Structural basis for iron piracy by pathogenic Neisseria
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Neisseria are obligate human pathogens causing bacterial meningitis, septicaemia and gonorrhoea. Neisseria require iron for survival and can extract it directly from human transferrin for transport across the outer membrane. The transport system consists of TbpA, an integral outer membrane protein, and TbpB, a co-receptor attached to the cell surface; both proteins are potentially important vaccine and therapeutic targets. Two key questions driving Neisseria research are how human transferrin is specifically targeted, and how the bacteria liberate iron from transferrin at neutral pH. To address these questions, we solved crystal structures of the TbpA-transferrin complex and of the corresponding co-receptor TbpB. We characterized the TbpB-transferrin complex by small-angle X-ray scattering and the TbpA-TbpB-transferrin complex by electron microscopy. Our studies provide a rational basis for the specificity of TbpA for human transferrin, show how TbpA promotes iron release from transferrin, and elucidate how TbpB facilitates this process.
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Neisseria species take up transferrin only from hominids, a specificity that helps them live in humans and some other hominids.
“The uptake of transferrin by Neisseria species is specific to hominid transferrin, indicating that this specialized uptake mechanism facilitates their residence in the human host and several other hominids83.”
From Iron homeostasis in host defence and inflammation (2015) · cites this paper as [83]
TbpA and TbpB are induced along with several other outer membrane proteins in N. meningitidis under Fe-restricted conditions.
“TbpA and TbpB are induced along with several other proteins in the outer membranes of N. meningitidis under Fe-restricted conditions [30].”
From Strategies of intracellular pathogens for obtaining iron from the environment (2015) · cites this paper as [30]
Neisseria extracts iron from the C-lobe of transferrin even at neutral pH.
“In the case of Neisseria iron is extracted from the C-lobe of transferrin even at neutral pH”
From Iron in immune cell function and host defense (2021) · cites this paper as [15]
TbpA is an important virulence factor in several human and agricultural pathogens.
“transferrin-binding protein A (TbpA), an important virulence factor in several human pathogens including Neisseria meningitidis, Neisseria gonorrhoeae, Haemophilus influenzae, and Moraxella catarrhalis, as well as a number of agricultural pathogens (Figure 2A) 21, 37, 38, 39, 40, 41.”
From Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy (2015) · cites this paper as [41]
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VMD: visual molecular dynamics
Humphrey, W., Dalke, A., & Schulten, K. (1996) · Journal of Molecular Graphics · doi:10.1016/0263-7855(96)00018-5 · Cited by 66,952 · see citing works
UCSF Chimera—A visualization system for exploratory research and analysis
Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004) · Journal of Computational Chemistry · doi:10.1002/jcc.20084 · Cited by 45,260 · see citing works
[20] Processing of X-ray diffraction data collected in oscillation mode
Otwinowski, Z., & Minor, W. (1997) · Methods in Enzymology · doi:10.1016/s0076-6879(97)76066-x · Cited by 33,475 · see citing works
<i>Coot</i> : model-building tools for molecular graphics
Emsley, P., & Cowtan, K. (2004) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444904019158 · Cited by 30,571 · see citing works
<i>Phaser</i> crystallographic software
McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., & Read, R. J. (2007) · Journal of Applied Crystallography · doi:10.1107/s0021889807021206 · Cited by 20,612 · see citing works
Scalable molecular dynamics with NAMD
Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., & Schulten, K. (2005) · Journal of Computational Chemistry · doi:10.1002/jcc.20289 · Cited by 16,914 · see citing works
Self-citationJalview Version 2—a multiple sequence alignment editor and analysis workbench
