An updated structural classification of substrate-binding proteins.
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Substrate-binding proteins (SBPs) play an important role in solute uptake and signal transduction. In 2010, Berntsson et al. classified the 114 organism-specific SBP structures available at that time and defined six protein clusters, based on their structural similarity. Since then, the number of unique SBP structures has increased almost fivefold, whereas the number of protein entries in the Protein Data Bank (PDB) nearly doubled. On the basis of the much larger dataset, we now subclassify the SBPs within the original clusters. Moreover, we propose a 7th cluster based on a small group of SBPs with structural features significantly different from those observed in the other proteins.
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The PyMOL Molecular Graphics System
DeLano, W. L. (2002) · Medical Entomology and Zoology · Cited by 18,147 · see citing works
PHYLIP-Phylogeny inference package (Version 3.2)
Felsenstein, J. (1989) · Cladistics · Cited by 17,848 · see citing works
Letunic, I., & Bork, P. (2016) · Nucleic Acids Res. · doi:10.1093/nar/gkw290 · Cited by 4,851 · see citing works
ABC Transporters: From Microorganisms to Man
Higgins, C. F. (1992) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.08.110192.000435 · Cited by 3,985 · see citing works
Krissinel, E., & Henrick, K. (2004) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444904026460 · Cited by 3,785 · see citing works
ABC transporters: the power to change
Rees, D. C., Johnson, E., & Lewinson, O. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2646 · Cited by 1,454 · see citing works
Mechanistic diversity in ATP-binding cassette (ABC) transporters.
Locher, K. P. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3216 · Cited by 804 · see citing works
Tam, R., & Saier, M. H. (1993) · Microbiological Reviews · doi:10.1128/mr.57.2.320-346.1993 · Cited by 732 · see citing works
O’Hara, P. J., Sheppard, P. O., Thøgersen, H., Venezia, D., Haldeman, B. A., McGrane, V., Houamed, K. M., Thomsen, C., Gilbert, T., & Mulvihill, E. R. (1993) · Neuron · doi:10.1016/0896-6273(93)90269-w · Cited by 707 · see citing works
Mechanism of glutamate receptor desensitization
Sun, Y., Olson, R., Horning, M. S., Armstrong, N., Mayer, M. L., & Gouaux, E. (2002) · Nature · doi:10.1038/417245a · Cited by 662 · see citing works
FFAS03: a server for profile-profile sequence alignments
Jaroszewski, L., Rychlewski, L., Li, Z., Li, W., & Godzik, A. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki418 · Cited by 590 · see citing works
A structural classification of substrate‐binding proteins
Berntsson, R. P. ‐., Smits, S. H. J., Schmitt, L., Slotboom, D.-J., & Poolman, B. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.04.043 · Cited by 552 · see citing works
Self-citationStructure of an ABC transporter in complex with its binding protein
Hollenstein, K., Frei, D. C., & Locher, K. P. (2007) · Nature · doi:10.1038/nature05626 · Cited by 506 · see citing works
Crystal Structure of LacI Member, PurR, Bound to DNA: Minor Groove Binding by α Helices
Schumacher, M. A., Choi, K. Y., Zalkin, H., & Brennan, R. G. (1994) · Science · doi:10.1126/science.7973627 · Cited by 371 · see citing works
Hinge-bending in L-arabinose-binding protein. The “Venus's-flytrap” model.
Mao, B., Pear, M. R., McCammon, J. A., & Quiocho, F. A. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)68161-5 · Cited by 268 · see citing works
The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter
Borths, E. L., Locher, K. P., Lee, A. T., & Rees, D. C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.262659699 · Cited by 225 · see citing works
Fukami-Kobayashi, K., Tateno, Y., & Nishikawa, K. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2454 · Cited by 219 · see citing works
Allosteric Activation of a Spring-Loaded Natriuretic Peptide Receptor Dimer by Hormone
He, X. L., Chow, D., Martick, M. M., & García, K. C. (2001) · Science · doi:10.1126/science.1062246 · Cited by 170 · see citing works
Treponema pallidum TroA is a periplasmic zinc-binding protein with a helical backbone.
