Regulation of maximal open probability is a separable function of Ca vβ subunit in L-type Ca2+ channel, dependent on NH2 terminus of α1C (Cav1.2α)

Journal of General Physiology

Volumn 128, Issue 1, 2006, Pages 15-36

  Kanevsky, Nataly ^a   Dascal, Nathan ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

VOLTAGE GATED CALCIUM CHANNEL;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BETA CHAIN; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; MATHEMATICAL ANALYSIS; NONHUMAN; OOCYST; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; BARIUM; CADMIUM CHLORIDE; CALCIUM CHANNELS, L-TYPE; CELL MEMBRANE; FEMALE; GENE EXPRESSION; GENETIC VECTORS; MEMBRANE POTENTIALS; MOLECULAR SEQUENCE DATA; MUTATION; OOCYTES; PROTEIN SUBUNITS; RABBITS; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; XENOPUS LAEVIS;

EID: 33745640270     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200609485     Document Type: Article

References (118)

1. 2+ channel: perspectives for new pharmacological targets. J. Pharmacol. Exp. Ther. 300:724-728.
2. + channel. Neuron. 16:1169-1177.
3. 2+ channels. Neuron. 46:891-904.
4. Aldrich, R.W., D.P. Corey, and C.F. Stevens. 1983. A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature. 306:436-441.
5. Altier, C., S.J. Dubel, C. Barrere, S.E. Jarvis, S.C. Stotz, R.L. Spaetgens, J.D. Scott, V. Cornet, M. DeWaard, G.W. Zamponi, et al. 2002. Trafficking of L-type calcium channels mediated by the postsynaptic scaffolding protein AKAP79. J. Biol. Chem. 277:33598-33603.
6. Barrett, C.F., Y.Q. Cao, and R.W. Tsien. 2005. Gating deficiency in a familial hemiplegic migraine type 1 mutant P/Q-type calcium channel. J. Biol. Chem. 280:24064-24071.
7. 2+ channel α1 subunit contains an endoplasmic reticulum retention signal antagonized by the β subunit. Neuron. 25:177-190.
8. Biel, M., R. Hullin, S. Freundner, D. Singer, N. Dascal, V. Flockerzi, and F. Hofmann. 1991. Tissue-specific expression of high-voltage-activated dihydropyridine-sensitive L-type calcium channels. Eur. J. Biochem. 200:81-88.
9. Biel, M., P. Ruth, E. Bosse, R. Hullin, W. Stuhmer, V. Flockerzi, and F. Hofmann. 1990. Primary structure and functional expression of a high voltage activated calcium channel from rabbit lung. FEBS Lett. 269:409-412.
10. Birnbaumer, L., N. Qin, R. Olcese, E. Tareilus, D. Platano, J. Costantin, and E. Stefani. 1998. Structures and functions of calcium channel β subunits. J. Bioenerg. Biomembr. 30:357-375.
11. 2+ channel is up-regulated by protein kinase C. J. Biol. Chem. 277:3419-3423.
12. 1A antibody. Eur. J. Neurosci. 9:749-759.
13. Bunemann, M., B.L. Gerhardstein, T. Gao, and M.M. Hosey. 1999. Functional regulation of L-type calcium channels via protein kinase A-mediated phosphorylation of the β2 subunit. J. Biol. Chem. 274:33851-33854.
14. 1B calcium channels. Biophys. J. 81:1439-1451.
15. 2+ channels. Proc. Natl. Acad. Sci. USA. 102:11230-11235.
16. 1B critical for inhibition of the voltage-dependent calcium channel by Gβγ. J. Neurosci. 19:6855-6864.
17. Castellano, A., X. Wei, L. Birnbaumer, and E. Perez Reyes. 1993. Cloning and expression of a neuronal calcium channel β subunit. J. Biol. Chem. 268:12359-12366.
18. 2+ channels. Annu. Rev. Cell Dev. Biol. 16:521-555.
19. 2+ channels. Nature. 429:675-680.
