Pore structure influences gating properties of the T-type Ca2+ channel α1G

Journal of General Physiology

Volumn 121, Issue 6, 2003, Pages 529-540

  Talavera, Karel ^a,c   Janssens, Annelies ^a   Klugbauer, Norbert ^b   Droogmans, Guy ^a   Nilius, Bernd ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTO DE CARDIOLOGÍA Y CIRUGÍA CARDIOVASCULAR   (Cuba)

Author keywords

Activation; CaV3.1; pH; Pore mutant; Selectivity filter

Indexed keywords

ASPARTIC ACID; CADMIUM; CALCIUM CHANNEL T TYPE; CALCIUM ION; GLUTAMIC ACID;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CHANNEL GATING; CONTROLLED STUDY; HUMAN; HUMAN CELL; ION CONDUCTANCE; KINETICS; PH; PROTEIN DOMAIN; PROTON TRANSPORT; REPOLARIZATION; STEADY STATE;

ASPARTIC ACID; CALCIUM CHANNELS, T-TYPE; ELECTROPHYSIOLOGY; GLUTAMIC ACID; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; KIDNEY; KINETICS; MODELS, THEORETICAL; POINT MUTATION; TRANSFECTION;

EID: 0037872659     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200308794     Document Type: Article

References (46)

1. Alvarez, J.L., A. Artiles, K. Talavera, and G. Vassort. 2000. Modulation of voltage-dependent facilitation of the T-type calcium current by sodium ion in isolated frog atrial cells. Pflugers Arch. 441: 39-48.
2. Balser, J.R., H.B. Nuss, N. Chiamvimonvat, M.T. Perez-Garcia, E. Marban, and G.F. Tomaselli. 1996. External pore residue mediates slow inactivation in μ1 rat skeletal muscle sodium channels. J. Physiol. 494:431-442.
3. Becker, D., I. Dreyer, S. Hoth,J.D. Reid, H. Busch, M. Lehnen, K. Palme, and R. Hedrich. 1996. Changes in voltage activation, Cs+ sensitivity and ion permeability in H5 mutants of the plant K+ channel KAT1. Proc. Natl. Acad. Sci. USA. 93:8123-8128.
4. Benitah, J.P., Z. Chen, J.R. Balser, G.F. Tomaselli, and E. Marban. 1999. Molecular dynamics of the sodium channel pore vary with gating: interactions between P-segment motions and inactivation. J. Neurosci. 19:1577-1585.
5. Benitah, J.P., R. Ranjan, T. Yamagishi, M. Janecki, G.E Tomaselli, and E. Marban. 1997. Molecular motions within the pore of voltage-dependent sodium channels. Biophys. J. 73:603-613.
6. Burgess, D.E., O. Crawford, B.P. Delisle, and J. Satin. 2002. Mechanism of inactivation gating of human T-type (low-voltage activated) calcium channels. Biophys. J. 82:1894-1906.
7. Chen, C.F., and P. Hess. 1990. Mechanism of gating of T-type calcium channels. J. Gen. Physiol. 96:603-630.
8. Cloues, R.K., and W.A. Sather. 2000. Permeant ion binding affinity in subconductance states of an L-type Ca2+ channel expressed in Xenopus laevis oocytes. J. Physiol. 524:19-36.
9. Delisle, B.P., and J. Satin. 2000. pH modification of human T-type calcium channel gating. Biophys. J. 78:1895-1905.
10. Droogmans, G., and B. Nilius. 1989. Kinetic properties of the cardiac T-type calcium channel in the guinea-pig. J. Physiol. 419: 627-650.
11. Elinder, F., R. Mannikko, and H.P. Larsson. 2001. S4 charges move close to residues in the pore domain during activation in a K channel. J. Gen. Physiol. 118:1-10.
12. Flynn, G.E.,J.P. Johnson, Jr., and W.N. Zagotta. 2001. Cyclic nucleotide-gated channels: shedding light on the opening of a channel pore. Nat. Rev. Neurosci. 2:643-651.
13. Gandhi, C.S., E. Loots, and E.Y. Isacoff. 2000. Reconstructing voltage sensor-pore interaction from a fluorescence scan of a voltage-gated K+ channel. Neuron. 27:585-595.
14. Heginbotham, L., Z. Lu, T. Abramson, and R. MacKinnon. 1994. Mutations in the K+ channel signature sequence. Biophys. J. 66: 1061-1067.
15. Hilber, K., W. Sandtner, O. Kudlacek, I.W. Glaaser, E. Weisz, J.W. Kyle, R.J. French, H.A. Fozzard, S.C. Dudley, and H. Todt. 2001. The selectivity filter of the voltage-gated sodium channel is involved in channel activation. J. Biol. Chem. 276:27831-27839.
16. Hille, B. 2001. Ion Channels of Excitable Membranes. 3rd edition. Sinauer Associates, Inc., Sunderland, MA. 646-662.
17. Hofmann, E, L. Lacinova, and N. Klugbauer. 1999. Voltage-dependent calcium channels: from structure to function. Rev. Physiol. Biochem. Pharmacol. 139:33-87.
18. Kiss, L., J. LoTurco, and S.J. Korn. 1999. Contribution of the selectivity filter to inactivation in potassium channels. Biophys. J. 76: 253-263.
19. Klugbauer, N., E. Marais, L. Lacinova, and F. Hofmann. 1999. A T-type calcium channel from mouse brain. Pflugers Arch. 437: 710-715.
20. Kuhn, F.J., and N.G. Greeff. 2002. Mutation D384N alters recovery of the immobilized gating charge in rat brain IIA sodium channels. J. Membr. Biol. 185:145-155.