Hasemann, C. A., Lee, Y.-H., Deka, R. K., Norgard, M. V., & Radolf, J. D. (1999) · Nature Structural Biology · doi:10.1038/10677 · Cited by 164 · see citing works
Diversity in ABC transporters: Type I, II and III importers
Rice, A. J., Park, A., & Pinkett, H. W. (2014) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2014.953626 · Cited by 160 · see citing works
Maqbool, A., Horler, R. S. P., Müller, A., Wilkinson, A. J., Wilson, K. S., & Thomas, G. H. (2015) · Biochemical Society Transactions · doi:10.1042/bst20150135 · Cited by 141 · see citing works
Conformational dynamics in substrate-binding domains influences transport in the ABC importer GlnPQ
Gouridis, G., Schuurman‐Wolters, G. K., Ploetz, E., Husada, F., Vietrov, R., de Boer, M., Cordes, T., & Poolman, B. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2929 · Cited by 132 · see citing works
Self-citationVetting, M. W., Al-Obaidi, N. F., Zhao, S., Francisco, B. S., Kim, J., Wichelecki, D. J., Bouvier, J. T., Solbiati, J., Vu, H., Zhang, X., et al. (2014) · Biochemistry · doi:10.1021/bi501388y · Cited by 128 · see citing works
Tyrrell, R., Verschueren, K. H. G., Dodson, E. J., Murshudov, G. N., Addy, C., & Wilkinson, A. J. (1997) · Structure · doi:10.1016/s0969-2126(97)00254-2 · Cited by 127 · see citing works
Metabolic sensor governing bacterial virulence in Staphylococcus aureus
Ding, Y., Liu, X., Chen, F., Di, H., Xu, B., Zhou, L., Deng, X., Wu, M., Yang, C., & Lan, L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411077111 · Cited by 100 · see citing works
The structural basis for peptide selection by the transport receptor OppA
Berntsson, R. P. ‐., Doeven, M. K., Fusetti, F., Duurkens, R. H., Sengupta, D., Marrink, . J., Thunnissen, A. M. W. H., Poolman, B., & Slotboom, D.-J. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.65 · Cited by 96 · see citing works
Self-citationThe tripartite tricarboxylate transporter (TTT) family
Winnen, B., Hvorup, R. N., & Saier, M. H. (2003) · Research in Microbiology · doi:10.1016/s0923-2508(03)00126-8 · Cited by 91 · see citing works
Detmers, F. J. M., Lanfermeijer, F. C., Abele, R., Jack, R. W., Tampé, R., Konings, W. N., & Poolman, B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.220308797 · Cited by 79 · see citing works
Self-citationFulyani, F., Schuurman‐Wolters, G. K., Žagar, A. V., Guskov, A., Slotboom, D. J., & Poolman, B. (2013) · Structure · doi:10.1016/j.str.2013.07.020 · Cited by 65 · see citing works
Self-citationCaught in a TRAP: substrate-binding proteins in secondary transport
Fischer, M. M., Zhang, Q. Y., Hubbard, R. E., & Thomas, G. H. (2010) · Trends in Microbiology · doi:10.1016/j.tim.2010.06.009 · Cited by 63 · see citing works
Stec‐Martyna, E., Witkowska-Zimny, M., Hryniewicz, M. M., Neumann, P., Wilkinson, A. J., Brzozowski, A. M., Verma, C. S., Zaim, J., Wysocki, S., & Bujacz, G. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.06.033 · Cited by 58 · see citing works
Vigonsky, E., Ovcharenko, E., & Lewinson, O. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213598110 · Cited by 52 · see citing works
Manganese uptake and streptococcal virulence
Eijkelkamp, B. A., McDevitt, C. A., & Kitten, T. O. (2015) · BioMetals · doi:10.1007/s10534-015-9826-z · Cited by 49 · see citing works
Lecher, J., Pittelkow, M., Zobel, S., Bursy, J., Bönig, T., Smits, S. H. J., Schmitt, L., & Bremer, E. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.03.077 · Cited by 48 · see citing works
