Crystal structures of bacterial small multidrug resistance transporter EmrE in complex with structurally diverse substrates

Kermani, Ali A.; Burata, Olive E.; Koff, B Ben; Koide, Akiko; Koide, Shohei; Stockbridge, Randy B.

doi:10.7554/eLife.76766

Crystal structures of bacterial small multidrug resistance transporter EmrE in complex with structurally diverse substrates

Journal Article · Mon Feb 28 23:00:00 EST 2022 · eLife

DOI:https://doi.org/10.7554/eLife.76766· OSTI ID:1865443

Kermani, Ali A.; Burata, Olive E.; Koff, B Ben; Koide, Akiko; Koide, Shohei; Stockbridge, Randy B.

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - Office Of Science; NIH; NSF; OTHER

OSTI ID:: 1865443

Journal Information:: eLife, Journal Name: eLife Vol. 11; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.

Country of Publication:: United States

Language:: ENGLISH

References (60)

The C terminus of the bacterial multidrug transporter EmrE couples drug binding to proton release Thomas, Nathan E.; Wu, Chao; Morrison, Emma A. Journal of Biological Chemistry, Vol. 293, Issue 49 https://doi.org/10.1074/jbc.RA118.005430	journal	October 2018
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
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
Teaching an Old Scaffold New Tricks: Monobodies Constructed Using Alternative Surfaces of the FN3 Scaffold Koide, Akiko; Wojcik, John; Gilbreth, Ryan N. Journal of Molecular Biology, Vol. 415, Issue 2 https://doi.org/10.1016/j.jmb.2011.12.019	journal	January 2012
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
Engineering of recombinant crystallization chaperones Koide, Shohei Current Opinion in Structural Biology, Vol. 19, Issue 4 https://doi.org/10.1016/j.sbi.2009.04.008	journal	August 2009
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
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
Metabolism of Free Guanidine in Bacteria Is Regulated by a Widespread Riboswitch Class Nelson, James W.; Atilho, Ruben M.; Sherlock, Madeline E. Molecular Cell, Vol. 65, Issue 2 https://doi.org/10.1016/j.molcel.2016.11.019	journal	January 2017
Asymmetric protonation of glutamate residues drives a preferred transport pathway in EmrE Li, Jianping; Sae Her, Ampon; Traaseth, Nathaniel J. Proceedings of the National Academy of Sciences, Vol. 118, Issue 41 https://doi.org/10.1073/pnas.2110790118	journal	October 2021
EmrE, a model for studying evolution and mechanism of ion-coupled transporters Schuldiner, Shimon Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1794, Issue 5 https://doi.org/10.1016/j.bbapap.2008.12.018	journal	May 2009
Scanning Cysteine Accessibility of EmrE, an H+-coupled Multidrug Transporter from Escherichia coli, Reveals a Hydrophobic Pathway for Solutes Mordoch, Sonia Steiner; Granot, Dorit; Lebendiker, Mario Journal of Biological Chemistry, Vol. 274, Issue 27 https://doi.org/10.1074/jbc.274.27.19480	journal	July 1999
ConSeq: the identification of functionally and structurally important residues in protein sequences Berezin, C.; Glaser, F.; Rosenberg, J. Bioinformatics, Vol. 20, Issue 8 https://doi.org/10.1093/bioinformatics/bth070	journal	February 2004
Structure of the EmrE multidrug transporter and its use for inhibitor peptide design Ovchinnikov, Victor; Stone, Tracy A.; Deber, Charles M. Proceedings of the National Academy of Sciences, Vol. 115, Issue 34 https://doi.org/10.1073/pnas.1802177115	journal	August 2018
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Molecular mechanism of proton-coupled ligand translocation by the bacterial efflux pump EmrE Jurasz, Jakub; Bagiński, Maciej; Czub, Jacek PLOS Computational Biology, Vol. 17, Issue 10 https://doi.org/10.1371/journal.pcbi.1009454	journal	October 2021
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
A Structured Loop Modulates Coupling between the Substrate-binding and Dimerization Domains in the Multidrug Resistance Transporter EmrE Banigan, James R.; Gayen, Anindita; Cho, Min-Kyu Journal of Biological Chemistry, Vol. 290, Issue 2 https://doi.org/10.1074/jbc.M114.601963	journal	January 2015
Conformational Changes in the Multidrug Transporter EmrE Associated with Substrate Binding Tate, Christopher G.; Ubarretxena-Belandia, Iban; Baldwin, Joyce M. Journal of Molecular Biology, Vol. 332, Issue 1 https://doi.org/10.1016/s0022-2836(03)00895-7	journal	September 2003
