May 18, 2024
Structure of an endogenous mycobacterial MCE lipid transporter – Nature

Structure of an endogenous mycobacterial MCE lipid transporter – Nature

  • Pandey, A. K. & Sassetti, C. M. Mycobacterial persistence requires the utilization of host cholesterol. Proc. Natl Acad. Sci. USA 105, 4376–4380 (2008).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, W., VanderVen, B. C., Fahey, R. J. & Russell, D. G. Intracellular Mycobacterium tuberculosis exploits host-derived fatty acids to limit metabolic stress. J. Biol. Chem. 288, 6788–6800 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gioffré, A. et al. Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. Microbes Infect. 7, 325–334 (2005).

    Article 
    PubMed 

    Google Scholar
     

  • Nazarova, E. V. et al. Rv3723/LucA coordinates fatty acid and cholesterol uptake in Mycobacterium tuberculosis. eLife 6, e26969 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nazarova, E. V. et al. The genetic requirements of fatty acid import by Mycobacterium tuberculosis within macrophages. eLife 8, e43621 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Laval, T. et al. De novo synthesized polyunsaturated fatty acids operate as both host immunomodulators and nutrients for. eLife 10, e71946 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cantrell, S. A. et al. Free mycolic acid accumulation in the cell wall of the mce1 operon mutant strain of Mycobacterium tuberculosis. J. Microbiol. 51, 619–626 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • García-Fernández, J., Papavinasasundaram, K., Galán, B., Sassetti, C. M. & García, J. L. Molecular and functional analysis of the mce4 operon in Mycobacterium smegmatis. Environ. Microbiol. 19, 3689–3699 (2017).

    Article 
    PubMed 

    Google Scholar
     

  • Cohen, A., Mathiasen, V. D., Schön, T. & Wejse, C. The global prevalence of latent tuberculosis: a systematic review and meta-analysis. Eur. Respir. J. 54, 1900655 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Rodriguez, G. M. & Smith, I. Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J. Bacteriol. 188, 424–430 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arnold, F. M. et al. The ABC exporter IrtAB imports and reduces mycobacterial siderophores. Nature 580, 413–417 (2020).

  • Rempel, S. et al. A mycobacterial ABC transporter mediates the uptake of hydrophilic compounds. Nature 580, 409–412 (2020).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Rank, L., Herring, L. E. & Braunstein, M. Evidence for the mycobacterial Mce4 transporter being a multiprotein complex. J. Bacteriol. 203, e00685-20 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, Y. & Chng, S.-S. A conserved membrane protein negatively regulates Mce1 complexes in mycobacteria. Preprint at bioRxiv https://doi.org/10.1101/2022.06.08.495402 (2022).

  • García-Fernández, J., Papavinasasundaram, K., Galán, B., Sassetti, C. M. & García, J. L. Unravelling the pleiotropic role of the MceG ATPase in Mycobacterium smegmatis. Environ. Microbiol. 19, 2564–2576 (2017).

  • Klepp, L. I. et al. Impact of the deletion of the six mce operons in Mycobacterium smegmatis. Microbes Infect. 14, 590–599 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nakamura, S. et al. Molecular basis of increased serum resistance among pulmonary isolates of non-typeable Haemophilus influenzae. PLoS Pathog. 7, e1001247 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, L. et al. The mammalian cell entry (Mce) protein of pathogenic Leptospira species is responsible for RGD motif-dependent infection of cells and animals. Mol. Microbiol. 83, 1006–1023 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Senaratne, R. H. et al. Mycobacterium tuberculosis strains disrupted in mce3 and mce4 operons are attenuated in mice. J. Med. Microbiol. 57, 164–170 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Arruda, S., Bomfim, G., Knights, R., Huima-Byron, T. & Riley, L. Cloning of an M. tuberculosis DNA fragment associated with entry and survival inside cells. Science 261, 1454–1457 (1993).

