A cysteine scan of the inner vestibule of cyclic nucleotide-gated channels reveals architecture and rearrangement of the pore

Journal of General Physiology

Volumn 121, Issue 6, 2003, Pages 563-582

  Flynn, Galen E ^a   Zagotta, William N ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cyclic nucleotide gated channel; Cysteine; Ion channel gating; Protein structure

Indexed keywords

2 AMINOETHYL METHANETHIOSULFONATE; CYCLIC AMP; CYCLIC GMP; CYCLIC IMP; CYCLIC NUCLEOTIDE; CYSTEINE; ION CHANNEL; PROTEIN; PROTEIN KCSA; PROTEIN MTHK; SHAKER POTASSIUM CHANNEL; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; CYCLIC NUCLEOTIDE GATED CHANNEL; ION CONDUCTANCE; NONHUMAN; OOCYTE; PROTEIN MODIFICATION; PROTEIN STRUCTURE; XENOPUS;

AMINO ACID SEQUENCE; CYCLIC AMP; CYSTEINE; ETHYL METHANESULFONATE; HUMANS; INDICATORS AND REAGENTS; ION CHANNEL GATING; ION CHANNELS; MOLECULAR SEQUENCE DATA; OOCYTES; PATCH-CLAMP TECHNIQUES; PERMEABILITY; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY;

EID: 0037904401     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200308819     Document Type: Article

References (67)

