Principles of Alternating Access in Multidrug and Toxin Extrusion (MATE) Transporters
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The multidrug and toxin extrusion (MATE) transporters catalyze active efflux of a broad range of chemically- and structurally-diverse compounds including antimicrobials and chemotherapeutics, thus contributing to multidrug resistance in pathogenic bacteria and cancers. Multiple methodological approaches have been taken to investigate the structural basis of energy transduction and substrate translocation in MATE transporters. Crystal structures representing members from all three MATE subfamilies have been interpreted within the context of an alternating access mechanism that postulates occupation of distinct structural intermediates in a conformational cycle powered by electrochemical ion gradients. Here we review the structural biology of MATE transporters, integrating the crystallographic models with biophysical and computational studies to define the molecular determinants that shape the transport energy landscape. This holistic analysis highlights both shared and disparate structural and functional features within the MATE family, which underpin an emerging theme of mechanistic diversity within the framework of a conserved structural scaffold.
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The divergence in performance may stem from the composition of the AF2 training set, which featured structures of many active GPCRs but no structures of IF MATEs.
“This divergence in performance may stem from the composition of the AF2 training set, which featured the structures of many active GPCRs but no structures, for example, of IF MATEs (Claxton et al., 2021).”
From Sampling alternative conformational states of transporters and receptors with AlphaFold2 (2022) · cites this paper as Claxton et al., 2021
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MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · see citing works
Tacconelli, E., Carrara, E., Savoldi, A., Harbarth, S., Mendelson, M., Monnet, D. L., Pulcini, C., Kahlmeter, G., Kluytmans, J., Carmeli, Y., et al. (2018) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(17)30753-3 · Cited by 6,142 · see citing works
Multidrug resistance in cancer: role of ATP–dependent transporters
Gottesman, M. M., Fojo, T., & Bates, S. E. (2002) · Nature Reviews Cancer · doi:10.1038/nrc706 · Cited by 5,536 · see citing works
Molecular mechanisms of antibiotic resistance
Blair, J. M. A., Webber, M. A., Baylay, A. J., Ogbolu, D. O., & Piddock, L. J. V. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3380 · Cited by 4,092 · see citing works
Crystal structure of a bacterial homologue of Na+/Cl--dependent neurotransmitter transporters
Yamashita, A., Singh, S. K., Kawate, T., Jin, Y., & Gouaux, E. (2005) · Nature · doi:10.1038/nature03978 · Cited by 1,660 · see citing works
Structure and Mechanism of the Lactose Permease of Escherichia coli
Abramson, J., Smirnova, I., Kasho, V. N., Verner, G., Kaback, H. R., & Iwata, S. (2003) · Science · doi:10.1126/science.1088196 · Cited by 1,389 · see citing works
Simple Allosteric Model for Membrane Pumps
Jardetzky, O. (1966) · Nature · doi:10.1038/211969a0 · Cited by 1,293 · see citing works
Structure and Mechanism of the Glycerol-3-Phosphate Transporter from Escherichia coli
Huang, Y., Lemieux, M. J., Song, J., Auer, M., & Wang, D. (2003) · Science · doi:10.1126/science.1087619 · Cited by 1,015 · see citing works
The Transporter Classification Database (TCDB): recent advances
Saier, M. H., Reddy, V. S., Tsu, B. V., Ahmed, M. S., Li, C., & Moreno‐Hagelsieb, G. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1103 · Cited by 989 · see citing works
Multiple molecular mechanisms for multidrug resistance transporters
Higgins, C. F. (2007) · Nature · doi:10.1038/nature05630 · Cited by 863 · see citing works
