Electrostatic lock in the transport cycle of the multidrug resistance transporter EmrE

Vermaas, Josh V.; Rempe, Susan B.; Tajkhorshid, Emad

doi:10.1073/pnas.1722399115

Electrostatic lock in the transport cycle of the multidrug resistance transporter EmrE

Journal Article · Thu Jul 19 00:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1722399115· OSTI ID:1460924

; Rempe, Susan B.;

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC04-94AL85000; NA0003525

OSTI ID:: 1460924

Alternate ID(s):: OSTI ID: 1485839

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: 32 Vol. 115; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

References (77)

Comparative Protein Structure Modeling Using MODELLER Eswar, Narayanan; Webb, Ben; Marti-Renom, Marc A. Current Protocols in Protein Science, Vol. 50, Issue 1 https://doi.org/10.1002/0471140864.ps0209s50	journal	November 2007
Ligand-Induced Conformational Changes of the Multidrug Resistance Transporter EmrE Probed by Oriented Solid-State NMR Spectroscopy Gayen, Anindita; Banigan, James R.; Traaseth, Nathaniel J. Angewandte Chemie International Edition, Vol. 52, Issue 39 https://doi.org/10.1002/anie.201303091	journal	August 2013
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
GROMACS: Fast, flexible, and free Van Der Spoel, David; Lindahl, Erik; Hess, Berk Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20291	journal	January 2005
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 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
Rapid parameterization of small molecules using the force field toolkit Mayne, Christopher G.; Saam, Jan; Schulten, Klaus Journal of Computational Chemistry, Vol. 34, Issue 32 https://doi.org/10.1002/jcc.23422	journal	September 2013
Exploring protein native states and large-scale conformational changes with a modified generalized born model Onufriev, Alexey; Bashford, Donald; Case, David A. Proteins: Structure, Function, and Bioinformatics, Vol. 55, Issue 2 https://doi.org/10.1002/prot.20033	journal	March 2004
Knowledge-based protein secondary structure assignment Frishman, Dmitrij; Argos, Patrick Proteins: Structure, Function, and Genetics, Vol. 23, Issue 4 https://doi.org/10.1002/prot.340230412	journal	December 1995
A simple method for displaying the hydropathic character of a protein Kyte, Jack; Doolittle, Russell F. Journal of Molecular Biology, Vol. 157, Issue 1, p. 105-132 https://doi.org/10.1016/0022-2836(82)90515-0	journal	May 1982
Hydrophobic ion interactions with membranes. Thermodynamic analysis of tetraphenylphosphonium binding to vesicles Flewelling, R. F.; Hubbell, W. L. Biophysical Journal, Vol. 49, Issue 2 https://doi.org/10.1016/S0006-3495(86)83663-3	journal	February 1986
Hydrogen bonding stabilizes globular proteins Myers, J. K.; Pace, C. N. Biophysical Journal, Vol. 71, Issue 4 https://doi.org/10.1016/S0006-3495(96)79401-8	journal	October 1996
Small multidrug resistance proteins: A multidrug transporter family that continues to grow Bay, Denice C.; Rommens, Kenton L.; Turner, Raymond J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 9 https://doi.org/10.1016/j.bbamem.2007.08.015	journal	September 2008
Conformational heterogeneity of α -synuclein in membrane Vermaas, Josh V.; Tajkhorshid, Emad Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 12 https://doi.org/10.1016/j.bbamem.2014.08.012	journal	December 2014
Structural and dynamic changes adopted by EmrE, multidrug transporter protein—Studies by molecular dynamics simulation Padariya, Monikaben; Kalathiya, Umesh; Baginski, Maciej Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1848, Issue 10 https://doi.org/10.1016/j.bbamem.2015.05.014	journal	October 2015