Class 1 integrons as invasive species Gillings, Michael R. Current Opinion in Microbiology, Vol. 38 https://doi.org/10.1016/j.mib.2017.03.002	journal	August 2017
N-terminal Transmembrane-Helix Epitope Tag for X-ray Crystallography and Electron Microscopy of Small Membrane Proteins McIlwain, Benjamin C.; Erwin, Amanda L.; Davis, Alexander R. Journal of Molecular Biology, Vol. 433, Issue 16 https://doi.org/10.1016/j.jmb.2021.166909	journal	August 2021
Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 5 https://doi.org/10.1107/S0907444908004319	journal	April 2008
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Synthetic antibodies against BRIL as universal fiducial marks for single−particle cryoEM structure determination of membrane proteins Mukherjee, Somnath; Erramilli, Satchal K.; Ammirati, Mark Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15363-0	journal	March 2020
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
Substrate-Induced Tryptophan Fluorescence Changes in EmrE, the Smallest Ion-Coupled Multidrug Transporter ^† Elbaz, Yael; Tayer, Naama; Steinfels, Emmanuelle Biochemistry, Vol. 44, Issue 19 https://doi.org/10.1021/bi050356t	journal	May 2005
Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential Pal, Chandan; Bengtsson-Palme, Johan; Kristiansson, Erik BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2153-5	journal	November 2015
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
Electrostatic lock in the transport cycle of the multidrug resistance transporter EmrE Vermaas, Josh V.; Rempe, Susan B.; Tajkhorshid, Emad Proceedings of the National Academy of Sciences, Vol. 115, Issue 32 https://doi.org/10.1073/pnas.1722399115	journal	July 2018
DIALS : implementation and evaluation of a new integration package Winter, Graeme; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2 https://doi.org/10.1107/S2059798317017235	journal	February 2018
Inducing conformational preference of the membrane protein transporter EmrE through conservative mutations Leninger, Maureen; Sae Her, Ampon; Traaseth, Nathaniel J. eLife, Vol. 8 https://doi.org/10.7554/eLife.48909	journal	October 2019
Structure, Dynamics, and Substrate-induced Conformational Changes of the Multidrug Transporter EmrE in Liposomes Amadi, Sepan T.; Koteiche, Hanane A.; Mishra, Sanjay Journal of Biological Chemistry, Vol. 285, Issue 34 https://doi.org/10.1074/jbc.M110.132621	journal	June 2010
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
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
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
1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life Mukherjee, Supratim; Seshadri, Rekha; Varghese, Neha J. Nature Biotechnology, Vol. 35, Issue 7 https://doi.org/10.1038/nbt.3886	journal	June 2017
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
An Amino Acid Cluster around the Essential Glu-14 Is Part of the Substrate- and Proton-binding Domain of EmrE, a Multidrug Transporter from Escherichia coli Gutman, Natalia; Steiner-Mordoch, Sonia; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 278, Issue 18 https://doi.org/10.1074/jbc.M213120200	journal	May 2003
Guanidinium export is the primal function of SMR family transporters Kermani, Ali A.; Macdonald, Christian B.; Gundepudi, Roja Proceedings of the National Academy of Sciences, Vol. 115, Issue 12 https://doi.org/10.1073/pnas.1719187115	journal	March 2018
Introduction of biocides into clinical practice and the impact on antibiotic-resistant bacteria: BIOCIDES AND ANTIBIOTIC RESISTANCE Russell, A. D. Journal of Applied Microbiology, Vol. 92 https://doi.org/10.1046/j.1365-2672.92.5s1.12.x	journal	May 2002
Direct Evidence for Substrate-induced Proton Release in Detergent-solubilized EmrE, a Multidrug Transporter Soskine, Misha; Adam, Yoav; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 279, Issue 11 https://doi.org/10.1074/jbc.M312853200	journal	March 2004
A portable RNA sequence whose recognition by a synthetic antibody facilitates structural determination Koldobskaya, Yelena; Duguid, Erica M.; Shechner, David M. Nature Structural & Molecular Biology, Vol. 18, Issue 1 https://doi.org/10.1038/nsmb.1945	journal	December 2010