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. E., & Barton, G. J. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp033 · Cited by 10,011 · see citing works
The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
Arnold, K., Bordoli, L., Kopp, J., & Schwede, T. F. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti770 · Cited by 6,951 · see citing works
<i>PHENIX</i> : building new software for automated crystallographic structure determination
Adams, P. D., Grosse-Kunstleve, R. W., Hung, L.-W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., & Terwilliger, T. C. (2002) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444902016657 · Cited by 4,361 · see citing works
<i>DAMMIF</i> , a program for rapid <i>ab-initio</i> shape determination in small-angle scattering
Franke, D., & Svergun, D. I. (2009) · Journal of Applied Crystallography · doi:10.1107/s0021889809000338 · Cited by 2,021 · see citing works
Uniqueness of ab initio shape determination in small-angle scattering
Волков, В. В., & Svergun, D. I. (2003) · Journal of Applied Crystallography · doi:10.1107/s0021889803000268 · Cited by 1,980 · see citing works
Determination of Domain Structure of Proteins from X-Ray Solution Scattering
Svergun, D. I., Petoukhov, M. V., & Koch, M. H. J. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)76260-1 · Cited by 1,425 · see citing works
TonB-dependent transporters: regulation, structure, and function
Noinaj, N., Guillier, M., Barnard, & Buchanan, S. K. (2010) · Annual Review of Microbiology · doi:10.1146/annurev.micro.112408.134247 · Cited by 989 · see citing works
Self-citationRefinement of severely incomplete structures with maximum likelihood inBUSTER–TNT
Blanc, E., Roversi, P., Vonrhein, C., Flensburg, C., Lea, S. M., & Bricogne, G. (2004) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444904016427 · Cited by 719 · see citing works
Structure of the human transferrin receptor-transferrin complex
Cheng, Y., Zak, O., Aisen, P., Harrison, S. C., & Walz, T. (2004) · Cell · doi:10.1016/s0092-8674(04)00130-8 · Cited by 571 · see citing works
Self-citationSingle-Molecule Experiments in Vitro and in Silico
Sotomayor, M., & Schulten, K. J. (2007) · Science · doi:10.1126/science.1137591 · Cited by 550 · see citing works
Bsoft: Image processing and molecular modeling for electron microscopy
Heymann, J. B., & Belnap, D. M. (2006) · Journal of Structural Biology · doi:10.1016/j.jsb.2006.06.006 · Cited by 516 · see citing works
Shaikh, T., Gao, H., Baxter, W., Asturias, F., Boisset, N., Leith, A., & Frank, J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.156 · Cited by 499 · see citing works
Identification and characterization of the transferrin receptor from Neisseria meningitidis
Schryvers, A. B., & Morris, L. J. (1988) · Molecular Microbiology · doi:10.1111/j.1365-2958.1988.tb00029.x · Cited by 258 · see citing works
Wally, J. L., Halbrooks, P. J., Vonrhein, C., Rould, M. A., Everse, S. J., Mason, A. B., & Buchanan, S. K. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604592200 · Cited by 254 · see citing works
Self-citationAnalysis of X-ray and neutron scattering from biomacromolecular solutions
Petoukhov, M. V., & Svergun, D. I. (2007) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2007.06.009 · Cited by 215 · see citing works
STRAP: editor for STRuctural Alignments of Proteins
Gille, C., & Frömmel, C. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.4.377 · Cited by 211 · see citing works
Anderson, J. E., Sparling, P. F., & Cornelissen, C. N. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.11.3162-3170.1994 · Cited by 188 · see citing works
Grifantini, R., Sebastian, S., Frigimelica, E., Draghi, M., Bartolini, E., Muzzi, A., Rappuoli, R., Grandi, G., & Genco, C. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1033001100 · Cited by 187 · see citing works
Eckenroth, B. E., Steere, A. N., Chasteen, N. D., Everse, S. J., & Mason, A. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105786108 · Cited by 154 · see citing works
Self-citationRational Design of a Meningococcal Antigen Inducing Broad Protective Immunity
