62
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Molecular insights into ferric-siderophore transport by the putative TonB-dependent transporter in Mycobacterium tuberculosis

&
Received 09 Nov 2023, Accepted 19 Feb 2024, Published online: 05 Mar 2024

References

  • Abel, R., Young, T., Farid, R., Berne, B. J., & Friesner, R. A. (2008). Role of the active-site solvent in the thermodynamics of factor Xa ligand binding. Journal of the American Chemical Society, 130(9), 2817–2831. https://doi.org/10.1021/ja0771033
  • Awuh, J. A., & Flo, T. H. (2017). Molecular basis of mycobacterial survival in macrophages. Cellular and Molecular Life Sciences: CMLS, 74(9), 1625–1648. https://doi.org/10.1007/s00018-016-2422-8
  • Bayles, K. W. (2014). Bacterial programmed cell death: Making sense of a paradox. Nature Reviews. Microbiology, 12(1), 63–69. https://doi.org/10.1038/nrmicro3136
  • Biggin, P. C., & Bond, P. J. (2015). Molecular dynamics simulations of membrane proteins. Molecular Modeling of Proteins, 1215, 91–108.
  • Braun, M., Endriss, F., Killmann, H., & Braun, V. (2003). In vivo reconstitution of the FhuA transport protein of Escherichia coli K-12. Journal of Bacteriology, 185(18), 5508–5518. https://doi.org/10.1128/JB.185.18.5508-5518.2003
  • Brillet, K., Journet, L., Célia, H., Paulus, L., Stahl, A., Pattus, F., & Cobessi, D. (2007). A β strand lock exchange for signal transduction in TonB-dependent transducers on the basis of a common structural motif. Structure (London, England: 1993), 15(11), 1383–1391. https://doi.org/10.1016/j.str.2007.08.013
  • Buchanan, S. K., Smith, B. S., Venkatramani, L., Xia, D., Esser, L., Palnitkar, M., Chakraborty, R., Van Der Helm, D., & Deisenhofer, J. (1999). Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nature Structural Biology, 6(1), 56–63. https://doi.org/10.1038/4931
  • Cai, J., Wang, X., Ma, A., Wang, Q., Han, X., & Li, Y. (2015). Factors associated with patient and provider delays for tuberculosis diagnosis and treatment in Asia: A systematic review and meta-analysis. PLoS One, 10(3), e0120088. https://doi.org/10.1371/journal.pone.0120088
  • Carter, D. M., Gagnon, J.-N., Damlaj, M., Mandava, S., Makowski, L., Rodi, D. J., Pawelek, P. D., & Coulton, J. W. (2006). Phage display reveals multiple contact sites between FhuA, an outer membrane receptor of Escherichia coli, and TonB. Journal of Molecular Biology, 357(1), 236–251. https://doi.org/10.1016/j.jmb.2005.12.039
  • Ceccarelli, M., Danelon, C., Laio, A., & Parrinello, M. (2004). Microscopic mechanism of antibiotics translocation through a porin. Biophysical Journal, 87(1), 58–64. https://doi.org/10.1529/biophysj.103.037283
  • Chakaya, J., Petersen, E., Nantanda, R., Mungai, B. N., Migliori, G. B., Amanullah, F., Lungu, P., Ntoumi, F., Kumarasamy, N., Maeurer, M., & Zumla, A. (2022). The WHO Global Tuberculosis 2021 Report–Not so good news and turning the tide back to End TB. International Journal of Infectious Diseases, 124, S26–S29. https://doi.org/10.1016/j.ijid.2022.03.011
  • Chenge, J. T., Duyet, L. V., Swami, S., McLean, K. J., Kavanagh, M. E., Coyne, A. G., Rigby, S. E. J., Cheesman, M. R., Girvan, H. M., Levy, C. W., Rupp, B., von Kries, J. P., Abell, C., Leys, D., & Munro, A. W. (2017). Structural characterization and ligand/inhibitor identification provide functional insights into the Mycobacterium tuberculosis cytochrome P450 CYP126A1. The Journal of Biological Chemistry, 292(4), 1310–1329. https://doi.org/10.1074/jbc.M116.748822
  • Chimento, D. P., Kadner, R. J., & Wiener, M. C. (2005). Comparative structural analysis of TonB‐dependent outer membrane transporters: Implications for the transport cycle. Proteins, 59(2), 240–251. https://doi.org/10.1002/prot.20416
  • Chipperfield, J. R., & Ratledge, C. (2000). Salicylic acid is not a bacterial siderophore: A theoretical study. Biometals, 13(2), 165–168. https://doi.org/10.1023/a:1009227206890
  • Dajnowicz, S., Ghoreishi, D., Modugula, K., Damm, W., Harder, E. D., Abel, R., Wang, L., & Yu, H. S. (2020). Advancing free-energy calculations of metalloenzymes in drug discovery via implementation of LFMM potentials. Journal of Chemical Theory and Computation, 16(11), 6926–6937. https://doi.org/10.1021/acs.jctc.0c00615
  • De Voss, J. J., Rutter, K., Schroeder, B. G., & Barry, C. E. III. (1999). Iron acquisition and metabolism by mycobacteria. Journal of Bacteriology, 181(15), 4443–4451. https://doi.org/10.1128/JB.181.15.4443-4451.1999
