Architecture of the type IV coupling protein complex of Legionella pneumophila
Wallden, K., Rivera-Calzada, A. & Waksman, G. Microreview: type IV secretion systems: versatility and diversity in function. Cell. Microbiol. 12, 1203–1212 (2010).
Vincent, C. D., Friedman, J. R., Jeong, K. C., Sutherland, M. C. & Vogel, J. P. Identification of the DotL coupling protein subcomplex of the Legionella Dot/Icm type IV secretion system. Mol. Microbiol. 85, 378–391 (2012).
Gomis-Ruth, F. X., Sola, M., de la Cruz, F. & Coll, M. Coupling factors in macromolecular type-IV secretion machineries. Curr. Pharm. Des. 10, 1551–1565 (2004).
Zechner, E. L., Lang, S. & Schildbach, J. F. Assembly and mechanisms of bacterial type IV secretion machines. Phil. Trans. R. Soc. Lond. B 367, 1073–1087 (2012).
Vergunst, A. C. et al. Virb/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290, 979–982 (2000).
Schrammeijer, B., den Dulk-Ras, A., Vergunst, A. C., Jacome, E. J. & Hooykaas, P. J. J. Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: evidence for transport of a novel effector protein VirE3. Nucleic Acids Res. 31, 860–868 (2003).
Atmakuri, K., Cascales, E. & Christie, P. J. Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol. Microbiol. 54, 1199–1211 (2004).
Jakubowski, S. J., Krishnamoorthy, V., Cascales, E. & Christie, P. J. Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion system. J. Mol. Biol. 341, 961–977 (2004).
Isberg, R. R., O’Connor, T. J. & Heidtman, M. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat. Rev. Microbiol. 7, 13–24 (2009).
Finsel, I. & Hilbi, H. Formation of a pathogen vacuole according to Legionella pneumophila: how to kill one bird with many stones. Cell. Microbiol. 17, 935–950 (2015).
Berger, K. H. & Isberg, R. R. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7, 7–19 (1993).
Marra, A., Blander, S. J., Horwitz, M. A. & Shuman, H. A. Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc. Natl Acad. Sci. USA 89, 9607–9611 (1992).
Segal, G., Purcell, M. & Shuman, H. A. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl Acad. Sci. USA 95, 1669–1674 (1998).
Vogel, J. P., Andrews, H. L., Wong, S. K. & Isberg, R. R. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873–876 (1998).
Juhas, M., Crook, D. W. & Hood, D. W. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell. Microbiol. 10, 2377–2386 (2008).
Christie, P. J. & Vogel, J. P. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8, 354–360 (2000).
Vincent, C. D. et al. Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol. Microbiol. 62, 1278–1291 (2006).
Buscher, B. A. et al. The DotL protein, a member of the TraG-coupling protein family, is essential for viability of Legionella pneumophila strain Lp02. J. Bacteriol. 187, 2927–2938 (2005).
Gomis-Ruth, F. X., Moncalian, G., de la Cruz, F. & Coll, M. Conjugative plasmid protein TrwB, an integral membrane type IV secretion system coupling protein—detailed structural features and mapping of the active site cleft. J. Biol. Chem. 277, 7556–7566 (2002).
Sutherland, M. C., Nguyen, T. L., Tseng, V. & Vogel, J. P. The Legionella IcmSW complex directly interacts with DotL to mediate translocation of adaptor-dependent substrates. PLoS Pathog. 8, e1002910 (2012).
Cambronne, E. D. & Roy, C. R. The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation. PLoS Pathog. 3, e188 (2007).
Holm, L. & Rosenström, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545–W549 (2010).
Alva, V., Nam, S. Z., Soding, J. & Lupas, A. N. The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis. Nucleic Acids Res. 44, W410–W415 (2016).
Edelstein, P. H., Hu, B., Higa, F. & Edelstein, M. A. C. lvgA, a novel Legionella pneumophila virulence factor. Infect. Immun. 71, 2394–2403 (2003).
Vincent, C. D. & Vogel, J. P. The Legionella pneumophila IcmS–LvgA protein complex is important for Dot/Icm-dependent intracellular growth. Mol. Microbiol. 61, 596–613 (2006).
Fiser, A., Do, R. K. & Sali, A. Modeling of loops in protein structures. Protein Sci. 9, 1753–1773 (2000).
Webb, B. & Sali, A. Comparative protein structure modeling using MODELLER. Curr. Protoc. Bioinformatics 47, 5.6.1–5.6.37 (2014).
Bardill, J. P., Miller, J. L. & Vogel, J. P. IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol. 56, 90–103 (2005).
Coers, J. et al. Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth. Mol. Microbiol. 38, 719–736 (2000).
Habyarimana, F., Price, C. T., Santic, M., Al-Khodor, S. & Kwaik, Y. A. Molecular characterization of the Dot/Icm-translocated AnkH and AnkJ eukaryotic-like effectors of Legionella pneumophila. Infect. Immun. 78, 1123–1134 (2010).
