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Structural basis for antibacterial peptide self-immunity by the bacterial ABC transporter McjD.

Bountra K, Hagelueken G, Choudhury HG, Corradi V, El Omari K, Wagner A, Mathavan I, Zirah S, Yuan Wahlgren W, Tieleman DP, Schiemann O, Rebuffat S, Beis K
EMBO J 36 3062-3079 (2017)
Related entries: 4pl0, 5ofr

Cited: 38 times
EuropePMC logo PMID: 28864543

Abstract

Certain pathogenic bacteria produce and release toxic peptides to ensure either nutrient availability or evasion from the immune system. These peptides are also toxic to the producing bacteria that utilize dedicated ABC transporters to provide self-immunity. The ABC transporter McjD exports the antibacterial peptide MccJ25 in Escherichia coli Our previously determined McjD structure provided some mechanistic insights into antibacterial peptide efflux. In this study, we have determined its structure in a novel conformation, apo inward-occluded and a new nucleotide-bound state, high-energy outward-occluded intermediate state, with a defined ligand binding cavity. Predictive cysteine cross-linking in E. coli membranes and PELDOR measurements along the transport cycle indicate that McjD does not undergo major conformational changes as previously proposed for multi-drug ABC exporters. Combined with transport assays and molecular dynamics simulations, we propose a novel mechanism for toxic peptide ABC exporters that only requires the transient opening of the cavity for release of the peptide. We propose that shielding of the cavity ensures that the transporter is available to export the newly synthesized peptides, preventing toxic-level build-up.

Reviews - 5ofp mentioned but not cited (1)

  1. Mechanics and pharmacology of substrate selection and transport by eukaryotic ABC exporters. Srikant S, Gaudet R. Nat Struct Mol Biol 26 792-801 (2019)

Articles - 5ofp mentioned but not cited (3)

  1. Structural basis for antibacterial peptide self-immunity by the bacterial ABC transporter McjD. Bountra K, Hagelueken G, Choudhury HG, Corradi V, El Omari K, Wagner A, Mathavan I, Zirah S, Yuan Wahlgren W, Tieleman DP, Schiemann O, Rebuffat S, Beis K. EMBO J 36 3062-3079 (2017)
  2. Conformational trapping of an ABC transporter in polymer lipid nanoparticles. Pollock NL, Lloyd J, Montinaro C, Rai M, Dafforn TR. Biochem J 479 145-159 (2022)
  3. Bactericidal Properties of Proline-Rich Aedes aegypti Trypsin Modulating Oostatic Factor (AeaTMOF). Borovsky D, Rougé P, Shatters RG. Life (Basel) 13 19 (2022)


Reviews citing this publication (14)

