Pore opening and closing of a pentameric ligand-gated ion channel

被引:133
作者
Zhu, Fangqiang [1 ]
Hummer, Gerhard [1 ]
机构
[1] NIDDKD, Chem Phys Lab, NIH, Bethesda, MD 20892 USA
基金
美国国家卫生研究院;
关键词
ELIC; nicotinic acetylcholine receptor; hydrophobic gate; conformational change; string method; NICOTINIC ACETYLCHOLINE-RECEPTOR; MOLECULAR-DYNAMICS SIMULATIONS; X-RAY-STRUCTURE; STRING METHOD; CONDUCTION; STATE; PERMEATION; TRANSITION; GRAMICIDIN; HOMOLOG;
D O I
10.1073/pnas.1009313107
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Nerve signaling in humans and chemical sensing in bacteria both rely on the controlled opening and closing of the ion-conducting pore in pentameric ligand-gated ion channels. With the help of a multiscale simulation approach that combines mixed elastic network model calculations with molecular dynamics simulations, we study the opening and closing of the pore in Gloeobacter violaceus channel GLIC at atomic resolution. In our simulations of the GLIC transmembrane domain, we first verify that the two endpoints of the transition are open and closed to sodium ion conduction, respectively. We then show that a two-stage tilting of the pore-lining helices induces cooperative drying and iris-like closing of the channel pore. From the free energy profile of the gating transition and from unrestrained simulations, we conclude that the pore of the isolated GLIC transmembrane domain closes spontaneously. The mechanical work of opening the pore is performed primarily on the M2-M3 loop. Strong interactions of this short and conserved loop with the extracellular domain are therefore crucial to couple ligand binding to channel opening.
引用
收藏
页码:19814 / 19819
页数:6
相关论文
共 33 条
[1]   Ion permeation through a narrow channel: Using gramicidin to ascertain all-atom molecular dynamics potential of mean force methodology and biomolecular force fields [J].
Allen, TW ;
Andersen, OS ;
Roux, B .
BIOPHYSICAL JOURNAL, 2006, 90 (10) :3447-3468
[2]  
Anishkin A, 2004, BIOPHYS J, V86, p6A
[3]   Gating of acetylcholine receptor channels: Brownian motion across a broad transition state [J].
Auerbach, A .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (05) :1408-1412
[4]   The gating isomerization of neuromuscular acetylcholine receptors [J].
Auerbach, Anthony .
JOURNAL OF PHYSIOLOGY-LONDON, 2010, 588 (04) :573-586
[5]   A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor [J].
Beckstein, Oliver ;
Sansom, Mark S. P. .
PHYSICAL BIOLOGY, 2006, 3 (02) :147-159
[6]   A gate in the selectivity filter of potassium channels [J].
Bernèche, S ;
Roux, BI .
STRUCTURE, 2005, 13 (04) :591-600
[7]   A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family [J].
Bocquet, Nicolas ;
de Carvalho, Lia Prado ;
Cartaud, Jean ;
Neyton, Jacques ;
Le Poupon, Chantal ;
Taly, Antoine ;
Grutter, Thomas ;
Changeux, Jean-Pierre ;
Corringer, Pierre-Jean .
NATURE, 2007, 445 (7123) :116-119
[8]   X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation [J].
Bocquet, Nicolas ;
Nury, Hugues ;
Baaden, Marc ;
Le Poupon, Chantal ;
Changeux, Jean-Pierre ;
Delarue, Marc ;
Corringer, Pierre-Jean .
NATURE, 2009, 457 (7225) :111-114
[9]   Embedded cholesterol in the nicotinic acetylcholine receptor [J].
Brannigan, Grace ;
Henin, Jerome ;
Law, Richard ;
Eckenhoff, Roderic ;
Klein, Michael L. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (38) :14418-14423
[10]   A single residue in the M2-M3 loop is a major determinant of coupling between binding and gating in neuronal nicotinic receptors [J].
CamposCaro, A ;
Sala, S ;
Ballesta, JJ ;
VicenteAgullo, F ;
Criado, M ;
Sala, F .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1996, 93 (12) :6118-6123