1. Becchetti, A., K. Gamel, and V. Torre. 1999. Cyclic nucleotide-gated channels. Pore topology studied through the accessibility of reporter cysteines. J. Gen. Physiol. 114:377-392.
2. Becchetti, A., and P. Roncaglia. 2000. Cyclic nucleotide-gated channels: intra- and extracellular accessibility to Cd2+ of substituted cysteine residues within the P-loop. Pflugers Arch. 440:556-565.
3. Bucossi, G., M. Nizzari, and V. Torre. 1997. Single-channel properties of ionic channels gated by cyclic nucleotides. Biophys. J. 72: 1165-1181.
4. Burns, M.E., and D.A. Baylor. 2001. Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu. Rev. Neurosci. 24:779-805.
5. Careaga, C.L., and J.J. Falke. 1992. Structure and dynamics of Escherichia coli chemosensory receptors. Engineered sulfhydryl studies. Biophys. J. 62:209-216.
6. Creighton, T.E. 1984. Disulfide bond formation in proteins. Methods Enzymol. 107:305-329.
7. Creighton, T.E. 1993. Proteins: structures and molecular properties, second edition. W.H. Freeman and Company, New York. 6 pp.
8. Doyle, D.A., J. Morais-Cabral, R.A. Pfuetzner, A. Kuo, J.M. Gulbis, S.L. Cohen, B.T. Chait, and R. MacKinnon. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science. 280:69-77.
9. Enkvetchakul, D., G. Loussouarn, E. Makhina, S.L. Shyng, and C.G. Nichols. 2000. The kinetic and physical basis of K(ATP) channel gating: toward a unified molecular understanding. Biophys. J. 78: 2334-2348.
10. Espinosa, F., R. Fleischhauer, A. McMahon, and R.H. Joho. 2001. Dynamic interaction of S5 and S6 during voltage-controlled gating in a potassium channel. J. Gen. Physiol. 118:157-170.
11. Falke,J.J., A.F. Dernburg, D.A. Sternberg, N. Zalkin, D.L. Milligan, and D.E. Koshland, Jr. 1988. Structure of a bacterial sensory receptor. A site-directed sulfhydryl study. J. Biol. Chem. 263:14850-14858.
12. Fesenko, E.E., S.S. Kolesnikov, and A.L. Lyubarsky. 1985. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 313:310-313.
13. 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.
14. Flynn, G.E., and W.N. Zagotta. 2001. Conformational changes in S6 coupled to the opening of cyclic nucleotide-gated channels. Neuron. 30:689-698.
15. Fodor, A.A., S.E. Gordon, and W.N. Zagotta. 1997. Mechanism of tetracaine block of cyclic nucleotide-gated channels. J. Gen. Physiol. 109:3-14.
16. Gordon, S.E., and W.N. Zagotta. 1995a. A histidine residue associated with the gate of the cyclic nucleotide-activated channels in rod photoreceptors. Neuron. 14:177-183.
17. 2+ in cyclic nucleotide-gated channels. Proc. Natl. Acad. Sci. USA. 92:10222-10226.
18. Goulding, E.H., G.R. Tibbs, D. Liu, and S.A. Siegelbaum. 1993. Role of H5 domain in determining pore diameter and ion permeation through cyclic nucleotide-gated channels. Nature. 364: 61-64.
19. Guex, N., and M.C. Peitsch. 1997. SWISS-MODEL and the Swiss PdbViewer: an environment for comparative protein modeling. Electrohoresis. 18:2714-2723.
20. Hackos, D.H., T.H. Chang, and K.J. Swartz. 2002. Scanning the intracellular S6 activation gate in the shaker K+ channel. J. Gen. Physiol. 119:521-532.
21. Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391:85-100.
22. Heginbotham, L., Z. Lu, T. Abramson, and R. MacKinnon. 1994. Mutations in the K+ channel signature sequence. Biophys. J. 66: 1061-1067.
23. Henn, D.K., A. Baumann, and U.B. Kaupp. 1995. Probing the transmembrane topology of cyclic nucleotide-gated ion channels with a gene fusion approach. Proc. Natl. Acad. Sci. USA. 92:7425-7429.
24. Jan, L.Y., and Y.N. Jan. 1990. A superfamily of ion channels. Nature. 345:672.
25. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002a. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:515-522.
26. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002b. The open pore conformation of potassium channels. Nature. 417:523-526.
27. Jin, T., L. Peng, T. Mirshahi, T. Rohacs, K.W. Chan, R. Sanchez, and D.E. Logothetis. 2002. The (beta)gamma subunits of G proteins gate a K(+) channel by pivoted bending of a transmembrane segment. Mol. Cell. 10:469-481.
28. Johnson, J.P., Jr., and W.N. Zagotta. 2001. Rotational movement during cyclic nucleotide-gated channel opening. Nature. 412: 917-921.
29. Kaupp, U.B., T. Niidome, T. Tanabe, S. Terada, W. Bonigk, W. Stuhmer, N.J. Cook, K. Kangawa, H. Matsuo, T. Hirose, et al. 1989. Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature. 342:762-766.
30. Kramer, R.H., and E. Molokanova. 2001. Modulation of cyclicnucleotide-gated channels and regulation of vertebrate phototransduction. J. Exp. Biol. 204:2921-2931.
31. Kraus-Friedmann, N. 2000. Cyclic nucleotide-gated channels in non-sensory organs. Cell Calcium. 27:127-138.
32. Lippiat, J.D., N.B. Standen, and N.W. Davies. 2000. A residue in the intracellular vestibule of the pore is critical for gating and permeation in Ca2+-activated K+ (BKCa) channels. J. Physiol. 529: 131-138.
33. Li-Smerin, Y., D.H. Hackos, and K.J. Swartz. 2000. A localized interaction surface for voltage-sensing domains on the pore domain of a K+ channel. Neuron. 25:411-423.
34. Liu, D.T., G.R. Tibbs, P. Paoletti, and S.A. Siegelbaum. 1998. Constraining ligand-binding site stoichiometry suggests that a cyclicnucleotide-gated channel is composed of two functional dimers. Neuron. 21:235-248.
35. Liu, D.T., G.R. Tibbs, and S.A. Siegelbaum. 1996. Subunit stoichiometry of cyclic nucleotide-gated channels and effects on subunit order on channel function. Neuron. 16:983-990.