  • Dheda, K., Barry, C. E., & Maartens, G. (2016). Tuberculosis. Lancet (London, England), 387(10024), 1211–1226. https://doi.org/10.1016/S0140-6736(15)00151-8
  • Ekins, S., Freundlich, J. S., Choi, I., Sarker, M., & Talcott, C. (2011). Computational databases, pathway and cheminformatics tools for tuberculosis drug discovery. Trends in Microbiology, 19(2), 65–74. https://doi.org/10.1016/j.tim.2010.10.005
  • Fanucci, G. E., Cadieux, N., Kadner, R. J., & Cafiso, D. S. (2003). Competing ligands stabilize alternate conformations of the energy coupling motif of a TonB-dependent outer membrane transporter. Proceedings of the National Academy of Sciences of the United States of America, 100(20), 11382–11387. https://doi.org/10.1073/pnas.1932486100
  • Ferguson, A. D., Chakraborty, R., Smith, B. S., Esser, L., Van Der Helm, D., & Deisenhofer, J. (2002). Structural basis of gating by the outer membrane transporter FecA. Science (New York, N.Y.), 295(5560), 1715–1719. https://doi.org/10.1126/science.1067313
  • Ferguson, A. D., & Deisenhofer, J. (2004). Metal import through microbial membranes. Cell, 116(1), 15–24. https://doi.org/10.1016/s0092-8674(03)01030-4
  • Ferguson, A. D., Hofmann, E., Coulton, J. W., Diederichs, K., & Welte, W. (1998). Siderophore-mediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide. Science (New York, N.Y.), 282(5397), 2215–2220. https://doi.org/10.1126/science.282.5397.2215
  • Gaieb, Z., Liu, S., Gathiaka, S., Chiu, M., Yang, H., Shao, C., Feher, V. A., Walters, W. P., Kuhn, B., Rudolph, M. G., Burley, S. K., Gilson, M. K., & Amaro, R. E. (2018). D3R Grand Challenge 2: Blind prediction of protein–ligand poses, affinity rankings, and relative binding free energies. Journal of Computer-Aided Molecular Design, 32(1), 1–20. https://doi.org/10.1007/s10822-017-0088-4
  • Gnann, A. D., Xia, Y., Soule, J., Barthélemy, C., Mawani, J., Musoke, S. N., Castellano, B., Brignole, E., Frueh, D., & Dowling, D. P. (2022). High-resolution structures of a siderophore-producing cyclization domain from Yersinia pestis offer a refined proposal of substrate binding. Journal of Biological Chemistry, 298(10), 102454. https://doi.org/10.1016/j.jbc.2022.102454
  • Gómez-Santos, N., Glatter, T., Koebnik, R., Świątek-Połatyńska, M. A., & Søgaard-Andersen, L. (2019). A TonB-dependent transporter is required for secretion of protease PopC across the bacterial outer membrane. Nature Communications, 10(1), 1360. https://doi.org/10.1038/s41467-019-09366-9
  • Gopinath, P., & Kathiravan, M. K. (2021). Docking studies and molecular dynamics simulation of triazole benzene sulfonamide derivatives with human carbonic anhydrase IX inhibition activity. RSC Advances, 11(60), 38079–38093. https://doi.org/10.1039/d1ra07377j
  • Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M., & Engelhardt, H. (2008). Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proceedings of the National Academy of Sciences of the United States of America, 105(10), 3963–3967. https://doi.org/10.1073/pnas.0709530105
  • Jones, C. M., & Niederweis, M. (2010). Role of porins in iron uptake by Mycobacterium smegmatis. Journal of Bacteriology, 192(24), 6411–6417. https://doi.org/10.1128/JB.00986-10
  • Kadner, R. J., & Heller, K. J. (1995). Mutual inhibition of cobalamin and siderophore uptake systems suggests their competition for TonB function. Journal of Bacteriology, 177(17), 4829–4835. https://doi.org/10.1128/jb.177.17.4829-4835.1995
  • Klebba, P. E., Newton, S. M. C., Six, D. A., Kumar, A., Yang, T., Nairn, B. L., Munger, C., & Chakravorty, S. (2021). Iron acquisition systems of gram-negative bacterial pathogens define TonB-dependent pathways to novel antibiotics. Chemical Reviews, 121(9), 5193–5239. https://doi.org/10.1021/acs.chemrev.0c01005
  • Korkhov, V. M., Mireku, S. A., & Locher, K. P. (2012). Structure of AMP-PNP-bound vitamin B12 transporter BtuCD–F. Nature, 490(7420), 367–372. https://doi.org/10.1038/nature11442
  • Korkhov, V. M., Mireku, S. A., Veprintsev, D. B., & Locher, K. P. (2014). Structure of AMP-PNP–bound BtuCD and mechanism of ATP-powered vitamin B12 transport by BtuCD–F. Nature Structural & Molecular Biology, 21(12), 1097–1099. https://doi.org/10.1038/nsmb.2918
  • Krewulak, K. D., & Vogel, H. J. (2008). Structural biology of bacterial iron uptake. Biochimica et Biophysica Acta, 1778(9), 1781–1804. https://doi.org/10.1016/j.bbamem.2007.07.026
  • Liu, J., Barry, C. E. III, & Nikaido, H. (1999). Cell wall: Physical structure and permeability. In C. Ratledge & J. Dale (Eds.), Mycobacteria: Molecular Biology and Virulence (pp. 220–239). Blackwell Science.