20. 2a subunit and effects on channel function. J. Biol. Chem. 271:26465-26468.
21. 2a subunit. J. Biol. Chem. 273:23590-23597.
22. 2+ channels. J. Biol. Chem. 270:30036-30044.
23. Chu, P.-J., J.K. Larsen, C.-C. Chen, and P.M. Best. 2004. Distribution and relative expression levels of calcium channel β subunits within the chambers of the rat heart. J. Mol. Cell. Cardiol. 36:423-434.
24. 1d subunit present in cardiac muscle. Am. J. Physiol. 288:H2363-H2374.
25. 2+ channel β subunits revealed by their expression in adult rat heart cells. J. Physiol. 541:435-452.
26. Colquhoun, D., and F.J. Sigworth. 1995. Fitting and statistical analysis of single-channel records. In Single-channel Recording. B. Sakmann and E. Neher, editors. Plenum Press, New York. pp. 483-587.
27. 2+ channels. J. Physiol. 507:93-103.
28. v1.2. Biochem. Biophys. Res. Commun. 296:429-433.
29. Vβ can reconstitute both trafficking and macroscopic conductance of voltage-dependent calcium channels. J. Physiol. 567:757-769.
30. Dascal, N. 1987. The use of Xenopus oocytes for the study of ion channels. CRC Crit. Rev. Biochem. 22:317-387.
31. Dascal, N., and I. Lotan. 1992. Expression of exogenous ion channels and neurotransmitter receptors in RNA-injected Xenopus oocytes. In Protocols in Molecular Neurobiology. Volume 13. A. Longstaff and P. Revest, editors. Humana Press, Totowa, NJ. pp. 205-225.
32. Dascal, N., I. Lotan, E. Karni, and A. Gigi. 1992. Calcium channel currents in Xenopus oocytes injected with rat skeletal muscle RNA. J. Physiol. 450:469-490.
33. De Waard, M., C.A. Gurnett, and K.P. Campbell. 1996. Structural and functional diversity of voltage-activated calcium channels. Ion Channels. 4:41-87.
34. Dolphin, A.C. 2003. β subunits of voltage-gated calcium channels. J. Bioenerg. Biomembr. 35:599-620.
35. Ertel, E.A., K.P. Campbell, M.M. Harpold, F. Hofmann, Y. Mori, E. Perez-Reyes, A. Schwartz, T.P. Snutch, T. Tanabe, L. Birnbaumer, et al. 2000. Nomenclature of voltage-gated calcium channels. Neuron. 25:533-535.
36. 2+ channel-regulated neuronal gene expression. J. Neurobiol. 37:171-189.
37. 1C and β subunits generate the necessary signal for membrane targeting of class C L-type calcium channels. J. Biol. Chem. 274:2137-2144.
38. 1C subunits. J. Biol. Chem. 276:21089-21097.
39. 2+ channels of skeletal muscle. J. Physiol. 545:407-419.
40. 1C subunit are independent functions of the β subunit. J. Physiol. 517:353-368.
41. 1 subunit and eliminates excitation-contraction coupling. Proc. Natl. Acad. Sci. USA. 93:13961-13966.
42. v1.2 channel. J. Biol. Chem. 279:46367-46372.
43. Hille, B. 2002. Ion Channels of Excitable Membranes. Sinauer, Sunderland, MA. 722 pp.
44. 1C-b) by the β2a subunit: a peptide which inhibits binding of β to the I-II linker of α1 induces functional uncoupling. Biochem. J. 348(Pt 3):657-665.
45. Hullin, R., I.F. Khan, S. Wirtz, P. Mohacsi, G. Varadi, A. Schwartz, and S. Herzig. 2003. Cardiac L-type calcium channel β-subunits expressed in human heart have differential effects on single channel characteristics. J. Biol. Chem. 278:21623-21630.
46. Hullin, R., D. Singer-Lahat, M. Freichel, M. Biel, N. Dascal, F. Hofmann, and V. Flockerzi. 1992. Calcium channel β subunit heterogeneity: functional expression of cloned cDNA from heart, aorta and brain. EMBO J. 11:885-890.
