Formation of the Legionella Replicative Compartment at the Crossroads of Retrograde Trafficking

Retrograde trafficking from the endosomal system through the Golgi apparatus back to the endoplasmic reticulum is an essential pathway in eukaryotic cells, serving to maintain organelle identity and to recycle empty cargo receptors delivered by the secretory pathway. Intracellular replication of several bacterial pathogens, including Legionella pneumophila, is restricted by the retrograde trafficking pathway. L. pneumophila employs the Icm/Dot type IV secretion system (T4SS) to form the replication-permissive Legionella-containing vacuole (LCV), which is decorated with multiple components of the retrograde trafficking machinery as well as retrograde cargo receptors. The L. pneumophila effector protein RidL is secreted by the T4SS and interferes with retrograde trafficking. Here, we review recent evidence that the LCV interacts with the retrograde trafficking pathway, discuss the possible sites of action and function of RidL in the retrograde route, and put forth the hypothesis that the LCV is an acceptor compartment of retrograde transport vesicles.

• Publication year

  2017

• Venue

  Frontiers in Cellular and Infection Microbiology

• Publication date

  2017-11-24

• Fields of study

  Biology, Medicine, Chemistry

• Identifiers
  DOI 10.3389/fcimb.2017.00482PMID 29226112PMCID 5706426
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Structural insights into Legionella RidL-Vps29 retromer subunit interaction reveal displacement of the regulator TBC1D5

  2017influential reference
• Comparative Proteomics of Purified Pathogen Vacuoles Correlates Intracellular Replication of Legionella pneumophila with the Small GTPase Ras-related protein 1 (Rap1) *

  2017influential reference
• Molecular basis for the binding and modulation of V-ATPase by a bacterial effector protein

  2017cited by this paper
• Legionella pneumophila, armed to the hilt: justifying the largest arsenal of effectors in the bacterial world.

  2016cited by this paper
• Probable Person-to-Person Transmission of Legionnaires' Disease.

  2016cited by this paper
• Bidirectional traffic between the Golgi and the endosomes – machineries and regulation

  2016cited by this paper
• Structural and mechanistic insights into regulation of the retromer coat by TBC1d5

  2016influential reference
• Structural Mechanism for Cargo Recognition by the Retromer Complex.

  2016cited by this paper
• Subversion of Retrograde Trafficking by Translocated Pathogen Effectors.

  2016cited by this paper
• Global Mapping of the Inc-Human Interactome Reveals that Retromer Restricts Chlamydia Infection.

  2015cited by this paper
• Formation of a pathogen vacuole according to Legionella pneumophila: how to kill one bird with many stones

  2015influential reference
• Subversion of Cell-Autonomous Immunity and Cell Migration by Legionella pneumophila Effectors

  2015cited by this paper
• The role of the Lowe syndrome protein OCRL in the endocytic pathway

  2015cited by this paper
• Phosphatidylinositol 4-phosphate and phosphatidylinositol 3-phosphate regulate phagolysosome biogenesis

  2015cited by this paper
• Purification and proteomics of pathogen-modified vacuoles and membranes

  2015influential reference
• The Proteome of the Isolated Chlamydia trachomatis Containing Vacuole Reveals a Complex Trafficking Platform Enriched for Retromer Components

  2015cited by this paper
• A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer

  2014cited by this paper
• Live-Cell Imaging of Phosphoinositide Dynamics and Membrane Architecture during Legionella Infection

  2014cited by this paper
• Rab proteins and the compartmentalization of the endosomal system.

  2014cited by this paper
• The natural alternative: protozoa as cellular models for Legionella infection

  2014influential reference
• Functional analysis of novel Rab GTPases identified in the proteome of purified Legionella‐containing vacuoles from macrophages

  2014influential reference
• From endosomes to the trans-Golgi network.

  2014cited by this paper
• Retromer: a master conductor of endosome sorting.

  2014cited by this paper
• Host Pathways Important for Coxiella burnetii Infection Revealed by Genome-Wide RNA Interference Screening

  2013cited by this paper
• Phosphoinositide lipids and the Legionella pathogen vacuole.

  2013cited by this paper
• A global analysis of SNX27–retromer assembly and cargo specificity reveals a function in glucose and metal ion transport

  2013cited by this paper
• The Legionella effector RidL inhibits retrograde trafficking to promote intracellular replication.

  2013influential reference
• A Rab-centric perspective of bacterial pathogen-occupied vacuoles.

