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Journal of Bioenergetics and Biomembranes

, Volume 35, Issue 6, pp 599–620 | Cite as

β Subunits of Voltage-Gated Calcium Channels

  • Annette C. Dolphin
Article

Abstract

Calcium channel β subunits have marked effects on the trafficking and on several of the biophysical properties of all high voltage activated calcium channels. In this article I shall review information on the different genes, on the structure of the β subunits, and on their differential expression and post-translational modification. Their role in trafficking and assembly of the calcium channel heteromultimer will be described, and I will then review their effects on voltage-dependent and kinetic properties, stressing the differences between palmitoylated β2a and the other β subunits. Evidence for effects on calcium channel pharmacology will also be examined. I shall discuss the hypothesis that β subunits can bind reversibly to calcium channels, and examine their role in the G protein modulation of calcium channels. Finally, I shall describe the consequences of knock-out of different β subunit genes, and describe evidence for the involvement of β subunits in disease.

Calcium channel β subunit palmitoylation phosphorylation trafficking gene targeting G-protein assembly inactivation 

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References

  1. Ball, S. L., Powers, P. A., Shin, H. S., Morgans, C. W., Peachey, N. S., and Gregg, R. G., (2002). Invest. Ophthalmol. Vis. Sci. 43, 1595–1603.PubMedGoogle Scholar
  2. Barclay, J., Balaguero, N., Mione, M., Ackerman, S. L., Letts, V. A., Brodbeck, J., Canti, C., Meir, A., Page, K. M., Kusumi, K., PerezReyes, E., Lander, E. S., Frankel, W. N., Gardiner, R. M., Dolphin, A. C., and Rees, M., (2001). J. Neurosci. 21, 6095–6104.PubMedGoogle Scholar
  3. Beguin, P., Nagashima, K., Gonoi, T., Shibasaki, T., Takahashi, K., Kashima, Y., Ozaki, N., Geering, T., Iwanaga, T., and Seino, S., (2001). Nature, 411, 701–706.PubMedGoogle Scholar
  4. Bell, D. C., Butcher, A. J., Berrow, N. S., Page, K. M., Brust, P. F., Nesterova, A., Stauderman, K. A., Seabrook, G. R., Nurnberg, B., and Dolphin, A. C., (2001). J. Neurophysiol. 85, 816–828.PubMedGoogle Scholar
  5. Berjukow, S., Marksteiner, R., Gapp, F., Sinnegger, M. J., and Hering, S., (2000). J. Biol. Chem. 275, 22114–22120.PubMedGoogle Scholar
  6. Berrou, L., Bernatchez, G., and Parent, L., (2001). Biophys. J. 80, 215–228.Google Scholar
  7. Berrou, L., Klein, H., Bernatchez, G., and Parent, L., (2002). Biophys. J. 83, 1429–1442.PubMedGoogle Scholar
  8. Berrow, N. S., Campbell, V., Fitzgerald, E. G., Brickley, K., and Dolphin, A. C., (1995). J. Physiol. (Lond.), 482, 481–491.Google Scholar
  9. Bichet, D., Cornet, V., Geib, S., Carlier, E., Volsen, S., Hoshi, T., Mori, Y., and De Waard, M., (2000). Neuron, 25, 177–190.PubMedGoogle Scholar
  10. Birnbaumer, L., Qin, N., Olcese, R., Tareilus, E., Platano, D., Costantin, J., and Stefani, E., (1998). J. Bioenerg. Biomembr. 30, 357–375.PubMedGoogle Scholar
  11. Black, J. L., and Lennon, V. A., (1999). Mayo Clin. Proc. 74, 357–361.PubMedGoogle Scholar