Structure of a glutamate transporter homologue from Pyrococcus horikoshii
Yernool, D., Boudker, O., Jin, Y., & Gouaux, E. (2004) · Nature · doi:10.1038/nature03018 · Cited by 784 · see citing works
Membrane protein assembly into Nanodiscs
Bayburt, T. H., & Sligar, S. G. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.10.024 · Cited by 730 · see citing works
A human transporter protein that mediates the final excretion step for toxic organic cations
Otsuka, M., Matsumoto, T., Morimoto, R., Arioka, S., Omote, H., & Moriyama, Y. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506483102 · Cited by 571 · see citing works
Detergents as Tools in Membrane Biochemistry
Garavito, R. M., & Ferguson-Miller, S. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.r100031200 · Cited by 568 · see citing works
Shared Molecular Mechanisms of Membrane Transporters
Drew, D., & Boudker, O. (2016) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060815-014520 · Cited by 506 · see citing works
Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter
Boudker, O., Ryan, R. M., Yernool, D., Shimamoto, K., & Gouaux, E. (2007) · Nature · doi:10.1038/nature05455 · Cited by 485 · see citing works
The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations
Omote, H., Hiasa, M., Matsumoto, T., Otsuka, M., & Moriyama, Y. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.09.001 · Cited by 433 · see citing works
Multidrug efflux transporters in the MATE family
Kuroda, T., & Tsuchiya, T. (2008) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2008.11.012 · Cited by 402 · see citing works
Morita, Y., Kodama, K., Shiota, S., Mine, T., Kataoka, A., Mizushima, T., & Tsuchiya, T. (1998) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.42.7.1778 · Cited by 391 · see citing works
The multidrug efflux protein NorM is a prototype of a new family of transporters
Brown, M. H., Paulsen, I. T., & Skurray, R. A. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01162.x · Cited by 382 · see citing works
Masuda, S., Terada, T., Yonezawa, A., Tanihara, Y., Kishimoto, K., Katsura, T., Ogawa, O., & Inui, K. (2006) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006030205 · Cited by 370 · see citing works
Phylogeny of multidrug transporters
Saier, M. H., & Paulsen, I. T. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0246 · Cited by 333 · see citing works
Maron, L. G., Piñeros, M. A., Guimarães, C. T., de Magalhães, J. V., Pleiman, J. K., Mao, C., Shaff, J. E., Belicuas, S. N. J., & Kochian, L. V. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2009.04103.x · Cited by 316 · see citing works
Zhang, H., Zhu, H., Pan, Y., Yu, Y., Luan, S., & Li, L. (2014) · Molecular Plant · doi:10.1093/mp/ssu063 · Cited by 289 · see citing works
A General Theory of Membrane Transport From Studies of Bacteria
Mitchell, P. D. (1957) · Nature · doi:10.1038/180134a0 · Cited by 279 · see citing works
Kaatz, G. W., McAleese, F., & Seo, S. M. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.5.1857-1864.2005 · Cited by 279 · see citing works
Structure of a cation-bound multidrug and toxic compound extrusion transporter
He, X., Szewczyk, P., Karyakin, A., Evin, M., Hong, W., Zhang, Q., & Chang, G. A. (2010) · Nature · doi:10.1038/nature09408 · Cited by 272 · see citing works
The multidrug/oligosaccharidyl‐lipid/polysaccharide (MOP) exporter superfamily
Hvorup, R. N., Winnen, B., Chang, A. B., Jiang, Y., Zhou, X., & Saier, M. H. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03418.x · Cited by 255 · see citing works
Differential hydrogen/deuterium exchange mass spectrometry analysis of protein–ligand interactions
Chalmers, M. J., Busby, S. A., Pascal, B. D., West, G. M., & Griffin, P. R. (2011) · Expert Review of Proteomics · doi:10.1586/epr.10.109 · Cited by 255 · see citing works