Scarselli, M., Aricò, B., Brunelli, B., Savino, S., Marcello, F. D., Palumbo, E., Veggi, D., Ciucchi, L., Cartocci, E., Bottomley, M. J., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002234 · Cited by 140 · see citing works
Hobbs, M. M., Sparling, P. F., Cohen, M. S., Shafer, W. M., Deal, C. D., & Jerse, A. E. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00123 · Cited by 129 · see citing works
Kinetics of iron release from transferrin bound to the transferrin receptor at endosomal pH
Steere, A. N., Byrne, S. L., Chasteen, N. D., & Mason, A. B. (2011) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2011.06.003 · Cited by 116 · see citing works
Self-citationIrwin, S. W., Averill, N., Cheng, C. Y., & Schryvers, A. B. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01657.x · Cited by 108 · see citing works
Mechanics of Force Propagation in TonB-Dependent Outer Membrane Transport
Gumbart, J. C., Wiener, M. C., & Tajkhorshid, E. (2007) · Biophysical Journal · doi:10.1529/biophysj.107.104158 · Cited by 105 · see citing works
Self-citationWeynants, V. E., Feron, C. M., Goraj, K. K., Bos, M. P., Denoël, P., Verlant, V., Tommassen, J., Peak, I. R. A., Judd, R. C., Jennings, M. P., et al. (2007) · Infection and Immunity · doi:10.1128/iai.00411-07 · Cited by 97 · see citing works
Schryvers, A. B., & Gonzalez, G. C. (1989) · Infection and Immunity · doi:10.1128/iai.57.8.2425-2429.1989 · Cited by 95 · see citing works
Moraes, T. F., Yu, R.-H., Strynadka, N. C. J., & Schryvers, A. B. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.06.029 · Cited by 89 · see citing works
Cephalosporin Susceptibility Among Neisseria gonorrhoeae Isolates—United States, 2000-2010
(2011) · JAMA · doi:10.1001/jama.306.6.599 · Cited by 86 · see citing works
Rokbi, B., Mignon, M., Maitre-Wilmotte, G., Lissolo, L., Danve, B., Caugant, D. A., & Quentin-Millet, M. J. (1997) · Infection and Immunity · doi:10.1128/iai.65.1.55-63.1997 · Cited by 84 · see citing works
The structural basis of transferrin sequestration by transferrin-binding protein B
Calmettes, C., Alcantara, J., Yu, R., Schryvers, A. B., & Moraes, T. F. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2251 · Cited by 78 · see citing works
Halbrooks, P. J., He, Q., Briggs, S. K., Everse, S. J., Smith, V. C., MacGillivray, R. T. A., & Mason, A. B. (2003) · Biochemistry · doi:10.1021/bi027071q · Cited by 67 · see citing works
Self-citationPrice, G. A., Masri, H. P., Hollander, A. M., Russell, M. W., & Cornelissen, C. N. (2007) · Vaccine · doi:10.1016/j.vaccine.2007.07.038 · Cited by 60 · see citing works
3-D Structures of Macromolecules Using Single-Particle Analysis in EMAN
Ludtke, S. J. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-842-3_9 · Cited by 59 · see citing works
Cornelissen, C. N., Anderson, J. E., & Sparling, P. F. (1997) · Infection and Immunity · doi:10.1128/iai.65.2.822-828.1997 · Cited by 50 · see citing works
Boulton, I. C., GORRINGE, A. R., Allison, N., Robinson, A., Gorinsky, B. A., Joannou, C. L., & Evans, R. W. (1998) · Biochemical Journal · doi:10.1042/bj3340269 · Cited by 49 · see citing works
Self-citationCornelissen, C. N., Biswas, G. D., & Sparling, P. F. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.8.2448-2450.1993 · Cited by 49 · see citing works
Structural Variations within the Transferrin Binding Site on Transferrin-binding Protein B, TbpB
Calmettes, C., Yu, R., Silva, L. P., Curran, D., Schriemer, D. C., Schryvers, A. B., & Moraes, T. F. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.206102 · Cited by 47 · see citing works
Krell, T., Renauld‐Mongénie, G., Nicolaï, M., Fraysse, S., Chevalier, M., Bérard, Y., Oakhill, J. S., Evans, R. W., GORRINGE, A. R., & Lissolo, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m204461200 · Cited by 44 · see citing works
Self-citationMason, A. B., Halbrooks, P. J., Larouche, J. R., Briggs, S. K., Moffett, M. L., Ramsey, J. E., Connolly, S. A., Smith, V. C., & MacGillivray, R. T. A. (2004) · Protein Expression and Purification · doi:10.1016/j.pep.2004.04.013 · Cited by 40 · see citing works
