Structural basis for the blockade of MATE multidrug efflux pumps

Radchenko, Martha; Symersky, Jindrich; Nie, Rongxin; Lu, Min

doi:10.1038/ncomms8995

Structural basis for the blockade of MATE multidrug efflux pumps

Journal Article · Thu Jun 30 04:00:00 EDT 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms8995· OSTI ID:1245872

Radchenko, Martha; Symersky, Jindrich; Nie, Rongxin; Lu, Min ^[1]

Rosalind

Abstract not provided

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

Sponsoring Organization:: UNIVERSITY

OSTI ID:: 1245872

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 7995 Vol. 6; ISSN 2041-1723

Country of Publication:: United States

Language:: ENGLISH

References (51)

A structure-based mechanism for drug binding by multidrug transporters Zheleznova, Ekaterina E.; Markham, Penelope; Edgar, Rotem Trends in Biochemical Sciences, Vol. 25, Issue 2 https://doi.org/10.1016/S0968-0004(99)01514-5	journal	February 2000
A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE Muth, T. R.; Schuldiner, S. The EMBO Journal, Vol. 19, Issue 2 https://doi.org/10.1093/emboj/19.2.234	journal	January 2000
A MATE Family Multidrug Efflux Transporter Pumps out Fluoroquinolones in Bacteroides thetaiotaomicron Miyamae, S.; Ueda, O.; Yoshimura, F. Antimicrobial Agents and Chemotherapy, Vol. 45, Issue 12 https://doi.org/10.1128/aac.45.12.3341-3346.2001	journal	December 2001
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations Omote, Hiroshi; Hiasa, Miki; Matsumoto, Takuya Trends in Pharmacological Sciences, Vol. 27, Issue 11 https://doi.org/10.1016/j.tips.2006.09.001	journal	November 2006
AbeM, an H+-Coupled Acinetobacter baumannii Multidrug Efflux Pump Belonging to the MATE Family of Transporters Su, X. -Z.; Chen, J.; Mizushima, T. Antimicrobial Agents and Chemotherapy, Vol. 49, Issue 10 https://doi.org/10.1128/AAC.49.10.4362-4364.2005	journal	September 2005
Na ⁺ –Substrate Coupling in the Multidrug Antiporter NorM Probed with a Spin-Labeled Substrate Steed, P. Ryan; Stein, Richard A.; Mishra, Smriti Biochemistry, Vol. 52, Issue 34 https://doi.org/10.1021/bi4008935	journal	August 2013
The electrochemical gradient of protons and its relationship to active transport in Escherichia coli membrane vesicles. Ramos, S.; Schuldiner, S.; Kaback, H. R. Proceedings of the National Academy of Sciences, Vol. 73, Issue 6 https://doi.org/10.1073/pnas.73.6.1892	journal	June 1976
Interaction of Verapamil with Lipid Membranes and P-Glycoprotein: Connecting Thermodynamics and Membrane Structure with Functional Activity Meier, M.; Blatter, X. Li; Seelig, A. Biophysical Journal, Vol. 91, Issue 8 https://doi.org/10.1529/biophysj.106.089581	journal	October 2006
Multidrug Transport Protein NorM from Vibrio cholerae Simultaneously Couples to Sodium- and Proton-Motive Force Jin, Yoonhee; Nair, Asha; van Veen, Hendrik W. Journal of Biological Chemistry, Vol. 289, Issue 21 https://doi.org/10.1074/jbc.M113.546770	journal	April 2014
An H+-Coupled Multidrug Efflux Pump, PmpM, a Member of the MATE Family of Transporters, from Pseudomonas aeruginosa He, G. -X.; Kuroda, T.; Mima, T. Journal of Bacteriology, Vol. 186, Issue 1 https://doi.org/10.1128/jb.186.1.262-265.2004	journal	December 2003
