Cooperative and uncooperative cyclic-nucleotide-gated ion channels.

Ion channels gated by cyclic nucleotides serve multiple functions in sensory signaling in diverse cell types ranging from neurons to sperm. Newly discovered members from bacteria and marine invertebrates provide a wealth of structural and functional information on this channel family. A hallmark of classical tetrameric cyclic-nucleotide-gated channels is their cooperative activation by binding of several ligands. By contrast, the new members seem to be uncooperative, and binding of a single ligand molecule suffices to open these channels. These new findings provide a fresh look at the mechanism of allosteric activation of ion channels.

[1]  S. Siegelbaum,et al.  Constraining Ligand-Binding Site Stoichiometry Suggests that a Cyclic Nucleotide–Gated Channel Is Composed of Two Functional Dimers , 1998, Neuron.

[2]  Benoît Roux,et al.  A gate in the selectivity filter of potassium channels. , 2005, Structure.

[3]  U. Kaupp Olfactory signalling in vertebrates and insects: differences and commonalities , 2010, Nature Reviews Neuroscience.

[4]  M. Biel,et al.  Cyclic nucleotide-gated channels. , 2009, Handbook of experimental pharmacology.

[5]  M. de Bono,et al.  Neuronal substrates of complex behaviors in C. elegans. , 2005, Annual review of neuroscience.

[6]  Francisco Bezanilla,et al.  A single charged voltage sensor is capable of gating the Shaker K+ channel , 2009, The Journal of general physiology.

[7]  V. Torre,et al.  Cyclic nucleotide-gated channels. Pore topology studied through the accessibility of reporter cysteines. , 1999 .

[8]  C. Wahl-Schott,et al.  Hyperpolarization-activated cation channels: from genes to function. , 2009, Physiological reviews.

[9]  W. Bönigk,et al.  Subunits act independently in a cyclic nucleotide‐activated K+ channel , 2007, EMBO reports.

[10]  Ganesh S Anand,et al.  cAMP activation of PKA defines an ancient signaling mechanism , 2007, Proceedings of the National Academy of Sciences.

[11]  V. Vacquier,et al.  Sp-tetraKCNG: A novel cyclic nucleotide gated K(+) channel. , 2007, Biochemical and biophysical research communications.

[12]  Bernard Katz,et al.  Interaction at end-plate receptors between different choline derivatives , 1957, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[13]  S. Siegelbaum,et al.  Efficient Coupling of Ligand Binding to Channel Opening by the Binding Domain of a Modulatory (β) Subunit of the Olfactory Cyclic Nucleotide-Gated Channel , 2001, The Journal of general physiology.

[14]  S. Lockery,et al.  Ammonium-Acetate Is Sensed by Gustatory and Olfactory Neurons in Caenorhabditis elegans , 2008, PloS one.

[15]  D. Colquhoun,et al.  Binding, gating, affinity and efficacy: The interpretation of structure‐activity relationships for agonists and of the effects of mutating receptors , 1998, British journal of pharmacology.

[16]  Susan S. Taylor,et al.  RIalpha subunit of PKA: a cAMP-free structure reveals a hydrophobic capping mechanism for docking cAMP into site B. , 2004, Structure.

[17]  K. Yau,et al.  Calmodulin permanently associates with rat olfactory CNG channels under native conditions , 2004, Nature Neuroscience.

[18]  N. Xuong,et al.  Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains , 1995, Science.

[19]  A. Wittinghofer,et al.  Structure and regulation of the cAMP-binding domains of Epac2 , 2003, Nature Structural Biology.

[20]  S. Siegelbaum,et al.  Gating of HCN channels by cyclic nucleotides: residue contacts that underlie ligand binding, selectivity, and efficacy. , 2007, Structure.

[21]  Akihisa Terakita,et al.  Parietal-Eye Phototransduction Components and Their Potential Evolutionary Implications , 2006, Science.

[22]  W. N. Zagotta,et al.  Conformational Changes in S6 Coupled to the Opening of Cyclic Nucleotide-Gated Channels , 2001, Neuron.

[23]  Daniel Ramot,et al.  Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans , 2008, Nature Neuroscience.

[24]  A. Fodor,et al.  Mechanism of Tetracaine Block of Cyclic Nucleotide-gated Channels , 1997, The Journal of general physiology.

[25]  A. Wittinghofer,et al.  Capturing cyclic nucleotides in action: snapshots from crystallographic studies , 2007, Nature Reviews Molecular Cell Biology.

[26]  Thomas A. Steitz,et al.  Structure of catabolite gene activator protein at 2.9 Å resolution suggests binding to left-handed B-DNA , 1981, Nature.

[27]  Benoît Roux,et al.  Molecular determinants of gating at the potassium-channel selectivity filter , 2006, Nature Structural &Molecular Biology.

[28]  W. Bönigk,et al.  Control of ligand specificity in cyclic nucleotide-gated channels from rod photoreceptors and olfactory epithelium. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[29]  U. Kaupp,et al.  Mechanisms of sperm chemotaxis. , 2008, Annual review of physiology.

