A Single Legionella Effector Catalyzes a Multistep Ubiquitination Pathway to Rearrange Tubular Endoplasmic Reticulum for Replication

Abu Kwaik, 1996, The phagosome containing Legionella pneumophila within the protozoan Hartmannella vermiformis is surrounded by the rough endoplasmic reticulum, Appl. Environ. Microbiol., 62, 2022, 10.1128/AEM.62.6.2022-2028.1996 Bardill, 2005, IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system, Mol. Microbiol., 56, 90, 10.1111/j.1365-2958.2005.04539.x Barth, 1998, Characterization of the catalytic site of the ADP-ribosyltransferase Clostridium botulinum C2 toxin by site-directed mutagenesis, J. Biol. Chem., 273, 29506, 10.1074/jbc.273.45.29506 Berger, 1993, Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila, Mol. Microbiol., 7, 7, 10.1111/j.1365-2958.1993.tb01092.x Bhogaraju, 2016, Phosphoribosylation of ubiquitin promotes serine ubiquitination and impairs conventional ubiquitination, Cell, 167, 1636, 10.1016/j.cell.2016.11.019 Chuyen, 2006, Toxicity of the AGEs generated from the Maillard reaction: on the relationship of food-AGEs and biological-AGEs, Mol. Nutr. Food Res., 50, 1140, 10.1002/mnfr.200600144 Copenhaver, 2014, Alveolar macrophages and neutrophils are the primary reservoirs for Legionella pneumophila and mediate cytosolic surveillance of type IV secretion, Infect. Immun., 82, 4325, 10.1128/IAI.01891-14 Daniels, 2015, Nudix hydrolases degrade protein-conjugated ADP-ribose, Sci. Rep., 5, 18271, 10.1038/srep18271 English, 2009, Peripheral ER structure and function, Curr. Opin. Cell Biol., 21, 596, 10.1016/j.ceb.2009.04.004 Haenssler, 2015, Endoplasmic reticulum tubule protein Reticulon 4 associates with the Legionella pneumophila vacuole and with translocated substrate Ceg9, Infect. Immun., 83, 3479, 10.1128/IAI.00507-15 Horenkamp, 2014, Legionella pneumophila subversion of host vesicular transport by SidC effector proteins, Traffic, 15, 488, 10.1111/tra.12158 Hsu, 2014, The Legionella effector SidC defines a unique family of ubiquitin ligases important for bacterial phagosomal remodeling, Proc. Natl. Acad. Sci. USA, 111, 10538, 10.1073/pnas.1402605111 Jeong, 2015, Spatiotemporal regulation of a Legionella pneumophila T4SS substrate by the metaeffector SidJ, PLoS Pathog., 11, e1004695, 10.1371/journal.ppat.1004695 Kagan, 2002, Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites, Nat. Cell Biol., 4, 945, 10.1038/ncb883 Klebl, 1997, Specificity and target proteins of arginine-specific mono-ADP-ribosylation in T-tubules of rabbit skeletal muscle, Arch. Biochem. Biophys., 347, 155, 10.1006/abbi.1997.0330 Krebs, 2003, Flow cytometric and immunoblot assays for cell surface ADP-ribosylation using a monoclonal antibody specific for ethenoadenosine, Anal. Biochem., 314, 108, 10.1016/S0003-2697(02)00640-1 Lam, 2015, Directed evolution of APEX2 for electron microscopy and proximity labeling, Nat. Methods, 12, 51, 10.1038/nmeth.3179 Losick, 2010, LnaB: a Legionella pneumophila activator of NF-kappaB, Cell. Microbiol., 12, 1083, 10.1111/j.1462-5822.2010.01452.x Michard, 2015, Post-translational modifications are key players of the Legionella pneumophila infection strategy, Front. Microbiol., 6, 87, 10.3389/fmicb.2015.00087 Morar, 2015, Crystal structure of the Legionella pneumophila Lem10 effector reveals a new member of the HD protein superfamily, Proteins, 83, 2319, 10.1002/prot.24933 