MacAB Is Involved in the Secretion of Escherichia coli Heat-Stable Enterotoxin II Yamanaka, H.; Kobayashi, H.; Takahashi, E. Journal of Bacteriology, Vol. 190, Issue 23 https://doi.org/10.1128/JB.00853-08	journal	September 2008
Author Correction: Structural basis for the drug extrusion mechanism by a MATE multidrug transporter Tanaka, Yoshiki; Hipolito, Christopher J.; Maturana, Andrés D. Nature, Vol. 578, Issue 7794 https://doi.org/10.1038/s41586-019-1762-6	journal	January 2020
Long-range electrostatic interaction in the bacterial photosynthetic reaction centre Maróti, Péter; Hanson, Deborah K.; Schiffer, Marianne Nature Structural & Molecular Biology, Vol. 2, Issue 12 https://doi.org/10.1038/nsb1295-1057	journal	December 1995
The multidrug-resistance-reverser verapamil interferes with cellular P-glycoprotein-mediated pumping of daunorubicin as a non-competing substrate Spoelstra, Ellen C.; Westerhoff, Hans V.; Pinedo, Herbert M. European Journal of Biochemistry, Vol. 221, Issue 1 https://doi.org/10.1111/j.1432-1033.1994.tb18748.x	journal	April 1994
Conformational entropy in molecular recognition by proteins Frederick, Kendra King; Marlow, Michael S.; Valentine, Kathleen G. Nature, Vol. 448, Issue 7151 https://doi.org/10.1038/nature05959	journal	July 2007
Multiple molecular mechanisms for multidrug resistance transporters Higgins, Christopher F. Nature, Vol. 446, Issue 7137 https://doi.org/10.1038/nature05630	journal	April 2007
Functional Cloning and Characterization of the Multidrug Efflux Pumps NorM from Neisseria gonorrhoeae and YdhE from Escherichia coli Long, F.; Rouquette-Loughlin, C.; Shafer, W. M. Antimicrobial Agents and Chemotherapy, Vol. 52, Issue 9 https://doi.org/10.1128/aac.00475-08	journal	June 2008
A structure-based mechanism for drug binding by multidrug transporters Zheleznova, Ekaterina E.; Markham, Penelope; Edgar, Rotem Trends in Biochemical Sciences, Vol. 25, Issue 2 https://doi.org/10.1016/s0968-0004(99)01514-5	journal	February 2000
Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances Wiegand, Irith; Hilpert, Kai; Hancock, Robert E. W. Nature Protocols, Vol. 3, Issue 2 https://doi.org/10.1038/nprot.2007.521	journal	January 2008
Functional Cloning and Characterization of the Multidrug Efflux Pumps NorM from Neisseria gonorrhoeae and YdhE from Escherichia coli Long, F.; Rouquette-Loughlin, C.; Shafer, W. M. Antimicrobial Agents and Chemotherapy, Vol. 52, Issue 9 https://doi.org/10.1128/AAC.00475-08	journal	June 2008
Structural insights into H+-coupled multidrug extrusion by a MATE transporter Lu, Min; Radchenko, Martha; Symersky, Jindrich Nature Structural & Molecular Biology, Vol. 20, Issue 11 https://doi.org/10.1038/nsmb.2687	journal	October 2013
Structure of a cation-bound multidrug and toxic compound extrusion transporter He, Xiao; Szewczyk, Paul; Karyakin, Andrey Nature, Vol. 467, Issue 7318 https://doi.org/10.1038/nature09408	journal	September 2010
Last of the multidrug transporters van Veen, Hendrik W. Nature, Vol. 467, Issue 7318 https://doi.org/10.1038/467926a	journal	October 2010
The CCP4 suite programs for protein crystallography No authors listed Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