  2013influential reference
• Snx3 regulates recycling of the transferrin receptor and iron assimilation.

  2013cited by this paper
• Activation of Ran GTPase by a Legionella Effector Promotes Microtubule Polymerization, Pathogen Vacuole Motility and Infection

  2013cited by this paper
• A mechanism for retromer endosomal coat complex assembly with cargo

  2013influential reference
• Secretive Bacterial Pathogens and the Secretory Pathway

  2012cited by this paper
• Coordination between RAB GTPase and phosphoinositide regulation and functions

  2012cited by this paper
• Salmonella Inhibits Retrograde Trafficking of Mannose-6-Phosphate Receptors and Lysosome Function

  2012cited by this paper
• The retromer complex – endosomal protein recycling and beyond

  2012cited by this paper
• Dynamics of Rab7b‐Dependent Transport of Sorting Receptors

  2012cited by this paper
• Insights into the PX (phox-homology) domain and SNX (sorting nexin) protein families: structures, functions and roles in disease.

  2012cited by this paper
• The Legionella pneumophila effector DrrA is sufficient to stimulate SNARE-dependent membrane fusion.

  2012cited by this paper
• Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules

  2012cited by this paper
• The PH domain proteins IPIP27A and B link OCRL1 to receptor recycling in the endocytic pathway

  2011cited by this paper
• SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signaling receptors

  2011cited by this paper
• A structural basis for Lowe syndrome caused by mutations in the Rab‐binding domain of OCRL1

  2011cited by this paper
• Sorting nexins provide diversity for retromer-dependent trafficking events

  2011cited by this paper
• Retrograde Transport: Two (or More) Roads Diverged in an Endosomal Tree?

  2011cited by this paper
• OCRL controls trafficking through early endosomes via PtdIns4,5P2‐dependent regulation of endosomal actin

  2011cited by this paper
• Covalent coercion by Legionella pneumophila.

  2011cited by this paper
• Legionella spp. outdoors: colonization, communication and persistence.

  2011cited by this paper
• The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics

  2010cited by this paper
• Molecular Pathogenesis of Infections Caused by Legionella pneumophila

  2010cited by this paper
• Modulation of host cell function by Legionella pneumophila type IV effectors.

  2010cited by this paper
• Rab7b controls trafficking from endosomes to the TGN

  2010cited by this paper
• Transport vesicle uncoating: it’s later than you think

  2010cited by this paper
• Legionella pneumophila Promotes Functional Interactions between Plasma Membrane Syntaxins and Sec22b

  2010cited by this paper
• Inhibition of Host Vacuolar H+-ATPase Activity by a Legionella pneumophila Effector

  2010cited by this paper
• Proteomic analysis of Legionella-containing phagosomes isolated from Dictyostelium.

  2009cited by this paper
• The inositol polyphosphate 5‐phosphatase OCRL1 restricts intracellular growth of Legionella, localizes to the replicative vacuole and binds to the bacterial effector LpnE

  2009influential reference
• A FAM21-containing WASH complex regulates retromer-dependent sorting.

  2009cited by this paper
• Proteome Analysis of Legionella Vacuoles Purified by Magnetic Immunoseparation Reveals Secretory and Endosomal GTPases

  2009cited by this paper
• The Retromer Coat Complex Coordinates Endosomal Sorting and Dynein-Mediated Transport, with Carrier Recognition by the trans-Golgi Network

  2009cited by this paper
• The BAR domain superfamily: membrane-molding macromolecules.

  2009cited by this paper
• Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5

  2009cited by this paper
• Endosomal and secretory markers of the Legionella-containing vacuole

  2009influential reference
• A PH domain within OCRL bridges clathrin‐mediated membrane trafficking to phosphoinositide metabolism

  2009cited by this paper
• Rab GTPases as coordinators of vesicle traffic

  2009cited by this paper
• The Legionella pneumophila replication vacuole: making a cosy niche inside host cells

  2009cited by this paper
• Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7

  2008cited by this paper
• Tracing the retrograde route in protein trafficking.

