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XFEL structures of the influenza M2 proton channel: Room temperature water networks and insights into proton conduction

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [4];  [4];  [5];  [6];  [2];  [7];  [1];  [8];  [4];  [4];  [9];  [10];  [4];  [6];  [4];  [3];  [11] more »;  [11];  [4];  [12];  [5];  [2];  [1] « less
  1. Department of Pharmaceutical Chemistry, University of California, San Francisco, CA 94158,
  2. Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, CA 94158,
  3. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan,
  4. SPring-8 Angstrom Compact Free Electron Laser (SACLA) Science Research Group, RIKEN SPring-8 Center, Saitama 351-0198, Japan,
  5. Structural Biology Research Center, High Energy Accelerator Research Organization (KEK), Ibaraki 305-0801, Japan,
  6. Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720,
  7. School of Applied and Engineering Physics, Cornell University, Ithaca, NY 14853,
  8. Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA 94305,, Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305,, Department of Neurology and Neurological Sciences, Stanford University, Palo Alto, CA 94304,, Department of Photon Science, Stanford University, Stanford, CA 94305,, Department of Structural Biology, Stanford University, Stanford, CA 94305,
  9. SPring-8 Angstrom Compact Free Electron Laser (SACLA) Science Research Group, RIKEN SPring-8 Center, Saitama 351-0198, Japan,, Division of Food Science and Biotechnology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan,
  10. SPring-8 Angstrom Compact Free Electron Laser (SACLA) Science Research Group, RIKEN SPring-8 Center, Saitama 351-0198, Japan,, Institute for Protein Research, Osaka University, Osaka 565-0871, Japan,
  11. Experimental Instrumentation Team, Japan Synchrotron Radiation Research Institute, Hyogo 679-5198, Japan,
  12. SPring-8 Angstrom Compact Free Electron Laser (SACLA) Science Research Group, RIKEN SPring-8 Center, Saitama 351-0198, Japan,, Department of Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan
+ Show Author Affiliations
Significance

The influenza M2 channel is among the smallest proton-selective channels found in nature. High-resolution structures of this channel further our understanding of how protons are transported across a membrane bilayer through a constricted membrane protein environment. This study also has broader implications for the structural interpretation of water in channels using X-ray crystallographic techniques. Previous crystallographic structure determined using synchrotron radiation with cryocooling were biased by the low temperature, and room temperature data collection was limited by radiation damage. These problems have been avoided through room temperature diffraction at an X-ray free-electron laser (XFEL) source.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
Grant/Contract Number:
AC02-05CH11231; AC02-76SF00515
OSTI ID:
1376273
Alternate ID(s):
OSTI ID: 1417656
OSTI ID: 1439226
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 51 Vol. 114; ISSN 0027-8424
Publisher:
Proceedings of the National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English

References (71)

