About this Journal Submit a Manuscript Table of Contents
ISRN Molecular Biology
Volume 2012 (2012), Article ID 691341, 10 pages
http://dx.doi.org/10.5402/2012/691341
Review Article

Molecular Determinants of Cav1.2 Calcium Channel Inactivation

Humgenex Inc., Kensington, MD 20895, USA

Received 24 August 2012; Accepted 13 September 2012

Academic Editors: M. W. Berchtold, E. Caffarelli, and H.-C. Lee

Copyright © 2012 Nikolai M. Soldatov. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. M. Bers, “Calcium cycling and signaling in cardiac myocytes,” Annual Review of Physiology, vol. 70, no. 1, pp. 23–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. M. T. Nelson, N. B. Standen, J. E. Brayden, and J. F. Worley, “Noradrenaline contracts arteries by activating voltage-dependent calcium channels,” Nature, vol. 336, no. 6197, pp. 382–385, 1988. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Bading, D. D. Ginty, and M. E. Greenberg, “Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways,” Science, vol. 260, no. 5105, pp. 181–186, 1993. View at Scopus
  4. D. Johnston, S. Williams, D. Jaffe, and R. Gray, “NMDA-receptor-independent long-term potentiation,” Annual Review of Physiology, vol. 54, pp. 489–505, 1992. View at Scopus
  5. C. R. Artalejo, M. E. Adams, and A. P. Fox, “Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells,” Nature, vol. 367, no. 6458, pp. 72–76, 1994. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Carafoli, “Intracellular calcium homeostasis.,” Annual Review of Biochemistry, vol. 56, pp. 395–433, 1987. View at Scopus
  7. V. Flockerzi, H. J. Oeken, and F. Hofmann, “Purification of a functional receptor for calcium-channel blockers from rabbit skeletal-muscle microsomes,” European Journal of Biochemistry, vol. 161, no. 1, pp. 217–224, 1986. View at Scopus
  8. M. Takahashi, M. J. Seagar, J. F. Jones, B. F. X. Reber, and W. A. Catterall, “Subunit structure of dihydropyridine-sensitive calcium channels from skeletal muscle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 15, pp. 5478–5482, 1987. View at Scopus
  9. A. C. Dolphin, “β Subunits of voltage-gated calcium channels,” Journal of Bioenergetics and Biomembranes, vol. 35, no. 6, pp. 599–620, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Klugbauer, E. Marais, and F. Hofmann, “Calcium channel α2δ subunits: differential expression, function, and drug binding,” Journal of Bioenergetics and Biomembranes, vol. 35, no. 6, pp. 639–647, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. Q. Z. Lao, E. Kobrinsky, Z. Liu, and N. M. Soldatov, “Oligomerization of Cavβ subunits is an essential correlate of Ca2+ channel activity,” FASEB Journal, vol. 24, no. 12, pp. 5013–5023, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. H. M. Colecraft, B. Alseikhan, S. X. Takahashi et al., “Novel functional properties of Ca2+ channel β subunits revealed by their expression in adult rat heart cells,” Journal of Physiology, vol. 541, no. 2, pp. 435–452, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Tiwari, Y. Zhang, J. Heller, D. R. Abernethy, and N. M. Soldatov, “Artherosclerosis-related molecular alteration of the human Cav1.2 calcium channel α1C subunit,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 45, pp. 17024–17029, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. N. M. Soldatov, “Genomic structure of human L-type Ca2+ channel,” Genomics, vol. 22, no. 1, pp. 77–87, 1994. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Berjukow, F. Döring, M. Froschmayr, M. Grabner, H. Glossmann, and S. Hering, “Endogenous calcium channels in human embryonic kidney (HEK293) cells,” British Journal of Pharmacology, vol. 118, no. 3, pp. 748–754, 1996. View at Scopus
  16. M. Kurejová, B. Uhrík, Z. Sulová, B. Sedláková, O. Križanová, and L. Lacinová, “Changes in ultrastructure and endogenous ionic channels activity during culture of HEK 293 cell line,” European Journal of Pharmacology, vol. 567, no. 1-2, pp. 10–18, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Meir, D. C. Bell, G. J. Stephens, K. M. Page, and A. C. Dolphin, “Calcium channel β subunit promotes voltage-dependent modulation of α1B by Gβγ,” Biophysical Journal, vol. 79, no. 2, pp. 731–746, 2000. View at Scopus