The cellular membrane as a mediator for small molecule interaction with membrane proteins Mayne, Christopher G.; Arcario, Mark J.; Mahinthichaichan, Paween Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 10 https://doi.org/10.1016/j.bbamem.2016.04.016	journal	October 2016
Quantifying the membrane potential during E. coli growth stages Bot, Corina Teodora; Prodan, Camelia Biophysical Chemistry, Vol. 146, Issue 2-3 https://doi.org/10.1016/j.bpc.2009.11.005	journal	February 2010
Functional response of the small multidrug resistance protein EmrE to mutations in transmembrane helix 2 Wang, Jun; Rath, Arianna; Deber, Charles M. FEBS Letters, Vol. 588, Issue 20 https://doi.org/10.1016/j.febslet.2014.08.018	journal	August 2014
The Escherichia coli Multidrug Transporter EmrE is a Dimer in the Detergent-solubilised State Butler, P. J. G.; Ubarretxena-Belandia, I.; Warne, T. Journal of Molecular Biology, Vol. 340, Issue 4 https://doi.org/10.1016/j.jmb.2004.05.014	journal	July 2004
Quasi-symmetry in the Cryo-EM Structure of EmrE Provides the Key to Modeling its Transmembrane Domain Fleishman, Sarel J.; Harrington, Susan E.; Enosh, Angela Journal of Molecular Biology, Vol. 364, Issue 1 https://doi.org/10.1016/j.jmb.2006.08.072	journal	November 2006
Electron Crystallography Reveals Plasticity within the Drug Binding Site of the Small Multidrug Transporter EmrE Korkhov, Vladimir M.; Tate, Christopher G. Journal of Molecular Biology, Vol. 377, Issue 4 https://doi.org/10.1016/j.jmb.2008.01.056	journal	April 2008
Specificity Determinants in Small Multidrug Transporters Brill, Shlomo; Sade-Falk, Ofir; Elbaz-Alon, Yael Journal of Molecular Biology, Vol. 427, Issue 2 https://doi.org/10.1016/j.jmb.2014.11.015	journal	January 2015
BLaTM 2.0, a Genetic Tool Revealing Preferred Antiparallel Interaction of Transmembrane Helix 4 of the Dual-Topology Protein EmrE Julius, Ayse; Laur, Lisa; Schanzenbach, Christoph Journal of Molecular Biology, Vol. 429, Issue 11 https://doi.org/10.1016/j.jmb.2017.04.003	journal	June 2017
Membrane protein structure quality in molecular dynamics simulation Law, Richard J.; Capener, Charlotte; Baaden, Marc Journal of Molecular Graphics and Modelling, Vol. 24, Issue 2 https://doi.org/10.1016/j.jmgm.2005.05.006	journal	October 2005
GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers Abraham, Mark James; Murtola, Teemu; Schulz, Roland SoftwareX, Vol. 1-2 https://doi.org/10.1016/j.softx.2015.06.001	journal	September 2015
Flexible Fitting of Atomic Structures into Electron Microscopy Maps Using Molecular Dynamics Trabuco, Leonardo G.; Villa, Elizabeth; Mitra, Kakoli Structure, Vol. 16, Issue 5 https://doi.org/10.1016/j.str.2008.03.005	journal	May 2008
Molecular dynamics flexible fitting: A practical guide to combine cryo-electron microscopy and X-ray crystallography Trabuco, Leonardo G.; Villa, Elizabeth; Schreiner, Eduard Methods, Vol. 49, Issue 2 https://doi.org/10.1016/j.ymeth.2009.04.005	journal	October 2009
TopoGromacs: Automated Topology Conversion from CHARMM to GROMACS within VMD Vermaas, Josh V.; Hardy, David J.; Stone, John E. Journal of Chemical Information and Modeling, Vol. 56, Issue 6 https://doi.org/10.1021/acs.jcim.6b00103	journal	May 2016
Constant pH Molecular Dynamics Reveals How Proton Release Drives the Conformational Transition of a Transmembrane Efflux Pump Yue, Zhi; Chen, Wei; Zgurskaya, Helen I. Journal of Chemical Theory and Computation, Vol. 13, Issue 12 https://doi.org/10.1021/acs.jctc.7b00874	journal	November 2017
