Pore-to-gate coupling of HCN channels revealed by a pore variant that contributes to gating but not permeation

Biochemical and Biophysical Research Communications

Volumn 327, Issue 4, 2005, Pages 1131-1142

  Azene, Ezana M ^a   Sang, Dongpei ^a   Tsang, Suk Ying ^a   Li, Ronald A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cyclic nucleotide gated; Hyperpolarization activated; Pacemaker

Indexed keywords

MEMBRANE PROTEIN; POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL SURFACE; CHANNEL GATING; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE MODULATED CHANNEL; IMMUNOFLUORESCENCE MICROSCOPY; MEMBRANE CHANNEL; NONHUMAN; OOCYTE; PRIORITY JOURNAL; STEADY STATE;

ALANINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELL MEMBRANE PERMEABILITY; GENE EXPRESSION; ION CHANNEL GATING; ION CHANNELS; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OOCYTES; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; XENOPUS LAEVIS;

EID: 12344302101     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2004.12.127     Document Type: Article

References (53)

1. H.F. Brown, W. Giles, and S.J. Noble Membrane currents underlying activity in frog sinus venosus J. Physiol. 271 1977 783 816
2. D. DiFrancesco Pacemaker mechanisms in cardiac tissue Annu. Rev. Physiol. 55 1993 455 472
3. D. DiFrancesco A new interpretation of the pace-maker current in calf Purkinje fibres J. Physiol. 314 1981 359 376
4. D. DiFrancesco A study of the ionic nature of the pace-maker current in calf Purkinje fibres J. Physiol. 314 1981 377 393
5. R. Gauss, R. Seifert, and U.B. Kaupp Molecular identification of a hyperpolarization-activated channel in sea urchin sperm Nature 393 1998 583 587
6. A. Ludwig, X. Zong, M. Jeglitsch, F. Hofmann, and M. Biel A family of hyperpolarization-activated mammalian cation channels Nature 393 1998 587 591
7. H.C. Pape Queer current and pacemaker: the hyperpolarization-activated cation current in neurons Annu. Rev. Physiol. 58 1996 299 327
8. B. Santoro, D.T. Liu, H. Yao, D. Bartsch, E.R. Kandel, S.A. Siegelbaum, and G.R. Tibbs Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain Cell 93 1998 717 729
9. K. Yanagihara, and H. Irisawa Potassium current during the pacemaker depolarization in rabbit sinoatrial node cell Pflugers Arch. 388 1980 255 260
10. A. Ludwig, X. Zong, J. Stieber, R. Hullin, F. Hofmann, and M. Biel Two pacemaker channels from human heart with profoundly different activation kinetics EMBO J. 18 1999 2323 2329
11. B. Santoro, S. Chen, A. Luthi, P. Pavlidis, G.P. Shumyatsky, G.R. Tibbs, and S.A. Siegelbaum Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS J. Neurosci. 20 2000 5264 5275
12. B. Santoro, and G.R. Tibbs The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels Ann. N.Y. Acad. Sci. 868 1999 741 764
13. W. Shi, R. Wymore, H. Yu, J. Wu, R.T. Wymore, Z. Pan, R.B. Robinson, J.E. Dixon, D. McKinnon, and I.S. Cohen Distribution and prevalence of hyperpolarization-activated cation channel (HCN) mRNA expression in cardiac tissues Circ. Res. 85 1999 e1 e6
14. S. Chen, J. Wang, and S.A. Siegelbaum Properties of hyperpolarization- activated pacemaker current defined by coassembly of HCN1 and HCN2 subunits and basal modulation by cyclic nucleotide J. Gen. Physiol. 117 2001 491 504
15. C. Ulens, and J. Tytgat Functional heteromerization of HCN1 and HCN2 pacemaker channels J. Biol. Chem. 276 2001 6069 6072
16. T. Xue, E. Marban, and R.A. Li Dominant-negative suppression of HCN1- and HCN2-encoded pacemaker currents by an engineered HCN1 construct: insights into structure-function relationships and multimerization Circ. Res. 90 2002 1267 1273
17. R. Mannikko, F. Elinder, and H.P. Larsson Voltage-sensing mechanism is conserved among ion channels gated by opposite voltages Nature 419 2002 837 841
18. G. Yellen The voltage-gated potassium channels and their relatives Nature 419 2002 35 42
19. + conduction and selectivity Science 280 1998 69 77
20. K.S. Shin, C. Maertens, C. Proenza, B.S. Rothberg, and G. Yellen Inactivation in HCN channels results from reclosure of the activation gate: desensitization to voltage Neuron 41 2004 737 744
21. B.S. Rothberg, K.S. Shin, and G. Yellen Movements near the gate of a hyperpolarization-activated cation channel J. Gen. Physiol. 122 2003 501 510
22. J. Chen, J.S. Mitcheson, M. Tristani-Firouzi, M. Lin, and M.C. Sanguinetti The S4-S5 linker couples voltage sensing and activation of pacemaker channels Proc. Natl. Acad. Sci. USA 98 2001 11277 11282
23. B. Hille Ion Channels of Excitable Membranes third ed. 2001 Sinauer Associates, Inc. Sunderland, Massachusetts, USA
