May 24, 2024
Structural basis of BAM-mediated outer membrane β-barrel protein assembly – Nature

Structural basis of BAM-mediated outer membrane β-barrel protein assembly – Nature

  • Lundquist, K., Billings, E., Bi, M., Wellnitz, J. & Noinaj, N. The assembly of β‐barrel membrane proteins by BAM and SAM. Mol. Microbiol. 115, 425–435 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Walther, D. M., Rapaport, D. & Tommassen, J. Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell. Mol. Life Sci. 66, 2789–2804 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tommassen, J. Assembly of outer-membrane proteins in bacteria and mitochondria. Microbiology 156, 2587–2596 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gentle, I., Gabriel, K., Beech, P., Waller, R. & Lithgow, T. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J. Cell Biol. 164, 19–24 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Noinaj, N., Gumbart, J. C. & Buchanan, S. K. The β-barrel assembly machinery in motion. Nat. Rev. Microbiol. 15, 197–204 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Knowles, T. J., Scott-Tucker, A., Overduin, M. & Henderson, I. R. Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat. Rev. Microbiol. 7, 206–214 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sasaki, K. et al. VDAC: old protein with new roles in diabetes. Am. J. Physiol. Physiol. 303, C1055–C1060 (2012).

    Article 
    CAS 

    Google Scholar
     

  • Bender, A. et al. TOM40 mediates mitochondrial dysfunction induced by α-synuclein accumulation in Parkinson’s disease. PLoS ONE 8, e62277 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Webb, C. T., Heinz, E. & Lithgow, T. Evolution of the β-barrel assembly machinery. Trends Microbiol. 20, 612–620 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Malinverni, J. C. et al. YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol. Microbiol. 61, 151–164 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu, T. et al. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121, 235–245 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tellez, R. Jr & Misra, R. Substitutions in the BamA β-barrel domain overcome the conditional lethal phenotype of a ΔbamB ΔbamE strain of Escherichia coli. J. Bacteriol. 194, 317–324 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Imai, Y. et al. A new antibiotic selectively kills Gram-negative pathogens. Nature 576, 459–464 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaur, H. et al. The antibiotic darobactin mimics a β-strand to inhibit outer membrane insertase. Nature 593, 125–129 (2021).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Luther, A. et al. Chimeric peptidomimetic antibiotics against Gram-negative bacteria. Nature 576, 452–458 (2019).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Hart, E. M. et al. A small-molecule inhibitor of BamA impervious to efflux and the outer membrane permeability barrier. Proc. Natl Acad. Sci. USA 116, 21748–21757 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mori, H. & Ito, K. The Sec protein-translocation pathway. Trends Microbiol. 9, 494–500 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Manting, E. H., van der Does, C., Remigy, H., Engel, A. & Driessen, A. J. M. SecYEG assembles into a tetramer to form the active protein translocation channel. EMBO J. 19, 852–861 (2000).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ranava, D., Caumont-Sarcos, A., Albenne, C. & Ieva, R. Bacterial machineries for the assembly of membrane-embedded β-barrel proteins. FEMS Microbiol. Lett. 365, fny087 (2018).

    Article 

    Google Scholar
     

  • Noinaj, N. et al. Structural insight into the biogenesis of β-barrel membrane proteins. Nature 501, 385–390 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bakelar, J., Buchanan, S. K. & Noinaj, N. The structure of the β-barrel assembly machinery complex. Science 351, 180–186 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gu, Y. et al. Structural basis of outer membrane protein insertion by the BAM complex. Nature 531, 64–69 (2016).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Iadanza, M. G. et al. Lateral opening in the intact β-barrel assembly machinery captured by cryo-EM. Nat. Commun. 7, 12865 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Han, L. et al. Structure of the BAM complex and its implications for biogenesis of outer-membrane proteins. Nat. Struct. Mol. Biol. 23, 192–196 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dong, C., Yang, X., Hou, H.-F., Shen, Y.-Q. & Dong, Y.-H. Structure of Escherichia coli BamB and its interaction with POTRA domains of BamA. Acta Crystallogr. Sect. D Biol. Crystallogr. 68, 1134–1139 (2012).

