Modulation of host microtubule dynamics by pathogenic bacteria

Abstract The eukaryotic cytoskeleton is a vulnerable target of many microbial pathogens during the course of infection. Rearrangements of host cytoskeleton benefit microbes in various stages of their infection cycle such as invasion, motility, and persistence. Bacterial pathogens deliver a number of effector proteins into host cells for modulating the dynamics of actin and microtubule cytoskeleton. Alteration of the actin cytoskeleton is generally achieved by bacterial effectors that target the small GTPases of the host. Modulation of microtubule dynamics involves direct interaction of effector proteins with the subunits of microtubules or recruiting cellular proteins that affect microtubule dynamics. This review will discuss effector proteins from animal and human bacterial pathogens that either destabilize or stabilize host microtubules to advance the infectious process. A compilation of these research findings will provide an overview of known and unknown strategies used by various bacterial effectors to modulate the host microtubule dynamics. The present review will undoubtedly help direct future research to determine the mechanisms of action of many bacterial effector proteins and contribute to understanding the survival strategies of diverse adherent and invasive bacterial pathogens.

• Publication year

  2012

• Venue

  Biomolecular Concepts

• Publication date

  2012-12-01

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1515/bmc-2012-0030PMID 23585820PMCID PMC3625037
• 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.

• WAVE2 Protein Complex Coupled to Membrane and Microtubules

  2012cited by this paper
• Edwardsiella tarda - virulence mechanisms of an emerging gastroenteritis pathogen.

  2012cited by this paper
• Actin as target for modification by bacterial protein toxins

  2011cited by this paper
• Cell biology and immunology of Listeria monocytogenes infections: novel insights

  2011influential reference
• Salmonella-induced tubular networks.

  2011cited by this paper
• Recent advances in Chlamydia subversion of host cytoskeletal and membrane trafficking pathways.

  2011cited by this paper
• Bacterial protein toxins that modify host regulatory GTPases

  2011cited by this paper
• Disruption of Microtubule Network Rescues Aberrant Actin Comets in Dynamin2-Depleted Cells

  2011cited by this paper
• How HIV Takes Advantage of the Cytoskeleton in Entry and Replication

  2011cited by this paper
• The Chlamydia Effector Chlamydial Outer Protein N (CopN) Sequesters Tubulin and Prevents Microtubule Assembly*

  2011influential reference
• Actin in Herpesvirus Infection

  2011cited by this paper
• Modulation of microtubule dynamics by a TIR domain protein from the intracellular pathogen Brucella melitensis.

  2011cited by this paper
• EseG, an Effector of the Type III Secretion System of Edwardsiella tarda, Triggers Microtubule Destabilization

  2010cited by this paper
• Cytoskeleton‐modulating effectors of enteropathogenic and enterohaemorrhagic Escherichia coli: Tir, EspFU and actin pedestal assembly

  2010cited by this paper
• Rapid microtubule bundling and stabilization by the Streptococcus pneumoniae neurotoxin pneumolysin in a cholesterol‐dependent, non‐lytic and Src‐kinase dependent manner inhibits intracellular trafficking

  2009cited by this paper
• Subversion of Innate Immune Responses by Brucella through the Targeted Degradation of the TLR Signaling Adapter, MAL

  2009cited by this paper
• Clostridium difficile Toxin CDT Induces Formation of Microtubule-Based Protrusions and Increases Adherence of Bacteria

  2009cited by this paper
• Cytokinesis is blocked in mammalian cells transfected with Chlamydia trachomatis gene CT223

  2009cited by this paper
• Brucella TIR Domain-containing Protein Mimics Properties of the Toll-like Receptor Adaptor Protein TIRAP*

  2009cited by this paper
• Dynamic instability of microtubules requires dynamin 2 and is impaired in a Charcot-Marie-Tooth mutant

  2009cited by this paper
• Life on the inside: the intracellular lifestyle of cytosolic bacteria

  2009cited by this paper
• New insights into determinants of Listeria monocytogenes virulence.

  2008cited by this paper
• The essential role of the CopN protein in Chlamydia pneumoniae intracellular growth

  2008cited by this paper
• Structural and functional studies indicate that Shigella VirA is not a protease and does not directly destabilize microtubules.