Structural basis for the drug extrusion mechanism by a MATE multidrug transporter
Tanaka, Y., Hipolito, C. J., Maturana, A. D., Ito, K., Kuroda, T., Higuchi, T., Katoh, T., KATO, H. E., Hattori, M., Kumazaki, K., et al. (2013) · Nature · doi:10.1038/nature12014 · Cited by 250 · see citing works
Energy transduction and alternating access of the mammalian ABC transporter P-glycoprotein
Verhalen, B., Dastvan, R., Thangapandian, S., Peskova, Y. B., Koteiche, H. A., Nakamoto, R. K., Tajkhorshid, E., & Mchaourab, H. S. (2017) · Nature · doi:10.1038/nature21414 · Cited by 249 · see citing works
McAleese, F., Petersen, P. J., Ruzin, A. V., Dunman, P. M., Murphy, E., Projan, S. J., & Bradford, P. A. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.5.1865-1871.2005 · Cited by 233 · see citing works
Disruption of multidrug and toxin extrusion MATE1 potentiates cisplatin-induced nephrotoxicity
Nakamura, T., Yonezawa, A., Hashimoto, S., Katsura, T., & Inui, K. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.08.019 · Cited by 221 · see citing works
Yonezawa, A., & Inui, K. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01394.x · Cited by 196 · see citing works
Arabidopsis ALF5 , a Multidrug Efflux Transporter Gene Family Member, Confers Resistance to Toxins
Diener, A. C., Gaxiola, R. A., & Fink, G. R. (2001) · The Plant Cell · doi:10.1105/tpc.010035 · Cited by 195 · see citing works
Tal, N., & Schuldiner, S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902400106 · Cited by 194 · see citing works
Tsuda, M., Terada, T., Ueba, M., Sato, T., Masuda, S., Katsura, T., & Inui, K. (2009) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.108.147918 · Cited by 194 · see citing works
NorM of Vibrio parahaemolyticus Is an Na + -Driven Multidrug Efflux Pump
Morita, Y., Kataoka, A., Shiota, S., Mizushima, T., & Tsuchiya, T. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.23.6694-6697.2000 · Cited by 182 · see citing works
Probing protein interactions with hydrogen/deuterium exchange and mass spectrometry—A review
Percy, A. J., Rey, M., Burns, K. M., & Schriemer, D. C. (2012) · Analytica Chimica Acta · doi:10.1016/j.aca.2012.01.037 · Cited by 166 · see citing works
Structure, mechanism and cooperation of bacterial multidrug transporters
Du, D., van Veen, H. W., Murakami, S., Pos, K. M., & Luisi, B. F. (2015) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2015.07.015 · Cited by 155 · see citing works
Ito, S., Kusuhara, H., Kuroiwa, Y., Wu, C., Moriyama, Y., Inoue, K., Kondo, T., Yuasa, H., Nakayama, H., Horita, S., et al. (2010) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.163642 · Cited by 153 · see citing works
Hassan, K. A., Liu, Q., Elbourne, L. D. H., Ahmad, I., Sharples, D. J., Naidu, V., Chan, C. L., Li, L., Harborne, S. P. D., Pokhrel, A., et al. (2018) · Research in Microbiology · doi:10.1016/j.resmic.2018.01.001 · Cited by 146 · see citing works
Conformational dynamics of ligand-dependent alternating access in LeuT
Kazmier, K. N., Sharma, S., Quick, M., Islam, S. M., Roux, B., Weinstein, H., Javitch, J., & Mchaourab, H. (2014) · Nature Structural &Molecular Biology · doi:10.1038/nsmb.2816 · Cited by 145 · see citing works
Structures of a Na + -coupled, substrate-bound MATE multidrug transporter
Lu, M., Symersky, J., Radchenko, M. V., Koide, A., Guo, Y., Nie, R., & Koide, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219901110 · Cited by 142 · see citing works
Direct protein-lipid interactions shape the conformational landscape of secondary transporters
Martens, C., Shekhar, M., Borysik, A. J., Lau, A. M., Reading, E., Tajkhorshid, E., Booth, P. J., & Politis, A. (2018) · Nature Communications · doi:10.1038/s41467-018-06704-1 · Cited by 134 · see citing works
Conformational ensemble of the sodium-coupled aspartate transporter
Georgieva, E. R., Borbat, P. P., Ginter, C. S., Freed, J. H., & Boudker, O. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2494 · Cited by 129 · see citing works