    Article 
    CAS 

    Google Scholar
     

  • Gatzeva-Topalova, P. Z., Warner, L. R., Pardi, A. & Sousa, M. C. Structure and flexibility of the complete periplasmic domain of BamA: the protein insertion machine of the outer membrane. Structure 18, 1492–1501 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kim, K. H., Aulakh, S. & Paetzel, M. Crystal structure of β-barrel assembly machinery BamCD protein complex. J. Biol. Chem. 286, 39116–39121 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tomasek, D. et al. Structure of a nascent membrane protein as it folds on the BAM complex. Nature 583, 473–478 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xiao, L. et al. Structures of the β‐barrel assembly machine recognizing outer membrane protein substrates. FASEB J. 35, e21207 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Doyle, M. T. & Bernstein, H. D. Bacterial outer membrane proteins assemble via asymmetric interactions with the BamA β-barrel. Nat. Commun. 10, 3358 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Doyle, M. T. et al. Cryo-EM structures reveal multiple stages of bacterial outer membrane protein folding. Cell 185, 1143–1156 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu, R. et al. Plasticity within the barrel domain of BamA mediates a hybrid-barrel mechanism by BAM. Nat. Commun. 12, 7131 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brunder, W., Schmidt, H. & Karch, H. EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157: H7 cleaves human coagulation factor V. Mol. Microbiol. 24, 767–778 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Khan, S., Mian, H. S., Sandercock, L. E., Chirgadze, N. Y. & Pai, E. F. Crystal structure of the passenger domain of the Escherichia coli autotransporter EspP. J. Mol. Biol. 413, 985–1000 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barnard, T. J., Dautin, N., Lukacik, P., Bernstein, H. D. & Buchanan, S. K. Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat. Struct. Mol. Biol. 14, 1214–1220 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yuan, X. et al. Molecular basis for the folding of β-helical autotransporter passenger domains. Nat. Commun. 9, 1395 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Peterson, J. H., Hussain, S. & Bernstein, H. D. Identification of a novel post‐insertion step in the assembly of a bacterial outer membrane protein. Mol. Microbiol. 110, 143–159 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Doyle, M. T. & Bernstein, H. D. BamA forms a translocation channel for polypeptide export across the bacterial outer membrane. Mol. Cell 81, 2000–2012 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lundquist, K., Bakelar, J., Noinaj, N. & Gumbart, J. C. C-terminal kink formation is required for lateral gating in BamA. Proc. Natl Acad. Sci. USA 115, E7942–E7949 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • White, P. et al. The role of membrane destabilisation and protein dynamics in BAM catalysed OMP folding. Nat. Commun. 12, 4174 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Doerner, P. A. & Sousa, M. C. Extreme dynamics in the BamA β-barrel seam. Biochemistry 56, 3142–3149 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, J. & Gumbart, J. C. Membrane thinning and lateral gating are consistent features of BamA across multiple species. PLoS Comput. Biol. 16, e1008355 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Roman-Hernandez, G., Peterson, J. H. & Bernstein, H. D. Reconstitution of bacterial autotransporter assembly using purified components. eLife 3, e04234 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tang, X. et al. Structural insights into outer membrane asymmetry maintenance in Gram-negative bacteria by MlaFEDB. Nat. Struct. Mol. Biol. 28, 81–91 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mastronarde, D. N. SerialEM: a program for automated tilt series acquisition on Tecnai microscopes using prediction of specimen position. Microsc. Microanal. 9, 1182–1183 (2003).

    Article 
    ADS 

    Google Scholar
     

  • Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scheres, S. H. W. Semi-automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189, 114–122 (2015).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 213–221 (2010).

    Article 
    CAS 

    Google Scholar
     

  • Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 486–501 (2010).

    Article 
    CAS 

    Google Scholar
     

  • Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Varadi, M. et al. AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 50, D439–D444 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Trabuco, L. G., Villa, E., Mitra, K., Frank, J. & Schulten, K. in Single-Particle Cryo-Electron Microscopy: The Path Toward Atomic Resolution: Selected Papers of Joachim Frank with Commentaries (ed. Frank, J.) 433–443 (World Scientific, 2008).

  • Huang, J. et al. CHARMM36m: an improved force field for folded and intrinsically disordered proteins. Nat. Methods 14, 71–73 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jo, S., Kim, T., Iyer, V. G. & Im, W. CHARMM‐GUI: a web‐based graphical user interface for CHARMM. J. Comput. Chem. 29, 1859–1865 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781–1802 (2005).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Klauda, J. B. et al. Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J. Phys. Chem. B 114, 7830–7843 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Darden, T., York, D. & Pedersen, L. Particle mesh Ewald: an N log (N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089–10092 (1993).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Feller, S. E., Zhang, Y., Pastor, R. W. & Brooks, B. R. Constant pressure molecular dynamics simulation: the Langevin piston method. J. Chem. Phys. 103, 4613–4621 (1995).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Miyamoto, S. & Kollman, P. A. Settle—an analytical version of the shake and rattle algorithm for rigid water models. J. Comput. Chem. 13, 952–962 (1992).

    Article 
    CAS 

    Google Scholar
     

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