Ninio, S., Zuckman-Cholon, D. M., Cambronne, E. D. & Roy, C. R. The Legionella IcmS–IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol. Microbiol. 55, 912–926 (2005).
Jain, A. et al. Probing cellular protein complexes using single-molecule pull-down. Nature 473, 484–488 (2011).
Ninio, S., Celli, J. & Roy, C. R. A Legionella pneumophila effector protein encoded in a region of genomic plasticity binds to Dot/Icm-modified vacuoles. PLoS Pathog. 5, e1000278 (2009).
Gomis-Rüth, F. X. et al. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409, 637–641 (2001).
Lu, J. et al. Structural basis of specific TraD–TraM recognition during F plasmid-mediated bacterial conjugation. Mol. Microbiol. 70, 89–99 (2008).
Atmakuri, K., Ding, Z. Y. & Christie, P. J. Vire2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens. Mol. Microbiol. 49, 1699–1713 (2003).
Whitaker, N. et al. Chimeric coupling proteins mediate transfer of heterologous type IV effectors through the Escherichia coli pKM101-encoded conjugation machine. J. Bacteriol. 198, 2701–2718 (2016).
Whitaker, N. et al. The all-alpha domains of coupling proteins from the Agrobacterium tumefaciens VirB/VirD4 and Enterococcus faecalis pCF10-encoded type IV secretion systems confer specificity to binding of cognate DNA substrates. J. Bacteriol. 197, 2335–2349 (2015).
Voth, D. E., Broederdorf, L. J. & Graham, J. G. Bacterial type IV secretion systems: versatile virulence machines. Future Microbiol. 7, 241–257 (2012).
Bennett, J. C. Q. & Hughes, C. From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol. 8, 202–204 (2000).
Parsot, C., Hamiaux, C. & Page, A. L. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6, 7–14 (2003).
Stebbins, C. E. & Galan, J. E. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414, 77–81 (2001).
Nagai, H. et al. A C-terminal translocation signal required for Dot/lcm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl Acad. Sci. USA 102, 826–831 (2005).
Huang, L. et al. The E block motif is associated with Legionella pneumophila translocated substrates. Cell. Microbiol. 13, 227–245 (2011).
Lifshitz, Z. et al. Computational modeling and experimental validation of the Legionella and Coxiella virulence-related type-IVB secretion signal. Proc. Natl Acad. Sci. USA 110, E707–E715 (2013).
Sexton, J. A., Yeo, H. J. & Vogel, J. P. Genetic analysis of the Legionella pneumophila DotB ATPase reveals a role in type IV secretion system protein export. Mol. Microbiol. 57, 70–84 (2005).
Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10037–10041 (2001).
Shen, A. et al. Mechanistic and structural insights into the proteolytic activation of Vibrio cholerae MARTX toxin. Nat. Chem. Biol. 5, 469–478 (2009).
Adams, P. D. et al. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
Mccoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol. 276, 307–326 (1997).
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905–921 (1998).
Svergun, D. I., Petoukhov, M. V. & Koch, M. H. J. Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80, 2946–2953 (2001).
Svergun, D., Barberato, C. & Koch, M. H. J. CRYSOL—a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768–773 (1995).
Semenyuk, A. V. & Svergun, D. I. GNOM—a program package for small-angle scattering data-processing. J. Appl. Crystallogr. 24, 537–540 (1991).
Lee, N. K. et al. Accurate FRET measurements within single diffusing biomolecules using alternating-laser excitation. Biophys. J. 88, 2939–2953 (2005).
Kim, C., Lee, O. C., Kim, J. Y., Sung, W. & Lee, N. K. Dynamic release of bending stress in short dsDNA by formation of a kink and forks. Angew. Chem. Int. Ed. 54, 8943–8947 (2015).
Roy, R., Hohng, S. & Ha, T. A practical guide to single-molecule FRET. Nat. Methods 5, 507–516 (2008).
Jain, A., Liu, R., Xiang, Y. K. & Ha, T. Single-molecule pull-down for studying protein interactions. Nat. Protoc. 7, 445–452 (2012).
Joo, K. et al. Template based protein structure modeling by global optimization in CASP11. Proteins 84(Suppl. 1), 221–232 (2016).
Joo, K., Lee, J., Kim, I., Lee, S. J. & Lee, J. Multiple sequence alignment by conformational space annealing. Biophys. J. 95, 4813–4819 (2008).
Lee, J., Scheraga, H. A. & Rackovsky, S. New optimization method for conformational energy calculations on polypeptides: conformational space annealing. J. Comput. Chem. 18, 1222–1232 (1997).
Lee, J., Lee, I. H. & Lee, J. Unbiased global optimization of Lennard–Jones clusters for N < or = 201 using the conformational space annealing method. Phys. Rev. Lett. 91, 080201 (2003).
Joo, K. et al. All-atom chain-building by optimizing MODELLER energy function using conformational space annealing. Proteins 75, 1010–1023 (2009).
Krivov, G. G., Shapovalov, M. V. & Dunbrack, R. L. Jr. Improved prediction of protein side-chain conformations with SCWRL4. Proteins 77, 778–795 (2009).
Comments