47. Isom, L.L., K.S. De Jongh, and W.A. Catterall. 1994. Auxiliary sub units of voltage-gated ion channels. Neuron. 12:1183-1194.
48. 1C. J. Biol. Chem. 275:39846-39854.
49. Jones, S.W. 2002. Calcium channels: when is a subunit not a subunit? J. Physiol. 545:334.
50. 2+ channels. Biophys. J. 70:1285-1293.
51. Jurkat-Rott, K., and F. Lehmann-Horn. 2004. The impact of splice isoforms on voltage-gated calcium channel α1 subunits. J. Physiol. 554:609-619.
52. 1C subunit in a human embryonic kidney cell line. J. Physiol. 492:89-96.
53. Klockner, U., G. Mikala, M. Varadi, G. Varadi, and A. Schwartz. 1995. Involvement of the carboxyl-terminal region of the α1 subunit in voltage-dependent inactivation of cardiac calcium channels. J. Biol. Chem. 270:17306-17310.
54. 2+ channel inactivation. Biophys. J. 87:844-857.
55. Koch, W.J., P.T. Ellinor, and A. Schwartz. 1990. cDNA cloning of a dihydropyridine-sensitive calcium channel from rat aorta. Evidence for the existence of alternatively spliced forms. J. Biol. Chem. 265:17786-17791.
56. Lacinova, L., A. Ludwig, E. Bosse, V. Flockerzi, and F. Hofmann. 1995. The block of the expressed L-type calcium channel is modulated by the β3 subunit. FEBS Lett. 373:103-107.
57. Leroy, J., M.S. Richards, A.J. Butcher, M. Nieto-Rostro, W.S. Pratt, A. Davies, and A.C. Dolphin. 2005. Interaction via a key tryptophan in the I-II linker of N-type calcium channels is required for β1 but not for palmitoylated β2, implicating an additional binding site in the regulation of channel voltage-dependent properties. J. Neurosci. 25:6984-6996.
58. Leuranguer, V., E. Bourinet, P. Lory, and J. Nargeot. 1998. Antisense depletion of β subunits fails to affect T-type calcium channels properties in a neuroblastoma cell line. Neuropharmacology. 37:701-708.
59. + channel determined by construction of multimeric cDNAs. Neuron. 9:861-871.
60. Lipscombe, D., T.D. Helton, and W. Xu. 2004. L-type calcium channels: the low down. J. Neurophysiol. 92:2633-2641.
61. 1 subunit as expressed in mouse L cells. FEBS Lett. 315:167-172.
62. vβ modulatory properties are AID-independent. Nat. Struct. Mol. Biol. 12:372-377.
63. McGee, A.W., D.A. Nunziato, J.M. Maltez, K.E. Prehoda, G.S. Pitt, and D.S. Bredt. 2004. Calcium channel function regulated by the SH3-GK module in β subunits. Neuron. 42:89-99.
64. Mikala, G., I. Bodi, U. Klockner, M. Varadi, G. Varadi, S.E. Koch, and A. Schwartz. 2003. Characterization of auto-regulation of the human cardiac α1 subunit of the L-type calcium channel: importance of the C-terminus. Mol. Cell. Biochem. 250:81-89.
65. Mikami, A., K. Imoto, T. Tanabe, T. Niidome, Y. Mori, H. Takeshima, S. Narumiya, and S. Numa. 1989. Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature. 340:230-233.
66. Mori, Y., T. Friedrich, M.S. Kim, A. Mikami, J. Nakai, P. Ruth, E. Bosse, F. Hofmann, V. Flockerzi, T. Furuichi, et al. 1991. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature. 350:398-402.
67. 2+ channels in neurons. Proc. Natl. Acad. Sci. USA. 95:12010-12015.
68. 1b subunit by size-exclusion chromatography and its role on channel function. J. Biol. Chem. 279:21689-21694.