  2008cited by this paper
• Large Scale Screening for Novel Rab Effectors Reveals Unexpected Broad Rab Binding Specificity*S

  2008cited by this paper
• Regulation of Phagocytosis in Dictyostelium by the Inositol 5‐Phosphatase OCRL Homolog Dd5P4

  2007cited by this paper
• Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval

  2007cited by this paper
• VAMP4 cycles from the cell surface to the trans-Golgi network via sorting and recycling endosomes

  2007influential reference
• Rab6‐interacting Protein 1 Links Rab6 and Rab11 Function

  2007cited by this paper
• EHD1 Interacts with Retromer to Stabilize SNX1 Tubules and Facilitate Endosome‐to‐Golgi Retrieval

  2007cited by this paper
• Phosphoinositides in cell regulation and membrane dynamics

  2006cited by this paper
• Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila

  2006cited by this paper
• Membrane targeting and activation of the Lowe syndrome protein OCRL1 by rab GTPases

  2006cited by this paper
• Retrograde transport from endosomes to the trans-Golgi network

  2006cited by this paper
• Interchangeable but Essential Functions of SNX1 and SNX2 in the Association of Retromer with Endosomes and the Trafficking of Mannose 6-Phosphate Receptors

  2006cited by this paper
• Phosphoinositides in cell regulation and membrane dynamics

  2006cited by this paper
• A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer

  2006cited by this paper
• Legionella pneumophila Exploits PI(4)P to Anchor Secreted Effector Proteins to the Replicative Vacuole

  2006cited by this paper
• Dynamic properties of Legionella‐containing phagosomes in Dictyostelium amoebae

  2005cited by this paper
• Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides.

  2004cited by this paper
• The inositol polyphosphate 5-phosphatase Ocrl associates with endosomes that are partially coated with clathrin.

  2004cited by this paper
• Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor

  2004cited by this paper
• Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites

  2002cited by this paper
• Rab proteins as membrane organizers

  2001cited by this paper
• Antigenic and genetic characterization of Legionella proteins: contributions to taxonomy, diagnosis and pathogenesis.

  1997cited by this paper
• Endosome to Golgi Retrieval of the Vacuolar Protein Sorting Receptor, Vps10p, Requires the Function of the VPS29, VPS30, and VPS35 Gene Products

  1997cited by this paper
• Antigenic and genetic characterization of Leaionella Proteins: Contribution to taxonomy, diagnosis and pathogenesis

  1997cited by this paper
• Cholera toxin binding affinity and specificity for gangliosides determined by surface plasmon resonance.

  1996cited by this paper
• The protein deficient in Lowe syndrome is a phosphatidylinositol-4,5-bisphosphate 5-phosphatase.

  1995cited by this paper
• Association of Legionella pneumophila with the macrophage endoplasmic reticulum

  1995cited by this paper
• Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network

  1994cited by this paper
• Rab9 functions in transport between late endosomes and the trans Golgi network.

  1993cited by this paper
• Verotoxins and their glycolipid receptors.

  1993cited by this paper
• The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes

  1983cited by this paper

• Pathogen-induced rerouting of host membrane trafficking.

  2025cites this paper
• Characterizing host-microbe interactions with bacterial effector proteins using proximity-dependent biotin identification (BioID)

  2025cites this paper
• A genetically-encoded fluorescence-based reporter to spatiotemporally investigate mannose-6-phosphate pathway

  2024cites this paper
• Legionella‐ and host‐driven lipid flux at LCV‐ER membrane contact sites promotes vacuole remodeling

  2023cites this paper
• Imaging Flow Cytometry of Legionella-Containing Vacuoles in Intact and Homogenized Wild-Type and Mutant Dictyostelium.

  2023cites this paper
• Pathogen vacuole membrane contact sites – close encounters of the fifth kind

  2023cites this paper
• Ubiquitination of Sec22b by a novel Legionella pneumophila ubiquitin E3 ligase

  2023cites this paper
• The large GTPase Sey1/atlastin mediates lipid droplet- and FadL-dependent intracellular fatty acid metabolism of Legionella pneumophila

  2023cites this paper
• The Legionella-driven PtdIns(4)P gradient at LCV-ER membrane contact sites promotes Vap-, OSBP- and Sac1-dependent pathogen vacuole remodeling

  2022cites this paper
• An Insight into the Microbiology, Epidemiology, and Host Cell Biology of Legionella Pneumophila: A Review of Literature

  2022cites this paper
• Human Cytomegalovirus Manipulates Syntaxin 6 for Successful Trafficking and Subsequent Infection of Monocytes

  2022influential citation
• Glycosylating Effectors of Legionella pneumophila: Finding the Sweet Spots for Host Cell Subversion

  2022cites this paper
• The large GTPase Sey1/atlastin mediates lipid droplet- and FadL-dependent intracellular fatty acid metabolism of Legionella pneumophila

  2022cites this paper
• Modulation of phagosome phosphoinositide dynamics by a Legionella phosphoinositide 3‐kinase

  2021cites this paper
• Dictyostelium Dynamin Superfamily GTPases Implicated in Vesicle Trafficking and Host-Pathogen Interactions

  2021cites this paper
• The Polar Legionella Icm/Dot T4SS Establishes Distinct Contact Sites with the Pathogen Vacuole Membrane

  2021cites this paper
• Potential Therapies and Diagnosis Based on Golgi-targeted Nano Drug Delivery Systems.