Structure of a Bacterial ABC Transporter Involved in the Import of an Acidic Polysaccharide Alginate
Maruyama, Y., Itoh, T., Kaneko, A., Nishitani, Y., Mikami, B., Hashimoto, W., & Murata, K. (2015) · Structure · doi:10.1016/j.str.2015.06.021 · Cited by 45 · see citing works
Momma, K., Mishima, Y., Hashimoto, W., Mikami, B., & Murata, K. (2005) · Biochemistry · doi:10.1021/bi047781r · Cited by 44 · see citing works
Acquisition and Role of Molybdate in Pseudomonas aeruginosa
Pederick, V. G., Eijkelkamp, B. A., Ween, M. P., Neville, S. L., Paton, J. C., & McDevitt, C. A. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.02465-14 · Cited by 40 · see citing works
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Hollenstein, K., Comellas-Bigler, M., Bevers, L. E., Feiters, M. C., Meyer‐Klaucke, W., Hagedoorn, P., & Locher, K. P. (2009) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-009-0479-7 · Cited by 39 · see citing works
Tirado-Lee, L., Lee, A. T., Rees, D. C., & Pinkett, H. W. (2011) · Structure · doi:10.1016/j.str.2011.10.004 · Cited by 36 · see citing works
Mishima, Y., Momma, K., Hashimoto, W., Mikami, B., & Murata, K. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209932200 · Cited by 35 · see citing works
Huvent, I., Belrhali, H., Antoine, R., Bompard, C., Locht, C., Jacob‐Dubuisson, F., & Villeret, V. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.11.096 · Cited by 32 · see citing works
Tan, K., Chang, C., Cuff, M. E., Osipiuk, J., Landorf, E. V., Mack, J. C., Zerbs, S. M., Joachimiak, A., & Collart, F. (2013) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.24305 · Cited by 25 · see citing works
The structure of LsrB from Yersinia pestis complexed with autoinducer-2
Kavanaugh, J. S., Gakhar, L., & Horswill, A. R. (2011) · Acta Crystallographica Section F Structural Biology and Crystallization Communications · doi:10.1107/s1744309111042953 · Cited by 22 · see citing works
Structure–based Mechanism of Ligand Binding for Periplasmic Solute-binding Protein of the Bug Family
Herrou, J., Bompard, C., Antoine, R., Leroy, A., Rucktooa, P., Hot, D., Huvent, I., Locht, C., Villeret, V., & Jacob‐Dubuisson, F. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.08.006 · Cited by 21 · see citing works
Structural analysis ofBordetella pertussisBugE solute receptor in a bound conformation
Huvent, I., Belrhali, H., Antoine, R., Bompard, C., Locht, C., Jacob‐Dubuisson, F., & Villeret, V. (2006) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444906032653 · Cited by 21 · see citing works
Rice, A. J., Harrison, A., Alvarez, F. J. D., Davidson, A. L., & Pinkett, H. W. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.563783 · Cited by 14 · see citing works
Berntsson, R. P. ‐., Smits, S. H. J., Schmitt, L., Slotboom, D.-J., & Poolman, B. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.09.044 · Cited by 9 · see citing works
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Tanaka, K. J., Song, S., Mason, K. M., & Pinkett, H. W. (2017) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2017.08.011 · Cited by 184 · see citing works
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Kaczmarski, J. A., Mahawaththa, M. C., Feintuch, A., Clifton, B. E., Adams, L. A., Goldfarb, D., Otting, G., & Jackson, C. J. (2020) · Nature Communications · doi:10.1038/s41467-020-19695-9 · Cited by 62 · see citing works