  12. Blackstone, C., and Sheng, M., (1999). Cell Calcium, 26, 181–192.PubMedGoogle Scholar
  13. Blair, L. A. C., and Marshall, J., (1997). Neuron, 19, 421–429.PubMedGoogle Scholar
  14. Bogdanov, Y., Brice, N. L., Canti, C., Page, K. M., Li, M., Volsen, S. G., and Dolphin, A. C., (2000). Eur. J. Neurosci. 12, 894–902.PubMedGoogle Scholar
  15. Bourinet, E., Charnet, P., Tomlinson, W. J., Stea, A., Snutch, T. P., and Nargeot, J., (1994). EMBO J. 13, 5032–5039.PubMedGoogle Scholar
  16. Bourinet, E., Soong, T. W., Stea, A., and Snutch, T. P., (1996). Proc. Natl. Acad. Sci. U.S.A. 93, 1486–1491.PubMedGoogle Scholar
  17. Bourinet, E., Soong, T. W., Sutton, K., Slaymaker, S., Mathews, E., Monteil, A., Zamponi, G. W., Nargeot, J., and Snutch, T. P., (1999). Nat. Neurosci. 2, 407–415.PubMedGoogle Scholar
  18. Brice, N. L., Berrow, N. S., Campbell, V., Page, K. M., Brickley, K., Tedder, I., and Dolphin, A. C., (1997). Eur. J. Neurosci. 9, 749–759.PubMedGoogle Scholar
  19. Brice, N. L., and Dolphin, A. C., (1999). J. Physiol. (Lond.), 515, 685–694.Google Scholar
  20. Brodbeck, J., Davies, A., Courtney, J.-M., Meir, A., Balaguero, N., Canti, C., Moss, F. J., Page, K. M., Pratt, W. S., Hunt, S. P., Barclay, J., Rees, M., and Dolphin, A. C., (2002). J. Biol. Chem. 277, 7684–7693.PubMedGoogle Scholar
  21. Burgess, D. L., Jones, J. M., Meisler, M. H., and Noebels, J. L., (1997). Cell, 88, 385–392.PubMedGoogle Scholar
  22. Burks, D. J., Wang, J., Towery, H., Ishibashi, O., Lowe, D., Riedel, H., and White, M. F., (1998). J. Biol. Chem. 273, 31061–31067.PubMedGoogle Scholar
  23. Caddick, S. J., Wang, C. S., Fletcher, C. F., Jenkins, N. A., Copeland, N. G., and Hosford, D. A., (1999). J. Neurophysiol. 81, 2066–2074.PubMedGoogle Scholar
  24. Campbell, V., Berrow, N. S., Fitzgerald, E. M., Brickley, K., and Dolphin, A. C., (1995). J. Physiol. (Lond.), 485, 365–372.Google Scholar
  25. Canti, C., Bogdanov, Y., and Dolphin, A. C., (2000). J. Physiol. (Lond.), 527, 419–432.Google Scholar
  26. Canti, C., Davies, A., Berrow, N. S., Butcher, A. J., Page, K. M., and Dolphin, A. C., (2001). Biophys. J. 81, 1439–1451.PubMedGoogle Scholar
  27. Canti, C., Page, K. M., Stephens, G. J., and Dolphin, A. C., (1999). J. Neurosci. 19, 6855–6864.PubMedGoogle Scholar
  28. Castellano, A., Wei, X., Birnbaumer, L., and Perez-Reyes, E., (1993a). J. Biol. Chem. 268, 12359–12366.PubMedGoogle Scholar
  29. Castellano, A., Wei, X., Birnbaumer, L., and Perez-Reyes, E., (1993b). J. Biol. Chem. 268, 3450–3455.PubMedGoogle Scholar
  30. Cens, T., Restituito, S., Galas, S., and Charnet, P., (1999). J. Biol. Chem. 274, 5483–5490.PubMedGoogle Scholar
  31. Chang, F. C., and Hosey, M. M., (1988). J. Biol. Chem. 263, 18929–18937.PubMedGoogle Scholar
  32. Chapman, M. L., VanDongen, H. M. A., and VanDongen, A. M. J., (1998). Biophys. J. 72, 708–719.Google Scholar
  33. Chien, A. J., Carr, K. M., Shirokov, R. E., Rios, E., and Hosey, M. M., (1996). J. Biol. Chem. 271, 26465–26469.PubMedGoogle Scholar
  34. Chien, A. J., Gao, T., Perez-Reyes, E., and Hosey, M. M., (1998). J. Biol. Chem. 273, 23590–23597.PubMedGoogle Scholar