36. Liu, J., and S.A. Siegelbaum. 2000. Change of pore helix conformational state upon opening of cyclic nucleotide-gated channels. Neuron. 28:899-909.
37. Loussouarn, G., E.N. Makhina, T. Rose, and C.G. Nichols. 2000. Structure and dynamics of the pore of inwardly rectifying K(ATP) channels. J. Biol. Chem. 275:1137-1144.
38. Loussouarn, G., L.R. Phillips, R. Masia, T. Rose, and C.G. Nichols. 2001. Flexibility of the Kir6.2 inward rectifier K(+) channel pore. Proc. Natl. Acad. Sci. USA. 98:4227-4232.
39. Lu, T., B. Nguyen, X. Zhang, and J. Yang. 1999. Architecture of a K+ channel inner pore revealed by stoichiometric covalent modification. Neuron. 22:571-580.
40. Lu, Z., A.M. Klem, and Y. Ramu. 2002. Coupling between voltage sensors and activation gate in voltage-gated K(+) channels. J. Gen. Physiol. 120:663-676.
41. Matulef, K., G.E. Flynn, and W.N. Zagotta. 1999. Molecular rearrangements in the ligand-binding domain of cyclic nucleotidegated channels. Neuron. 24:443-452.
42. Matulef, K., and W. Zagotta. 2002. Multimerization of the ligand binding domains of cyclic nucleotide-gated channels. Neuron. 36: 93-103.
43. Minor, D.L., Jr., S.J. Masseling, Y.N. Jan, and L.Y. Jan. 1999. Transmembrane structure of an inwardly rectifying potassium channel. Cell. 96:879-891.
44. Molday, R.S., L.L. Molday, A. Dose, L.I. Clark, M. Illing, N.J. Cook, E. Eismann, and U.B. Kaupp. 1991. The cGMP-gated channel of the rod photoreceptor cell: characterization and orientation of the amino terminus. J. Biol. Chem. 266:21917-21922.
45. Molokanova, E., F. Maddox, C.W. Luetje, and R.H. Kram. 1999. Activity-dependent modulation of rod photoreceptor cyclic nucleotide-gated channels mediated by phosphorylation of a specific tyrosine residue. J. Neurosci. 19:4786-4795.
46. Nakamura, T., and G.H. Gold. 1987. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature. 325:442-444.
47. Panchenko, V.A., C.R. Glasser, and M.L. Mayer. 2001. Structural similarities between glutamate receptor channels and K(+) channels examined by scanning mutagenesis. J. Gen. Physiol. 117: 345-360.
48. Roux, B., and R. MacKinnon. 1999. The cavity and pore helices in the KcsA K+ channel: electrostatic stabilization of monovalent cations. Science. 285:100-102.
49. Sadja, R., K. Smadja, N. Alagem, and E. Reuveny. 2001. Coupling Gβγ-dependent activation to channel opening xSa via pore elements in inwardly rectifying potassium channels. Neuron. 29:669-680.
50. Shabb, J.B., and J.D. Corbin. 1992. Cyclic nucleotide-binding domains in proteins having diverse functions. J. Biol. Chem. 267: 5723-5726.
51. Shyng, S., T. Ferrigni, and C.G. Nichols. 1997. Control of rectification and gating of cloned KATP channels by the Kir6.2 subunit. J. Gen. Physiol. 110:141-153.
52. Stotz, S.C., and L.W. Haynes. 1996. Block of the cGMP-gated cation channel of catfish rod and cone photoreceptors by organic cations. Biophys. J. 71:3136-3147.
53. Sun, Z.P., M.H. Akabas, E.H. Goulding, A. Karlin, and S.A. Siegelbaum. 1996. Exposure of residues in the cyclic nucleotide-gated channel pore: P region structure and function in gating. Neuron. 16:141-149.
54. Sunderman, E.R., and W.N. Zagotta. 1999. Mechanism of allosteric modulation of rod cyclic nucleotide-gated channels. J. Gen. Physiol. 113:601-620.
55. Varnum, M.D., K.D. Black, and W.N. Zagotta. 1995. Molecular mechanism for ligand discrimination of cyclic nucleotide-gated channels. Neuron. 15:619-625.
56. Varnum, M.D., and W.N. Zagotta. 1996. Subunit interactions in the activation of cyclic nucleotide-gated channels. Biophys. J. 70: 2667-2679.
57. - channels in Xenopus oocytes. Mol. Pharmacol. 37:720-724.
58. Wohlfart, P., W. Haase, R.S. Molday, and N.J. Cook. 1992. Antibodies against synthetic peptides used to determine the topology and site of glycosylation of the cGMP-gated channel from bovine rod photoreceptors. J. Biol. Chem. 267:644-648.
59. Yau, K.W., and D.A. Baylor. 1989. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu. Rev. Neurosci. 12:289-327.
60. Yi, B.A., Y.F. Lin, Y.N. Jan, and L.Y. Jan. 2001a. Yeast screen for constitutively active mutant G protein-activated potassium channels. Neuron. 29:657-667.
61. Yi, B.A., D.L. Minor, Jr., Y.F. Lin, Y.N. Jan, and L.Y. Jan. 2001b. Controlling potassium channel activities: Interplay between the membrane and intracellular factors. Proc. Natl. Acad. Sci. USA. 98: 11016-11023.
62. Yifrach, O., and R. MacKinnon. 2002. Energetics of pore opening in a voltage-gated K(+) channel. Cell. 111:231-239.
63. Zagotta, W.N., T. Hoshi, and R.W. Aldrich. 1989. Gating of single Shaker potassium channels in Drosophila muscle and in Xenopus oocytes injected with Shaker mRNA. Proc. Natl. Acad. Sci. USA. 86: 7243-7247.
64. Zeidner, G., R. Sadja, and E. Reuveny. 2001. Redox-dependent gating of G protein-coupled inwardly rectifying K+ channels. J. Biol. Chem. 276:35564-35570.
65. Zhou, Y., J.H. Morais-Cabral, A. Kaufman, and R. MacKinnon. 2001. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature. 414:43-48.
66. Zimmerman, A.L., J.W. Karpen, and D.A. Baylor. 1988. Hindered diffusion in excised membrane patches from retinal rod outer segments. Biophys. J. 54:351-355.
67. Zufall, F., and S.D. Munger. 2001. From odor and pheromone transduction to the organization of the sense of smell. Trends Neurosci. 24:191-193.