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Repoila, F., Wessner, F., Guérin, C., Lacoux, C., Tiwari, S., Jaiswal, A. K., Santana, M. P., Kennedy, S., Quinquis, B., Rainteau, D. P., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-12552-3 · Cited by 45 · see citing works
Goudsmits, J. M. H., Slotboom, D. J., & van Oijen, A. M. (2017) · Nature Communications · doi:10.1038/s41467-017-01815-7 · Cited by 41 · see citing works
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Chandravanshi, M., Sharma, A., Dasgupta, P., Mandal, S., & Kanaujia, S. P. (2019) · Gene · doi:10.1016/j.gene.2019.02.035 · Cited by 24 · see citing works
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Liu, L., Gueguen‐Chaignon, V., Gonçalves, I., Rascle, C., Rigault, M., Dellagi, A., Loisel, E., Poussereau, N., Rodrigue, A., Terradot, L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12826-x · Cited by 30 · see citing works
Bailey, D. C., Bohac, T. J., Shapiro, J. A., Giblin, D. E., Wencewicz, T. A., & Gulick, A. M. (2018) · Biochemistry · doi:10.1021/acs.biochem.8b00986 · Cited by 30 · see citing works
Steglich, M., Hofmann, J. D., Koblitz, J., Sikorski, J., Spröer, C., Riedel, T., Bunk, B., Overmann, J., Neumann‐Schaal, M., & Nübel, U. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00901 · Cited by 29 · see citing works
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Yero, D., Díaz‐Lobo, M., Costenaro, L., Conchillo‐Solé, O., Mayo, A., Ferrer‐Navarro, M., Vilaseca, M., Gibert, I., & Daura, X. (2021) · Communications Biology · doi:10.1038/s42003-021-01968-8 · Cited by 28 · see citing works
Fettach, S., Thari, F. Z., Hafidi, Z., Karrouchi, K., Bouathmany, K., Cherrah, Y., Achouri, M. E., Benbacer, L., Mzibri, M. E., Sefrioui, H., et al. (2021) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2021.2017348 · Cited by 27 · see citing works
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Sen, H., Aggarwal, N., Ishionwu, C., Hussain, N., Parmar, C., Jamshad, M., Bavro, V. N., & Lund, P. A. (2017) · Journal of Bacteriology · doi:10.1128/jb.00310-17 · Cited by 27 · see citing works
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Yang, X., Hu, T., Liang, J., Xiong, Z., Lin, Z., Zhao, Y., Zhou, X., Gao, Y., Sun, S., Yang, X., et al. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01256-z · Cited by 26 · see citing works
Clifton, M. C., Rupert, P. B., Hoette, T. M., Raymond, K. N., Abergel, R. J., & Strong, R. K. (2019) · Journal of Structural Biology X · doi:10.1016/j.yjsbx.2019.100008 · Cited by 25 · see citing works
Ill Communication: Host Metabolites as Virulence-Regulating Signals for Plant-Pathogenic Bacteria
Anderson, J. C. (2023) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-021621-114026 · Cited by 25 · see citing works
Remelli, M., Bellotti, D., & Rowińska‐Żyrek, M. (2021) · Current Medicinal Chemistry · doi:10.2174/1389200222666210514012945 · Cited by 24 · see citing works
A new family of periplasmic-binding proteins that sense arsenic oxyanions
Badilla, C., Osborne, T. H., Cole, A. R., Watson, C., Djordjević, S., & Santini, J. M. (2018) · Scientific Reports · doi:10.1038/s41598-018-24591-w · Cited by 24 · see citing works
Structural basis of trehalose recognition by the mycobacterial LpqY-SugABC transporter
Furze, C. M., Delso, I., Casal, E., Guy, C. S., Seddon, C., Brown, C. M., Parker, H. L., Radhakrishnan, A., Pacheco‐Gómez, R., Stansfeld, P. J., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100307 · Cited by 24 · see citing works
Polyviou, D., Machelett, M. M., Hitchcock, A., Baylay, A. J., MacMillan, F., Moore, C. M., Bibby, T. S., & Tews, I. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.001929 · Cited by 24 · see citing works