  2021cites this paper
• Pathogenicity and Virulence of Legionella: Intracellular replication and host response

  2021cites this paper
• The Role of Lipids in Legionella-Host Interaction

  2021cites this paper
• Structural and functional study of Legionella pneumophila effector RavA

  2021cites this paper
• Structural biology of the invasion arsenal of Gram‐negative bacterial pathogens

  2021cites this paper
• Dictyostelium lacking the single atlastin homolog Sey1 shows aberrant ER architecture, proteolytic processes and expansion of the Legionella‐containing vacuole

  2021cites this paper
• Evolution and function of bacterial RCC1 repeat effectors.

  2020cites this paper
• Phosphoinositides and the Fate of Legionella in Phagocytes

  2020cites this paper
• The vacuole guard hypothesis: how intravacuolar pathogens fight to maintain the integrity of their beloved home.

  2020cites this paper
• Legionella quorum sensing meets cyclic-di-GMP signaling.

  2020cites this paper
• Divergent Evolution of Legionella RCC1 Repeat Effectors Defines the Range of Ran GTPase Cycle Targets

  2020cites this paper
• Paradoxical Pro-inflammatory Responses by Human Macrophages to an Amoebae Host-Adapted Legionella Effector.

  2020cites this paper
• New insights into the evasion of host innate immunity by Mycobacterium tuberculosis

  2020cites this paper
• Legionella pneumophila Infection Rewires the Acanthamoeba castellanii Transcriptome, Highlighting a Class of Sirtuin Genes

  2020cites this paper
• Quantitative Imaging Flow Cytometry of Legionella-Containing Vacuoles in Dually Fluorescence-Labeled Dictyostelium.

  2019cites this paper
• Harnessing Macrophages for Controlled-Release Drug Delivery: Lessons From Microbes

  2019cites this paper
• Legionella

  2019influential citation
• Interaction of the Ankyrin H Core Effector of Legionella with the Host LARP7 Component of the 7SK snRNP Complex

  2019cites this paper
• Intracellular parasitism, the driving force of evolution of Legionella pneumophila and the genus Legionella.

  2019cites this paper
• Hostile Takeover: Hijacking of Endoplasmic Reticulum Function by T4SS and T3SS Effectors Creates a Niche for Intracellular Pathogens

  2019cites this paper
• Intracellular parasitism, the driving force of evolution of Legionella pneumophila and the genus Legionella

  2019cites this paper
• A Mycobacterium tuberculosis surface protein recruits ubiquitin to trigger host xenophagy

  2019cites this paper
• Exploitation of Phosphoinositides by the Intracellular Pathogen, Legionella pneumophila

  2019cites this paper
• A Legionella pneumophila Kinase Phosphorylates the Hsp70 Chaperone Family to Inhibit Eukaryotic Protein Synthesis.

  2019cites this paper
• Quantitative Imaging Flow Cytometry of Legionella-Infected Dictyostelium Amoebae Reveals the Impact of Retrograde Trafficking on Pathogen Vacuole Composition

  2018cites this paper
• Nutritional virulence of Legionella pneumophila.

  2018cites this paper
• Highlighting the Potency of Biosurfactants Produced by Pseudomonas Strains as Anti-Legionella Agents

  2018cites this paper
• Evasion of phagotrophic predation by protist hosts and innate immunity of metazoan hosts by Legionella pneumophila

  2018cites this paper
• Evolution of the Arsenal of Legionella pneumophila Effectors To Modulate Protist Hosts

  2018cites this paper
• Mammalian Solute Carrier (SLC)-like transporters of Legionella pneumophila

  2018cites this paper
• Emerging Role of Retromer in Modulating Pathogen Growth.

  2018cites this paper
• A Legionella pneumophila amylase is essential for intracellular replication in human macrophages and amoebae

  2018cites this paper
• Endosomal receptor trafficking: Retromer and beyond

  2018cites this paper
• Acanthamoeba and Dictyostelium as Cellular Models for Legionella Infection

  2018cites this paper