Self-citationIdentification of TbpA Residues Required for Transferrin-Iron Utilization by Neisseria gonorrhoeae
Noto, J. M., & Cornelissen, C. N. (2008) · Infection and Immunity · doi:10.1128/iai.00020-08 · Cited by 39 · see citing works
Gumbart, J. C., Wiener, M. C., & Tajkhorshid, E. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.09.004 · Cited by 33 · see citing works
Self-citationDetermination of Surface-Exposed, Functional Domains of Gonococcal Transferrin-Binding Protein A
Yost-Daljev, M. K., & Cornelissen, C. N. (2004) · Infection and Immunity · doi:10.1128/iai.72.3.1775-1785.2004 · Cited by 28 · see citing works
Zak, O., & Aisen, P. (2002) · Biochemistry · doi:10.1021/bi015868w · Cited by 26 · see citing works
Self-citationConserved Interaction between Transferrin and Transferrin-binding Proteins from Porcine Pathogens
Silva, L. P., Yu, R., Calmettes, C., Yang, X., Moraes, T. F., Schryvers, A. B., & Schriemer, D. C. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.226449 · Cited by 19 · see citing works
Stokes, R. H., Oakhill, J. S., Joannou, C. L., GORRINGE, A. R., & Evans, R. W. (2005) · Infection and Immunity · doi:10.1128/iai.73.2.944-952.2005 · Cited by 15 · see citing works
Self-citationChallenges for development of meningococcal vaccines in infants and children
Deasy, A. M., & Read, R. C. (2011) · Expert Review of Vaccines · doi:10.1586/erv.11.3 · Cited by 10 · see citing works
Steere, A. N., Roberts, S. E., Byrne, S. L., Chasteen, N. D., Bobst, C. E., Kaltashov, I. A., Smith, V. C., MacGillivray, R. T. A., & Mason, A. B. (2010) · Protein Expression and Purification · doi:10.1016/j.pep.2010.01.008 · Cited by 5 · see citing works
Self-citationSvergun, O. I., & Genkina, O. A. (1992) · PubMed · Cited by 1 · see citing works
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Cassat, J. E., & Skaar, E. P. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.04.010 · Cited by 1,214 · see citing works
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Agirre, J., Atanasova, M., Bagdonas, H., Ballard, C. C., Baslé, A., Beilsten‐Edmands, J., Borges, R. J., Brown, D. G., Burgos-Mármol, J. J., Berrisford, J. M., et al. (2023) · Acta Crystallographica Section D Structural Biology · doi:10.1107/s2059798323003595 · Cited by 930 · see citing works
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Radolf, J. D., Deka, R. K., Anand, A., Šmajs, D., Norgard, M. V., & Yang, X. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.141 · Cited by 323 · see citing works
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Lin, J., Zhang, W., Cheng, J., Xu, Y., Zhu, K., Wang, Y., Wei, G., Qian, P., Luo, Z., & Shen, X. (2017) · Nature Communications · doi:10.1038/ncomms14888 · Cited by 311 · see citing works
Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans
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Sand and Dust Storms: Impact Mitigation
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Sequestration and scavenging of iron in infection
Parrow, N. L., Fleming, R. E., & Minnick, M. F. (2013) · Infection and Immunity · doi:10.1128/iai.00602-13 · Cited by 261 · see citing works
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Vogel, H. J. (2012) · Biochemistry and Cell Biology · doi:10.1139/o2012-016 · Cited by 262 · see citing works
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Sheldon, J. R., Laakso, H. A., & Heinrichs, D. E. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.vmbf-0010-2015 · Cited by 219 · see citing works
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Noinaj, N., Buchanan, S. K., & Cornelissen, C. N. (2012) · Molecular Microbiology · doi:10.1111/mmi.12002 · Cited by 77 · see citing works
Self-citationGating of TonB-dependent transporters by substrate-specific forced remodelling
Hickman, S. J., Cooper, R. E. M., Bellucci, L., Paci, E., & Brockwell, D. J. (2017) · Nature Communications · doi:10.1038/ncomms14804 · Cited by 74 · see citing works
Plasticity within the barrel domain of BamA mediates a hybrid-barrel mechanism by BAM