  • Locher, K. P., Rees, B., Koebnik, R., Mitschler, A., Moulinier, L., Rosenbusch, J. P., & Moras, D. (1998). Transmembrane signaling across the ligand-gated FhuA receptor: Crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell, 95(6), 771–778. https://doi.org/10.1016/s0092-8674(00)81700-6
  • Luria, S. E., & Delbrück, M. (1943). Mutations of bacteria from virus sensitivity to virus resistance. Genetics, 28(6), 491–511. https://doi.org/10.1093/genetics/28.6.491
  • Mey, A. R., Gómez-Garzón, C., & Payne, S. M. (2021). Iron transport and metabolism in Escherichia, Shigella, and Salmonella. EcoSal Plus, 9(2), eESP-0034. https://doi.org/10.1128/ecosalplus.ESP-0034-2020
  • Mori, T., Miyashita, N., Im, W., Feig, M., & Sugita, Y. (2016). Molecular dynamics simulations of biological membranes and membrane proteins using enhanced conformational sampling algorithms. Biochimica et Biophysica Acta, 1858(7 Pt B), 1635–1651. https://doi.org/10.1016/j.bbamem.2015.12.032
  • Morris, A. L., MacArthur, M. W., Hutchinson, E. G., & Thornton, J. M. (1992). Stereochemical quality of protein structure coordinates. Proteins, 12(4), 345–364. https://doi.org/10.1002/prot.340120407
  • Niederweis, M., Ehrt, S., Heinz, C., Klöcker, U., Karosi, S., Swiderek, K. M., Riley, L. W., & Benz, R. (1999). Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Molecular Microbiology, 33(5), 933–945. https://doi.org/10.1046/j.1365-2958.1999.01472.x
  • Nikaido, H. (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews: MMBR, 67(4), 593–656. https://doi.org/10.1128/MMBR.67.4.593-656.2003
  • Pauli, I., dos Santos, R. N., Rostirolla, D. C., Martinelli, L. K., Ducati, R. G., Timmers, L. F. S. M., Basso, L. A., Santos, D. S., Guido, R. V. C., Andricopulo, A. D., & Norberto de Souza, O. (2013). Discovery of new inhibitors of Mycobacterium tuberculosis InhA enzyme using virtual screening and a 3D-pharmacophore-based approach. Journal of Chemical Information and Modeling, 53(9), 2390–2401. https://doi.org/10.1021/ci400202t
  • Pawelek, P. D., Croteau, N., Ng-Thow-Hing, C., Khursigara, C. M., Moiseeva, N., Allaire, M., & Coulton, J. W. (2006). Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science (New York, N.Y.), 312(5778), 1399–1402. https://doi.org/10.1126/science.1128057
  • Pellegrini-Calace, M., Maiwald, T., & Thornton, J. M. (2009). PoreWalker: A novel tool for the identification and characterization of channels in transmembrane proteins from their three-dimensional structure. PLoS Computational Biology, 5(7), e1000440. https://doi.org/10.1371/journal.pcbi.1000440
  • Piggot, T. J., Holdbrook, D. A., & Khalid, S. (2013). Conformational dynamics and membrane interactions of the E. coli outer membrane protein FecA: A molecular dynamics simulation study. Biochimica et Biophysica Acta, 1828(2), 284–293. https://doi.org/10.1016/j.bbamem.2012.08.021
  • Podkowa, K. J., Briere, L.-A. K., Heinrichs, D. E., & Shilton, B. H. (2014). Crystal and solution structure analysis of FhuD2 from Staphylococcus aureus in multiple unliganded conformations and bound to ferrioxamine-B. Biochemistry, 53(12), 2017–2031. https://doi.org/10.1021/bi401349d
  • Pollet, R. M., Martin, L. M., & Koropatkin, N. M. (2021). TonB‐dependent transporters in the Bacteroidetes: Unique domain structures and potential functions. Molecular Microbiology, 115(3), 490–501. https://doi.org/10.1111/mmi.14683