  • Dulberger, C. L., Rubin, E. J. & Boutte, C. C. The mycobacterial cell envelope—a moving target. Nat. Rev. Microbiol. 18, 47–59 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, Y., Orlando, B. J. & Liao, M. Structural basis of lipopolysaccharide extraction by the LptB2FGC complex. Nature 567, 486–490 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Owens, T. W. et al. Structural basis of unidirectional export of lipopolysaccharide to the cell surface. Nature 567, 550–553 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sherman, D. J. et al. Lipopolysaccharide is transported to the cell surface by a membrane-to-membrane protein bridge. Science 359, 798–801 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Okuda, S., Freinkman, E. & Kahne, D. Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338, 1214–1217 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Du, D. et al. Structure of the AcrAB–TolC multidrug efflux pump. Nature 509, 512–515 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Costa, T. R. D. et al. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13, 343–359 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Casali, N. & Riley, L. W. A phylogenomic analysis of the Actinomycetales mce operons. BMC Genom. 8, 60 (2007).

    Article 

    Google Scholar
     

  • Joshi, S. M. et al. Characterization of mycobacterial virulence genes through genetic interaction mapping. Proc. Natl. Acad. Sci. USA 103, 11760–11765 (2006).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fieweger, R. A. et al. MceG stabilizes the Mce1 and Mce4 transporters in Mycobacterium tuberculosis. J. Biol. Chem. 299, 102910 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Forrellad, M. A. et al. Role of the Mce1 transporter in the lipid homeostasis of Mycobacterium tuberculosis. Tuberculosis 94, 170–177 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Malinverni, J. C. & Silhavy, T. J. An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. Proc. Natl Acad. Sci. USA 106, 8009–8014 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thong, S. et al. Defining key roles for auxiliary proteins in an ABC transporter that maintains bacterial outer membrane lipid asymmetry. eLife 5, e19042 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ekiert, D. C. et al. Architectures of lipid transport systems for the bacterial outer membrane. Cell 169, 273–285 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Asthana, P. et al. Structural insights into the substrate-binding proteins Mce1A and Mce4A from. IUCrJ 8, 757–774 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M. & Engelhardt, H. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl Acad. Sci. USA 105, 3963–3967 (2008).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ahn, V. E. et al. A hydrocarbon ruler measures palmitate in the enzymatic acylation of endotoxin. EMBO J. 23, 2931–2941 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rhys, G. G. et al. Navigating the structural landscape of de novo α-helical bundles. J. Am. Chem. Soc. 141, 8787–8797 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • van den Berg, B., Black, P. N., Clemons, W. M. Jr & Rapoport, T. A. Crystal structure of the long-chain fatty acid transporter FadL. Science 304, 1506–1509 (2004).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Thomas, C. et al. Structural and functional diversity calls for a new classification of ABC transporters. FEBS Lett. 594, 3767–3775 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Coudray, N. et al. Structure of bacterial phospholipid transporter MlaFEDB with substrate bound. eLife 9, e62518 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ekiert, D. C., Coudray, N. & Bhabha, G. Structure and mechanism of the bacterial lipid ABC transporter, MlaFEDB. Curr. Opin. Struct. Biol. 76, 102429 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chi, X. et al. Structural mechanism of phospholipids translocation by MlaFEDB complex. Cell Res. 30, 1127–1135 (2020).

    Article 
    CAS 
    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
     

  • Luo, Q. et al. Structural basis for lipopolysaccharide extraction by ABC transporter LptB2FG. Nat. Struct. Mol. Biol. 24, 469–474 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dong, H., Zhang, Z., Tang, X., Paterson, N. G. & Dong, C. Structural and functional insights into the lipopolysaccharide ABC transporter LptB2FG. Nat. Commun. 8, 222 (2017).

  • Kolich, L. R. et al. Structure of MlaFB uncovers novel mechanisms of ABC transporter regulation. eLife 9, e60030 (2020).