  2008influential reference
• Streptococcus pneumoniae deficient in pneumolysin or autolysin has reduced virulence in meningitis.

  2008cited by this paper
• Novel fold of VirA, a type III secretion system effector protein from Shigella flexneri

  2008cited by this paper
• Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain–containing proteins

  2008cited by this paper
• Clostridium difficile--more difficult than ever.

  2008cited by this paper
• Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation.

  2008cited by this paper
• Identification of a Novel Citrobacter rodentium Type III Secreted Protein, EspI, and Roles of This and Other Secreted Proteins in Infection

  2007influential reference
• Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens

  2007cited by this paper
• Epidemiology of human listeriosis.

  2007cited by this paper
• Microtubule-Severing Activity of Shigella Is Pivotal for Intercellular Spreading

  2006influential reference
• Actin-dependent movement of bacterial pathogens

  2006cited by this paper
• Bacterial virulence strategies that utilize Rho GTPases.

  2005cited by this paper
• Brucellosis.

  2005cited by this paper
• Modulation of Rho GTPases and the actin cytoskeleton by YopT of Yersinia.

  2005cited by this paper
• Enteropathogenic Escherichia coli Type III Effectors EspG and EspG2 Disrupt the Microtubule Network of Intestinal Epithelial Cells

  2005cited by this paper
• The multidomain protooncogenic protein c-Cbl binds to tubulin and stabilizes microtubules.

  2005cited by this paper
• Enteropathogenic and Enterohemorrhagic Escherichia coli Infections: Translocation, Translocation, Translocation

  2005cited by this paper
• Modulation of Host Cytoskeleton Function by the Enteropathogenic Escherichia coli and Citrobacter rodentium Effector Protein EspG

  2005cited by this paper
• CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex

  2005cited by this paper
• Bacterial cytotoxins: targeting eukaryotic switches

  2005cited by this paper
• Triggered phagocytosis by Salmonella: bacterial molecular mimicry of RhoGTPase activation/deactivation.

  2005cited by this paper
• Dynamin 2 binds γ-tubulin and participates in centrosome cohesion

  2004cited by this paper
• Structural insights into bacterial modulation of the host cytoskeleton.

  2004cited by this paper
• Pathogenic Escherichia coli

  2004cited by this paper
• PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia

  2004cited by this paper
• The Human c-Fes Tyrosine Kinase Binds Tubulin and Microtubules through Separate Domains and Promotes Microtubule Assembly

  2004cited by this paper
• Ectodomains 3 and 4 of Human Polymeric Immunoglobulin Receptor (hpIgR) Mediate Invasion of Streptococcus pneumoniae into the Epithelium*

  2004cited by this paper
• Enteropathogenic Escherichia coli activates the RhoA signaling pathway via the stimulation of GEF‐H1

  2004influential reference
• Effector Proteins Encoded by Salmonella Pathogenicity Island 2 Interfere with the Microtubule Cytoskeleton after Translocation into Host Cells

  2004influential reference
• Regulating Actin Dynamics at Membranes: A Focus on Dynamin

  2004cited by this paper
• Identification of a Novel Citrobacter rodentium Type III Secreted Protein, EspI, and Roles of This and Other Secreted Proteins in Infection

  2004cited by this paper
• Dynamin 2 binds gamma-tubulin and participates in centrosome cohesion.

  2004cited by this paper
• Tissue-specific contributions of pneumococcal virulence factors to pathogenesis.

  2004cited by this paper
• The dynamin superfamily: universal membrane tubulation and fission molecules?

  2004cited by this paper
• Actin lessons from pathogens.

  2004cited by this paper
• Identification of a tight junction–associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability

  2003cited by this paper
• Hijacking Rho GTPases by protein toxins and apoptosis: molecular strategies of pathogenic bacteria

  2003cited by this paper
• Chlamydia trachomatis uses host cell dynein to traffic to the microtubule-organizing center in a p50 dynamitin-independent process

  2003cited by this paper
• Microbial pathogenesis and cytoskeletal function

  2003cited by this paper
• Exploiting host microtubule dynamics: a new aspect of bacterial invasion.

  2003cited by this paper
• The oncoprotein 18/stathmin family of microtubule destabilizers.