[30]  Matthew D. Pagel,et al.  The structure of the prokaryotic cyclic nucleotide-modulated potassium channel MloK1 at 16 A resolution. , 2007, Structure.

[31]  María del Pilar Gomez,et al.  Activation of light-dependent K+ channels in ciliary invertebrate photoreceptors involves cGMP but not the IP3/Ca2+ cascade , 1995, Neuron.

[32]  M. Nishiyama,et al.  Cyclic GMP-Gated CNG Channels Function in Sema3A-Induced Growth Cone Repulsion , 2008, Neuron.

[33]  Joel E. Brown,et al.  A K+-selective cGMP-gated ion channel controls chemosensation of sperm , 2006, Nature Cell Biology.

[34]  K. Yau,et al.  Phototransduction Motifs and Variations , 2009, Cell.

[35]  S. Siegelbaum,et al.  Change of Pore Helix Conformational State upon Opening of Cyclic Nucleotide-Gated Channels , 2000, Neuron.

[36]  W. N. Zagotta,et al.  Localization of regions affecting an allosteric transition in cyclic nucleotide-activated channels , 1995, Neuron.

[37]  Sheng Ye,et al.  Atomic structure of a Na+- and K+-conducting channel , 2006, Nature.

[38]  J. W. Karpen,et al.  Single cyclic nucleotide-gated channels locked in different ligand-bound states , 1997, Nature.

[39]  Youxing Jiang,et al.  Structural insight into Ca2+ specificity in tetrameric cation channels , 2007, Proceedings of the National Academy of Sciences.

[40]  Nir Ben-Tal,et al.  Cooperative Transition between Open and Closed Conformations in Potassium Channels , 2008, PLoS Comput. Biol..

[41]  Susan S. Taylor,et al.  The cAMP binding domain: an ancient signaling module. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  H. Fromm,et al.  Cyclic nucleotide‐gated channels in plants , 2007, FEBS letters.

[43]  Matthew D. Pagel,et al.  Ligand binding and activation in a prokaryotic cyclic nucleotide-modulated channel. , 2007, Journal of molecular biology.

[44]  I. Weber,et al.  Predicted structures of the cGMP binding domains of the cGMP-dependent protein kinase: a key alanine/threonine difference in evolutionary divergence of cAMP and cGMP binding sites. , 1989, Biochemistry.

[45]  M. Varnum,et al.  Subunit Configuration of Heteromeric Cone Cyclic Nucleotide-Gated Channels , 2004, Neuron.

[46]  P. Kirchhof,et al.  Cardiac pacemaker function of HCN4 channels in mice is confined to embryonic development and requires cyclic AMP , 2008, The EMBO journal.

[47]  Zhaoyang Feng,et al.  Light-sensitive neurons and channels mediate phototaxis in C. elegans , 2008, Nature Neuroscience.

[48]  Evan Z. Macosko,et al.  Innate Immunity in Caenorhabditis elegans Is Regulated by Neurons Expressing NPR-1/GPCR , 2008, Science.

[49]  F. Müller,et al.  A single negative charge within the pore region of a cGMP-gated channel controls rectification, Ca2+ blockage, and ionic selectivity. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  W. Bönigk,et al.  An Atypical CNG Channel Activated by a Single cGMP Molecule Controls Sperm Chemotaxis , 2009, Science Signaling.

[51]  K. Yau,et al.  An unusual cGMP pathway underlying depolarizing light response of the vertebrate parietal-eye photoreceptor , 1998, Nature Neuroscience.

[52]  E. Kremmer,et al.  Subunit Stoichiometry of the CNG Channel of Rod Photoreceptors , 2002, Neuron.

[53]  Tao Xu,et al.  C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog , 2010, Nature Neuroscience.

[54]  E. Perozo New structural perspectives on K(+) channel gating. , 2002, Structure.

[55]  J. Morais-Cabral,et al.  Structure of the transmembrane regions of a bacterial cyclic nucleotide-regulated channel , 2008, Proceedings of the National Academy of Sciences.

[56]  Adrian O. Olivares,et al.  Structural and energetic analysis of activation by a cyclic nucleotide binding domain. , 2008, Journal of molecular biology.

[57]  W. N. Zagotta,et al.  The carboxyl-terminal region of cyclic nucleotide-modulated channels is a gating ring, not a permeation path. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Jie Zheng,et al.  Stoichiometry and Assembly of Olfactory Cyclic Nucleotide-Gated Channels , 2004, Neuron.

[59]  J. W. Karpen,et al.  Opening Mechanism of a Cyclic Nucleotide–gated Channel Based on Analysis of Single Channels Locked in Each Liganded State , 1999, The Journal of general physiology.

[60]  J. Contreras,et al.  Gating at the selectivity filter in cyclic nucleotide-gated channels , 2008, Proceedings of the National Academy of Sciences.

[61]  Cori Bargmann Comparative chemosensation from receptors to ecology , 2006, Nature.

