Oriented chiral water wires in artificial transmembrane channels

Kocsis, Istvan; Sorci, Mirco; Vanselous, Heather; Murail, Samuel; Sanders, Stephanie E.; Licsandru, Erol; Legrand, Yves-Marie; van der Lee, Arie; Baaden, Marc; Petersen, Poul B.; Belfort, Georges; Barboiu, Mihail

doi:10.1126/sciadv.aao5603

Title: Oriented chiral water wires in artificial transmembrane channels

Journal Article · 23 March 2018 · Science Advances

DOI: https://doi.org/10.1126/sciadv.aao5603 · OSTI ID:1499944

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^[2]; Vanselous, Heather ^[3];

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^[3]; Licsandru, Erol ^[1];

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Université de Montpellier, ENSCM, CNRS (France)
Rensselaer Polytechnic Inst., Troy, NY (United States)
Cornell Univ., Ithaca, NY (United States)
Université Paris Diderot (France)

Aquaporins (AQPs) feature highly selective water transport through cell membranes, where the dipolar orientation of structured water wires spanning the AQP pore is of considerable importance for the selective translocation of water over ions. We recently discovered that water permeability through artificial water channels formed by stacked imidazole I-quartet superstructures increases when the channel water molecules are highly organized. Correlating water structure with molecular transport is essential for understanding the underlying mechanisms of (fast) water translocation and channel selectivity. Chirality adds another factor enabling unique dipolar oriented water structures. We show that water molecules exhibit a dipolar oriented wire structure within chiral I-quartet water channels both in the solid state and embedded in supported lipid bilayer membranes (SLBs). X-ray single-crystal structures show that crystallographic water wires exhibit dipolar orientation, which is unique for chiral I-quartets. The integration of I-quartets into SLBs was monitored with a quartz crystal microbalance with dissipation, quantizing the amount of channel water molecules. Nonlinear sum-frequency generation vibrational spectroscopy demonstrates the first experimental observation of dipolar oriented water structures within artificial water channels inserted in bilayer membranes. Confirmation of the ordered confined water is obtained via molecular simulations, which provide quantitative measures of hydrogen bond strength, connectivity, and the stability of their dipolar alignment in a membrane environment. Together, uncovering the interplay between the dipolar aligned water structure and water transport through the self-assembled I-quartets is critical to understanding the behavior of natural membrane channels and will accelerate the systematic discovery for developing artificial water channels for water desalting.

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Research Organization:: Rensselaer Polytechnic Inst., Troy, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-09ER16005

OSTI ID:: 1499944

Journal Information:: Science Advances, Vol. 4, Issue 3; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

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Artificial Water Channels Barboiu, Mihail Angewandte Chemie International Edition, Vol. 51, Issue 47 https://doi.org/10.1002/anie.201205819	journal	October 2012
Ion-Conduction Pathways in Self-Organised Ureidoarene–Heteropolysiloxane Hybrid Membranes Michau, Mathieu; Barboiu, Mihail; Caraballo, Rémi Chemistry - A European Journal, Vol. 14, Issue 6 https://doi.org/10.1002/chem.200700943	journal	February 2008
CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields Vanommeslaeghe, K.; Hatcher, E.; Acharya, C. Journal of Computational Chemistry https://doi.org/10.1002/jcc.21367	journal	January 2009
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Both Inter- and Intramolecular Coupling of O–H Groups Determine the Vibrational Response of the Water/Air Interface Schaefer, Jan; Backus, Ellen H. G.; Nagata, Yuki The Journal of Physical Chemistry Letters, Vol. 7, Issue 22 https://doi.org/10.1021/acs.jpclett.6b02513	journal	November 2016
Phosphate Ions Affect the Water Structure at Functionalized Membrane Surfaces Barrett, Aliyah; Imbrogno, Joseph; Belfort, Georges Langmuir, Vol. 32, Issue 35 https://doi.org/10.1021/acs.langmuir.6b01936	journal	August 2016
From Natural to Bioassisted and Biomimetic Artificial Water Channel Systems Barboiu, Mihail; Gilles, Arnaud Accounts of Chemical Research, Vol. 46, Issue 12 https://doi.org/10.1021/ar400025e	journal	January 2013
Automation of the CHARMM General Force Field (CGenFF) II: Assignment of Bonded Parameters and Partial Atomic Charges Vanommeslaeghe, K.; Raman, E. Prabhu; MacKerell, A. D. Journal of Chemical Information and Modeling, Vol. 52, Issue 12 https://doi.org/10.1021/ci3003649	journal	November 2012
Liquid Interfaces Probed by Second-Harmonic and Sum-Frequency Spectroscopy Eisenthal, K. B. Chemical Reviews, Vol. 96, Issue 4 https://doi.org/10.1021/cr9502211	journal	January 1996
GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation Hess, Berk; Kutzner, Carsten; van der Spoel, David Journal of Chemical Theory and Computation, Vol. 4, Issue 3 https://doi.org/10.1021/ct700301q	journal	February 2008
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Salt-Excluding Artificial Water Channels Exhibiting Enhanced Dipolar Water and Proton Translocation Licsandru, Erol; Kocsis, Istvan; Shen, Yue-xiao Journal of the American Chemical Society, Vol. 138, Issue 16 https://doi.org/10.1021/jacs.6b01811	journal	January 2016
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Quartz crystal microbalance with dissipation monitoring of supported lipid bilayers on various substrates Cho, Nam-Joon; Frank, Curtis W.; Kasemo, Bengt Nature Protocols, Vol. 5, Issue 6 https://doi.org/10.1038/nprot.2010.65	journal	May 2010
Aquaporins: important but elusive drug targets Verkman, Alan S.; Anderson, Marc O.; Papadopoulos, Marios C. Nature Reviews Drug Discovery, Vol. 13, Issue 4 https://doi.org/10.1038/nrd4226	journal	March 2014
Ordering of water molecules between phospholipid bilayers visualized by coherent anti-Stokes Raman scattering microscopy Cheng, J. -X.; Pautot, S.; Weitz, D. A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 17 https://doi.org/10.1073/pnas.1732202100	journal	August 2003
Mechanisms of Proton Conduction and Gating in Influenza M2 Proton Channels from Solid-State NMR Hu, F.; Luo, W.; Hong, M. Science, Vol. 330, Issue 6003 https://doi.org/10.1126/science.1191714	journal	October 2010
Subangstrom Resolution X-Ray Structure Details Aquaporin-Water Interactions Kosinska Eriksson, U.; Fischer, G.; Friemann, R. Science, Vol. 340, Issue 6138 https://doi.org/10.1126/science.1234306	journal	June 2013
Membrane Desalination: Where Are We, and What Can We Learn from Fundamentals? Imbrogno, Joseph; Belfort, Georges Annual Review of Chemical and Biomolecular Engineering, Vol. 7, Issue 1 https://doi.org/10.1146/annurev-chembioeng-061114-123202	journal	June 2016
Chirality in Nonlinear Optics Haupert, Levi M.; Simpson, Garth J. Annual Review of Physical Chemistry, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.physchem.59.032607.093712	journal	May 2009

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