Predicting Catalytic Proton Donors and Nucleophiles in Enzymes: How Adding Dynamics Helps Elucidate the Structure–Function Relationships Huang, Yandong; Yue, Zhi; Tsai, Cheng-Chieh The Journal of Physical Chemistry Letters, Vol. 9, Issue 6 https://doi.org/10.1021/acs.jpclett.8b00238	journal	February 2018
GPU/CPU Algorithm for Generalized Born/Solvent-Accessible Surface Area Implicit Solvent Calculations Tanner, David E.; Phillips, James C.; Schulten, Klaus Journal of Chemical Theory and Computation, Vol. 8, Issue 7 https://doi.org/10.1021/ct3003089	journal	June 2012
Optimization of the Additive CHARMM All-Atom Protein Force Field Targeting Improved Sampling of the Backbone ϕ, ψ and Side-Chain χ ₁ and χ ₂ Dihedral Angles Best, Robert B.; Zhu, Xiao; Shim, Jihyun Journal of Chemical Theory and Computation, Vol. 8, Issue 9 https://doi.org/10.1021/ct300400x	journal	August 2012
Computational Recipe for Efficient Description of Large-Scale Conformational Changes in Biomolecular Systems Moradi, Mahmoud; Tajkhorshid, Emad Journal of Chemical Theory and Computation, Vol. 10, Issue 7 https://doi.org/10.1021/ct5002285	journal	June 2014
Semianalytical treatment of solvation for molecular mechanics and dynamics Still, W. Clark; Tempczyk, Anna; Hawley, Ronald C. Journal of the American Chemical Society, Vol. 112, Issue 16 https://doi.org/10.1021/ja00172a038	journal	August 1990
Effect of Hydrogen Bonds on p K _a Values: Importance of Networking Shokri, Alireza; Abedin, Azardokht; Fattahi, Alireza Journal of the American Chemical Society, Vol. 134, Issue 25 https://doi.org/10.1021/ja3037349	journal	June 2012
Detecting Substrates Bound to the Secondary Multidrug Efflux Pump EmrE by DNP-Enhanced Solid-State NMR Ong, Yean Sin; Lakatos, Andrea; Becker-Baldus, Johanna Journal of the American Chemical Society, Vol. 135, Issue 42 https://doi.org/10.1021/ja402605s	journal	October 2013
Intrinsic Conformational Plasticity of Native EmrE Provides a Pathway for Multidrug Resistance Cho, Min-Kyu; Gayen, Anindita; Banigan, James R. Journal of the American Chemical Society, Vol. 136, Issue 22 https://doi.org/10.1021/ja503145x	journal	May 2014
The Development of Replica-Exchange-Based Free-Energy Methods Woods, Christopher J.; Essex, Jonathan W.; King, Michael A. The Journal of Physical Chemistry B, Vol. 107, Issue 49 https://doi.org/10.1021/jp0356620	journal	December 2003
Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types Klauda, Jeffery B.; Venable, Richard M.; Freites, J. Alfredo The Journal of Physical Chemistry B, Vol. 114, Issue 23 https://doi.org/10.1021/jp101759q	journal	June 2010
Simple Allosteric Model for Membrane Pumps Jardetzky, Oleg Nature, Vol. 211, Issue 5052 https://doi.org/10.1038/211969a0	journal	August 1966
Antiparallel EmrE exports drugs by exchanging between asymmetric structures Morrison, Emma A.; DeKoster, Gregory T.; Dutta, Supratik Nature, Vol. 481, Issue 7379 https://doi.org/10.1038/nature10703	journal	December 2011
Protonation of a glutamate residue modulates the dynamics of the drug transporter EmrE Gayen, Anindita; Leninger, Maureen; Traaseth, Nathaniel J. Nature Chemical Biology, Vol. 12, Issue 3 https://doi.org/10.1038/nchembio.1999	journal	January 2016
Atomic-level characterization of transport cycle thermodynamics in the glycerol-3-phosphate:phosphate antiporter Moradi, Mahmoud; Enkavi, Giray; Tajkhorshid, Emad Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9393	journal	September 2015
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