Fenn, J. S., Nepravishta, R., Guy, C. S., Harrison, J., Angulo, J., Cameron, A. D., & Fullam, E. (2019) · ACS Chemical Biology · doi:10.1021/acschembio.9b00204 · Cited by 23 · see citing works
Structural dynamics in the evolution of a bilobed protein scaffold
Gouridis, G., Muthahari, Y. A., de Boer, M., Griffith, D. A., Tsirigotaki, A., Tassis, K., Zijlstra, N., Xu, R., Eleftheriadis, N., Sugijo, Y., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2026165118 · Cited by 25 · see citing works
A Biosensor Strategy forE. coliBased on Ligand-Dependent Stabilization
Brandsen, B. M., Mattheisen, J. M., Noel, T., & Fields, S. (2018) · ACS Synthetic Biology · doi:10.1021/acssynbio.8b00052 · Cited by 21 · see citing works
Ma, Y., Li, X., Wang, F., Zhang, L., Zhou, S., Che, X., Yu, D., Liu, X., Li, Z., Sun, H., et al. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002189 · Cited by 21 · see citing works
Virulence regulation in plant-pathogenic bacteria by host-secreted signals
Asif, M., Xie, X., & Zhao, Z. (2024) · Microbiological Research · doi:10.1016/j.micres.2024.127883 · Cited by 21 · see citing works
Chandravanshi, M., Gogoi, P., & Kanaujia, S. P. (2019) · FEBS Journal · doi:10.1111/febs.15093 · Cited by 21 · see citing works
Rosa, L. T., Dix, S. R., Rafferty, J. B., & Kelly, D. J. (2017) · FEBS Journal · doi:10.1111/febs.14304 · Cited by 21 · see citing works
Currie, M. J., Davies, J. S., Scalise, M., Gulati, A., Wright, J. D., Newton-Vesty, M. C., Abeysekera, G. S., Subramanian, R., Wahlgren, W. Y., Friemann, R., et al. (2024) · eLife · doi:10.7554/elife.92307 · Cited by 20 · see citing works
Li, Y., Jin, K., Pérez‐Valdespino, A., Federkiewicz, K., Davis, A., Maciejewski, M. W., Setlow, P., & Hao, B. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1903675116 · Cited by 20 · see citing works
Qu, F., ElOmari, K., Wagner, A., Simone, A. D., & Beis, K. (2019) · Biochemical Journal · doi:10.1042/bcj20190779 · Cited by 20 · see citing works
Single‐molecule studies of conformational states and dynamics in the ABC importer OpuA
Tassis, K., Vietrov, R., de Koning, M., de Boer, M., Gouridis, G., & Cordes, T. (2020) · FEBS Letters · doi:10.1002/1873-3468.14026 · Cited by 19 · see citing works
Licht, A., Bommer, M., Werther, T., Neumann, K., Hobe, C., & Schneider, E. (2018) · Research in Microbiology · doi:10.1016/j.resmic.2018.08.006 · Cited by 19 · see citing works
Multitask ATPases (NBDs) of bacterial ABC importers type I and their interspecies exchangeability
Leisico, F., Godinho, L. M., Gonçalves, I. C., Silva, S. P., Carneiro, B. M., Romão, M. J., Santos‐Silva, T., & Sá‐Nogueira, I. (2020) · Scientific Reports · doi:10.1038/s41598-020-76444-0 · Cited by 19 · see citing works
Energy Coupling Efficiency in the Type I ABC Transporter GlnPQ
Nijeholt, J. A. L. A., Vietrov, R., Schuurman‐Wolters, G. K., & Poolman, B. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.02.001 · Cited by 18 · see citing works
Self-citationModeled Structure of the Cell Envelope Proteinase of Lactococcus lactis
Hansen, E. B., & Marcatili, P. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.613986 · Cited by 16 · see citing works
Deciphering Cellodextrin and Glucose Uptake in Clostridium thermocellum
Yan, F., Dong, S., Liu, Y., Yao, X., Chen, C., Xiao, Y., Bayer, E. A., Shoham, Y., You, C., Cui, Q., et al. (2022) · mBio · doi:10.1128/mbio.01476-22 · Cited by 16 · see citing works