  2002cited by this paper
• Bacterial toxins that modify the actin cytoskeleton.

  2002cited by this paper
• Shigella deliver an effector protein to trigger host microtubule destabilization, which promotes Rac1 activity and efficient bacterial internalization

  2002cited by this paper
• Dynamin at actin tails

  2002cited by this paper
• SifA, a Type III Secreted Effector of Salmonella typhimurium, Directs Salmonella‐Induced Filament (Sif) Formation Along Microtubules

  2002cited by this paper
• Activation of the Arp2/3 Complex by the Listeria ActA Protein

  2001cited by this paper
• Locus of Enterocyte Effacement from Citrobacter rodentium: Sequence Analysis and Evidence for Horizontal Transfer among Attaching and Effacing Pathogens

  2001influential reference
• Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts.

  2001cited by this paper
• Cell motility: can Rho GTPases and microtubules point the way?

  2001cited by this paper
• Salmonella: a model for bacterial pathogenesis.

  2001cited by this paper
• Opsonic phagocytosis of Streptococcus pneumoniae by alveolar macrophages is not impaired in human immunodeficiency virus-infected Malawian adults.

  2001cited by this paper
• EspG, a Novel Type III System-Secreted Protein from Enteropathogenic Escherichia coli with Similarities to VirA of Shigella flexneri

  2001cited by this paper
• Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia.

  2001cited by this paper
• Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside

  2000cited by this paper
• Small GTP binding proteins and bacterial virulence.

  2000cited by this paper
• Salmonella maintains the integrity of its intracellular vacuole through the action of SifA

  2000cited by this paper
• Structural insights into microtubule function.

  2000cited by this paper
• LaXp180, a mammalian ActA‐binding protein, identified with the yeast two‐hybrid system, co‐localizes with intracellular Listeria monocytogenes

  2000cited by this paper
• Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/stathmin.

  1999cited by this paper
• Enteropathogenic E. coli, Salmonella, and Shigella: masters of host cell cytoskeletal exploitation.

  1999cited by this paper
• Regulation of the small GTP‐binding protein Rho by cell adhesion and the cytoskeleton

  1999influential reference
• Tubulin structure: insights into microtubule properties and functions.

  1998cited by this paper
• Microtubule depolymerization induces stress fibers, focal adhesions, and DNA synthesis via the GTP-binding protein Rho.

  1998cited by this paper
• Kinesin and dynein superfamily proteins and the mechanism of organelle transport.

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• Induction of type III secretion in Shigella flexneri is associated with differential control of transcription of genes encoding secreted proteins

  1998cited by this paper
• Enteropathogenic and enterohaemorrhagic Escherichia coli : more subversive elements

  1998cited by this paper
• Rho proteins: targets for bacterial toxins.

  1997cited by this paper
• Microtubule polymerization dynamics.

  1997cited by this paper
• Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells

  1996cited by this paper
• Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules.

  1996cited by this paper
• Identification of a novel virulence gene, virA, on the large plasmid of Shigella, involved in invasion and intercellular spreading

  1995cited by this paper
• Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals.

  1995cited by this paper
• Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals

  1995cited by this paper
• Stathmin interaction with a putative kinase and coiled-coil-forming protein domains.

  1995cited by this paper
• Molecular studies on the virulence of Listeria monocytogenes.

  1995cited by this paper
• Acute bacterial meningitis in adults. A review of 493 episodes.

  1993cited by this paper
• Interaction of chlamydiae and host cells in vitro.

  1991cited by this paper

• The jasmonic acid-regulated TaG3LEA-25 gene mediates wheat resistance to Fusarium head blight.

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• Unravelling bacterial virulence factors in yeast: From identification to the elucidation of their mechanisms of action

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• Quantitative ubiquitylome crosstalk with proteome analysis revealed cytoskeleton proteins influence CLas pathogen infection in Diaphorina citri.