Wu, R., Bakelar, J., Lundquist, K. P., Zhang, Z., Kuo, K. M., Ryoo, D., Pang, Y. T., Sun, C., White, T., Klose, T., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27449-4 · Cited by 74 · see citing works
Self-citationParticle exposures and infections
Ghio, A. J. (2014) · Infection · doi:10.1007/s15010-014-0592-6 · Cited by 72 · see citing works
Control of Iron Metabolism in Bacteria
Andrews, S., Norton, I., Salunkhe, A. S., Goodluck, H., Aly, W. S. M., Mourad-Agha, H., & Cornelis, P. (2013) · Metal Ions in Life Sciences · doi:10.1007/978-94-007-5561-1_7 · Cited by 72 · see citing works
The molecular mechanism of Zinc acquisition by the neisserial outer-membrane transporter ZnuD
Calmettes, C., Ing, C., Buckwalter, C. M., El Bakkouri, M., Chieh-Lin Lai, C., Pogoutse, A., Gray-Owen, S. D., Pomès, R., & Moraes, T. F. (2015) · Nature Communications · doi:10.1038/ncomms8996 · Cited by 71 · see citing works
Shu, Q., Li, M., Shu, L., An, Z., Wang, J., Lv, H., Yang, M., Cai, T., Hu, Y., Fu, Y., et al. (2020) · Molecular & Cellular Proteomics · doi:10.1074/mcp.ra119.001791 · Cited by 67 · see citing works
Tinoco, A. D., Saxena, M., Sharma, S., Noinaj, N., Delgado, Y., González, E. P. Q., Conklin, S. E., Zambrana, N., Loza-Rosas, S. A., & Parks, T. B. (2016) · Journal of the American Chemical Society · doi:10.1021/jacs.6b01966 · Cited by 65 · see citing works
Self-citationMolecular Evolution of Transition Metal Bioavailability at the Host–Pathogen Interface
Antelo, G. T., Vila, A. J., Giedroc, D. P., & Capdevila, D. A. (2021) · Trends in Microbiology · doi:10.1016/j.tim.2020.08.001 · Cited by 63 · see citing works
Protein Crystallography in Vaccine Research and Development
Malito, E., Carfı́, A., & Bottomley, M. J. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160613106 · Cited by 61 · see citing works
Frandoloso, R., Martínez-Martínez, S., Calmettes, C., Fegan, J. E., Costa, E., Curran, D., Yu, R., Gutiérrez-Martín, C. B., Ferri, E. F. R., Moraes, T. F., et al. (2014) · Infection and Immunity · doi:10.1128/iai.02572-14 · Cited by 60 · see citing works
TonB-dependent transport by the gut microbiota: novel aspects of an old problem
Bolam, D. N., & van den Berg, B. (2018) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2018.03.001 · Cited by 55 · see citing works
Rodríguez, I., Gautam, R., & Tinoco, A. D. (2020) · Biomimetics · doi:10.3390/biomimetics6010001 · Cited by 55 · see citing works
Brabin, L., Brabin, B. J., & Gies, S. (2013) · Nutrition Reviews · doi:10.1111/nure.12049 · Cited by 54 · see citing works
Strategies of intracellular pathogens for obtaining iron from the environment
Leon-Sicairos, N., Reyes-Cortes, R., Guadrón-Llanos, A. M., Madueña-Molina, J., Leon-Sicairos, C., & Canizalez-Román, A. (2015) · BioMed Research International · doi:10.1155/2015/476534 · Cited by 51 · see citing works
“meningitidis under Fe-restricted conditions [30].”
BackgroundResultAll-atom 3D structure prediction of transmembrane β-barrel proteins from sequences
Hayat, S., Sander, C., Marks, D. S., & Elofsson, A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419956112 · Cited by 51 · see citing works
Interaction of apo-transferrin with anticancer ruthenium complexes NAMI-A and its reduced form
Mazuryk, O., Kurpiewska, K., Lewiński, K., Stochel, G., & Brindell, M. (2012) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2012.07.017 · Cited by 51 · see citing works
Dickson, C. F., Kumar, K. K., Jacques, D. A., Malmirchegini, G. R., Spirig, T., Mackay, J. P., Clubb, R., Guss, J. M., & Gell, D. A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.545566 · Cited by 51 · see citing works
Structural basis for haem piracy from host haemopexin by Haemophilus influenzae
Zambolin, S., Clantin, B., Chami, M., Hoos, S., Haouz, A., Villeret, V., & Delepelaire, P. (2016) · Nature Communications · doi:10.1038/ncomms11590 · Cited by 48 · see citing works
Saxena, M., Loza-Rosas, S. A., Gaur, K., Sharma, S., Otero, S. C. P., & Tinoco, A. D. (2018) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2018.03.006 · Cited by 51 · see citing works
The big BAM theory: An open and closed case?