  1. Multidrug efflux pumps: structure, function and regulation. Du D, Wang-Kan X, Neuberger A, van Veen HW, Pos KM, Piddock LJV, Luisi BF. Nat Rev Microbiol 16 523-539 (2018)
  2. Bacteriocins as a new generation of antimicrobials: toxicity aspects and regulations. Soltani S, Hammami R, Cotter PD, Rebuffat S, Said LB, Gaudreau H, Bédard F, Biron E, Drider D, Fliss I. FEMS Microbiol Rev 45 fuaa039 (2021)
  3. Antibiotic Resistance Mediated by the MacB ABC Transporter Family: A Structural and Functional Perspective. Greene NP, Kaplan E, Crow A, Koronakis V. Front Microbiol 9 950 (2018)
  4. Structure, Assembly, and Function of Tripartite Efflux and Type 1 Secretion Systems in Gram-Negative Bacteria. Alav I, Kobylka J, Kuth MS, Pos KM, Picard M, Blair JMA, Bavro VN. Chem Rev 121 5479-5596 (2021)
  5. The manifold roles of microbial ribosomal peptide-based natural products in physiology and ecology. Li Y, Rebuffat S. J Biol Chem 295 34-54 (2020)
  6. Bacteriocins to Thwart Bacterial Resistance in Gram Negative Bacteria. Telhig S, Ben Said L, Zirah S, Fliss I, Rebuffat S. Front Microbiol 11 586433 (2020)
  7. Where is crystallography going? Grimes JM, Hall DR, Ashton AW, Evans G, Owen RL, Wagner A, McAuley KE, von Delft F, Orville AM, Sorensen T, Walsh MA, Ginn HM, Stuart DI. Acta Crystallogr D Struct Biol 74 152-166 (2018)
  8. Lasso Peptides: Heterologous Production and Potential Medical Application. Cheng C, Hua ZC. Front Bioeng Biotechnol 8 571165 (2020)
  9. Lipid Membrane Mimetics in Functional and Structural Studies of Integral Membrane Proteins. Majeed S, Ahmad AB, Sehar U, Georgieva ER. Membranes (Basel) 11 685 (2021)
  10. Structural Insights into Transporter-Mediated Drug Resistance in Infectious Diseases. Kim J, Cater RJ, Choy BC, Mancia F. J Mol Biol 433 167005 (2021)
  11. Changes in Membrane Protein Structural Biology. Birch J, Cheruvara H, Gamage N, Harrison PJ, Lithgo R, Quigley A. Biology (Basel) 9 E401 (2020)
  12. Enzymatic trans-bilayer lipid transport: Mechanisms, efficiencies, slippage, and membrane curvature. Shukla S, Baumgart T. Biochim Biophys Acta Biomembr 1863 183534 (2021)
  13. Immunomodulation, Bioavailability and Safety of Bacteriocins. Guryanova SV. Life (Basel) 13 1521 (2023)
  14. Interaction of Vanadium Complexes with Proteins: Revisiting the Reported Structures in the Protein Data Bank (PDB) since 2015. Santos MFA, Pessoa JC. Molecules 28 6538 (2023)

Articles citing this publication (20)