  35. Chien, A. J., and Hosey, M. M., (1998). J. Bioenerg. Biomembr. 30, 377–386.PubMedGoogle Scholar
  36. Chien, A. J., Zhao, X. L., Shirokov, R. E., Puri, T. S., Chang, C. F., Sun, D., Rios, E., and Hosey, M. M., (1995). J. Biol. Chem. 270, 30036–30044.PubMedGoogle Scholar
  37. Chishti, A. H., (1998). Curr. Opin. Hematol. 5, 116–121.PubMedGoogle Scholar
  38. Cohen, A. R., Woods, D. F., Marfatia, S. M., Walther, Z., Chishti, A. H., Anderson, J. M., and Wood, D. F., (1998). J. Cell Biol. 142, 129–138.PubMedGoogle Scholar
  39. Colecraft, H. M., Alseikhan, B. A., Takahashi, S. X., Chaudhuri, D., Mittman, S., Yegnasubramanian, V., Alvania, R. S., John, D. C., Marban, E., and Yue, D. T., (2002). J. Physiol. 541, 435–452.PubMedGoogle Scholar
  40. Cuadra, A. E., Liu, J., Cheng, T., Hosey, M. M., Nelson, D. J., and Ten Eick, R., (2001). Biophys. J. 80, 618.Google Scholar
  41. De Jongh, K. S., Merrick, D. K., and Catterall, W. A., (1989). Proc. Natl. Acad. Sci. U.S.A. 86, 8585–8589.PubMedGoogle Scholar
  42. De Jongh, K. S., Murphy, B. J., Colvin, A. A., Hell, J. W., Takahashi, M., and Catterall, W. A., (1996). Biochemistry, 35, 10392–10402.PubMedGoogle Scholar
  43. Delmas, P., Abogadie, F. C., Buckley, N. J., and Brown, D. A., (2000). Nat. Neurosci. 3, 670–678.PubMedGoogle Scholar
  44. De Waard, M., and Campbell, K. P., (1995). J. Physiol. (Lond.), 485, 619–634.Google Scholar
  45. De Waard, M., Liu, H. Y., Walker, D., Scott, V. E. S., Gurnett, C. A., and Campbell, K. P., (1997). Nature, 385, 446–450.PubMedGoogle Scholar
  46. De Waard, M., Pragnell, M., and Campbell, K. P., (1994). Neuron, 13, 495–503.PubMedGoogle Scholar
  47. De Waard, M., Scott, V. E. S., Pragnell, M., and Campbell, K. P., (1996). FEBS Lett. 380, 272–276.PubMedGoogle Scholar
  48. De Waard, M., Witcher, D. R., Pragnell, M., Liu, H., and Campbell, K. P., (1995). J. Biol. Chem. 270, 12056–12064.PubMedGoogle Scholar
  49. Dolphin, A. C., (1996). TiNS, 19, 35–43.PubMedGoogle Scholar
  50. Dolphin, A. C., (2003). Pharmacol. Rev. 55, 607–627.PubMedGoogle Scholar
  51. Dolphin, A. C., Wyatt, C. N., Richards, J., Beattie, R. E., Craig, P., Lee, J.-H., Cribbs, L. L., Volsen, S. G., and Perez-Reyes, E., (1999). J. Physiol. 519, 35–45.PubMedGoogle Scholar
  52. Dzhura, I., Kostyuk, P., Lyubanova, O., Naidenov, V., and Shuba, Y., (1994). Neuroreport, 5, 1960–1962.PubMedGoogle Scholar
  53. Escayg, A., De Waard, M., Lee, D. D., Bichet, D., Wolf, P., Mayer, T., Johnston, J., Baloh, R., Sander, T., and Meisler, M. H., (2000). Am. J. Hum. Genet. 66, 1531–1539.PubMedGoogle Scholar
  54. Feldmeyer, D., Melzer, W., Pohl, B., and Zöllner, P., (1992). J. Physiol. 457, 639–653.PubMedGoogle Scholar
  55. Fenwick, E. M., Marty, A., and Neher, E., (1982). J. Physiol. 331, 599–635.PubMedGoogle Scholar
  56. Fitzgerald, E. M., (2000). J. Physiol. 527, 433–444.PubMedGoogle Scholar
  57. Fitzgerald, E. M., (2002). J. Physiol. 543, 425–437.PubMedGoogle Scholar
  58. Fletcher, C. F., Lutz, C. M., O'Sullivan, T. N., Shaughnessy, J. D., Jr., Hawkes, R., Frankel, W. N., Copeland, N. G., and Jenkins, N. A., (1996). Cell, 87, 607–617.PubMedGoogle Scholar