Wu, R., Stephenson, R. E., Gichaba, A., & Noinaj, N. (2019) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2019.183062 · Cited by 51 · see citing works
Self-citationBacterial metabolism in the host and its association with virulence
Bhagwat, A. C., Haldar, T., Kanojiya, P., & Saroj, S. D. (2025) · Virulence · doi:10.1080/21505594.2025.2459336 · Cited by 50 · see citing works
Insertion of proteins and lipopolysaccharide into the bacterial outer membrane
Botos, I., Noinaj, N., & Buchanan, S. K. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0224 · Cited by 50 · see citing works
Self-citationSubversion of nutritional immunity by the pathogenic Neisseriae
Cornelissen, C. N. (2017) · Pathogens and Disease · doi:10.1093/femspd/ftx112 · Cited by 50 · see citing works
Nanocrystal facet modulation to enhance transferrin binding and cellular delivery
Qi, Y., Zhang, T., Jing, C., Liu, S., Zhang, C., Alvarez, P. J. J., & Chen, W. (2020) · Nature Communications · doi:10.1038/s41467-020-14972-z · Cited by 50 · see citing works
The surface lipoproteins of gram-negative bacteria: Protectors and foragers in harsh environments
Cole, G. B., Bateman, T. J., & Moraes, T. F. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.008745 · Cited by 51 · see citing works
Fegan, J. E., Calmettes, C., Islam, E. A., Ahn, S. K., Chaudhuri, S., Yu, R., Gray‐Owen, S. D., Moraes, T. F., & Schryvers, A. B. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00247 · Cited by 48 · see citing works
Mariotti, P., Malito, E., Biancucci, M., Surdo, P. L., Mishra, R. P. N., Nardi‐Dei, V., Savino, S., Nissum, M., Spraggon, G., Grandi, G., et al. (2012) · Biochemical Journal · doi:10.1042/bj20121426 · Cited by 47 · see citing works
Bacterial iron acquisition mediated by outer membrane translocation and cleavage of a host protein
Mosbahi, K., Wojnowska, M., Albalat, A., & Walker, D. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800672115 · Cited by 47 · see citing works
C-terminal kink formation is required for lateral gating in BamA
Lundquist, K. P., Bakelar, J., Noinaj, N., & Gumbart, J. C. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1722530115 · Cited by 47 · see citing works
Self-citationIdentification of a Large Family of Slam-Dependent Surface Lipoproteins in Gram-Negative Bacteria
Hooda, Y., Lai, C. C.-L., & Moraes, T. F. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00207 · Cited by 43 · see citing works
V IV O complexes with antibacterial quinolone ligands and their interaction with serum proteins
Sanna, D., Ugone, V., Sciortino, G., Buglyó, P., Bihari, Z., Parajdi-Losonczi, P. L., & Garribba, E. (2017) · Dalton Transactions · doi:10.1039/c7dt04216g · Cited by 46 · see citing works
Gentiluomo, L., Svilenov, H. L., Augustijn, D., Bialy, I. E., Greco, M. L., Kulakova, A., Indrakumar, S., Mahapatra, S., Morales, M. M., Pohl, C., et al. (2019) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.9b00852 · Cited by 46 · see citing works
Bernstein, H. D. (2015) · Molecular Microbiology · doi:10.1111/mmi.13031 · Cited by 44 · see citing works
Sikora, A. E., Wierzbicki, I. H., Zielke, R. A., Ryner, R. F., Korotkov, K. V., Buchanan, S. K., & Noinaj, N. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000437 · Cited by 43 · see citing works
Self-citationStructural insight into the lactoferrin receptors from pathogenic Neisseria
Noinaj, N., Cornelissen, C. N., & Buchanan, S. K. (2013) · Journal of Structural Biology · doi:10.1016/j.jsb.2013.02.009 · Cited by 42 · see citing works
Self-citationFungal physiology: Robbing the bank of haem iron