Rouquette, C., Dunham, S. A., Kuhn, M., Balthazar, J. T., & Shafer, W. M. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.3.1101-1106.2003 · Cited by 129 · see citing works
Structural basis for the blockade of MATE multidrug efflux pumps
Radchenko, M. V., Symersky, J., Nie, R., & Lu, M. (2015) · Nature Communications · doi:10.1038/ncomms8995 · Cited by 127 · see citing works
Structural biology of the multidrug and toxic compound extrusion superfamily transporters
Kusakizako, T., Miyauchi, H., Ishitani, R., & Nureki, O. (2019) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2019.183154 · Cited by 110 · see citing works
Structural insights into H+-coupled multidrug extrusion by a MATE transporter
Lu, M., Radchenko, M. V., Symersky, J., Nie, R., & Guo, Y. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2687 · Cited by 103 · see citing works
Structural basis for xenobiotic extrusion by eukaryotic MATE transporter
Miyauchi, H., Moriyama, S., Kusakizako, T., Kumazaki, K., Nakane, T., Yamashita, K., Hirata, K., Dohmae, N., Nishizawa, T., Ito, K., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01541-0 · Cited by 101 · see citing works
Interrogating Membrane Protein Conformational Dynamics within Native Lipid Compositions
Reading, E., Hall, Z., Martens, C., Haghighi, T., Findlay, H. E., Ahdash, Z., Politis, A., & Booth, P. J. (2017) · Angewandte Chemie International Edition · doi:10.1002/anie.201709657 · Cited by 100 · see citing works
Crystal structure of the MOP flippase MurJ in an inward-facing conformation
Kuk, A. C. Y., Mashalidis, E. H., & Lee, S. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3346 · Cited by 91 · see citing works
MATE transport of the E. coli-derived genotoxin colibactin
Mousa, J. J., Yang, Y., Tomkovich, S., Shima, A., Newsome, R. C., Tripathi, P., Oswald, É., Bruner, S. D., & Jobin, C. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2015.9 · Cited by 90 · see citing works
Long, F., Rouquette, C., Shafer, W. M., & Yu, E. W. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00475-08 · Cited by 82 · see citing works
Jia, R., Martens, C., Shekhar, M., Pant, S., Pellowe, G. A., Lau, A. M. C., Findlay, H. E., Harris, N. J., Tajkhorshid, E., Booth, P. J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-20032-3 · Cited by 82 · see citing works
Conformational dynamics of a neurotransmitter:sodium symporter in a lipid bilayer
Adhikary, S., Deredge, D. J., Nagarajan, A., Forrest, L. R., Wintrode, P. L., & Singh, S. K. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1613293114 · Cited by 80 · see citing works
Visualizing conformation transitions of the Lipid II flippase MurJ
Kuk, A. C. Y., Hao, A., Guan, Z., & Lee, S. (2019) · Nature Communications · doi:10.1038/s41467-019-09658-0 · Cited by 76 · see citing works
Structures of multidrug and toxic compound extrusion transporters and their mechanistic implications
Lu, M. (2015) · Channels · doi:10.1080/19336950.2015.1106654 · Cited by 74 · see citing works
Two MATE proteins play a role in iron efficiency in soybean
Rogers, E. E., Wu, X., Stacey, G. S., & Nguyen, H. T. (2009) · Journal of Plant Physiology · doi:10.1016/j.jplph.2009.02.009 · Cited by 68 · see citing works
Protonation-dependent conformational dynamics of the multidrug transporter EmrE
Dastvan, R., Fischer, A. W., Mishra, S., Meiler, J., & Mchaourab, H. S. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520431113 · Cited by 59 · see citing works
Jin, Y., Nair, A. V., & van Veen, H. W. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.546770 · Cited by 58 · see citing works
Begum, A., Rahman, M., Ogawa, W., Mizushima, T., Kuroda, T., & Tsuchiya, T. (2005) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2005.tb03690.x · Cited by 56 · see citing works