Structural basis for the drug extrusion mechanism by a MATE multidrug transporter Tanaka, Yoshiki; Hipolito, Christopher J.; Maturana, Andrés D. Nature, Vol. 496, Issue 7444 https://doi.org/10.1038/nature12014	journal	March 2013
Export of a single drug molecule in two transport cycles by a multidrug efflux pump Fluman, Nir; Adler, Julia; Rotenberg, Susan A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5615	journal	August 2014
Characterization of emeA, a norA Homolog and Multidrug Resistance Efflux Pump, in Enterococcus faecalis Jonas, B. M.; Murray, B. E.; Weinstock, G. M. Antimicrobial Agents and Chemotherapy, Vol. 45, Issue 12 https://doi.org/10.1128/AAC.45.12.3574-3579.2001	journal	December 2001
Structure of the Get3 targeting factor in complex with its membrane protein cargo Mateja, A.; Paduch, M.; Chang, H. -Y. Science, Vol. 347, Issue 6226 https://doi.org/10.1126/science.1261671	journal	March 2015
Practical applications and feasibility of efflux pump inhibitors in the clinic—A vision for applied use Lomovskaya, Olga; Bostian, Keith A. Biochemical Pharmacology, Vol. 71, Issue 7 https://doi.org/10.1016/j.bcp.2005.12.008	journal	March 2006
Improved methods for building protein models in electron density maps and the location of errors in these models Jones, T. A.; Zou, J. Y.; Cowan, S. W. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119 https://doi.org/10.1107/S0108767390010224	journal	March 1991
Functional Characteristics of Two Human MATE Transporters: Kinetics of Cimetidine Transport and Profiles of Iinhibition by Various Compounds Ohta, Kin-ya; Inoue, Katsuhisa; Yasujima, Tomoya Journal of Pharmacy & Pharmaceutical Sciences, Vol. 12, Issue 3 https://doi.org/10.18433/j3r59x	journal	September 2009
Antibiotics for Emerging Pathogens Agarwal, Vinayak; Nair, Satish K. Infectious Diseases https://doi.org/10.1007/978-1-4614-5719-0_2	book	December 2012
The Proton Electrochemical Gradient in Escherichia coli Cells Padan, Etana; Zilberstein, Dan; Rottenberg, Hagai European Journal of Biochemistry, Vol. 63, Issue 2 https://doi.org/10.1111/j.1432-1033.1976.tb10257.x	journal	April 1976
Functional Cloning and Characterization of a Plant Efflux Carrier for Multidrug and Heavy Metal Detoxification Li, Legong; He, Zengyong; Pandey, Girdhar K. Journal of Biological Chemistry, Vol. 277, Issue 7 https://doi.org/10.1074/jbc.M108777200	journal	December 2001
Structures of a Na+-coupled, substrate-bound MATE multidrug transporter Lu, M.; Symersky, J.; Radchenko, M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 6 https://doi.org/10.1073/pnas.1219901110	journal	January 2013
Antibiotic efflux pumps in Gram-negative bacteria: the inhibitor response strategy Mahamoud, Abdallah; Chevalier, Jacqueline; Alibert-Franco, Sandrine Journal of Antimicrobial Chemotherapy, Vol. 59, Issue 6 https://doi.org/10.1093/jac/dkl493	journal	January 2007
Identification and Functional Characterization of a New Human Kidney–Specific H ⁺ /Organic Cation Antiporter, Kidney-Specific Multidrug and Toxin Extrusion 2 Masuda, Satohiro; Terada, Tomohiro; Yonezawa, Atsushi Journal of the American Society of Nephrology, Vol. 17, Issue 8 https://doi.org/10.1681/ASN.2006030205	journal	June 2006
