Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella

Méresse, Stéphane; Unsworth, Kate E.; Habermann, Anja; Griffiths, Gareth; Fang, Ferric C.; Martínez‐Lorenzo, María José; Waterman, Scott R.; Gorvel, Jean‐Pierre; Holden, David W.

doi:10.1046/j.1462-5822.2001.00141.x

Cited by 148 publications

(180 citation statements)

References 53 publications

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“…Previous studies indicated SPI2-dependent modifications of the actin cytoskeleton (28,29). Infection of HeLa cells with S. bongori harboring SPI2 did not result in detectable alterations in the organization of the actin cytoskeleton (Fig.…”

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confidence: 62%

Functional Transfer of Salmonella Pathogenicity Island 2 to Salmonella bongori and Escherichia coli

2004

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The type III secretion system (T3SS) encoded by the Salmonella pathogenicity island 2 (SPI2) has a central role in systemic infections by Salmonella enterica and for the intracellular phenotype. Intracellular S. enterica uses the SPI2-encoded T3SS to translocate a set of effector proteins into the host cell, which modify host cell functions, enabling intracellular survival and replication of the bacteria. We sought to determine whether specific functions of the SPI2-encoded T3SS can be transferred to heterologous hosts Salmonella bongori and Escherichia coli Mutaflor, species that lack the SPI2 locus and loci encoding effector proteins. The SPI2 virulence locus was cloned and functionally expressed in S. bongori and E. coli. Here, we demonstrate that S. bongori harboring the SPI2 locus is capable of secretion of SPI2 substrate proteins under culture conditions, as well as of translocation of effector proteins under intracellular conditions. An SPI2-mediated cellular phenotype was induced by S. bongori harboring the SPI2 if the sifA locus was cotransferred. An interference with the host cell microtubule cytoskeleton, a novel SPI2-dependent phenotype, was observed in epithelial cells infected with S. bongori harboring SPI2 without additional effector genes. S. bongori harboring SPI2 showed increased intracellular persistence in a cell culture model, but SPI2 transfer was not sufficient to confer to S. bongori systemic pathogenicity in a murine model. Transfer of SPI2 to heterologous hosts offers a new tool for the study of SPI2 functions and the phenotypes of individual effectors.During the evolution of bacterial pathogenesis, the horizontal transfer of virulence genes has been a driving force for the emergence of new species and the adaptation of pathogens to new hosts and specific sites in these hosts. It has been concluded that large clusters of virulence genes are exchanged between various bacteria, and the acquisitions of so-called "pathogenicity islands" are considered as quantum leaps in the evolution of bacterial pathogenesis (13,35).Salmonella spp. form a complex group of gastrointestinal pathogens of animals and humans. Traditionally, a large number of isolates of Salmonella enterica have been defined as species due to distinct serological differences. However, molecular analyses indicated that most of these isolates represent serotypes of the species S. enterica, for example, S. enterica subspecies I serotype Typhimurium, and current taxonomy defines two species of Salmonella. Human infections are most frequently caused by various serovars of S. enterica. Disease outcomes associated with S. enterica can range from self-limiting localized gastrointestinal infections to life-threatening systemic infections such as typhoid fever (9). S. bongori, a second Salmonella species, is only rarely observed in human infections and is found as a commensal of cold-blooded animals (4, 38). Molecular analyses indicated that S. bongori represents a phylogenetically older separation from the genus Salmonella (4, 6).Beside...

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confidence: 62%

Functional Transfer of Salmonella Pathogenicity Island 2 to Salmonella bongori and Escherichia coli

2004

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“…The third phenotype associated with T3SS2 effectors is the formation of an F-actin meshwork in the vicinity of the SCV, also known as vacuole-associated actin polymerizations (VAP), a process that is associated with SCV membrane integrity [53]. Three T3SS2 effectors, namely SteC, SseI and SspH2, have been implicated in this process although their roles remain obtuse.…”

Section: T3ss2 Effectors Mediate Intermediate and Late Scv Biogenesismentioning

confidence: 99%

The Salmonella-containing vacuole—Moving with the times

Steele‐Mortimer¹

2008

Current Opinion in Microbiology

265

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SummarySalmonella pathogenesis is dependent on its ability to invade and replicate within host cells. Following invasion the bacteria remain within a modified phagosome known as the Salmonellacontaining vacuole (SCV), within which they will survive and replicate. Invasion and SCV biogenesis are dependent on two Type III Secretion Systems, T3SS1 & T3SS2, which are used to translocate distinct cohorts of bacterial effector proteins into the host cell. Elucidating the roles of individual effector proteins in SCV biogenesis has proven difficult but several distinct themes are now emerging and it is apparent that SCV biogenesis is an extremely dynamic process involving; extensive membrane remodeling, interactions with the endolysosomal pathway, actin rearrangements and microtubule-based movement and tubule extension.

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“…Correct modulation of the cytoskeleton has been shown to be required for expansion of both the Salmonella and Chlamydia vacuoles [2,3]. Finally, it has been shown that some PCVs are surrounded by a scaffold of F-actin and other cytoskeletal components that provide structural support for the vacuole [3,4].…”

Section: Role Of the Cytoskeleton In Vacuole Stabilitymentioning

confidence: 99%

“…Both the Salmonella and Chlamydia vacuoles are surrounded by a network of F-actin [3,4]. This network is required for vacuole stability of both these pathogens as treatment with Factin polymerisation inhibitors leads to the loss of integrity [3,4].…”

Section: Role Of the Cytoskeleton In Vacuole Stabilitymentioning

confidence: 99%

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Maintenance of vacuole integrity by bacterial pathogens

Creasey

Isberg²

2014

Current Opinion in Microbiology

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Many intracellular bacterial pathogens reside within a membrane-bound compartment. The biogenesis of these vacuolar compartments is complex, involving subversion of host cell secretory pathways by bacterial proteins. In recent years it has become clear that disruption of vacuole biogenesis may result in membrane rupture and escape of bacteria into the host cell cytosol. Correct modulation of the host cell cytoskeleton, signalling molecules such as small GTPases and the lipids of the vacuole membrane have all been shown to be critical in the maintenance of vacuole integrity. Increasing evidence suggests that vacuole rupture may result from aberrant mechanical forces exerted on the vacuole, possibly due to a defect in vacuole expansion.

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Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella

Cited by 148 publications

References 53 publications

Functional Transfer of Salmonella Pathogenicity Island 2 to Salmonella bongori and Escherichia coli

Functional Transfer of Salmonella Pathogenicity Island 2 to Salmonella bongori and Escherichia coli

The Salmonella-containing vacuole—Moving with the times

Maintenance of vacuole integrity by bacterial pathogens

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