X-ray structure of EmrE supports dual topology model Chen, Y. -J.; Pornillos, O.; Lieu, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 48 https://doi.org/10.1073/pnas.0709387104	journal	November 2007
A coordinated network of transporters with overlapping specificities provides a robust survival strategy Tal, N.; Schuldiner, S. Proceedings of the National Academy of Sciences, Vol. 106, Issue 22 https://doi.org/10.1073/pnas.0902400106	journal	May 2009
Transforming a drug/H+ antiporter into a polyamine importer by a single mutation Brill, S.; Falk, O. S.; Schuldiner, S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 42 https://doi.org/10.1073/pnas.1211831109	journal	October 2012
Membrane physical properties influence transmembrane helix formation Barrera, F. N.; Fendos, J.; Engelman, D. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 36 https://doi.org/10.1073/pnas.1212665109	journal	August 2012
Transient formation of water-conducting states in membrane transporters Li, J.; Shaikh, S. A.; Enkavi, G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 19 https://doi.org/10.1073/pnas.1218986110	journal	April 2013
Proton transfer through the water gossamer Hassanali, Ali; Giberti, Federico; Cuny, Jérôme Proceedings of the National Academy of Sciences, Vol. 110, Issue 34 https://doi.org/10.1073/pnas.1306642110	journal	July 2013
Local anesthetic and antiepileptic drug access and binding to a bacterial voltage-gated sodium channel Boiteux, C.; Vorobyov, I.; French, R. J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 36 https://doi.org/10.1073/pnas.1408710111	journal	August 2014
Protonation-dependent conformational dynamics of the multidrug transporter EmrE Dastvan, Reza; Fischer, Axel W.; Mishra, Smriti Proceedings of the National Academy of Sciences, Vol. 113, Issue 5 https://doi.org/10.1073/pnas.1520431113	journal	January 2016
New free-exchange model of EmrE transport Robinson, Anne E.; Thomas, Nathan E.; Morrison, Emma A. Proceedings of the National Academy of Sciences, Vol. 114, Issue 47 https://doi.org/10.1073/pnas.1708671114	journal	November 2017
EmrE, an Escherichia coli 12-kDa Multidrug Transporter, Exchanges Toxic Cations and H ⁺ and Is Soluble in Organic Solvents Yerushalmi, Hagit; Lebendiker, Mario; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 270, Issue 12 https://doi.org/10.1074/jbc.270.12.6856	journal	March 1995
Negative Dominance Studies Demonstrate the Oligomeric Structure of EmrE, a Multidrug Antiporter from Escherichia coli Yerushalmi, Hagit; Lebendiker, Mario; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 271, Issue 49 https://doi.org/10.1074/jbc.271.49.31044	journal	December 1996
An Essential Glutamyl Residue in EmrE, a Multidrug Antiporter from Escherichia coli Yerushalmi, Hagit; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 275, Issue 8 https://doi.org/10.1074/jbc.275.8.5264	journal	February 2000
A Lipid Pathway for Ligand Binding Is Necessary for a Cannabinoid G Protein-coupled Receptor Hurst, Dow P.; Grossfield, Alan; Lynch, Diane L. Journal of Biological Chemistry, Vol. 285, Issue 23 https://doi.org/10.1074/jbc.M109.041590	journal	March 2010
Transported Substrate Determines Exchange Rate in the Multidrug Resistance Transporter EmrE Morrison, Emma A.; Henzler-Wildman, Katherine A. Journal of Biological Chemistry, Vol. 289, Issue 10 https://doi.org/10.1074/jbc.M113.535328	journal	January 2014
EmrE, a Multidrug Transporter from Escherichia coli , Transports Monovalent and Divalent Substrates with the Same Stoichiometry Rotem, Dvir; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 279, Issue 47 https://doi.org/10.1074/jbc.M408187200	journal	September 2004