  59. Forsythe, I. D., Tsujimoto, T., Barnes-Davies, M., Cuttle, M. F., and Takahashi, T., (1998). Neuron, 20, 797–807.PubMedGoogle Scholar
  60. Gao, T., Yatani, A., Dell'Acqua, M. L., Sako, H., Green, S. A., Dascal, N., Scott, J. D., and Hosey, M. M., (1997). Neuron, 19, 185–196.PubMedGoogle Scholar
  61. Garcia, R., Carillo, E., Rebelledo, S., Garcia, M., and Sanchez, J., (2002). J. Physiol. Lond. 545, 407–419.PubMedGoogle Scholar
  62. Geib, S., Sandoz, G., Cornet, V., Mabrouk, K., Fund-Saunier, O., Bichet, D., Villaz, M., Hoshi, T., Sabatier, J. M., and De Waard, M., (2002). J. Biol. Chem. 277, 10003–10013.PubMedGoogle Scholar
  63. Gerster, U., Neuhuber, B., Groschner, K., Striessnig, J., and Flucher, B. E., (1999). J. Physiol. 517, 353–368.PubMedGoogle Scholar
  64. Gregg, R. G., Powers, P. A., and Hogan, K., (1993). Genomics, 15, 185–187.PubMedGoogle Scholar
  65. Haase, H., Karczewski, P., Beckert, R., and Krause, E. G., (1993). FEBS Lett. 335, 217–222.PubMedGoogle Scholar
  66. Haase, H., Kresse, A., Hohaus, A., Schulte, H. D., Maier, M., Osterziel, K. J., Lange, P. E., and Morano, I., (1996). J. Mol. Med. 74, 99–104.PubMedGoogle Scholar
  67. Hanlon, M. R., Berrow, N. S., Dolphin, A. C., and Wallace, B. A., (1999). FEBS Lett. 445, 366–370.PubMedGoogle Scholar
  68. Herlitze, S., Garcia, D. E., Mackie, K., Hille, B., Scheuer, T., and Catterall, W. A., (1996). Nature, 380, 258–262.PubMedGoogle Scholar
  69. Herlitze, S., Hockerman, G. H., Scheuer, T., and Catterall, W. A., (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 1512–1516.PubMedGoogle Scholar
  70. Herlitze, S., Zhong, H. J., Scheuer, T., and Catterall, W. A., (2001). Proc. Natl. Acad. Sci. U.S.A. 98, 4699–4704.PubMedGoogle Scholar
  71. Hibino, H., Pironkova, R., Onwumere, O., Rousset, M., Charnet, P., Hudspeth, A. J., and Lesage, F., (2003). Proc. Natl. Acad. Sci. U.S.A. 100, 307–312.PubMedGoogle Scholar
  72. Hofmann, F., Biel, M., and Flockerzi, V., (1994). Annu. Rev. Neurosci. 17, 399–418.PubMedGoogle Scholar
  73. Hohaus, A., Poteser, M., Romanin, C., Klugbauer, N., Hofmann, F., Morano, I., Haase, H., and Groschner, K., (2000). Biochem. J. 348, 657–665.PubMedGoogle Scholar
  74. Hopkins, C. R., (1991). Cell, 66, 827–829.PubMedGoogle Scholar
  75. Hosey, M. M., Chang, F. C., O'Callahan, C. M., and Ptasienski, J., (1989). Ann. N.Y. Acad. Sci. 560, 27–38.PubMedGoogle Scholar
  76. Hoshi, T., and Smith, S. J., (1987). J. Neurosci. 7, 571–580.PubMedGoogle Scholar
  77. Hullin, R., Asmus, F., Ludwig, A., Hersel, J., and Boekstegers, P., (1999). Circulation, 100, 155–163.PubMedGoogle Scholar
  78. Hullin, R., Khan, I. F. Y., Wirtz, S., Mohacsi, P., Varadi, G., Schwartz, A., and Herzig, S., (2003). J. Biol. Chem. 21623–21630.Google Scholar
  79. Hullin, R., Singer-Lahat, D., Freichel, M., Biel, M., Dascal, N., Hofmann, F., and Flockerzi, V., (1992). EMBO J. 11, 885–890.PubMedGoogle Scholar
  80. Huston, E., Cullen, G. P., Burley, J. R., and Dolphin, A. C., (1995). Neuroscience, 68, 465–478.PubMedGoogle Scholar