  18. A. Ravindran, Q. Z. Lao, J. B. Harry, P. Abrahimi, E. Kobrinsky, and N. M. Soldatov, “Calmodulin-dependent gating of Cav1.2 calcium channels in the absence of Cavβ subunits,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 23, pp. 8154–8159, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Kobrinsky, K. J. F. Kepplinger, A. Yu et al., “Voltage-gated rearrangements associated with differential β-subunit modulation of the L-type Ca2+ channel inactivation,” Biophysical Journal, vol. 87, no. 2, pp. 844–857, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Kobrinsky, J.-H. Lee, and N. M. Soldatov, “Selective fluorophore-assisted light inactivation of voltage-gated calcium channels,” Channels, vol. 6, no. 3, pp. 154–156, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Kobrinsky, E. Schwartz, D. R. Abernethy, and N. M. Soldatov, “Voltage-gated mobility of the Ca2+ channel cytoplasmic tails and its regulatory role,” Journal of Biological Chemistry, vol. 278, no. 7, pp. 5021–5028, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Herzig, I. F. Y. Khan, D. Gründemann et al., “Mechanism of Cav1.2 channel modulation by the amino terminus of cardiac β2-subunits,” FASEB Journal, vol. 21, no. 7, pp. 1527–1538, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. W. Y. W. Lew, L. V. Hryshko, and D. M. Bers, “Dihydropyridine receptors are primarily functional L-type calcium channels in rabbit ventricular myocytes,” Circulation Research, vol. 69, no. 4, pp. 1139–1145, 1991. View at Scopus
  24. J. W. Hell, R. E. Westenbroek, C. Warner et al., “Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel α1 subunits,” Journal of Cell Biology, vol. 123, no. 4, pp. 949–962, 1993. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Lipscombe, D. V. Madison, M. Poenie, H. Reuter, R. Y. Tsien, and R. W. Tsien, “Spatial distribution of calcium channels and cytosolic calcium transients in growth cones and cell bodies of sympathetic neurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 7, pp. 2398–2402, 1988. View at Publisher · View at Google Scholar · View at Scopus
  26. R. E. Westenbroek, M. K. Ahlijanian, and W. A. Catterall, “Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons,” Nature, vol. 347, no. 6290, pp. 281–284, 1990. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Franzini-Armstrong, F. Protasi, and P. Tijskens, “The assembly of calcium release units in cardiac muscle,” Annals of the New York Academy of Sciences, vol. 1047, pp. 76–85, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. D. V. Gathercole, D. J. Colling, J. N. Skepper, Y. Takagishi, A. J. Levi, and N. J. Severs, “Immunogold-labeled L-type calcium channels are clustered in the surface plasma membrane overlying junctional sarcoplasmic reticulum in guinea-pig myocytes—implications for excitation-contraction coupling in cardiac muscle,” Journal of Molecular and Cellular Cardiology, vol. 32, no. 11, pp. 1981–1994, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Takagishi, K. Yasui, N. J. Severs, and Y. Murata, “Species-specific difference in distribution of voltage-gated L-type Ca2+ channels of cardiac myocytes,” American Journal of Physiology, vol. 279, no. 6, pp. C1963–C1969, 2000. View at Scopus
  30. G. S. Harms, L. Cognet, P. H. M. Lommerse et al., “Single-molecule imaging of L-type Ca2+ channels in live cells,” Biophysical Journal, vol. 81, no. 5, pp. 2639–2646, 2001. View at Scopus
  31. E. Kobrinsky, P. Abrahimi, S. Q. Duong et al., “Effect of Cavβ subunits on structural organization of Cav1.2 calcium channels,” PLoS ONE, vol. 4, no. 5, Article ID e5587, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. K. S. Lee, E. Marban, and R. W. Tsien, “Inactivation of calcium channels in mammalian heart cells: joint dependence on membrane potential and intracellular calcium,” Journal of Physiology, vol. 364, pp. 395–411, 1985. View at Scopus
