644-8648
  125. Vargas E., Yarov-Yarovoy V., Khalili-Araghi F., Catterall W.A., Klein M.L., Tarek M., Lindahl E., Schulten K., Perozo E., Bezanilla F. // J. Gen. Physiol. 2012, V.140, P.587-594
  126. Delemotte L., Treptow W., Klein M.L., Tarek M. // Biophys. J. 2010, V.99, P.72-74
  127. Tarek M., Delemotte L. // Acc. Chem. Res. 2013, V.46, P.2755-2762

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