Philpott, C. C., & Protchenko, O. V. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.179 · Cited by 42 · see citing works
Bacteriocins active against plant pathogenic bacteria
Grinter, R., Milner, J. J., & Walker, D. (2012) · Biochemical Society Transactions · doi:10.1042/bst20120206 · Cited by 42 · see citing works
Living on the edge: Simulations of bacterial outer-membrane proteins
Pavlova, À., Hwang, H. J., Lundquist, K. P., Balusek, C., & Gumbart, J. C. (2016) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2016.01.020 · Cited by 41 · see citing works
Self-citationIron acquisition through the bacterial transferrin receptor
Pogoutse, A. K., & Moraes, T. F. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1293606 · Cited by 42 · see citing works
Gocheva, G., & Ivanova, A. (2019) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.9b00250 · Cited by 40 · see citing works
Current Management of Iron Deficiency Anemia in Inflammatory Bowel Diseases: A Practical Guide
Gomollón, F., & Gisbert, J. P. (2013) · Drugs · doi:10.1007/s40265-013-0131-2 · Cited by 38 · see citing works
Structure of the bacterial plant-ferredoxin receptor FusA
Grinter, R., Josts, I., Mosbahi, K., Roszak, A. W., Cogdell, R. J., Bonvin, A. M. J. J., Milner, J. J., Kelly, S. M., Byron, O., Smith, B. O., et al. (2016) · Nature Communications · doi:10.1038/ncomms13308 · Cited by 38 · see citing works
Advances in molecular simulations of protein mechanical properties and function
Franz, F., Daday, C., & Gräter, F. (2020) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2019.12.015 · Cited by 36 · see citing works
The Journey of Lipoproteins Through the Cell
Szewczyk, J., & Collet, J. (2016) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2016.07.003 · Cited by 35 · see citing works
Biological Functions of the Secretome of Neisseria meningitidis
Tommassen, J., & Arenas, J. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00256 · Cited by 36 · see citing works
Neisserial surface lipoproteins: structure, function and biogenesis
Hooda, Y., Shin, H. E., Bateman, T. J., & Moraes, T. F. (2017) · Pathogens and Disease · doi:10.1093/femspd/ftx010 · Cited by 33 · see citing works
Structure of the atypical bacteriocin pectocin M 2 implies a novel mechanism of protein uptake
Grinter, R., Josts, I., Zeth, K., Roszak, A. W., McCaughey, L. C., Cogdell, R. J., Milner, J. J., Kelly, S. M., Byron, O., & Walker, D. (2014) · Molecular Microbiology · doi:10.1111/mmi.12655 · Cited by 34 · see citing works
Sabbir, M. G. (2018) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2018.00099 · Cited by 34 · see citing works
From Homodimer to Heterodimer and Back: Elucidating the TonB Energy Transduction Cycle
Gresock, M. G., Kastead, K. A., & Postle, K. (2015) · Journal of Bacteriology · doi:10.1128/jb.00484-15 · Cited by 33 · see citing works
Lactoferrin binding protein B – a bi-functional bacterial receptor protein
Ostan, N. K. H., Yu, R.-H., Ng, D., Lai, C. C.-L., Pogoutse, A. K., Sarpe, V., Hepburn, M., Sheff, J., Raval, S., Schriemer, D. C., et al. (2017) · PLOS Pathogens · doi:10.1371/journal.ppat.1006244 · Cited by 33 · see citing works
Menezes, T. M., Barros, M. R., Ventura, G. T., Ferreira, D. D. S. P., Todeschini, A. R., Borges, R. M., Princival, J. L., Seabra, G. D. M., & Neves, J. L. (2020) · Journal of Molecular Liquids · doi:10.1016/j.molliq.2020.114021 · Cited by 31 · see citing works
Ironing Out the Unconventional Mechanisms of Iron Acquisition and Gene Regulation in Chlamydia
Pokorzynski, N. D., Thompson, C. C., & Carabeo, R. A. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00394 · Cited by 33 · see citing works