  33. X. Zong and F. Hofmann, “Ca2+-dependent inactivation of the class C L-type Ca2+ channel is a property of the α1 subunit,” FEBS Letters, vol. 378, no. 2, pp. 121–125, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. N. M. Soldatov, R. D. Zühlke, A. Bouron, and H. Reuter, “Molecular structures involved in L-type calcium channel inactivation. Role of the carboxyl-terminal region encoded by exons 40–42 in α1C subunit in the kinetics and Ca2+ dependence of inactivation,” Journal of Biological Chemistry, vol. 272, no. 6, pp. 3560–3566, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. N. M. Soldatov, M. Oz, K. A. O'Brien, D. R. Abernethy, and M. Morad, “Molecular determinants of L-type Ca2+ channel inactivation: segment exchange analysis of the carboxyl-terminal cytoplasmic motif encoded by exons 40-42 of the human α1C subunit gene,” Journal of Biological Chemistry, vol. 273, no. 2, pp. 957–963, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. R. D. Zühlke and H. Reuter, “Ca2+-sensitive inactivation of L-type Ca2+ channels depends on multiple cytoplasmic amino acid sequences of the α1C subunit,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 6, pp. 3287–3294, 1998. View at Scopus
  37. B. Z. Peterson, C. D. DeMaria, J. P. Adelman, and D. T. Yue, “Calmodulin is the Ca2+ sensor for Ca2+-dependent inactivation of L-type calcium channels,” Neuron, vol. 22, no. 3, pp. 549–558, 1999. View at Scopus
  38. N. Qin, R. Olcese, M. Bransby, T. Lin, and L. Birnbaumer, “Ca2+-induced inhibition of the cardiac Ca2+ channel depends on calmodulin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 5, pp. 2435–2438, 1999. View at Scopus
  39. R. D. Zühlke, G. S. Pitt, K. Deisseroth, R. W. Tsien, and H. Reuter, “Calmodulin supports both inactivation and facilitation of L-type calcium channels,” Nature, vol. 399, no. 6732, pp. 159–162, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. M. G. Erickson, B. A. Alseikhan, B. Z. Peterson, and D. T. Yue, “Preassociation of calmodulin with voltage-gated Ca2+ channels revealed by FRET in single living cells,” Neuron, vol. 31, no. 6, pp. 973–985, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Pate, J. Mochca-Morales, Y. Wu et al., “Determinants for calmodulin binding on voltage-dependent Ca2+ channels,” Journal of Biological Chemistry, vol. 275, no. 50, pp. 39786–39792, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Romanin, R. Gamsjaeger, H. Kahr et al., “Ca2+ sensors of L-type Ca2+ channel,” FEBS Letters, vol. 487, no. 2, pp. 301–306, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. M. X. Mori, M. G. Erickson, and D. T. Yue, “Functional stoichiometry and local enrichment of calmodulin interacting with Ca2+ channels,” Science, vol. 304, no. 5669, pp. 432–435, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Xiong, Q. K. Kleerekoper, R. He, J. A. Putkey, and S. L. Hamilton, “Sites on calmodulin that interact with the C-terminal tail of Cav1.2 channel,” Journal of Biological Chemistry, vol. 280, no. 8, pp. 7070–7079, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Zhang, I. Dzhura, C. E. Grueter, W. Thiel, R. J. Colbran, and M. E. Anderson, “A dynamic α-β inter-subunit agonist signaling complex is a novel feedback mechanism for regulating L-type Ca2+ channel opening,” FASEB Journal, vol. 19, no. 11, pp. 1573–1575, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. Q. Z. Lao, E. Kobrinsky, J. B. Harry, A. Ravindran, and N. M. Soldatov, “New determinant for the Cavβ2 subunit modulation of the Cav1.2 calcium channel,” Journal of Biological Chemistry, vol. 283, no. 23, pp. 15577–15588, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Kobrinsky, S. Tiwari, V. A. Maltsev et al., “Differential role of the α1C subunit tails in regulation of the Cav1.2 channel by membrane potential, β subunits, and Ca2+ ions,” Journal of Biological Chemistry, vol. 280, no. 13, pp. 12474–12485, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Hering, S. Berjukow, S. Aczél, and E. N. Timin, “Ca2+ channel block and inactivation: common molecular determinants,” Trends in Pharmacological Sciences, vol. 19, no. 11, pp. 439–443, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. N. M. Soldatov, “Ca2+ channel moving tail: link between Ca2+-induced inactivation and Ca2+ signal transduction,” Trends in Pharmacological Sciences, vol. 24, no. 4, pp. 167–171, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Hering, S. Berjukow, S. Sokolov et al., “Molecular determinants of inactivation in voltage-gated Ca2+ channels,” Journal of Physiology, vol. 528, no. 2, pp. 237–249, 2000. View at Scopus