  81. Jeziorski, M. C., Greenberg, R. M., and Anderson, P. A. V., (1999). Receptors Channels, 6, 375–386.PubMedGoogle Scholar
  82. Jeziorski, M. C., Greenberg, R. M., Clark, K. S., and Anderson, P. A. V., (1998). J. Biol. Chem. 273, 22792–22799.PubMedGoogle Scholar
  83. Johnson, B. D., Brousal, J. P., Peterson, B. Z., Gallombardo, P. A., Hockerman, G. H., Lai, Y., Scheuer, T., and Catterall, W. A., (1997). J. Neurosci. 17, 1243–1255.PubMedGoogle Scholar
  84. Jones, L. P., DeMaria, C. D., and Yue, D. T., (1999). Biophys. J. 76, 2530–2552.PubMedGoogle Scholar
  85. Jones, L. P., Wei, S. K., and Yue, D. T., (1998). J. Gen. Physiol. 112, 125–143.PubMedGoogle Scholar
  86. Josephson, I. R., and Varadi, G., (1996). Biophys. J. 70, 1285–1293.PubMedGoogle Scholar
  87. Kang, M. G., Chen, C. C., Felix, R., Letts, V. A., Frankel, W. N., Mori, Y., and Campbell, K. P., (2001). J. Biol. Chem. 276, 32917–32924PubMedGoogle Scholar
  88. Kistner, U., Garner, C. C., and Linial, M., (1995). FEBS Lett. 359, 159–163.PubMedGoogle Scholar
  89. Kleppisch, T., Pedersen, K., Strübing, C., Bosse-Doenecke, E., Flockerzi, V., Hofmann, F., and Hescheler, J., (1994). EMBO J. 13, 2502–2507.PubMedGoogle Scholar
  90. Klugbauer, N., Dai, S. P., Specht, V., LacinovÁa, L., Marais, E., Bohn, G., and Hofmann, F., (2000). FEBS Lett. 470, 189–197.PubMedGoogle Scholar
  91. Kohn, A. B., Anderson, P. A., Roberts–Misterly, J. M., and Greenberg, R. M., (2001). J. Biol. Chem. 276, 36873–36876.PubMedGoogle Scholar
  92. Lacinova, L., Ludwig, A., Bosse, E., Flockerzi, V., and Hofmann, F., (1995). FEBS Lett. 373, 103–107.PubMedGoogle Scholar
  93. Lee, H. K., and Elmslie, K. S., (2000). J. Neurosci. 20, 3115–3128.Google Scholar
  94. Letts, V. A., Felix, R., Biddlecome, G. H., Arikkath, J., Mahaffey, C. L., Valenzuela, A., Bartlett, F. S., Mori, Y., Campbell, K. P., and Frankel, W. N., (1998). Nat. Genet. 19, 340–347.PubMedGoogle Scholar
  95. Liu, H., De Waard, M., Scott, V. E. S., Gurnett, C. A., Lennon, V. A., and Campbell, K. P., (1996). J. Biol. Chem. 271, 13804–13810.PubMedGoogle Scholar
  96. Ludwig, A., Flockerzi, V., and Hofmann, F., (1997). J. Neurosci. 17, 1339–1349.PubMedGoogle Scholar
  97. Luebke, J. I., Dunlap, K., and Turner, T. J., (1993). Neuron, 11, 895–902.PubMedGoogle Scholar
  98. Masuko, N., Makino, K., Kuwahara, H., Fukunaga, K., Sudo, T., Araki, N., Yamamoto, H., Yamada, Y., Miyamoto, E., and Saya, H., (1999). J. Biol. Chem. 274, 5782–5790.PubMedGoogle Scholar
  99. McEnery, M. W., Copeland, T. D., and Vance, C. L., (1998). J. Biol. Chem. 273, 21435–21438.PubMedGoogle Scholar
  100. Mcgee, A. W., and Bredt, D. S., (1999). J. Biol. Chem. 274, 17431–17436.PubMedGoogle Scholar
  101. Mcgee, A. W., Dakoji, S. R., Olsen, O., Bredt, D. S., Lim, W. A., and Prehoda, K. E., (2001). Mol. Cell, 8, 1291–1301.PubMedGoogle Scholar
  102. McPherson, P. S., (1999). Cell. Signal. 11, 229–238.PubMedGoogle Scholar
  103. Meir, A., Bell, D. C., Stephens, G. J., Page, K. M., and Dolphin, A. C., (2000). Biophys. J. 79, 731–746.PubMedGoogle Scholar
  104. Meir, A., and Dolphin, A. C., (1998). Neuron, 20, 341–351.PubMedGoogle Scholar