Antibiotics for Emerging Pathogens Fischbach, M. A.; Walsh, C. T. Science, Vol. 325, Issue 5944 https://doi.org/10.1126/science.1176667	journal	August 2009
Multidrug efflux transporters in the MATE family Kuroda, Teruo; Tsuchiya, Tomofusa Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1794, Issue 5 https://doi.org/10.1016/j.bbapap.2008.11.012	journal	May 2009
Structural basis for the inhibition of bacterial multidrug exporters Nakashima, Ryosuke; Sakurai, Keisuke; Yamasaki, Seiji Nature, Vol. 500, Issue 7460, p. 102-106 https://doi.org/10.1038/nature12300	journal	June 2013
Competence-specific induction ofrecAis required for full recombination proficiency during transformation inStreptococcus pneumoniae Mortier-Barrière, Isabelle; de Saizieu, Antoine; Claverys, Jean-Pierre Molecular Microbiology, Vol. 27, Issue 1 https://doi.org/10.1046/j.1365-2958.1998.00668.x	journal	January 1998
A MATE Family Multidrug Efflux Transporter Pumps out Fluoroquinolones in Bacteroides thetaiotaomicron Miyamae, S.; Ueda, O.; Yoshimura, F. Antimicrobial Agents and Chemotherapy, Vol. 45, Issue 12 https://doi.org/10.1128/AAC.45.12.3341-3346.2001	journal	December 2001
Electrostatic activation of Escherichia coli methionine repressor Phillips, Kathryn; Phillips, Simon EV Structure, Vol. 2, Issue 4 https://doi.org/10.1016/S0969-2126(00)00032-0	journal	April 1994
Multidrug Transport Protein NorM from Vibrio cholerae Simultaneously Couples to Sodium- and Proton-Motive Force Jin, Yoonhee; Nair, Asha; van Veen, Hendrik W. Journal of Biological Chemistry, Vol. 289, Issue 21 https://doi.org/10.1074/jbc.m113.546770	journal	April 2014
An H+-Coupled Multidrug Efflux Pump, PmpM, a Member of the MATE Family of Transporters, from Pseudomonas aeruginosa He, G. -X.; Kuroda, T.; Mima, T. Journal of Bacteriology, Vol. 186, Issue 1 https://doi.org/10.1128/JB.186.1.262-265.2004	journal	December 2003
A human transporter protein that mediates the final excretion step for toxic organic cations Otsuka, M.; Matsumoto, T.; Morimoto, R. Proceedings of the National Academy of Sciences, Vol. 102, Issue 50 https://doi.org/10.1073/pnas.0506483102	journal	December 2005
The multidrug efflux protein NorM is a prototype of a new family of transporters Brown, Melissa H.; Paulsen, Ian T.; Skurray, Ronald A. Molecular Microbiology, Vol. 31, Issue 1 https://doi.org/10.1046/j.1365-2958.1999.01162.x	journal	January 1999
Functional Characteristics of Two Human MATE Transporters: Kinetics of Cimetidine Transport and Profiles of Iinhibition by Various Compounds Ohta, Kin-ya; Inoue, Katsuhisa; Yasujima, Tomoya Journal of Pharmacy & Pharmaceutical Sciences, Vol. 12, Issue 3 https://doi.org/10.18433/J3R59X	journal	September 2009
MacAB Is Involved in the Secretion of Escherichia coli Heat-Stable Enterotoxin II Yamanaka, H.; Kobayashi, H.; Takahashi, E. Journal of Bacteriology, Vol. 190, Issue 23 https://doi.org/10.1128/jb.00853-08	journal	September 2008
AbeM, an H+-Coupled Acinetobacter baumannii Multidrug Efflux Pump Belonging to the MATE Family of Transporters Su, X. -Z.; Chen, J.; Mizushima, T. Antimicrobial Agents and Chemotherapy, Vol. 49, Issue 10 https://doi.org/10.1128/aac.49.10.4362-4364.2005	journal	September 2005

