Local and global interpretations of a disease-causing mutation near the ligand entry path in hyperpolarization-activated cAMP-gated channel

Structure

Volumn 20, Issue 12, 2012, Pages 2116-2123

  Xu, Xinping ^a   Marni, Farzana ^a   Wu, Shengjun ^a   Su, Zhuocheng ^a   Musayev, Faik ^a   Shrestha, Sabisha ^a   Xie, Changan ^a   Gao, Weihua ^a   Liu, Qinglian ^a   Zhou, Lei ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; HYPERPOLARIZATION ACTIVATED CYCLIC AMP CHANNEL; ION CHANNEL; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUOROMETRY; LIGAND BINDING; MEMBRANE CHANNEL; MEMBRANE ELECTROPHYSIOLOGY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUTATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN DOMAIN;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYCLIC AMP; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; FLUORESCENCE POLARIZATION; HUMANS; KINETICS; MODELS, MOLECULAR; MUSCLE PROTEINS; MUTATION, MISSENSE; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; XENOPUS;

EID: 84870526279     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.09.017     Document Type: Article

References (42)

1. M. Baruscotti, G. Bottelli, R. Milanesi, J.C. DiFrancesco, and D. DiFrancesco HCN-related channelopathies Pflugers Arch. 460 2010 405 415
2. M. Baruscotti, A. Bucchi, C. Viscomi, G. Mandelli, G. Consalez, T. Gnecchi-Rusconi, N. Montano, K.R. Casali, S. Micheloni, A. Barbuti, and D. Difrancesco Deep bradycardia and heart block caused by inducible cardiac-specific knockout of the pacemaker channel gene Hcn4 Proc Natl Acad Sci USA 108 2011 1705 1710
3. D.C. Bell, H. Yao, R.C. Saenger, J.H. Riley, and S.A. Siegelbaum Changes in local S4 environment provide a voltage-sensing mechanism for mammalian hyperpolarization-activated HCN channels J. Gen. Physiol. 123 2004 5 19
4. C. Biskup, J. Kusch, E. Schulz, V. Nache, F. Schwede, F. Lehmann, V. Hagen, and K. Benndorf Relating ligand binding to activation gating in CNGA2 channels Nature 446 2007 440 443
5. S. Börner, F. Schwede, A. Schlipp, F. Berisha, D. Calebiro, M.J. Lohse, and V.O. Nikolaev FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells Nat. Protoc. 6 2011 427 438
6. H.F. Brown, D. DiFrancesco, and S.J. Noble How does adrenaline accelerate the heart? Nature 280 1979 235 236
7. J.P. Changeux, and S. Edelstein Conformational selection or induced fit? 50 years of debate resolved F1000 Biol Rep. 3 2011 19
8. 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
9. D. Colquhoun Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors Br. J. Pharmacol. 125 1998 924 947
10. D. DiFrancesco, and C. Ojeda Properties of the current if in the sino-atrial node of the rabbit compared with those of the current iK, in Purkinje fibres J. Physiol. 308 1980 353 367
11. R. Gauss, R. Seifert, and U.B. Kaupp Molecular identification of a hyperpolarization-activated channel in sea urchin sperm Nature 393 1998 583 587
12. M.K. Gilson, J.A. Given, B.L. Bush, and J.A. McCammon The statistical-thermodynamic basis for computation of binding affinities: a critical review Biophys. J. 72 1997 1047 1069
13. C.S. Goh, D. Milburn, and M. Gerstein Conformational changes associated with protein-protein interactions Curr. Opin. Struct. Biol. 14 2004 104 109
14. J.V. Halliwell, and P.R. Adams Voltage-clamp analysis of muscarinic excitation in hippocampal neurons Brain Res. 250 1982 71 92
15. O. Hauswirth, D. Noble, and R.W. Tsien Adrenaline: mechanism of action on the pacemaker potential in cardiac Purkinje fibers Science 162 1968 916 917
16. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J Mol Graph. 14 1996 33 38 27-38
17. H. Irisawa, and A. Noma Pacemaker currents in mammalian nodal cells J. Mol. Cell. Cardiol. 16 1984 777 781
18. L.Y. Jan, and Y.N. Jan A superfamily of ion channels Nature 345 1990 672
19. J. Kusch, C. Biskup, S. Thon, E. Schulz, V. Nache, T. Zimmer, F. Schwede, and K. Benndorf Interdependence of receptor activation and ligand binding in HCN2 pacemaker channels Neuron 67 2010 75 85