  105. Meir, A., and Dolphin, A. C., (2002). Pflugers Arch. 444, 263–275.PubMedGoogle Scholar
  106. Mintz, I. M., Adams, M. E., and Bean, B. P., (1992). Neuron, 9, 85–95.PubMedGoogle Scholar
  107. Moss, F. J., Viard, P., Davies, A., Bertaso, F., Page, K. M., Graham, A., Canti, C., Plumpton, M., Plumpton, M., Clare, J. J., and Dolphin, A. C., (2002). EMBO J. 21, 1514–1523.PubMedGoogle Scholar
  108. Murakami, M., Fleischmann, B., De Felipe, C., Freichel, M., Trost, C., Ludwig, A., Wissenbach, U., Schwegler, H., Hofmann, F., Hescheler, J., Flockerzi, V., and CavaliÁe, A., (2002). J. Biol. Chem. 277, 40342–40351.PubMedGoogle Scholar
  109. Murakami, M., Wissenbach, U., and Flockerzi, V., (1996). Eur. J. Biochem. 236, 138–143.PubMedGoogle Scholar
  110. Namkung, Y., Smith, S. M., Lee, S. B., Skrypnyk, N. V., Kim, H. L., Chin, H., Scheller, R. H., Tsien, R. W., and Shin, H. S., (1998). Proc. Natl. Acad. Sci. U.S.A. 95, 12010–12015.PubMedGoogle Scholar
  111. Neely, A., Wei, X., Olcese, R., Birnbaumer, L., and Stefani, E., (1993). Science, 262, 575–578.Google Scholar
  112. Olcese, R., Neely, A., Qin, N., Wei, X. Y., Birnbaumer, L., and Stefani, E., (1996). J. Physiol. (Lond.), 497, 675–686.Google Scholar
  113. Olcese, R., Qin, N., Schneider, T., Neely, A., Wei, X., Stefani, E., and Birnbaumer, L., (1994). Neuron, 13, 1433–1438.PubMedGoogle Scholar
  114. Park, S. H., Suh, Y. S., Kim, H., Rhyu, I. J., and Kim, H. L., (1997). Mol. Cells, 7, 200–203.PubMedGoogle Scholar
  115. Patil, P. G., De Leon, M., Reed, R. R., Dubel, S., Snutch, T. P., and Yue, D. T., (1996). Biophys. J. 71, 2509–2521.PubMedGoogle Scholar
  116. Perez-Reyes, E., Castellano, A., Kim, H. S., Bertrand, P., Baggstrom, E., Lacerda, A. E., Wei, X., and Birnbaumer, L., (1992). J. Biol. Chem. 267, 1792–1797.PubMedGoogle Scholar
  117. Perez-Reyes, E., and Schneider, T., (1994). Drug Dev. Res. 33, 295–318.Google Scholar
  118. Pietrobon, D., and Hess, P., (1990). Nature, 346, 651–655.PubMedGoogle Scholar
  119. Powers, P. A., Liu, S., Hogan, K., and Gregg, R. G., (1992). J. Biol. Chem. 267, 22967–22972.PubMedGoogle Scholar
  120. Pragnell, M., De Waard, M., Mori, Y., Tanabe, T., Snutch, T. P., and Campbell, K. P., (1994). Nature, 368, 67–70.PubMedGoogle Scholar
  121. Puri, T. S., Gerhardstein, B. L., Zhao, X. L., Ladner, M. B., and Hosey, M. M., (1997). Biochemistry, 36, 9605–9615.PubMedGoogle Scholar
  122. Qin, N., Platano, D., Olcese, R., Costantin, J. L., Stefani, E., and Birnbaumer, L., (1998). Proc. Natl. Acad. Sci. U.S.A. 95, 4690–4695.PubMedGoogle Scholar
  123. Qin, N., Platano, D., Olcese, R., Stefani, E., and Birnbaumer, L., (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 8866–8871.PubMedGoogle Scholar
  124. Raghib, A., Bertaso, F., Davies, A., Page, K. M., Meir, A., Bogdanov, Y., and Dolphin, A. C., (2001). J. Neurosci. 21, 8495–8504.PubMedGoogle Scholar
  125. Regehr, W. G., and Mintz, I. M., (1994). Neuron, 12, 605–613.PubMedGoogle Scholar
  126. Resh, M. D., (1999). Biochim. Biophy. Acta (BBA)—, Mol. Cell Res. 1451, 1–16.Google Scholar
  127. Roche, J. P., and Treistman, S. N., (1998). J. Neurosci. 18, 4883–4890.PubMedGoogle Scholar