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Broadly conserved Na ⁺ -binding site in the N-lobe of prokaryotic multidrug MATE transporters Ficici, Emel; Zhou, Wenchang; Castellano, Steven Proceedings of the National Academy of Sciences, Vol. 115, Issue 27 https://doi.org/10.1073/pnas.1802080115	journal	June 2018
Genomic and phenotypic characterisation of fluoroquinolone resistance mechanisms in Enterobacteriaceae in Durban, South Africa Osei Sekyere, John; Amoako, Daniel Gyamfi PLOS ONE, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pone.0178888	journal	June 2017
Sodium and proton coupling in the conformational cycle of a MATE antiporter from Vibrio cholerae Claxton, Derek P.; Jagessar, Kevin L.; Steed, P. Ryan Proceedings of the National Academy of Sciences, Vol. 115, Issue 27 https://doi.org/10.1073/pnas.1802417115	journal	June 2018
The multitasking abilities of MATE transporters in plants Upadhyay, Neha; Kar, Debojyoti; Deepak Mahajan, Bhagyashri Journal of Experimental Botany, Vol. 70, Issue 18 https://doi.org/10.1093/jxb/erz246	journal	May 2019
Inward-facing conformation of a multidrug resistance MATE family transporter Zakrzewska, Sandra; Mehdipour, Ahmad Reza; Malviya, Viveka Nand Proceedings of the National Academy of Sciences, Vol. 116, Issue 25 https://doi.org/10.1073/pnas.1904210116	journal	June 2019
Efflux pump inhibitors for bacterial pathogens: From bench to bedside Pathania, Ranjana; Sharma, Atin; Gupta, VivekKumar Indian Journal of Medical Research, Vol. 149, Issue 2 https://doi.org/10.4103/ijmr.ijmr_2079_17	journal	January 2019
Multidrug efflux pumps: structure, function and regulation Du, Dijun; Wang-Kan, Xuan; Neuberger, Arthur Nature Reviews Microbiology, Vol. 16, Issue 9 https://doi.org/10.1038/s41579-018-0048-6	journal	July 2018
Functional characterization and discovery of modulators of SbMATE, the agronomically important aluminium tolerance transporter from Sorghum bicolor Doshi, Rupak; McGrath, Aaron P.; Piñeros, Miguel Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-18146-8	journal	December 2017
Structural basis for xenobiotic extrusion by eukaryotic MATE transporter Miyauchi, Hirotake; Moriyama, Satomi; Kusakizako, Tsukasa Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01541-0	journal	November 2017
Tackling drug resistance with efflux pump inhibitors: from bacteria to cancerous cells Lowrence, Rene Christena; Subramaniapillai, Selva Ganesan; Ulaganathan, Venkatasubramanian Critical Reviews in Microbiology, Vol. 45, Issue 3 https://doi.org/10.1080/1040841x.2019.1607248	journal	April 2019
Functional characterization and discovery of modulators of SbMATE, the agronomically important aluminium tolerance transporter from Sorghum bicolor Doshi, Rupak; McGrath, Aaron P.; Pineros, Miguel Scientific Reports https://doi.org/10.1101/182964	journal	August 2017
Lipid Flippases for Bacterial Peptidoglycan Biosynthesis Ruiz, Natividad Lipid Insights, Vol. 8s1 https://doi.org/10.4137/lpi.s31783	journal	January 2015
Pacing across the membrane: the novel PACE family of efflux pumps is widespread in Gram-negative pathogens Hassan, Karl A.; Liu, Qi; Elbourne, Liam D. H. Research in Microbiology, Vol. 169, Issue 7-8 https://doi.org/10.1016/j.resmic.2018.01.001	journal	September 2018
Carbonyl Cyanide m-Chlorophenylhydrazine (CCCP) Reverses Resistance to Colistin, but Not to Carbapenems and Tigecycline in Multidrug-Resistant Enterobacteriaceae Osei Sekyere, John; Amoako, Daniel G. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00228	journal	February 2017
The putative drug efflux systems of the Bacillus cereus group Hassan, Karl A.; Fagerlund, Annette; Elbourne, Liam D. H. PLOS ONE, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pone.0176188	journal	May 2017
Structures of multidrug and toxic compound extrusion transporters and their mechanistic implications Lu, Min Channels, Vol. 10, Issue 2 https://doi.org/10.1080/19336950.2015.1106654	journal	January 2016
The N-terminal domain of an archaeal multidrug and toxin extrusion (MATE) transporter mediates proton coupling required for prokaryotic drug resistance Jagessar, Kevin L.; Mchaourab, Hassane S.; Claxton, Derek P. Journal of Biological Chemistry, Vol. 294, Issue 34 https://doi.org/10.1074/jbc.ra119.009195	journal	July 2019
Structure of an engineered multidrug transporter MdfA reveals the molecular basis for substrate recognition Wu, Hsin-Hui; Symersky, Jindrich; Lu, Min Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0446-y	journal	June 2019

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