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017
Few Conserved Amino Acids in the Small Multidrug Resistance Transporter EmrE Influence Drug Polyselectivity Saleh, Marwah; Bay, Denice C.; Turner, Raymond J. Antimicrobial Agents and Chemotherapy, Vol. 62, Issue 8 https://doi.org/10.1128/AAC.00461-18	journal	August 2018
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Identification of an Alternating-Access Dynamics Mutant of EmrE with Impaired Transport Wu, Chao; Wynne, Samantha A.; Thomas, Nathan E. Journal of Molecular Biology, Vol. 431, Issue 15 https://doi.org/10.1016/j.jmb.2019.05.035	journal	July 2019
Helix kinks are equally prevalent in soluble and membrane proteins Wilman, Henry R.; Shi, Jiye; Deane, Charlotte M. Proteins: Structure, Function, and Bioinformatics, Vol. 82, Issue 9 https://doi.org/10.1002/prot.24550	journal	April 2014
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
The structural basis of promiscuity in small multidrug resistance transporters Kermani, Ali A.; Macdonald, Christian B.; Burata, Olive E. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-19820-8	journal	November 2020
ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules Ashkenazy, Haim; Abadi, Shiran; Martz, Eric Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw408	journal	May 2016
SSM-Based Electrophysiology for Transporter Research Bazzone, Andre; Barthmes, Maria; Fendler, Klaus Methods in Enzymology https://doi.org/10.1016/bs.mie.2017.05.008	book	January 2017
Continental-scale pollution of estuaries with antibiotic resistance genes Zhu, Yong-Guan; Zhao, Yi; Li, Bing Nature Microbiology, Vol. 2, Issue 4 https://doi.org/10.1038/nmicrobiol.2016.270	journal	January 2017
PyShifts: A PyMOL Plugin for Chemical Shift-Based Analysis of Biomolecular Ensembles Xie, Jingru; Zhang, Kexin; Frank, Aaron T. Journal of Chemical Information and Modeling, Vol. 60, Issue 3 https://doi.org/10.1021/acs.jcim.9b01039	journal	February 2020
Development of “Plug and Play” Fiducial Marks for Structural Studies of GPCR Signaling Complexes by Single-Particle Cryo-EM Dutka, Przemyslaw; Mukherjee, Somnath; Gao, Xiang Structure, Vol. 27, Issue 12 https://doi.org/10.1016/j.str.2019.10.004	journal	December 2019
Structure and dynamics of the drug-bound bacterial transporter EmrE in lipid bilayers Shcherbakov, Alexander A.; Hisao, Grant; Mandala, Venkata S. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20468-7	journal	January 2021
Monobodies and other synthetic binding proteins for expanding protein science: Monobodies and Other Synthetic Binding Proteins Sha, Fern; Salzman, Gabriel; Gupta, Ankit Protein Science, Vol. 26, Issue 5 https://doi.org/10.1002/pro.3148	journal	March 2017
Predicting Protein Backbone Chemical Shifts From Cα Coordinates: Extracting High Resolution Experimental Observables from Low Resolution Models Frank, Aaron T.; Law, Sean M.; Ahlstrom, Logan S. Journal of Chemical Theory and Computation, Vol. 11, Issue 1 https://doi.org/10.1021/ct5009125	journal	December 2014
The fast release of sticky protons: Kinetics of substrate binding and proton release in a multidrug transporter Adam, Yoav; Tayer, Naama; Rotem, Dvir Proceedings of the National Academy of Sciences, Vol. 104, Issue 46 https://doi.org/10.1073/pnas.0704425104	journal	November 2007
The molecular modeling toolkit: A new approach to molecular simulations Hinsen, Konrad Journal of Computational Chemistry, Vol. 21, Issue 2 https://doi.org/10.1002/(SICI)1096-987X(20000130)21:2<79::AID-JCC1>3.0.CO;2-B	journal	January 2000

Similar Records

X-Ray Structure of the EmrE Multidrug Transporter in Complex With a Substrate

Journal Article · Wed Oct 11 00:00:00 EDT 2006 · Science 310:1950-1953,2005 · OSTI ID:893306

Structure of the multidrug resistance efflux transporter EmrE from escherichia coli

Journal Article · Wed Dec 31 23:00:00 EST 2003 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:831871

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 · OSTI ID:1460924

Crystal structures of bacterial small multidrug resistance transporter EmrE in complex with structurally diverse substrates

Citation Formats

References (60)

Similar Records

Related Subjects