Nixon-Abell, 2016, Increased spatiotemporal resolution reveals highly dynamic dense tubular matrices in the peripheral ER, Science, 354, 354, 10.1126/science.aaf3928 O’Connor, 2011, Minimization of the Legionella pneumophila genome reveals chromosomal regions involved in host range expansion, Proc. Natl. Acad. Sci. USA, 108, 14733, 10.1073/pnas.1111678108 Palazzo, 2015, Processing of protein ADP-ribosylation by Nudix hydrolases, Biochem. J., 468, 293, 10.1042/BJ20141554 Pickart, 2004, Ubiquitin: structures, functions, mechanisms, Biochim. Biophys. Acta, 1695, 55, 10.1016/j.bbamcr.2004.09.019 Pieters, 2016, Natural supramolecular protein assemblies, Chem. Soc. Rev., 45, 24, 10.1039/C5CS00157A Price, 2009, Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa, PLoS Pathog., 5, e1000704, 10.1371/journal.ppat.1000704 Qiu, 2016, Ubiquitination independent of E1 and E2 enzymes by bacterial effectors, Nature, 533, 120, 10.1038/nature17657 Ravikumar, 2015, Elucidating host-pathogen interactions based on post-translational modifications using proteomics approaches, Front. Microbiol., 6, 1313, 10.3389/fmicb.2015.01312 Ribet, 2010, Post-translational modifications in host cells during bacterial infection, FEBS Lett., 584, 2748, 10.1016/j.febslet.2010.05.012 Robinson, 2006, Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila, Cell. Microbiol., 8, 793, 10.1111/j.1462-5822.2005.00666.x Rowbotham, 1980, Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae, J. Clin. Pathol., 33, 1179, 10.1136/jcp.33.12.1179 Sheedlo, 2015, Structural basis of substrate recognition by a bacterial deubiquitinase important for dynamics of phagosome ubiquitination, Proc. Natl. Acad. Sci. USA, 112, 15090, 10.1073/pnas.1514568112 Solomon, 2000, Growth of Legionella pneumophila in Dictyostelium discoideum: a novel system for genetic analysis of host-pathogen interactions, Trends Microbiol., 8, 478, 10.1016/S0966-842X(00)01852-7 Swanson, 1995, Association of Legionella pneumophila with the macrophage endoplasmic reticulum, Infect. Immun., 63, 3609, 10.1128/IAI.63.9.3609-3620.1995 Tilney, 2001, How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane, J. Cell Sci., 114, 4637, 10.1242/jcs.114.24.4637 Treier, 1994, Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain, Cell, 78, 787, 10.1016/S0092-8674(94)90502-9 Voeltz, 2006, A class of membrane proteins shaping the tubular endoplasmic reticulum, Cell, 124, 573, 10.1016/j.cell.2005.11.047 Weber, 2014, Live-cell imaging of phosphoinositide dynamics and membrane architecture during Legionella infection, MBio, 5, 10.1128/mBio.00839-13 Wiater, 1998, Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila, Infect. Immun., 66, 4450, 10.1128/IAI.66.9.4450-4460.1998 Wong, 2015, Structure of the Legionella effector, lpg1496, suggests a role in nucleotide metabolism, J. Biol. Chem., 290, 24727, 10.1074/jbc.M115.671263 Yan, 2006, Reticulon proteins: emerging players in neurodegenerative diseases, Cell. Mol. Life Sci., 63, 877, 10.1007/s00018-005-5338-2 Yang, 2007, The reticulons: a family of proteins with diverse functions, Genome Biol., 8, 234, 10.1186/gb-2007-8-12-234 Zhou, 2015, Diversity of bacterial manipulation of the host ubiquitin pathways, Cell. Microbiol., 17, 26, 10.1111/cmi.12384 Zurek, 2011, Reticulon short hairpin transmembrane domains are used to shape ER tubules, Traffic, 12, 28, 10.1111/j.1600-0854.2010.01134.x