The AbgT family: A novel class of antimetabolite transporters
Delmar, J. A., & Yu, E. W. (2015) · Protein Science · doi:10.1002/pro.2820 · Cited by 55 · see citing works
Crystal Structure of a Plant Multidrug and Toxic Compound Extrusion Family Protein
Tanaka, Y., Iwaki, S., & Tsukazaki, T. (2017) · Structure · doi:10.1016/j.str.2017.07.009 · Cited by 51 · see citing works
Alibert, S., N'gompaza‐Diarra, J., Hernandez, J., Stutzmann, A., Fouad, M. A., Boyer, G., & Pagès, J. (2016) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1080/17425255.2017.1251581 · Cited by 50 · see citing works
Membrane Potential Is Required for MurJ Function
Rubino, F. A., Kumar, S., Ruiz, N., Walker, S., & Kahne, D. E. (2018) · Journal of the American Chemical Society · doi:10.1021/jacs.8b00942 · Cited by 49 · see citing works
The bacterial lipid II flippase MurJ functions by an alternating-access mechanism
Kumar, S., Rubino, F. A., Mendoza, A. G., & Ruiz, N. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006099 · Cited by 49 · see citing works
Inward-facing conformation of a multidrug resistance MATE family transporter
Zakrzewska, S., Mehdipour, A. R., Malviya, V. N., Nonaka, T., Koepke, J., Muenke, C., Hausner, W., Hummer, G., Safarian, S., & Michel, H. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904210116 · Cited by 49 · see citing works
Matsumoto, T., Kanamoto, T., Otsuka, M., Omote, H., & Moriyama, Y. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00504.2007 · Cited by 42 · see citing works
Sequence and structural determinants of ligand-dependent alternating access of a MATE transporter
Jagessar, K. L., Claxton, D. P., Stein, R. A., & Mchaourab, H. S. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1917139117 · Cited by 42 · see citing works
Competition as a Way of Life for H+-Coupled Antiporters
Schuldiner, S. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.05.020 · Cited by 37 · see citing works
Singh, A. K., Haldar, R., Mandal, D., & Kundu, M. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00460-06 · Cited by 36 · see citing works
Vanni, S., Campomanes, P., Marcia, M., & Röthlisberger, U. (2012) · Biochemistry · doi:10.1021/bi2015184 · Cited by 32 · see citing works
Mousa, J. J., Newsome, R. C., Yang, Y., Jobin, C., & Bruner, S. D. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.12.018 · Cited by 30 · see citing works
Song, J., Ji, C., & Zhang, J. Z. H. (2013) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.24368 · Cited by 27 · see citing works
Sodium and proton coupling in the conformational cycle of a MATE antiporter from Vibrio cholerae
Claxton, D. P., Jagessar, K. L., Steed, R., Stein, R. A., & Mchaourab, H. S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1802417115 · Cited by 27 · see citing works
Broadly conserved Na + -binding site in the N-lobe of prokaryotic multidrug MATE transporters
Ficici, E., Zhou, W., Castellano, S., & Faraldo‐Gómez, J. D. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1802080115 · Cited by 26 · see citing works
Structural Basis of H+-Dependent Conformational Change in a Bacterial MATE Transporter
Kusakizako, T., Claxton, D. P., Tanaka, Y., Maturana, A. D., Kuroda, T., Ishitani, R., Mchaourab, H. S., & Nureki, O. (2018) · Structure · doi:10.1016/j.str.2018.10.004 · Cited by 26 · see citing works
Nie, L., Grell, E., Malviya, V. N., Xie, H., Wang, J., & Michel, H. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.728618 · Cited by 24 · see citing works
Na+–Substrate Coupling in the Multidrug Antiporter NorM Probed with a Spin-Labeled Substrate
Steed, R., Stein, R. A., Mishra, S., Goodman, M., & Mchaourab, H. S. (2013) · Biochemistry · doi:10.1021/bi4008935 · Cited by 22 · see citing works
Leung, Y. M., Holdbrook, D. A., Piggot, T. J., & Khalid, S. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2014.06.005 · Cited by 21 · see citing works