Identification of Tyrosine Residues Critical for the Function of an Ion-coupled Multidrug Transporter Rotem, Dvir; Steiner-Mordoch, Sonia; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 281, Issue 27 https://doi.org/10.1074/jbc.M602088200	journal	May 2006
Using collective variables to drive molecular dynamics simulations Fiorin, Giacomo; Klein, Michael L.; Hénin, Jérôme Molecular Physics, Vol. 111, Issue 22-23 https://doi.org/10.1080/00268976.2013.813594	journal	December 2013
Asymmetric protonation of EmrE Morrison, Emma A.; Robinson, Anne E.; Liu, Yongjia The Journal of General Physiology, Vol. 146, Issue 6 https://doi.org/10.1085/jgp.201511404	journal	November 2015
TeXshade: shading and labeling of multiple sequence alignments using LaTeX2e Beitz, E. Bioinformatics, Vol. 16, Issue 2 https://doi.org/10.1093/bioinformatics/16.2.135	journal	February 2000
GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Pronk, Sander; Páll, Szilárd; Schulz, Roland Bioinformatics, Vol. 29, Issue 7 https://doi.org/10.1093/bioinformatics/btt055	journal	February 2013
Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer Ubarretxena-Belandia, I. The EMBO Journal, Vol. 22, Issue 23 https://doi.org/10.1093/emboj/cdg611	journal	December 2003
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
An emerging consensus for the structure of EmrE Korkhov, Vladimir M.; Tate, Christopher G. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 2 https://doi.org/10.1107/S0907444908036640	journal	January 2009
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Matplotlib: A 2D Graphics Environment Hunter, John D. Computing in Science & Engineering, Vol. 9, Issue 3 https://doi.org/10.1109/MCSE.2007.55	journal	January 2007
The NumPy Array: A Structure for Efficient Numerical Computation van der Walt, Stéfan; Colbert, S. Chris; Varoquaux, Gaël Computing in Science & Engineering, Vol. 13, Issue 2 https://doi.org/10.1109/MCSE.2011.37	journal	March 2011
A Single Adenosine with a Neutral pKa in the Ribosomal Peptidyl Transferase Center Muth, G. W. Science, Vol. 289, Issue 5481 https://doi.org/10.1126/science.289.5481.947	journal	August 2000
A system for interactive molecular dynamics simulation Stone, John E.; Gullingsrud, Justin; Schulten, Klaus Proceedings of the 2001 symposium on Interactive 3D graphics - SI3D '01 https://doi.org/10.1145/364338.364398	conference	January 2001
Helical Membrane Protein Folding, Stability, and Evolution Popot, Jean-Luc; Engelman, Donald M. Annual Review of Biochemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev.biochem.69.1.881	journal	June 2000
Comparative Protein Structure Modeling of Genes and Genomes Martí-Renom, Marc A.; Stuart, Ashley C.; Fiser, András Annual Review of Biophysics and Biomolecular Structure, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.biophys.29.1.291	journal	June 2000
Mechanism of lignin inhibition of enzymatic biomass deconstruction Vermaas, Josh V.; Petridis, Loukas; Qi, Xianghong Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0379-8	journal	December 2015
Automated Builder and Database of Protein/Membrane Complexes for Molecular Dynamics Simulations Jo, Sunhwan; Kim, Taehoon; Im, Wonpil PLoS ONE, Vol. 2, Issue 9 https://doi.org/10.1371/journal.pone.0000880	journal	September 2007
Repeat-swap homology modeling of secondary active transporters: updated protocol and prediction of elevator-type mechanisms Vergara-Jaque, Ariela; Fenollar-Ferrer, Cristina; Kaufmann, Desirée Frontiers in Pharmacology, Vol. 6 https://doi.org/10.3389/fphar.2015.00183	journal	September 2015

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