Mechanism of allosteric modulation of rod cyclic nucleotide-gated channels

Journal of General Physiology

Volumn 113, Issue 5, 1999, Pages 601-619

  Sunderman, Elizabeth R ^a   Zagotta, William N ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cyclic GMP; Electrophysiology; Ion channel gating; Kinetics; Open probability

Indexed keywords

CYCLIC AMP; CYCLIC GMP; CYCLIC IMP; CYCLIC NUCLEOTIDE; NICKEL;

ALLOSTERISM; ANIMAL CELL; ARTICLE; CATTLE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; LIGAND BINDING; NONHUMAN; OOCYTE; PATCH CLAMP; PHOTORECEPTOR CELL; RETINA ROD; SIGNAL PROCESSING; XENOPUS;

ALGORITHMS; ANIMALS; BINDING SITES; CATTLE; CYCLIC AMP; CYCLIC GMP; CYCLIC IMP; ELECTRIC STIMULATION; ION CHANNEL GATING; ION CHANNELS; LIGANDS; MARKOV CHAINS; MODELS, BIOLOGICAL; NICKEL; PATCH-CLAMP TECHNIQUES; PROTEIN CONFORMATION; RODS (RETINA); XENOPUS LAEVIS;

EID: 0032962379     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.113.5.601     Document Type: Article

References (43)

1. Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Automatic Control. 19:716-723.
2. Baum, L.E., T. Petrie, G. Soules, and N. Weiss. 1970. A maximization technique occurring in the statistical analysis of probabilistic Markov chains. The Annals of Mathematical Statistics. 41:164-171.
3. 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 Publishing Corp., New York. 483-588.
4. Colquhoun, D., and F.J. Sigworth. 1983. Fitting and statistical analysis of single-channel records. In Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum Publishing Corp., New York. 191-264.
5. 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.
6. Gordon, S.E., D.L. Brautigan, and A.L. Zimmerman. 1992. Protein phosphatases modulate the apparent agonist affinity of the light-regulated ion channel in retinal rods. Neuron. 9:739-748.
7. 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.
8. 2+ in cyclic nucleotide-gated channels. Proc. Natl. Acad. Sci. USA. 92:10222-10226.
9. Goulding, E.H., J. Ngai, R.H. Kramer, S. Colicos, R. Axel, S.A. Siegelbaum, and A. Chess. 1992. Molecular cloning and single-channel properties of the cyclic nucleotide-gated channel from catfish olfactory neurons. Neuron. 8:45-58.
10. 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.
11. 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. Pflügers Arch. 391:85-100.
12. Haynes, L.W., A.R. Kay, and K.W. Yau. 1986. Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature. 321:66-70.
13. + channels. Science. 258:1152-1155.
14. 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.
15. Ildefonse, M., and N. Bennett. 1991. Single-channel study of the cGMP-dependent conductance of retinal rods from incorporation of native vesicles into planar lipid bilayers. J. Membr. Biol. 123:133-147.
16. Ildefonse, M., S. Crouzy, and N. Bennett. 1992. Gating of retinal rod cation channel by different nucleotides: comparative study of unitary currents. J. Membr. Biol. 130:91-104.
17. Jan, L.Y., and Y.N. Jan. 1990. A superfamily of ion channels. Nature. 345:672.
18. Karpen, J.W., R.L. Brown, L. Stryer, and D.A. Baylor. 1993. Interactions between divalent cations and the gating machinery of cyclic GMP-activated channels in salamander retinal rods. J. Gen. Physiol. 101:1-25.
19. Karpen, J.W., A.L. Zimmerman, L. Stryer, and D.A. Baylor. 1988a. Gating kinetics of the cyclic-GMP-activated channel of retinal rods: flash photolysis and voltage-jump studies. Proc. Natl. Acad. Sci. USA. 85:1287-1291.
20. Karpen, J.W., A.L. Zimmerman, L. Stryer, and D.A. Baylor. 1988b. Molecular mechanics of the cyclic-GMP-activated channel of retinal rods. Cold Spring Harbor Symp. Quant. Biol. 1:325-332.
21. Kaupp, U.B., T. Niidome, T. Tanabe, S. Terada, W. Bonigk, W. Stühmer, 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.
22. Liu, D.T., G.R. Tibbs, P. Paoletti, and S.A. Siegelbaum, 1998. Constraining ligand-binding site stoichiometry suggests that a cyclic nucleotide-gated channel is composed of two functional dimers. Neuron. 21:235-248.
23. Liu, D.T., G.R. Tibbs, and S.A. Siegelbaum. 1996. Subunit stoichiometry of cyclic nucleotide-gated channels and effects of subunit order on channel function. Neuron. 16:983-990.
24. Molokanova, E., B. Trivedi, A. Savchenko, and R.H. Kramer. 1997. Modulation of rod photoreceptor cyclic nucleotide-gated channels by tyrosine phosphorylation. J. Neurosci. 17:9068-9076.
25. Monod, J., J. Wyman, and J.P. Changeux. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88-118.
26. Paoletti, P., E.C. Young, and S.A. Siegelbaum. 1999. C-linker of cyclic nucleotide-gated channels controls coupling of ligand binding to channel gating. J. Gen. Physiol. 113:17-34.
27. Qin, F., A. Auerbach, and F. Sachs. 1996. Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70:264-280.
28. Qin, F., A. Auerbach, and F. Sachs. 1997. Maximum likelihood estimation of aggregated Markov processes. Proc. R. Soc. Lond. B Biol. Sci. 264:375-383.
29. Root, M.J., and R. MacKinnon. 1994. Two identical noninteracting sites in an ion channel revealed by proton transfer. Science. 265: 1852-1856.
30. + channels suggests that the gating includes transitions through intermediate or secondary states. A mechanism for flickers. J. Gen. Physiol. 111:751-780.
31. Ruiz, M.L., and J.W. Karpen. 1997. Single cyclic nucleotide-gated channels locked in different ligand-bound states. Nature. 389: 389-392.
32. Sigworth, F.J., and S.M. Sine. 1987. Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys. J. 52:1047-1054.
33. Stryer, L. 1987. Visual transduction: design and recurring motifs. Chem. Scr. 27:161-171.
34. Tibbs, G.R., E.H. Goulding, and S.A. Siegelbaum. 1995. Spontaneous opening of cyclic nucleotide-gated channels supports an allosteric model of activation. Biophys. J. 68:A253. (Abstr.)
35. Tibbs, G.R., E.H. Goulding, and S.A. Siegelbaum. 1997. Allosteric activation and tuning of ligand efficacy in cyclic-nucleotide-gated channels. Nature. 386:612-615.
36. 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.
37. Varnum, M.D., and W.N. Zagotta. 1996. Subunit interactions in the activation of cyclic nucleotide-gated channels. Biophys. J. 70: 2667-2679.
38. Venkataramanan, L. 1998. Hidden Markov Modeling of Ion Channel Currents. Ph.D. dissertation. Yale University, New Haven, CT.
39. Venkataramanan, L., R. Kuc, and F.J. Sigworth. 1998a. Identification of hidden Markov models for ion channel currents. Part II: State-dependent excess noise. IEEE Trans. Signal Process. 46:1916-1929.
40. Venkataramanan, L., J.L. Walsh, R. Kuc, and F.J. Sigworth. 1998b. Identification of hidden Markov models for ion channel currents. Part I: Colored background noise. IEEE Trans. Signal Process. 46:1901-1915.
41. Yau, K.W., and D.A. Baylor. 1989. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu. Rev. Neurosci. 12:289-327.
42. 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.
43. Zimmerman, A.L., and D.A. Baylor. 1986. Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature. 321:70-72.