20. J. Kusch, S. Thon, E. Schulz, C. Biskup, V. Nache, T. Zimmer, R. Seifert, F. Schwede, and K. Benndorf How subunits cooperate in cAMP-induced activation of homotetrameric HCN2 channels Nat. Chem. Biol. 8 2012 162 169
21. M. Lolicato, M. Nardini, S. Gazzarrini, S. Möller, D. Bertinetti, F.W. Herberg, M. Bolognesi, H. Martin, M. Fasolini, and J.A. Bertrand Tetramerization dynamics of C-terminal domain underlies isoform-specific cAMP gating in hyperpolarization-activated cyclic nucleotide-gated channels J. Biol. Chem. 286 2011 44811 44820
22. A. Ludwig, X. Zong, M. Jeglitsch, F. Hofmann, and M. Biel A family of hyperpolarization-activated mammalian cation channels Nature 393 1998 587 591
23. A. Ludwig, S. Herrmann, E. Hoesl, and J. Stieber Mouse models for studying pacemaker channel function and sinus node arrhythmia Prog. Biophys. Mol. Biol. 98 2008 179 185
24. M.E. Mangoni, and J. Nargeot Genesis and regulation of the heart automaticity Physiol. Rev. 88 2008 919 982
25. R. Milanesi, M. Baruscotti, T. Gnecchi-Ruscone, and D. DiFrancesco Familial sinus bradycardia associated with a mutation in the cardiac pacemaker channel N. Engl. J. Med. 354 2006 151 157
26. S. Moosmang, J. Stieber, X. Zong, M. Biel, F. Hofmann, and A. Ludwig Cellular expression and functional characterization of four hyperpolarization- activated pacemaker channels in cardiac and neuronal tissues Eur. J. Biochem. 268 2001 1646 1652
27. D. Noble, and R.W. Tsien The kinetics and rectifier properties of the slow potassium current in cardiac Purkinje fibres J. Physiol. 195 1968 185 214
28. E. Nof, C. Antzelevitch, and M. Glikson The Contribution of HCN4 to normal sinus node function in humans and animal models Pacing Clin. Electrophysiol. 33 2010 100 106
29. A. Noma, and H. Irisawa Membrane currents in the rabbit sinoatrial node cell as studied by the double microelectrode method Pflugers Arch. 364 1976 45 52
30. 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
31. 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
32. J. Stieber, S. Herrmann, S. Feil, J. Löster, R. Feil, M. Biel, F. Hofmann, and A. Ludwig The hyperpolarization-activated channel HCN4 is required for the generation of pacemaker action potentials in the embryonic heart Proc. Natl. Acad. Sci. USA 100 2003 15235 15240
33. J. Stieber, A. Thomer, B. Much, A. Schneider, M. Biel, and F. Hofmann Molecular basis for the different activation kinetics of the pacemaker channels HCN2 and HCN4 J. Biol. Chem. 278 2003 33672 33680
34. G.R. Tibbs, D.T. Liu, B.G. Leypold, and S.A. Siegelbaum A state-independent interaction between ligand and a conserved arginine residue in cyclic nucleotide-gated channels reveals a functional polarity of the cyclic nucleotide binding site J. Biol. Chem. 273 1998 4497 4505
35. S. Vemana, S. Pandey, and H.P. Larsson S4 movement in a mammalian HCN channel J. Gen. Physiol. 123 2004 21 32
36. J. Wang, S. Chen, M.F. Nolan, and S.A. Siegelbaum Activity-dependent regulation of HCN pacemaker channels by cyclic AMP: signaling through dynamic allosteric coupling Neuron 36 2002 451 461
37. S. Wu, Z.V. Vysotskaya, X. Xu, C. Xie, Q. Liu, and L. Zhou State-dependent cAMP binding to functioning HCN channels studied by patch-clamp fluorometry Biophys. J. 100 2011 1226 1232
38. S. Wu, W. Gao, C. Xie, X. Xu, C. Vorvis, F. Marni, A.R. Hackett, Q. Liu, and L. Zhou Inner activation gate in S6 contributes to the state-dependent binding of cAMP in full-length HCN2 channel J. Gen. Physiol. 140 2012 29 39
39. X. Xu, Z.V. Vysotskaya, Q. Liu, and L. Zhou Structural basis for the cAMP-dependent gating in the human HCN4 channel J. Biol. Chem. 285 2010 37082 37091
40. W.N. Zagotta, N.B. Olivier, K.D. Black, E.C. Young, R. Olson, and E. Gouaux Structural basis for modulation and agonist specificity of HCN pacemaker channels Nature 425 2003 200 205
41. L. Zhou, and S.A. Siegelbaum Gating of HCN channels by cyclic nucleotides: residue contacts that underlie ligand binding, selectivity, and efficacy Structure 15 2007 655 670
42. L. Zhou, and S.A. Siegelbaum Pathway and endpoint free energy calculations for cyclic nucleotide binding to HCN channels Biophys. J. 94 2008 L90 L92