  • Puerta, D. T., Schames, J. R., Henchman, R. H., McCammon, J. A., & Cohen, S. M. (2003). From model complexes to metalloprotein inhibition: A synergistic approach to structure‐based drug discovery. Angewandte Chemie, 115(32), 3902–3904. https://doi.org/10.1002/ange.200351433
  • Ratledge, C. (2004). Iron, mycobacteria and tuberculosis. Tuberculosis (Edinburgh, Scotland), 84(1–2), 110–130. https://doi.org/10.1016/j.tube.2003.08.012
  • Samsudin, F., Boags, A., Piggot, T. J., & Khalid, S. (2017). Braun’s lipoprotein facilitates OmpA interaction with the Escherichia coli cell wall. Biophysical Journal, 113(7), 1496–1504. https://doi.org/10.1016/j.bpj.2017.08.011
  • Sauter, A., & Braun, V. (2004). Defined inactive FecA derivatives mutated in functional domains of the outer membrane transport and signaling protein of Escherichia coli K-12. Journal of Bacteriology, 186(16), 5303–5310. https://doi.org/10.1128/JB.186.16.5303-5310.2004
  • Schalk, I. J., Mislin, G. L. A., & Brillet, K. (2012). Structure, function and binding selectivity and stereoselectivity of siderophore–iron outer membrane transporters. Current Topics in Membranes, 69, 37–66. https://doi.org/10.1016/B978-0-12-394390-3.00002-1
  • Schauer, K., Gouget, B., Carrière, M., Labigne, A., & De Reuse, H. (2007). Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Molecular Microbiology, 63(4), 1054–1068. https://doi.org/10.1111/j.1365-2958.2006.05578.x
  • Song, H., Sandie, R., Wang, Y., Andrade-Navarro, M. A., & Niederweis, M. (2008). Identification of outer membrane proteins of Mycobacterium tuberculosis. Tuberculosis (Edinburgh, Scotland), 88(6), 526–544. https://doi.org/10.1016/j.tube.2008.02.004
  • Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
  • Wagner, D., Sangari, F. J., Parker, A., & Bermudez, L. E. (2005). fec B, a gene potentially involved in iron transport in Mycobacterium avium, is not induced within macrophages. FEMS Microbiology Letters, 247(2), 185–191. https://doi.org/10.1016/j.femsle.2005.05.005
  • Wang, J., Arantes, P. R., Bhattarai, A., Hsu, R. V., Pawnikar, S., Huang, Y. M., Palermo, G., & Miao, Y. (2021). Gaussian accelerated molecular dynamics: Principles and applications. Wiley Interdisciplinary Reviews: Computational Molecular Science, 11(5), e1521.
  • Wei, S. H. U., Yu-Xian, S. U. N., Li-Jie, Z., Shi-Heng, X. I. E., Jing-Tao, G. A. O., & Yu-Hong, L. I. U. (2022). Tuberculosis research and innovation: Interpretation of the WHO Global Tuberculosis Report 2021. Chinese Journal of Antituberculosis, 44(1), 45.
  • Wencewicz, T. A., Long, T. E., Möllmann, U., & Miller, M. J. (2013). Trihydroxamate siderophore–fluoroquinolone conjugates are selective sideromycin antibiotics that target Staphylococcus aureus. Bioconjugate Chemistry, 24(3), 473–486. https://doi.org/10.1021/bc300610f
  • WHO. (2021). Global tuberculosis report 2021. Geneva: World Health Organization. CC Licence.
  • Xu, J., & Zhang, Y. (2010). How significant is a protein structure similarity with TM-score= 0.5? Bioinformatics (Oxford, England), 26(7), 889–895. https://doi.org/10.1093/bioinformatics/btq066
  • Yue, W. W., Grizot, S., & Buchanan, S. K. (2003). Structural evidence for iron-free citrate and ferric citrate binding to the TonB-dependent outer membrane transporter FecA. Journal of Molecular Biology, 332(2), 353–368. https://doi.org/10.1016/s0022-2836(03)00855-6

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.