69. 1C) expressed in Xenopus oocytes. Biophys. J. 66:1895-1903.
70. Neely, A., X. Wei, R. Olcese, L. Birnbaumer, and E. Stefani. 1993. Potentiation by the β subunit of the ratio of the ionic current to the charge movement in the cardiac calcium channel. Science. 262:575-578.
71. Olcese, R., N. Qin, T. Schneider, A. Neely, X. Wei, E. Stefani, and L. Birnbaumer. 1994. The amino terminus of a calcium channel β subunit sets rates of channel inactivation independently of the subunit's effect on activation. Neuron. 13:1433-1438.
72. Opatowsky, Y., C.C. Chen, K.P. Campbell, and J.A. Hirsch. 2004. Structural analysis of the voltage-dependent calcium channel β subunit functional core and its complex with the α1 interaction domain. Neuron. 42:387-399.
73. v1.2 isoforms under the control of distinct 5′ flanking regulatory elements. FEBS Lett. 546:349-354.
74. + channel, GIRK. Neuron. 33:87-99.
75. 1 and β subunits. J. Gen. Physiol. 105:289-305.
76. Perez Reyes, E., A. Castellano, H.S. Kim, P. Bertrand, E. Baggstrom, A.E. Lacerda, X.Y. Wei, and L. Birnbaumer. 1992. Cloning and expression of a cardiac/brain β subunit of the L-type calcium channel. J. Biol. Chem. 267:1792-1797.
77. 1 subunit. Nature. 368:67-70.
78. Qin, N., R. Olcese, J. Zhou, O.A. Cabello, L. Birnbaumer, and E. Stefani. 1996. Identification of a second region of the beta-subunit involved in regulation of calcium channel inactivation. Am. J. Physiol. 271:C1539-C1545.
79. 2+ channel β subunit caused by palmitoylation. Proc. Natl. Acad. Sci. USA. 95:4690-4695.
80. Reuter, H. 1983. Calcium channel modulation by neurotransmitters, enzymes and drugs. Nature. 301:569-574.
81. V1.2 L-type calcium channel different from the principal heart form. Biochem. Biophys. Res. Commun. 302:23-28.
82. Schreibmayer, W., H.A. Lester, and N. Dascal. 1994. Voltage clamp of Xenopus laevis oocytes utilizing agarose cushion electrodes. Pflugers Arch. 426:453-458.
83. Schultz, D., G. Mikala, A. Yatani, D.B. Engle, D.E. Iles, B. Segers, R.J. Sinke, D.O. Weghuis, U. Klockner, M. Wakamori, et al. 1993. Cloning, chromosomal localization, and functional expression of the α1 subunit of the L-type voltage-dependent calcium channel from normal human heart. Proc. Natl. Acad. Sci. USA. 90:6228-6232.
84. + channel, GIRK, in Xenopus oocytes. J. Gen. Physiol. 109:477-490.
85. 2+ channel. J. Biol. Chem. 277:6813-6821.
86. 2+ channel and its modulation by protein kinase C. J. Biol. Chem. 273:17901-17909.
87. 1 protein level. J. Physiol. 489:55-62.
88. 1C subunit: the initial segment is ubiquitous and crucial for protein kinase C modulation, but it is not directly phosphorylated. J. Biol. Chem. 274:31145-31149.
89. Singer, D., M. Biel, I. Lotan, V. Flockerzi, F. Hofmann, and N. Dascal. 1991. The roles of the subunits in the function of the calcium channel. Science. 253:1553-1557.
90. Singer-Lahat, D., N. Dascal, L. Mittelman, S. Peleg, and I. Lotan. 2000. Imaging plasma membrane proteins in large membrane patches of Xenopus oocytes. Pflugers Arch. 440:627-633.
91. Singer-Lahat, D., I. Lotan, M. Biel, V. Flockerzi, F. Hofmann, and N. Dascal. 1994. Cardiac calcium channels expressed in Xenopus oocytes are modulated by dephosphorylation but not by cAMP-dependent phosphorylation. Receptors Channels. 2:215-226.