  128. Röhrkasten, A., Meyer, H. E., Nastainczyk, W., Sieber, M., and Hofmann, F., (1988). J. Biol. Chem. 263, 15325–15329.PubMedGoogle Scholar
  129. Ruth, P., Röhrkasten, A., Biel, M., Bosse, E., Regulla, S., Meyer, H. E., Flockerzi, V., and Hofmann, F., (1989). Science, 245, 1115–1118.PubMedGoogle Scholar
  130. Schroder, F., Handrock, R., Beuckelmann, D. J., Hirt, S., Hullin, R., Priebe, L., Schwinger, R. H., Weil, J., and Herzig, S., (1998). Circulation, 98, 969–976.PubMedGoogle Scholar
  131. Schwappach, B., Zerangue, N., Jan, Y. N., and Jan, L. Y., (2000). Neuron, 26, 155–167.PubMedGoogle Scholar
  132. Scott, V. E. S., De Waard, M., Liu, H. Y., Gurnett, C. A., Venzke, D. P., Lennon, V. A., and Campbell, K. P., (1996). J. Biol. Chem. 271, 3207–3212.PubMedGoogle Scholar
  133. Sculptoreanu, A., Rotman, E., Takahashi, M., Scheuer, T., and Catterall, W. A., (1993a). Proc. Natl. Acad. Sci. U.S.A. 90, 10135–10139.PubMedGoogle Scholar
  134. Sculptoreanu, A., Scheuer, T., and Catterall, W. A., (1993b). Nature, 364, 240–243.PubMedGoogle Scholar
  135. Sheng, M., and Wyszynski, M., (1997). Bioessays, 19, 847–853.PubMedGoogle Scholar
  136. Shirokov, R., (1999). J. Physiol. 518, 697–703.PubMedGoogle Scholar
  137. Singer, D., Biel, M., Lotan, I., Flockerzi, V., Hofmann, F., and Dascal, N., (1991). Science, 253, 1553–1557.PubMedGoogle Scholar
  138. Spaetgens, R. L., and Zamponi, G. W., (1999). J. Biol. Chem. 274, 22428–22436.PubMedGoogle Scholar
  139. Stephens, G. J., Brice, N. L., Berrow, N. S., and Dolphin, A. C., (1998). J. Physiol. (Lond.), 509, 15–27.Google Scholar
  140. Stephens, G. J., Page, K. M., Bogdanov, Y., and Dolphin, A. C., (2000). J. Physiol. (Lond.), 525, 377–390.Google Scholar
  141. Stotz, S. C., Hamid, J., Spaetgens, R. L., Jarvis, S. E., and Zamponi, G. W., (2000). J. Biol. Chem. 275, 24575–24582.PubMedGoogle Scholar
  142. Strube, C., Beurg, M., Powers, P. A., Gregg, R. G., and Coronado, R., (1996). Biophys. J. 71, 2531–2543.PubMedGoogle Scholar
  143. Takahashi, M., Seager, M. J., Jones, J. F., Reber, B. F. X., and Catterall, W. A., (1987). Proc. Natl. Acad. Sci. U.S.A. 84, 5478–5482.PubMedGoogle Scholar
  144. Takahashi, S. X., Mittman, S., and Colecraft, H. M., (2003). Biophys. J. 84, 3007–3021.PubMedGoogle Scholar
  145. Tanabe, T., Takeshima, H., Mikami, A., Flockerzi, V., Takahashi, H., Kangawa, K., Kojima, M., Matsuo, H., Hirose, T., and Numa, S., (1987). Nature, 328, 313–318.PubMedGoogle Scholar
  146. Tareilus, E., Roux, M., Qin, N., Olcese, R., Zhou, J. M., Stefani, E., and Birnbaumer, L., (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 1703–1708.PubMedGoogle Scholar
  147. Tavares, G. A., Panepucci, E. H., and Brunger, A. T., (2001). Mol. Cell, 8, 1313–1325.PubMedGoogle Scholar
  148. Taviaux, S., Williams, M. E., Harpold, M. M., Nargeot, J., and Lory, P., (1997). Hum. Genet. 100, 151–154.PubMedGoogle Scholar
  149. Toselli, M., Tosetti, P., and Taglietti, V., (1999). Biophys. J. 76, 2560–2574.PubMedGoogle Scholar
  150. Varadi, G., Lory, P., Schultz, D., Varadi, M., and Schwartz, A., (1991). Nature, 352, 159–162.PubMedGoogle Scholar