    Article 
    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
     

  • van Kempen, M. et al. Fast and accurate protein structure search with Foldseek. Nat. Biotechnol. https://doi.org/10.1038/s41587-023-01773-0 (2023).

  • García, J. et al. Mycobacterium tuberculosis Rv2536 protein implicated in specific binding to human cell lines. Protein Sci. 14, 2236–2245 (2005).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Choi, H. et al. Analyzing protein-protein interactions from affinity purification-mass spectrometry data with SAINT. Curr. Protoc. Bioinform. 8, 8.15.1–8.15.23 (2012).


    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
     

  • Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tian, W., Chen, C., Lei, X., Zhao, J. & Liang, J. CASTp 3.0: computed atlas of surface topography of proteins. Nucleic Acids Res. 46, W363–W367 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    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
     

  • Murphy, K. C. et al. ORBIT: a new paradigm for genetic engineering of mycobacterial chromosomes. MBio 9, e01467-18 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Snapper, S. B., Melton, R. E., Mustafa, S., Kieser, T. & Jacobs, W. R. Jr. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4, 1911–1919 (1990).

  • Pleiner, T. et al. Structural basis for membrane insertion by the human ER membrane protein complex. Science 369, 433–436 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).

    Article 
    PubMed 

    Google Scholar
     

  • Bepler, T., Kelley, K., Noble, A. J. & Berger, B. Topaz-Denoise: general deep denoising models for cryoEM and cryoET. Nat. Commun. 11, 5208 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Punjani, A., Zhang, H. & Fleet, D. J. Non-uniform refinement: adaptive regularization improves single-particle cryo-EM reconstruction. Nat. Methods 17, 1214–1221 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tan, Y. Z. et al. Addressing preferred specimen orientation in single-particle cryo-EM through tilting. Nat. Methods 14, 793–796 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. D 75, 861–877 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    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
     

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

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Evans, R. et al. Protein complex prediction with AlphaFold-Multimer. Preprint at bioRxiv https://doi.org/10.1101/2021.10.04.463034 (2022).

  • Cianfrocco, M. A., Wong-Barnum, M., Youn, C., Wagner, R. & Leschziner, A. COSMIC2: A Science Gateway for Cryo-Electron Microscopy Structure Determination. In Proc. PEARC17: Practice and Experience in Advanced Research Computing 2017 on Sustainability, Success and Impact 1–5 (Association for Computing Machinery, 2017).

  • Moriarty, N. W., Grosse-Kunstleve, R. W. & Adams, P. D. Electronic Ligand Builder and Optimization Workbench (eLBOW): a tool for ligand coordinate and restraint generation. Acta Crystallogr. D 65, 1074–1080 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sutcliffe, I. C. & Harrington, D. J. Lipoproteins of Mycobacterium tuberculosis: an abundant and functionally diverse class of cell envelope components. FEMS Microbiol. Rev. 28, 645–659 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Williams, C. J. et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Barad, B. A. et al. EMRinger: side chain-directed model and map validation for 3D cryo-electron microscopy. Nat. Methods 12, 943–946 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pravda, L. et al. MOLEonline: a web-based tool for analyzing channels, tunnels and pores (2018 update). Nucleic Acids Res. 46, W368–W373 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Suits, M. D. L., Sperandeo, P., Dehò, G., Polissi, A. & Jia, Z. Novel structure of the conserved Gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J. Mol. Biol. 380, 476–488 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Botos, I. et al. Structural and functional characterization of the LPS transporter LptDE from Gram-negative pathogens. Structure 24, 965–976 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fitzpatrick, A. W. P. et al. Structure of the MacAB-TolC ABC-type tripartite multidrug efflux pump. Nat. Microbiol. 2, 17070 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Isom, G. L. et al. LetB structure reveals a tunnel for lipid transport across the bacterial envelope. Cell 181, 653–664 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huerta-Cepas, J. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309–D314 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

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