On the ion coupling mechanism of the MATE transporter ClbM
Krah, A., Huber, R. G., Zachariae, U., & Bond, P. J. (2019) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2019.183137 · Cited by 20 · see citing works
The Xenobiotic Extrusion Mechanism of the MATE Transporter NorM_PS from Pseudomonas stutzeri
Eisinger, M., Nie, L., Dörrbaum, A. R., Langer, J. D., & Michel, H. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.03.012 · Cited by 19 · see citing works
Jagessar, K. L., Mchaourab, H. S., & Claxton, D. P. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.009195 · Cited by 16 · see citing works
Radchenko, M. V., Nie, R., & Lu, M. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.715227 · Cited by 15 · see citing works
Möller, I. R., Merkle, P. S., Calugareanu, D., Comamala, G., Schmidt, S. G., Loland, C. J., & Rand, K. D. (2020) · Journal of Proteomics · doi:10.1016/j.jprot.2020.103845 · Cited by 15 · see citing works
Castellano, S., Claxton, D. P., Ficici, E., Kusakizako, T., Stix, R., Zhou, W., Nureki, O., Mchaourab, H. S., & Faraldo‐Gómez, J. D. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100262 · Cited by 11 · see citing works
Visualizing Conformation Transitions of the Lipid Flippase MurJPreprint
Kuk, A. C. Y., Hao, A., Guan, Z., & Lee, S. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/552745 · Cited by 10 · see citing works
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Sampling alternative conformational states of transporters and receptors with AlphaFold2
del Alamo, D., Sala, D., Mchaourab, H. S., & Meiler, J. (2022) · eLife · doi:10.7554/elife.75751 · Cited by 511 · see citing works
“This divergence in performance may stem from the composition of the AF2 training set, which featured the structures of many active GPCRs but no structures, for example, of IF MATEs ( Claxton et al., 2021 ).”
BackgroundThe Bacterial Cell Wall: From Lipid II Flipping to Polymerization
Kumar, S., Mollo, A., Kahne, D. E., & Ruiz, N. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00773 · Cited by 105 · see citing works
Ion and lipid orchestration of secondary active transport
Drew, D., & Boudker, O. (2024) · Nature · doi:10.1038/s41586-024-07062-3 · Cited by 73 · see citing works
Plant Secondary Metabolite Transporters: Diversity, Functionality, and Their Modulation
Nogia, P., & Pati, P. K. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.758202 · Cited by 65 · see citing works
Membrane Efflux Pumps of Pathogenic Vibrio Species: Role in Antimicrobial Resistance and Virulence
Stephen, J., Lekshmi, M., Parvathi, A., Kumar, S. H., & Varela, M. F. (2022) · Microorganisms · doi:10.3390/microorganisms10020382 · Cited by 40 · see citing works
Lei, Y., Asamizu, S., Ishizuka, T., & Onaka, H. (2023) · Applied and Environmental Microbiology · doi:10.1128/aem.01822-22 · Cited by 16 · see citing works
Lin, K., Wang, R., Li, T., Zuo, Y., Yang, S., Dong, D., & Zhu, Y. (2025) · Biomolecules · doi:10.3390/biom15060864 · Cited by 16 · see citing works
Chu, Y., Chen, X., Li, S., Li, X., Xie, P., & Ho, S. (2024) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2024.136228 · Cited by 12 · see citing works
Zhang, S., Wu, H., Day, C. S., & Bierbach, U. (2023) · ACS Medicinal Chemistry Letters · doi:10.1021/acsmedchemlett.3c00266 · Cited by 11 · see citing works
Li, W., Zhang, Z., Liao, K., Shi, Q., Huang, X., & Xie, X. (2025) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2025.106096 · Cited by 11 · see citing works
Kumar, S. H., Lekshmi, M., Stephen, J., Ortiz-Alegria, A., Ayitah, M., & Varela, M. F. (2023) · Archives of Microbiology · doi:10.1007/s00203-023-03731-5 · Cited by 8 · see citing works
Chanket, W., Pipatthana, M., Sangphukieo, A., Harnvoravongchai, P., Chankhamhaengdecha, S., Janvilisri, T., & Phanchana, M. (2024) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2024.05.027 · Cited by 7 · see citing works