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• A conserved microtubule-binding region in Xanthomonas XopL is indispensable for induced plant cell death reactions

  2023cites this paper
• A Functional Yeast-Based Screen Identifies the Host Microtubule Cytoskeleton as a Target of Numerous Chlamydia pneumoniae Proteins

  2023cites this paper
• A conserved microtubule-binding region in Xanthomonas XopL is indispensable for induced plant cell death reactions

  2023cites this paper
• The C‐terminal extension of VgrG4 from Klebsiella pneumoniae remodels host cell microfilaments

  2022cites this paper
• Nanoscale characterization of drug-induced microtubule filament dysfunction using super-resolution microscopy

  2021cites this paper
• Tight Junctions as a Key for Pathogens Invasion in Intestinal Epithelial Cells

  2021cites this paper
• Application of a Chlamydia trachomatis Expression System To Identify Chlamydia pneumoniae Proteins Translocated into Host Cells

  2021cites this paper
• CSI-Microbes: Identifying cell-type specific intracellular microbes from single-cell RNA-seq data

  2021cites this paper
• Cell properties assessment using optimized dielectrophoresis-based cell stretching and lumped mechanical modeling

  2021influential citation
• Global Proteomic Profiling of Piscirickettsia salmonis and Salmon Macrophage-Like Cells during Intracellular Infection

  2020cites this paper
• Comparative functional genomic analysis of Alzheimer’s affected and naturally aging brains

  2020cites this paper
• Global Proteomic Profiling of Piscirickettsia

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• Ultra-Low Colcemid Doses Induce Microtubule Dysfunction as Revealed by Super-Resolution Microscopy

  2020cites this paper
• The responses of lungs and adjacent lymph nodes in responding to Yersinia pestis infection: A transcriptomic study using a non-human primate model

  2019cites this paper
• Engulfment, persistence and fate of Bdellovibrio bacteriovorus predators inside human phagocytic cells informs their future therapeutic potential

  2019cites this paper
• Klebsiella pneumoniae disassembles host microtubules in lung epithelial cells

  2018cites this paper
• Cytoskeletons in the Closet—Subversion in Alphaherpesvirus Infections

  2018cites this paper
• Stathmin recruits tubulin to Listeria monocytogenes-induced actin comets and promotes bacterial dissemination

  2018cites this paper
• Intracellular fate of Ureaplasma parvum entrapped by host cellular autophagy

  2017cites this paper
• Modulation of Microtubule Dynamics Affects Brucella abortus Intracellular Survival, Pathogen-Containing Vacuole Maturation, and Pro-inflammatory Cytokine Production in Infected Macrophages

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• RNA-seq analysis of early enteromyxosis in turbot (Scophthalmus maximus): new insights into parasite invasion and immune evasion strategies.

  2016cites this paper
• OHMS**: Phytoplasmas dictate changes in sieve-element ultrastructure to accommodate their requirements for nutrition, multiplication and translocation

  2016cites this paper
• Manipulation of the Host Cell Cytoskeleton by Chlamydia.

  2016cites this paper
• Two Small Molecules Block Oral Epithelial Cell Invasion by Porphyromons gingivalis

  2016cites this paper
• Bacillus anthracis TIR Domain-Containing Protein Localises to Cellular Microtubule Structures and Induces Autophagy

  2016cites this paper
• Differential profiles of gastrointestinal proteins interacting with peptidoglycans from Lactobacillus plantarum and Staphylococcus aureus.

  2015cites this paper
• Genome-wide Screen of Pseudomonas aeruginosa in Saccharomyces cerevisiae Identifies New Virulence Factors

  2015cites this paper
• A Chlamydia effector recruits CEP170 to reprogram host microtubule organization

  2015cites this paper
• Receptor-like cytoplasmic kinases as downstream effectors of RAC/ROP GTPases in the interaction of Arabidopsis and barley with powdery mildew fungi

  2015cites this paper
• Salmonella and the oxidative burst : tales of a complicated relationship.

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• Autophagy in the Infected Cell: Insights from Pathogenic Bacteria

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• Multiple Roles of the Cytoskeleton in Bacterial Autophagy

  2014cites this paper
• The Brucella TIR domain containing proteins BtpA and BtpB have a structural WxxxE motif important for protection against microtubule depolymerisation

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• To con protection: TIR-domain containing proteins (Tcp) and innate immune evasion.

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• Serogroup-Specific Interaction of Neisseria meningitidis Capsular Polysaccharide with Host Cell Microtubules and Effects on Tubulin Polymerization

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