92. Slish, D.F., D.B. Engle, G. Varadi, I. Lotan, D. Singer, N. Dascal, and A. Schwartz. 1989. Evidence for the existence of a cardiac specific isoform of the α1 subunit of the voltage dependent calcium channel. FEBS Lett. 250:509-514.
93. Snutch, T.P., W.J. Tomlinson, J.P. Leonard, and M.M. Gilbert. 1991. Distinct calcium channels are generated by alternative splicing and are differentially expressed in the mammalian CNS. Neuron. 7:45-57.
94. 2+ channel. Genomics. 22:77-87.
95. Spafford, J.D., J. Van Minnen, P. Larsen, A.B. Smit, N.I. Syed, and G.W. Zamponi. 2004. Uncoupling of calcium channel α1 and β subunits in developing neurons. J. Biol. Chem. 279:41157-41167.
96. Stotz, S.C., and G.W. Zamponi. 2001. Structural determinants of fast inactivation of high voltage-activated Ca2+ channels. Trends Neurosci. 24:176-182.
97. 2+ channels. Cell. Physiol. Biochem. 9:242-269.
98. 2+ transients in skeletal muscle deficient in dihydropyridine receptor β1 subunit. Biophys. J. 71:2531-2543.
99. 2+ channels. Proc. Natl. Acad. Sci. USA. 101:7193-7198.
100. 2+ channels. J. Gen. Physiol. 126:365-377.
101. v1.2 α1 subunit. J. Biol. Chem. 279:44335-44343.
102. Tareilus, E., M. Roux, N. Qin, R. Olcese, J. Zhou, E. Stefani, and L. Birnbaumer. 1997. A Xenopus oocyte β subunit: evidence for a role in the assembly/expression of voltage-gated calcium channels that is separate from its role as a regulatory subunit. Proc. Natl. Acad. Sci. USA. 94:1703-1708.
103. Van Petegem, F., K.A. Clark, F.C. Chatelain, and D.L. Minor Jr. 2004. Structure of a complex between a voltage-gated calcium channel β subunit and an α subunit domain. Nature. 429:671-675.
104. Varadi, G., P. Lory, D. Schultz, M. Varadi, and A. Schwartz. 1991. Acceleration of activation and inactivation by the β subunit of the skeletal muscle calcium channel. Nature. 352:159-162.
105. 2+ channel function and drug action. Trends Pharmacol. Sci. 16:43-49.
106. 1 subunit and the effects of a cardiac β subunit. Biochem. Biophys. Res. Commun. 196:1170-1176.
107. 2+ channel activation. J. Biol. Chem. 274:12383-12390.
108. 2+ channels: role in channel function. Trends Neurosci. 21:148-154.
109. 2+ channel modulation by recombinant auxiliary β subunits expressed in young adult heart cells. Circ. Res. 86:175-184.
110. 1 subunit. J. Biol. Chem. 269:1635-1640.
111. 1C subunit. Receptors Channels. 4:205-215.
112. 2+ channels. J. Biol. Chem. 266:21943-21947.
113. West, A.E., W.G. Chen, M.B. Dalva, R.E. Dolmetsch, J.M. Kornhauser, A.J. Shaywitz, M.A. Takasu, X. Tao, and M.E. Greenberg. 2001. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. USA. 98:11024-11031.
114. 2, and β subunits of a novel human neuronal calcium channel subtype. Neuron. 8:71-84.
115. 1C subunit. J. Biol. Chem. 273:19348-19356.
116. 1C subunit. Biochem. Biophys. Res. Commun. 267:156-163.
117. Yasuda, T., L. Chen, W. Barr, J.E. McRory, R.J. Lewis, D.J. Adams, and G.W. Zamponi. 2004. Auxiliary subunit regulation of high-voltage activated calcium channels expressed in mammalian cells. Eur. J. Neurosci. 20:1-13.
118. ATP channels. Neuron. 22:537-548.