24. E. Azene, T. Xue, and R.A. Li Molecular basis of the effects of potassium of heterologously-expressed pacemaker (HCN) channels J. Physiol. 547 542 2003 349 356
25. T. Xue, and R.A. Li An external determinant in the S5-P linker of the pacemaker (HCN) channel identified by sulfhydryl modification J. Biol. Chem. 277 2002 46233 46242
26. E.M. Ogielska, and R.W. Aldrich Functional consequences of a decreased potassium affinity in a potassium channel pore. Ion interactions and C-type inactivation J. Gen. Physiol. 113 1999 347 358
27. V. Marci, C. Proenza, and E.A. Accili Parallel modulation of pacemaker channel deactivation and fully-activated current by extracellular potassium and sodium Biophys. J. 82 2002 277a
28. + channels Science 258 1992 1152 1155
29. L. Heginbotham, and R. MacKinnon The aromatic binding site for tetraethylammonium ion on potassium channels Neuron 8 1992 483 491
30. M.P. Kavanaugh, M.D. Varnum, P.B. Osborne, M.J. Christie, A.E. Busch, J.P. Adelman, and R.A. North Interaction between tetraethylammonium and amino acid residues in the pore of cloned voltage-dependent potassium channels J. Biol. Chem. 266 1991 7583 7587
31. + channels Science 250 1990 276 279
32. J.S. Fan, M. Jiang, W. Dun, T.V. McDonald, and G.N. Tseng Effects of outer mouth mutations on hERG channel function: a comparison with similar mutations in the Shaker channel Biophys. J. 76 1999 3128 3140
33. E. Azene, T. Xue, and R.A. Li Pore variants contribute to the gating but not permeation phenotypes of HCN1-encoded pacemaker channels Suppl. Biophys. J. 84 2003 398
34. R.A. Li, R.G. Tsushima, K. Himmeldirk, D.S. Dime, and P.H. Backx Local anesthetic anchoring to cardiac sodium channels. Implications into tissue-selective drug targeting Circ. Res. 85 1999 88 98
35. T.M. Ishii, M. Takano, and H. Ohmori Determinants of activation kinetics in mammalian hyperpolarization-activated cation channels J. Physiol. (Lond.) 537 2001 93 100
36. D. DiFrancesco Characterization of single pacemaker channels in cardiac sino-atrial node cells Nature 324 1986 470 473
37. G. Maccaferri, M. Mangoni, A. Lazzari, and D. DiFrancesco Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells J. Neurophysiol. 69 1993 2129 2136
38. M.E. Mangoni, and J. Nargeot Properties of the hyperpolarization- activated current (I(f)) in isolated mouse sino-atrial cells Cardiovasc. Res. 52 2001 51 64
39. V. Macri, C. Proenza, E. Agranovich, D. Angoli, and E.A. Accili Separable gating mechanisms in a Mammalian pacemaker channel J. Biol. Chem. 277 2002 35939 35946
40. G. Yellen The moving parts of voltage-gated ion channels Q. Rev. Biophys. 31 1998 239 295
41. A. Becchetti, and K. Gamel The properties of cysteine mutants in the pore region of cyclic-nucleotide-gated channels Pflugers Arch. 438 1999 587 596
42. A. Becchetti, K. Gamel, and V. Torre Cyclic nucleotide-gated channels. Pore topology studied through the accessibility of reporter cysteines J. Gen. Physiol. 114 1999 377 392
43. G. Bucossi, M. Nizzari, and V. Torre Single-channel properties of ionic channels gated by cyclic nucleotides Biophys. J. 72 1997 1165 1181
44. G.E. Flynn, and W.N. Zagotta Conformational changes in S6 coupled to the opening of cyclic nucleotide-gated channels Neuron 30 2001 689 698
45. P. Gavazzo, C. Picco, E. Eismann, U.B. Kaupp, and A. Menini A point mutation in the pore region alters gating, Ca(2+) blockage, and permeation of olfactory cyclic nucleotide-gated channels J. Gen. Physiol. 116 2000 311 326
46. U.B. Kaupp, and R. Seifert Cyclic nucleotide-gated ion channels Physiol. Rev. 82 2002 769 824
47. M.J. Root, and R. MacKinnon Identification of an external divalent cation-binding site in the pore of a cGMP-activated channel Neuron 11 1993 459 466
48. J. Liu, and S.A. Siegelbaum Change of pore helix conformational state upon opening of cyclic nucleotide-gated channels Neuron 28 2000 899 909
49. Y. Jiang, A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon The open pore conformation of potassium channels Nature 417 2002 523 526
50. Y. Jiang, A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon Crystal structure and mechanism of a calcium-gated potassium channel Nature 417 2002 515 522
51. B.S. Rothberg, K.S. Shin, P.S. Phale, and G. Yellen Voltage-controlled gating at the intracellular entrance to a hyperpolarization-activated cation channel J. Gen. Physiol. 119 2002 83 91
52. R.B. Robinson, and S.A. Siegelbaum Hyperpolarization-activated cation currents: from molecules to physiological functions Annu. Rev. Physiol. 65 2003 453 480
53. + channel during gating Neuron 16 1996 859 867