[62]  S. Siegelbaum,et al.  A Conserved Tripeptide in CNG and HCN Channels Regulates Ligand Gating by Controlling C-Terminal Oligomerization , 2004, Neuron.

[63]  A. Wittinghofer,et al.  Structure of the cyclic-AMP-responsive exchange factor Epac2 in its auto-inhibited state , 2006, Nature.

[64]  Rajeevan Selvaratnam,et al.  Dynamically Driven Ligand Selectivity in Cyclic Nucleotide Binding Domains* , 2009, The Journal of Biological Chemistry.

[65]  M. Trudeau,et al.  Rod Cyclic Nucleotide-Gated Channels Have a Stoichiometry of Three CNGA1 Subunits and One CNGB1 Subunit , 2002, Neuron.

[66]  S. Siegelbaum,et al.  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* , 1998, The Journal of Biological Chemistry.

[67]  J. Bradley,et al.  The Native Rat Olfactory Cyclic Nucleotide-Gated Channel Is Composed of Three Distinct Subunits , 1999, The Journal of Neuroscience.

[68]  W. Hol,et al.  GAF domains: two-billion-year-old molecular switches that bind cyclic nucleotides. , 2002, Molecular interventions.

[69]  W. N. Zagotta,et al.  Absence of Direct Cyclic Nucleotide Modulation of mEAG1 and hERG1 Channels Revealed with Fluorescence and Electrophysiological Methods* , 2009, The Journal of Biological Chemistry.

[70]  C. Kung,et al.  Patch Clamp and Phenotypic Analyses of a Prokaryotic Cyclic Nucleotide-gated K+ Channel Using Escherichia coli as a Host* , 2007, Journal of Biological Chemistry.

[71]  J. Morais-Cabral,et al.  Structural Basis of Ligand Activation in a Cyclic Nucleotide Regulated Potassium Channel , 2004, Cell.

[72]  U. Kaupp,et al.  Molecular identification of a hyperpolarization-activated channel in sea urchin sperm , 1998, Nature.

[73]  P. Schuck,et al.  Use of surface plasmon resonance to probe the equilibrium and dynamic aspects of interactions between biological macromolecules. , 1997, Annual review of biophysics and biomolecular structure.

[74]  A Cyclic Nucleotide Modulated Prokaryotic K+ Channel , 2004, The Journal of general physiology.

[75]  E. C. Young,et al.  Distinct Structural Determinants of Efficacy and Sensitivity in the Ligand-binding Domain of Cyclic Nucleotide-gated Channels* , 2004, Journal of Biological Chemistry.

[76]  W. N. Zagotta,et al.  Molecular mechanism for ligand discrimination of cyclic nucleotide-gated channels , 1995, Neuron.

[77]  C. Bauer,et al.  Physiology of EAG K+ Channels , 2001, The Journal of Membrane Biology.

[78]  C. Altenbach,et al.  High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation , 2008, Proceedings of the National Academy of Sciences.

[79]  F. Bezanilla,et al.  Detection of the Opening of the Bundle Crossing in KcsA with Fluorescence Lifetime Spectroscopy Reveals the Existence of Two Gates for Ion Conduction , 2006, The Journal of general physiology.

[80]  K. Yau,et al.  The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry , 2002, Nature.

[81]  Rich Olson,et al.  Structural basis for modulation and agonist specificity of HCN pacemaker channels , 2003, Nature.

[82]  D. Willbold,et al.  Solution structure of the Mesorhizobium loti K1 channel cyclic nucleotide‐binding domain in complex with cAMP , 2009, EMBO reports.

[83]  W. N. Zagotta,et al.  Subunit interactions in coordination of Ni2+ in cyclic nucleotide-gated channels. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[84]  K. Benndorf,et al.  Relating ligand binding to activation gating in CNGA2 channels , 2007, Nature.

[85]  G. Yellen,et al.  The moving parts of voltage-gated ion channels , 1998, Quarterly Reviews of Biophysics.

[86]  E V Koonin,et al.  Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. , 2001, Journal of molecular biology.

[87]  W. N. Zagotta,et al.  CNG and HCN channels: two peas, one pod. , 2006, Annual review of physiology.

[88]  R. Horn Uncooperative Voltage Sensors , 2009, The Journal of general physiology.

[89]  W. N. Zagotta,et al.  Salt Bridges and Gating in the COOH-terminal Region of HCN2 and CNGA1 Channels , 2004, The Journal of General Physiology.

[90]  Roland Riek,et al.  Conformational dynamics of the KcsA potassium channel governs gating properties , 2007, Nature Structural &Molecular Biology.

[91]  W. N. Zagotta,et al.  A Cysteine Scan of the Inner Vestibule of Cyclic Nucleotide–gated Channels Reveals Architecture and Rearrangement of the Pore , 2003, The Journal of general physiology.

[92]  U. Kaupp,et al.  Cyclic nucleotide-gated ion channels. , 2002, Physiological reviews.