Travin, D. Y., Jouan, R., Vigouroux, A., Inaba‐Inoue, S., Lachat, J., Haq, F., Timchenko, T., Sutormin, D. A., Dubiley, S. A., Beis, K., et al. (2023) · mBio · doi:10.1128/mbio.00217-23 · Cited by 17 · see citing works
Radka, C. D., DeLucas, L. J., Wilson, L. S., Lawrenz, M. B., Perry, R. D., & Aller, S. G. (2017) · Acta Crystallographica Section D Structural Biology · doi:10.1107/s2059798317006349 · Cited by 17 · see citing works
Mandal, S. K., Nayak, S. G., & Kanaujia, S. P. (2021) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2021.06.126 · Cited by 16 · see citing works
Ortega, Á., Matilla, M. A., & Krell, T. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.02054-22 · Cited by 16 · see citing works
Bisson, C., Salmon, R. C., West, L., Rafferty, J. B., Hitchcock, A., Thomas, G. H., & Kelly, D. J. (2021) · FEBS Journal · doi:10.1111/febs.16156 · Cited by 16 · see citing works
Rahman, M. M., Machuca, M. A., Khan, M. F., Barlow, C. K., Schittenhelm, R. B., & Roujeinikova, A. (2019) · Journal of Bacteriology · doi:10.1128/jb.00400-19 · Cited by 16 · see citing works
Cryo-EM reveals unique structural features of the FhuCDB Escherichia coli ferrichrome importer
Hu, W., & Zheng, H. (2021) · Communications Biology · doi:10.1038/s42003-021-02916-2 · Cited by 15 · see citing works
Nichols, A. L., Blumenfeld, Z., Luebbert, L., Knox, H. J., Muthusamy, A. K., Marvin, J. S., Kim, C. H., Grant, S. N., Walton, D. P., Cohen, B. N., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1519-22.2022 · Cited by 15 · see citing works
Stealing Survival: Iron Acquisition Strategies of Mycobacterium tuberculosis.
Shankar, G., & Akhter, Y. (2024) · Biochimie · doi:10.1016/j.biochi.2024.06.006 · Cited by 12 · see citing works
Cuellar, J., Åstrand, M., Elovaara, H., Pietikäinen, A., Sirén, S., Liljeblad, A., Guédez, G., Salminen, T. A., & Hytönen, J. (2020) · Infection and Immunity · doi:10.1128/iai.00962-19 · Cited by 15 · see citing works
Comparing Nonbonded Metal Ion Models in the Divalent Cation Binding Protein PsaA
MacDermott-Opeskin, H., McDevitt, C. A., & O’Mara, M. L. (2020) · Journal of Chemical Theory and Computation · doi:10.1021/acs.jctc.9b01180 · Cited by 15 · see citing works
Ford, B. A., Ranjit, P., Mabbutt, B. C., Paulsen, I. T., & Shah, B. S. (2022) · Environmental Microbiology · doi:10.1111/1462-2920.16168 · Cited by 14 · see citing works
Nguyen, P., Lai, J. Y., Kaiser, J. T., & Rees, D. C. (2019) · Protein Science · doi:10.1002/pro.3694 · Cited by 14 · see citing works
Ploetz, E., Schuurman‐Wolters, G. K., Zijlstra, N., Jager, A. W., Griffith, D. A., Guskov, A., Gouridis, G., Poolman, B., & Cordes, T. (2021) · Open Biology · doi:10.1098/rsob.200406 · Cited by 14 · see citing works
Self-citationFluorescence-based sensing of the bioenergetic and physicochemical status of the cell
Mantovanelli, L., Gaastra, B. F., & Poolman, B. (2021) · Current topics in membranes · doi:10.1016/bs.ctm.2021.10.002 · Cited by 14 · see citing works
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Ho, J. V., & Cotruvo, J. A. (2019) · Biochemistry · doi:10.1021/acs.biochem.9b00358 · Cited by 13 · see citing works
Law, W. W. H., Kanelis, V., & Zamble, D. B. (2022) · Metallomics · doi:10.1093/mtomcs/mfac084 · Cited by 13 · see citing works
East, N. J., Clifton, B. E., Jackson, C. J., & Kaczmarski, J. A. (2022) · Protein Science · doi:10.1002/pro.4510 · Cited by 13 · see citing works