21. Kuo, C.C., and S. Yang. 2001. Recovery from inactivation of t-type Ca2+ channels in rat thalamic neurons. J. Neurosci. 21:1884- 1892.
22. Li-Smerin, Y., D.H. Hackos, and KJ. Swartz. 2000. A localized interaction surface for voltage-sensing domains on the pore domain of a K+ channel. Neuron. 25:411-423.
23. Lopez-Barneo, J., T. Hoshi, S.H. Heinemann, and R.W. Aldrich. 1993. Effects of external cations and mutations in the pore region on C-type inactivation of Shaker potassium channels. Receptors Channels. 1:61-71.
24. Marksteiner, R., P. Schurr, S. Berjukow, E. Margreiter, E. Perez-Reyes, and S. Hering. 2001. Inactivation determinants in segment IIIS6 of Ca(v) 3.1. J. Physiol. 537:27-34.
25. McCleskey, E.W. 1999. Calcium channel permeation: A field in flux. J. Gen. Physiol. 113:765-772.
26. Molina, A., P. Ortega-Saenz, and J. Lopez-Barneo. 1998. Pore mutations alter closing and opening kinetics in Shaker K+ channels. J. Physiol. 509:327-337.
27. Proks, P., C.E. Capener, P. Jones, and F.M. Ashcroft. 2001. Mutations within the P-loop of Kir6.2 modulate the intraburst kinetics of the ATP-sensitive potassium channel. J. Gen. Physiol. 118:341-353.
28. Serrano, J.R., S.R. Dashti, E. Perez-Reyes, and S.W. Jones. 2000. Mg2+ block unmasks Ca2+/Ba2+ selectivity of alpha1G T-type calcium channels. Biophys. J. 79:3052-3062.
29. Serrano, J.R., E. Perez-Reyes, and S.W. Jones. 1999. State-dependent inactivation of the alpha1G T-type calcium channel. J. Gen. Physiol. 114:185-201.
30. Sheng, S., J. Li, K.A. McNulty, T. Kieber-Emmons, and T.R. Kleyman. 2001. Epithelial sodium channel pore region. Structure and role in gating. J. Biol. Chem. 276:1326-1334.
31. Shuba, Y.M., V.I. Teslenko, A.N. Savchenko, and N.H. Pogorelaya. 1991. The effect of permeant ions on single calcium channel activation in mouse neuroblastoma cells: ion-channel interaction. J. Physiol. 443:25-44.
32. Staes, M., K. Talavera, N. Klugbauer, J. Prenen, L. Lacinova, G. Droogmans, F. Hofmann, and B. Nilius. 2001. The amino side of the C-terminus determines fast inactivation of the T-type calcium channel alpha1G. J. Physiol. 530:35-45.
33. Taglialatela, M., G.E. Kirsch, A.M. VanDongen, J.A. Drewe, H.A. Hartmann, R.H. Joho, E. Stefani, and A.M. Brown. 1992. Gating currents from a delayed rectifier K+ channel with altered pore structure and function. Biophys. J. 62:34-36.
34. Talavera, K., M. Staes, A. Janssens, N. Klugbauer, G. Droogmans, F, Hofmann, and B. Nilius. 2001. Aspartate residues of the Glu-Glu- Asp-Asp (EEDD) pore locus control selectivity and permeation of the T-type Ca2+ channel alpha(1G). J. Biol. Chem. 276:45628-45635.
35. v3.1). J. Gen. Physiol. 121:511-528.
36. Tomaselli, G.F., N. Chiamximonvat, H.B. Nuss, J.R. Balser, M.T. Perez-Garcia, R.H. Xu, D.W. Orias, P.H. Backx, and E. Marban. 1995. A mutation in the pore of the sodium channel alters gating. Biophys. J. 68:1814-1827.
37. Townsend, C., H.A. Hartmann, and R. Horn. 1997. Anomalous effect of permeant ion concentration on peak open probability of cardiac Na+ channels. J. Gen. Physiol. 110:11-21.
38. Townsend, C., and R. Horn. 1999. Interaction between the pore and a fast gate of the cardiac sodium channel. J. Gen. Physiol. 113: 321-332.
39. Tytgat,J., B. Nilius, and E. Carmeliet. 1990. Modulation of the T-type cardiac Ca channel by changes in proton concentration. J. Gen. Physiol. 96:973-990.
40. Ugarte, G., F. Perez, and R. Latorre. 1998. How do calcium channels transport calcium ions? Biol. Res. 31:17-32.
41. Varadi, G., M. Strobeck, S. Koch, L. Caglioti, C. Zucchi, and G. Palyi. 1999. Molecular elements of ion permeation and selectivity within calcium channels. Crit. Rev. Biochem. Mol. Biol. 34:181-214.
42. Yatani, A., A. Bahinski, M. Wakamori, S. Tang, Y. Mori, T. Kobayashi, and A. Schwartz. 1994. Alteration of channel characteristics by exchange of pore-forming regions between two structurally related Ca2+ channels. Mol. Cell. Biochem. 140:93-102.
43. Yellen, G. 1998. The moving parts of voltage-gated ion channels. Q. Rev. Biophys. 31:239-295.
44. Yellen, G. 2002. The voltage-gated potassium channels and their relatives. Nature. 419:35-42.
45. Zheng, J., and F.J. Sigworth. 1997. Selectivity changes during activation of mutant Shaker potassium channels. J. Gen. Physiol. 110: 101-117.
46. Zheng, J., and F.J. Sigworth. 1998. Intermediate conductances during deactivation of heteromultimeric Shaker potassium channels. J. Gen. Physiol. 112:457-474.