Baarda, B. I., Zielke, R. A., Holm, A. K., & Sikora, A. E. (2021) · mSphere · doi:10.1128/msphere.00977-20 · Cited by 31 · see citing works
Disorder is a critical component of lipoprotein sorting in Gram-negative bacteria
Rayes, J. E., Szewczyk, J., Deghelt, M., Csoma, N., Matagne, A., Iorga, B. I., Cho, S.-H., & Collet, J. (2021) · Nature Chemical Biology · doi:10.1038/s41589-021-00845-z · Cited by 32 · see citing works
Barrile, R., Kasendra, M. J., Paccani, S. R., Merola, M., Pizza, M., Baldari, C. T., Soriani, M., & Aricò, B. (2015) · Cellular Microbiology · doi:10.1111/cmi.12439 · Cited by 31 · see citing works
Intravenous iron in inflammatory bowel diseases
Gomollón, F., & Gisbert, J. P. (2012) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32835bdc2e · Cited by 30 · see citing works
Structural change of N-glycan exposes hydrophobic surface of human transferrin
Nagae, M., Morita‐Matsumoto, K., Arai, S., Wada, I., Matsumoto, Y., Saito, K., Hashimoto, Y., & Yamaguchi, Y. (2014) · Glycobiology · doi:10.1093/glycob/cwu033 · Cited by 31 · see citing works
Neumann, W., Hadley, R. C., & Nolan, E. M. (2017) · Essays in Biochemistry · doi:10.1042/ebc20160084 · Cited by 30 · see citing works
Structural analysis of haemoglobin binding by HpuA from the Neisseriaceae family
Wong, C. T., Xu, Y., Gupta, A., Garnett, J. A., Matthews, S. J., & Hare, S. A. (2015) · Nature Communications · doi:10.1038/ncomms10172 · Cited by 30 · see citing works
Dust Storms, Human Health and a Global Early Warning System
Sprigg, W. A. (2016) · Extreme weather and society · doi:10.1007/978-3-319-30626-1_4 · Cited by 30 · see citing works
- Authors
- Noinaj, N., Easley, N. C., Oke, M., Mizuno, N., Gumbart, J., Boura, E., Steere, A. N., Zak, O., Aisen, P., Tajkhorshid, E., Evans, R. W., Gorringe, A. R., Mason, A. B., Steven, A. C., & Buchanan, S. K.
- Affiliations
- National Institutes of Health (US)
- Argonne National Laboratory (US)
- University of Vermont (US)
- Albert Einstein College of Medicine (US)
- University of Illinois Urbana-Champaign (US)
- Brunel University of London (GB)
- Health Protection Agency (GB)
- Corresponding author
- Buchanan, Susan K.
- ORCID
- Venue
- Nature
- Published
- 2012-02-12
- Volume
- 483
- Issue
- 7387
- Pages
- 53-58
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3292680
- OpenAlex
- W2170163556
- Cited by
- 262
- References
- 54
- Citations by year
- 2026: 8 · 2025: 12 · 2024: 12 · 2023: 13 · 2022: 17 · 2021: 11 · 2020: 22 · 2019: 19 · 2018: 14 · 2017: 28 · 2016: 23 · 2015: 26 · 2014: 19 · 2013: 21 · 2012: 17
- FWCI
- 23.03
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (P41GM104601, R01GM086749, U54GM087519)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK21739, ZIADK036143, R01DK021739)
- National Center for Research Resources (P41 RR-05969, P41RR005969)
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Keywords
- Neisseria, iron acquisition, transferrin, TbpA, TbpB, outer membrane proteins, co-receptors, crystal structure, small-angle X-ray scattering, electron microscopy, vaccine targets, therapeutic target
- MeSH terms
- Animals, Apoproteins, Bacterial Proteins, Binding Sites, Biological Transport, Cattle, Humans, Iron, Models, Molecular, Neisseria, Protein Conformation, Species Specificity, Structure-Activity Relationship, Transferrin, X-Ray Diffraction, Crystallography, X-Ray, Transferrin-Binding Protein A, Transferrin-Binding Protein B, Mice, Scattering, Small Angle, Molecular Dynamics Simulation
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