Cai, J., Longo, A., & Dickstein, R. (2024) · Frontiers in Plant Science · doi:10.3389/fpls.2023.1306491 · Cited by 5 · see citing works
Handa, K., Sasaki, S., Asano, S., Kageyama, M., Iijima, T., & Bender, A. (2024) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.4c00921 · Cited by 6 · see citing works
Kovacec, V., Gregorio, S. D., Pajón, M., Crestani, C., Poklépovich, T., Campos, J., Khan, U. B., Bentley, S. D., Jamrozy, D. M., Mollerach, M. E., et al. (2024) · Microbial Genomics · doi:10.1099/mgen.0.001297 · Cited by 2 · see citing works
Ahmed, N., Biswas, P., Mogal, M. R., Sarker, M. R., Tareq, M. M. I., Ahmed, S., Akter, M., Miah, M. T., Kundo, N. K., Hasan, M. N., et al. (2024) · Informatics in Medicine Unlocked · doi:10.1016/j.imu.2024.101493 · Cited by 1 · see citing works
The Role of Protonation in the PfMATE Transporter Protein Structural Transitions
Hossen, M. L., Bhattarai, N., Chapagain, P. P., & Gerstman, B. S. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-4213-9_16 · Cited by 1 · see citing works
Conformational Landscape of the Di- and Tripeptide Permease A Transport Cycle
Singh, A. K., Apurva, S., Tazally, K. J., D’Costa, C. K., Prabhala, B. K., & Haider, S. M. (2025) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.5c00753 · Cited by 1 · see citing works
Inroads into Membrane Physiology through Transport Nanomachines
Stockbridge, R. B., Gaudet, R., Grabe, M., & Minor, D. L. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.167101 · Cited by 1 · see citing works
Flechsig, H. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.15.464530 · Cited by 1 · see citing works
The role of protonation in the PfMATE transporter protein structural transitionsPreprint
Gerstman, B. S., Hossen, M., Bhattarai, N., & Chapagain, P. P. (2023) · doi:10.22541/au.169645521.18264971/v1 · Cited by 1 · see citing works
Kumari, V., & Kanwar, S. S. (2022) · Chemistry Africa · doi:10.1007/s42250-022-00414-4
Lei, Y., Asamizu, S., Ishizuka, T., & Onaka, H. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.11.516236
Li, W., Tu, Z., Zhang, H., Lu, B., Liu, F., Lin, X., & Wang, G. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1689335
Mandal, S. K., Assaiya, A., & Prakash, V. S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-33702-4.00002-5
Ferrara, B. T., & Thompson, E. P. (2026) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2026.02.002
Pieters, J., Conradie, T. A., & Jacobs, K. (2026) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijsem.0.007213
Kushwaha, H., Mishra, J., & Mohapatra, H. (2026) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2026.184566
Paul, A., Xu, L., & Shukla, D. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.13.751325
- Authors
- Claxton, D. P., Jagessar, K. L., & Mchaourab, H. S.
- Affiliations
- Vanderbilt University (US)
- Corresponding author
- Mchaourab, Hassane S.
- Venue
- Journal of Molecular Biology
- Publisher
- Elsevier BV
- Published
- 2021-08
- Volume
- 433
- Issue
- 16
- Pages
- 166959
- ISSN
- 0022-2836 (ISSN-L)
- PMC
- PMC8292195
- OpenAlex
- W3136754634
- Cited by
- 29
- References
- 89
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 8 · 2023: 4 · 2022: 5 · 2021: 3
- FWCI
- 0.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Journal of Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (R01-GM077659)
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Keywords
- MATE transporters, alternating access mechanism, multidrug resistance, active efflux, crystal structure, conformational cycle, substrate translocation, energy transduction, antimicrobial resistance, chemoresistance
- MeSH terms
- Animals, Drug Resistance, Humans, Models, Molecular, Protein Conformation, Structure-Activity Relationship, Conserved Sequence, Organic Cation Transport Proteins
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