  51. N. M. Soldatov, S. Zhenochin, B. AlBanna, D. R. Abernethy, and M. Morad, “New molecular determinant for inactivation of the human L-type α1C Ca2+ channel,” Journal of Membrane Biology, vol. 177, no. 2, pp. 129–135, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. J. F. Zhang, P. T. Ellinor, R. W. Aldrich, and R. W. Tsien, “Molecular determinants of voltage-dependent inactivation in calcium channels,” Nature, vol. 372, no. 6501, pp. 97–100, 1994. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Shi and N. M. Soldatov, “Molecular determinants of voltage-dependent slow inactivation of the Ca2+ channel,” Journal of Biological Chemistry, vol. 277, no. 9, pp. 6813–6821, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Morad and N. Soldatov, “Calcium channel inactivation: possible role in signal transduction and Ca2+ signaling,” Cell Calcium, vol. 38, no. 3-4, pp. 223–231, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Blumenstein, N. Kanevsky, G. Sahar, R. Barzilai, T. Ivanina, and N. Dascal, “A novel long N-terminal isoform of human L-type Ca2+ channel is up-regulated by protein kinase C,” Journal of Biological Chemistry, vol. 277, no. 5, pp. 3419–3423, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Shistik, T. Ivanina, Y. Blumenstein, and N. Dascal, “Crucial role of N terminus in function of cardiac L-type Ca2+ channel and its modulation by protein kinase C,” Journal of Biological Chemistry, vol. 273, no. 28, pp. 17901–17909, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Ravindran, E. Kobrinsky, Q. Z. Lao, and N. M. Soldatov, “Functional properties of the Cav1.2 calcium channel activated by calmodulin in the absence of α2δ subunits,” Channels, vol. 3, no. 1, pp. 25–31, 2009. View at Scopus
  58. A. Benmocha, L. Almagor, S. Oz, J. A. Hirsch, and N. Dascal, “Characterization of the calmodulin-binding site in the N terminus of Cav1.2 .,” Channels, vol. 3, no. 5, pp. 337–342, 2009. View at Scopus
  59. T. Ivanina, Y. Blumenstein, E. Shistik, R. Barzilai, and N. Dascal, “Modulation of L-type Ca2+ channels by Gβγ and calmodulin via interactions with N and C termini of α1C,” Journal of Biological Chemistry, vol. 275, no. 51, pp. 39846–39854, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. Z. Buraei and J. Yang, “The β subunit of voltage-gated Ca2+ channels,” Physiological Reviews, vol. 90, no. 4, pp. 1461–1506, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Miranda-Laferte, G. Gonzalez-Gutierrez, S. Schmidt et al., “Homodimerization of the Src homology 3 domain of the calcium channel β-subunit drives dynamin-dependent endocytosis,” Journal of Biological Chemistry, vol. 286, no. 25, pp. 22203–22210, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. C. E. Grueter, S. A. Abiria, Y. Wu, M. E. Anderson, and R. J. Colbran, “Differential regulated interactions of calcium/calmodulin-dependent protein kinase II with isoforms of voltage-gated calcium channel β subunits,” Biochemistry, vol. 47, no. 6, pp. 1760–1767, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. O. M. Koval, X. Guan, Y. Wu et al., “Cav1.2β-subunit coordinates CaMKII-triggered cardiomyocyte death and afterdepolarizations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 11, pp. 4996–5000, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. P. Liao, D. Yu, S. Lu et al., “Smooth muscle-selective alternatively spliced exon generates functional variation in Cav1.2 calcium channels,” Journal of Biological Chemistry, vol. 279, no. 48, pp. 50329–50335, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Liao, D. Yu, G. Li et al., “A smooth muscle Cav1.2 calcium channel splice variant underlies hyperpolarized window current and enhanced state-dependent inhibition by nifedipine,” Journal of Biological Chemistry, vol. 282, no. 48, pp. 35133–35142, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. E. Kobrinsky, S. Q. Duong, A. Sheydina, and N. M. Soldatov, “Microdomain organization and frequency-dependence of CREB-dependent transcriptional signaling in heart cells,” FASEB Journal, vol. 25, no. 5, pp. 1544–1555, 2011. View at Publisher · View at Google Scholar · View at Scopus