Crystal structure of the drug-resistant S31N influenza M2 proton channel: Crystal Structure of M2 S31N Proton Channel journal May 2016
Direct Measurement of the Influenza A Virus M2 Protein Ion Channel Activity in Mammalian Cells journal November 1994
Number of water molecules coupled to the transport of sodium, potassium and hydrogen ions via gramicidin, nonactin or valinomycin journal September 1978
The Grotthuss mechanism journal October 1995
The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers journal September 1992
Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import journal October 1991
The Formation and Dynamics of Proton Wires in Channel Environments journal April 2001
Activation of the M2 ion channel of influenza virus: a role for the transmembrane domain histidine residue journal October 1995
Structure and dynamics of a proton wire: a theoretical study of H+ translocation along the single-file water chain in the gramicidin A channel journal July 1996
Ion selectivity and activation of the M2 ion channel of influenza virus journal March 1996
Solid-state NMR characterization of conformational plasticity within the transmembrane domain of the influenza A M2 proton channel journal December 2007
Conformational plasticity of the influenza A M2 transmembrane helix in lipid bilayers under varying pH, drug binding, and membrane thickness journal January 2011
Activation and Proton Transport Mechanism in Influenza A M2 Channel journal November 2013
Influenza Virus M2 Protein Mediates ESCRT-Independent Membrane Scission journal September 2010
Dynamic Short Hydrogen Bonds in Histidine Tetrad of Full-Length M2 Proton Channel Reveal Tetrameric Structural Heterogeneity and Functional Mechanism journal December 2015
pH-Dependent Tetramerization and Amantadine Binding of the Transmembrane Helix of M2 from the Influenza A Virus † journal November 2000
Proton Association Constants of His 37 in the Influenza-A M2 18–60 Dimer-of-Dimers journal September 2014
Functional Studies and Modeling of Pore-Lining Residue Mutants of the Influenza A Virus M2 Ion Channel journal February 2010
The Mechanism of Hydrated Proton Transport in Water journal December 2000
Kinetic Analysis of the M2 Proton Conduction of the Influenza Virus journal December 2010
NMR Detection of pH-Dependent Histidine–Water Proton Exchange Reveals the Conduction Mechanism of a Transmembrane Proton Channel journal October 2011
Influenza Virus A M2 Protein Generates Negative Gaussian Membrane Curvature Necessary for Budding and Scission journal September 2013
The Influenza M2 Cytoplasmic Tail Changes the Proton-Exchange Equilibria and the Backbone Conformation of the Transmembrane Histidine Residue to Facilitate Proton Conduction journal April 2015
Multiple Proton Confinement in the M2 Channel from the Influenza A Virus journal October 2010
A Secondary Gate As a Mechanism for Inhibition of the M2 Proton Channel by Amantadine journal July 2008
Potential for biomolecular imaging with femtosecond X-ray pulses journal August 2000
Structural basis for the function and inhibition of an influenza virus proton channel journal January 2008
Structure and mechanism of the M2 proton channel of influenza A virus journal January 2008
Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers journal February 2010
Femtosecond X-ray protein nanocrystallography journal February 2011
Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography journal February 2014
Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements journal December 2011
Preparation of microcrystals in lipidic cubic phase for serial femtosecond crystallography journal August 2014
Controlling influenza virus replication by inhibiting its proton channel journal January 2007
A Theory of Water and Ionic Solution, with Particular Reference to Hydrogen and Hydroxyl Ions journal August 1933
Biomolecular cryocrystallography: Structural changes during flash-cooling journal March 2004
Histidines, heart of the hydrogen ion channel from influenza A virus: Toward an understanding of conductance and proton selectivity journal April 2006
Molecular dynamics calculations suggest a conduction mechanism for the M2 proton channel from influenza A virus journal January 2009
Identification of the functional core of the influenza A virus A/M2 proton-selective ion channel journal July 2009
Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus journal August 2010
Proton and cation transport activity of the M2 proton channel from influenza A virus journal August 2010
Tidal surge in the M2 proton channel, sensed by 2D IR spectroscopy journal March 2011
Structure and inhibition of the drug-resistant S31N mutant of the M2 ion channel of influenza A virus journal January 2013
Multiscale simulation reveals a multifaceted mechanism of proton permeation through the influenza A M2 proton channel journal June 2014
High-resolution structures of the M2 channel from influenza A virus reveal dynamic pathways for proton stabilization and transduction journal November 2015
Acid activation mechanism of the influenza A M2 proton channel journal October 2016
Molecular mechanisms for proton transport in membranes. journal January 1978
Permeation and Activation of the M 2 Ion Channel of Influenza A Virus journal July 2000
The Gate of the Influenza Virus M 2 Proton Channel Is Formed by a Single Tryptophan Residue journal August 2002
Interaction of ions and water in gramicidin A channels: streaming potentials across lipid bilayer membranes journal September 1978
Radiation damage in protein serial femtosecond crystallography using an x-ray free-electron laser journal December 2011
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
New Python-based methods for data processing journal June 2013
Breaking the indexing ambiguity in serial crystallography journal December 2013
Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data journal May 2014
Data processing pipeline for serial femtosecond crystallography at SACLA journal April 2016
Diverse application platform for hard X-ray diffraction in SACLA (DAPHNIS): application to serial protein crystallography using an X-ray free-electron laser journal April 2015
High-density grids for efficient data collection from multiple crystals journal January 2016
Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. journal July 1996
Mechanisms of Proton Conduction and Gating in Influenza M2 Proton Channels from Solid-State NMR journal October 2010
Insight into the Mechanism of the Influenza A Proton Channel from a Structure in a Lipid Bilayer journal October 2010
Linking Crystallographic Model and Data Quality journal May 2012
Distinct Domains of the Influenza A Virus M2 Protein Cytoplasmic Tail Mediate Binding to the M1 Protein and Facilitate Infectious Virus Production journal July 2006
The Amphipathic Helix of Influenza A Virus M2 Protein Is Required for Filamentous Bud Formation and Scission of Filamentous and Spherical Particles journal July 2013
The M2 Ectodomain Is Important for Its Incorporation into Influenza A Virions journal March 1998
Definitive Assignment of Proton Selectivity and Attoampere Unitary Current to the M2 Ion Channel Protein of Influenza A Virus journal April 2001
Influenza A virus M2 ion channel protein: a structure-function analysis. journal January 1994
Effect of Cytosolic pH on Inward Currents Reveals Structural Characteristics of the Proton Transport Cycle in the Influenza A Protein M2 in Cell-Free Membrane Patches of Xenopus oocytes journal September 2014
Proton Transport Behavior through the Influenza A M2 Channel: Insights from Molecular Simulation journal November 2007
Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals journal March 2015
Advances in X-ray free electron laser (XFEL) diffraction data processing applied to the crystal structure of the synaptotagmin-1 / SNARE complex journal October 2016

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59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
XFEL
influenza
membrane protein
proton channel