  151. Viard, P., Exner, T., Maier, U., Mironneau, J., Nurnberg, B., and Macrez, N., (1999). FASEB J. 13, 685–694.PubMedGoogle Scholar
  152. Wakamori, M., Mikala, G., and Mori, Y., (1999). J. Physiol. (Lond.), 517, 659–672.Google Scholar
  153. Walker, D., Bichet, D., Campbell, K. P., and De Waard, M., (1998). J. Biol. Chem. 273, 2361–2367.PubMedGoogle Scholar
  154. Walker, D., Bichet, D., Geib, S., Mori, E., Cornet, V., Snutch, T. P., Mori, Y., and De Waard, M., (1999). J. Biol. Chem. 274, 12383–12390.PubMedGoogle Scholar
  155. Walker, D., and De Waard, M., (1998). TiNS, 21, 148–154.PubMedGoogle Scholar
  156. Wang, Z., Grabner, M., Berjukow, S., Savchenko, A., Glossmann, H., and Hering, S., (1995). J. Physiol. 486, 131–137.PubMedGoogle Scholar
  157. Wei, S. K., Colecraft, H. M., DeMaria, C. D., Peterson, B. Z., Zhang, R., Kohout, T. A., Rogers, T. B., and Yue, D. T., (2000). Circ. Res. 86, 175–184.PubMedGoogle Scholar
  158. Welling, A., Lacinova, L., Donatin, K., Ludwig, A., Bosse, E., Flockerzi, V., and Hofmann, F., (1995). Pflügers Arch. 429, 400–411.Google Scholar
  159. Westenbroek, R. E., Sakurai, T., Elliott, E. M., Hell, J. W., Starr, T. V. B., Snutch, T. P., and Catterall, W. A., (1995). J. Neurosci. 15, 6403–6418.PubMedGoogle Scholar
  160. Witcher, D. R., De Waard, M., Liu, H., Pragnell, M., and Campbell, K. P., (1995). J. Biol. Chem. 270, 18088–18093.PubMedGoogle Scholar
  161. Witcher, D. R., De Waard, M., Sakamoto, J., Franzini-Armstrong, C., Pragnell, M., Kahl, S. D., and Campbell, K. P., (1993). Science, 261, 486–489.PubMedGoogle Scholar
  162. Wu, H., Reissner, C., Kuhlendahl, S., Coblentz, B., Reuver, S., Kindler, S., Gundelfinger, E. D., and Garner, C. C., (2000). EMBO J. 19, 5740–5751.PubMedGoogle Scholar
  163. Wyatt, C. N., Page, K. M., Berrow, N. S., Brice, N. L., and Dolphin, A. C., (1998). J. Physiol. (Lond.), 510, 347–360.Google Scholar
  164. Yamada, Y., Nagashima, M., Tsutsuura, M., Kobayashi, T., Seki, S., Makita, N., Horio, Y., and Tohse, N., (2001). J. Biol. Chem. 276, 47163–47170.PubMedGoogle Scholar
  165. Yamaguchi, H., Hara, M., Strobeck, M., Fukasawa, K., Schwartz, A., and Varadi, G., (1998). J. Biol. Chem. 273, 19348–19356.PubMedGoogle Scholar
  166. Young, K., Lin, S., Sun, L., Lee, E., Modi, M., Hellings, S., Husbands, M., Ozenberger, B., and Franco, R., (1998). Nat. Biotechnol. 16, 946–950.PubMedGoogle Scholar
  167. Zamponi, G. W., and Snutch, T. P., (1998). Proc. Natl. Acad. Sci. U.S.A. 95, 4035–4039.PubMedGoogle Scholar
  168. Zamponi, G. W., Soong, T. W., Bourinet, E., and Snutch, T. P., (1996). J. Neurosci. 16, 2430–2443.PubMedGoogle Scholar
  169. Zhang, J.-F., Ellinor, P. T., Aldrich, R. W., and Tsien, R. W., (1994). Nature, 372, 97–100.PubMedGoogle Scholar
  170. Zheng, J., and Sigworth, F. J., (1998). J. Gen. Physiol. 110, 101–117.Google Scholar

Copyright information

© Plenum Publishing Corporation 2003

Authors and Affiliations

  • Annette C. Dolphin
    • 1
  1. 1.Department of Pharmacology (Medawar Building)LondonUnited Kingdom

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