Chan, C., Ng, D., Fraser, M. E., & Schryvers, A. B. (2022) · BioMetals · doi:10.1007/s10534-022-00466-6 · Cited by 15 · see citing works
Chen, J. Z., Gall, B., Pulsford, S. B., Tokuriki, N., & Jackson, C. J. (2025) · Molecular biology and evolution · doi:10.1093/molbev/msaf136 · Cited by 8 · see citing works
Structural and molecular basis for urea recognition by Prochlorococcus
Wang, C., Zhu, W., Ding, H., Liu, N.-H., Cao, H., Suo, C.-L., Liu, Z.-K., Zhang, Y., Sun, M., Fu, H., et al. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104958 · Cited by 12 · see citing works
Sensing preferences for prokaryotic solute binding protein families
Cerna‐Vargas, J. P., Sánchez‐Romera, B., Matilla, M. A., Ortega, Á., & Krell, T. (2023) · Microbial Biotechnology · doi:10.1111/1751-7915.14292 · Cited by 10 · see citing works
Zinc acquisition and its contribution to Klebsiella pneumoniae virulence
Maunders, E. A., Giles, M. W., Ganio, K., Cunningham, B. A., Bennett-Wood, V. R., Cole, G. B., Ng, D., Lai, C. C.-L., Neville, S. L., Moraes, T. F., et al. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1322973 · Cited by 12 · see citing works
Maruyama, Y., Hashimoto, W., & Murata, K. (2019) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2019.1578642 · Cited by 12 · see citing works
Rosa, L. T., Dix, S. R., Rafferty, J. B., & Kelly, D. J. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.11.016 · Cited by 12 · see citing works
Molecular mechanism of phosphate import by the bacterial PstSCAB transporter
Xiao, H., Li, S., Qi, R., Hu, Y., Jiang, X., Luo, J., Wu, J., Zhang, L., Xu, S., Lu, D., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-69153-1 · Cited by 11 · see citing works
Kienlein, M., & Zacharias, M. (2020) · Protein Science · doi:10.1002/pro.3981 · Cited by 11 · see citing works
The Impact of Chromate on Pseudomonas aeruginosa Molybdenum Homeostasis
Maunders, E. A., Ngu, D. H. Y., Ganio, K., Hossain, S. I., Lim, B. Y. J., Leeming, M. G., Luo, Z., Tan, A., Deplazes, E., Kobe, B., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.903146 · Cited by 11 · see citing works
Dutta, A., & Kanaujia, S. P. (2022) · Journal of Structural Biology · doi:10.1016/j.jsb.2022.107896 · Cited by 11 · see citing works
- Authors
- Scheepers, G. H., Lycklama a Nijeholt, J. A., & Poolman, B.
- Affiliations
- University of Groningen (NL)
- Department of Biochemistry Groningen Biomolecular Sciences and Biotechnology Institute Zernike Institute for Advanced Materials University of Groningen The Netherlands
- Corresponding author
- Poolman, Bert
- Venue
- FEBS Letters
- Publisher
- Wiley
- Published
- 2016-10-23
- Volume
- 590
- Issue
- 23
- Pages
- 4393-4401
- ISSN
- 0014-5793 (ISSN-L)
- 1873-3468
- OpenAlex
- W2528162531
- Cited by
- 260
- References
- 47
- Citations by year
- 2026: 7 · 2025: 24 · 2024: 26 · 2023: 29 · 2022: 31 · 2021: 51 · 2020: 28 · 2019: 28 · 2018: 22 · 2017: 13 · 2016: 1
- FWCI
- 9.79
- Type
- journal article
- Language
- en
- Open access
- green
- research.rug.nl
- Licence
- Locations
- FEBS Letters (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Funders
- European Research Council (670578)
- Topics
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Keywords
- substrate-binding protein, structural classification, protein clusters, solute uptake, signal transduction, protein structure, Protein Data Bank
- MeSH terms
- Protein Conformation, alpha-Helical, Models, Molecular, Protein Binding, Proteins, Computational Biology, Databases, Protein
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