  1. Conformational dynamics of the ABC transporter McjD seen by single-molecule FRET. Husada F, Bountra K, Tassis K, de Boer M, Romano M, Rebuffat S, Beis K, Cordes T. EMBO J 37 e100056 (2018)
  2. Allosteric activation of an ion channel triggered by modification of mechanosensitive nano-pockets. Kapsalis C, Wang B, El Mkami H, Pitt SJ, Schnell JR, Smith TK, Lippiat JD, Bode BE, Pliotas C. Nat Commun 10 4619 (2019)
  3. Molecular mechanism of SbmA, a promiscuous transporter exploited by antimicrobial peptides. Ghilarov D, Inaba-Inoue S, Stepien P, Qu F, Michalczyk E, Pakosz Z, Nomura N, Ogasawara S, Walker GC, Rebuffat S, Iwata S, Heddle JG, Beis K. Sci Adv 7 eabj5363 (2021)
  4. Bacteriocin Occurrence and Activity in Escherichia coli Isolated from Bovines and Wastewater. Cameron A, Zaheer R, Adator EH, Barbieri R, Reuter T, McAllister TA. Toxins (Basel) 11 E475 (2019)
  5. Lipid-Dependent Alternating Access Mechanism of a Bacterial Multidrug ABC Exporter. Immadisetty K, Hettige J, Moradi M. ACS Cent Sci 5 43-56 (2019)
  6. Solid immersion microscopy images cells under cryogenic conditions with 12 nm resolution. Wang L, Bateman B, Zanetti-Domingues LC, Moores AN, Astbury S, Spindloe C, Darrow MC, Romano M, Needham SR, Beis K, Rolfe DJ, Clarke DT, Martin-Fernandez ML. Commun Biol 2 74 (2019)
  7. A Leaderless Two-Peptide Bacteriocin, Enterocin DD14, Is Involved in Its Own Self-Immunity: Evidence and Insights. Ladjouzi R, Lucau-Danila A, Benachour A, Drider D. Front Bioeng Biotechnol 8 644 (2020)
  8. In-Lipid Structure of Pressure-Sensitive Domains Hints Mechanosensitive Channel Functional Diversity. Kapsalis C, Ma Y, Bode BE, Pliotas C. Biophys J 119 448-459 (2020)
  9. Substrate-bound and substrate-free outward-facing structures of a multidrug ABC exporter. Chaptal V, Zampieri V, Wiseman B, Orelle C, Martin J, Nguyen KA, Gobet A, Di Cesare M, Magnard S, Javed W, Eid J, Kilburg A, Peuchmaur M, Marcoux J, Monticelli L, Hogbom M, Schoehn G, Jault JM, Boumendjel A, Falson P. Sci Adv 8 eabg9215 (2022)
  10. In silico Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing Lasso Peptides. Sabino YNV, de Araújo KC, de Assis FGDV, Moreira SM, Lopes TDS, Mendes TAO, Huws SA, Mantovani HC. Front Microbiol 11 576738 (2020)
  11. Conversion of chemical to mechanical energy by the nucleotide binding domains of ABCB1. Szöllősi D, Chiba P, Szakacs G, Stockner T. Sci Rep 10 2589 (2020)
  12. Experimental phasing with vanadium and application to nucleotide-binding membrane proteins. El Omari K, Mohamad N, Bountra K, Duman R, Romano M, Schlegel K, Kwong HS, Mykhaylyk V, Olesen C, Moller JV, Bublitz M, Beis K, Wagner A. IUCrJ 7 1092-1101 (2020)
  13. Generation of Lasso Peptide-Based ClpP Binders. Malik IT, Hegemann JD, Brötz-Oesterhelt H. Int J Mol Sci 23 465 (2021)
  14. HDX-guided EPR spectroscopy to interrogate membrane protein dynamics. Lane BJ, Wang B, Ma Y, Calabrese AN, El Mkami H, Pliotas C. STAR Protoc 3 101562 (2022)
  15. PELDOR/DEER: An Electron Paramagnetic Resonance Method to Study Membrane Proteins in Lipid Bilayers. Peter MF, Bountra K, Beis K, Hagelueken G. Methods Mol Biol 2168 313-333 (2020)
  16. Asymmetric conformations and lipid interactions shape the ATP-coupled cycle of a heterodimeric ABC transporter. Tang Q, Sinclair M, Hasdemir HS, Stein RA, Karakas E, Tajkhorshid E, Mchaourab HS. Nat Commun 14 7184 (2023)
  17. Bioinformatic mining for RiPP biosynthetic gene clusters in Bacteroidales reveals possible new subfamily architectures and novel natural products. Fernandez-Cantos MV, Garcia-Morena D, Yi Y, Liang L, Gómez-Vázquez E, Kuipers OP. Front Microbiol 14 1219272 (2023)
  18. Cryo-EM structures of mitochondrial ABC transporter ABCB10 in apo and biliverdin-bound form. Cao S, Yang Y, He L, Hang Y, Yan X, Shi H, Wu J, Ouyang Z. Nat Commun 14 2030 (2023)
  19. Experimental phasing opportunities for macromolecular crystallography at very long wavelengths. El Omari K, Duman R, Mykhaylyk V, Orr CM, Latimer-Smith M, Winter G, Grama V, Qu F, Bountra K, Kwong HS, Romano M, Reis RI, Vogeley L, Vecchia L, Owen CD, Wittmann S, Renner M, Senda M, Matsugaki N, Kawano Y, Bowden TA, Moraes I, Grimes JM, Mancini EJ, Walsh MA, Guzzo CR, Owens RJ, Jones EY, Brown DG, Stuart DI, Beis K, Wagner A. Commun Chem 6 219 (2023)
  20. Structural basis of peptide secretion for Quorum sensing by ComA. Yu L, Xu X, Chua WZ, Feng H, Ser Z, Shao K, Shi J, Wang Y, Li Z, Sobota RM, Sham LT, Luo M. Nat Commun 14 7178 (2023)


Related citations provided by authors (1)

  1. Structure of an antibacterial peptide ATP-binding cassette transporter in a novel outward occluded state.. Choudhury HG, Tong Z, Mathavan I, Li Y, Iwata S, Zirah S, Rebuffat S, van Veen HW, Beis K Proc Natl Acad Sci U S A 111 9145-50 (2014)

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