Functional conservation of the <i>Salmonella</i> and <i>Shigella</i> effectors of entry into epithelial cells

Hermant, Daniel; Ménard, Robert; Arricau, Nathalie; Parsot, Claude; Popoff, M.Y.

doi:10.1111/j.1365-2958.1995.mmi_17040781.x

Cited by 121 publications

(101 citation statements)

References 38 publications

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“…The most likely explanation is that the secretion systems of SPI1 and SPI2 function independently, but missing or mutant Ssa proteins disturb the normal function of the SPI1 secretion system, possibly by stoichiometric interactions. It is clear from the sequence analysis of SPI2 that a number of ssa genes could encode proteins that might be capable of interacting with SPI1 gene products, and it is known that some of the proteins of type III secretion systems of Salmonella SPI1, Shigella and Yersinia are functionally conserved (Ginocchio and Galán, 1995;Hermant et al, 1995;Rosqvist et al, 1995). In this context it is interesting to note that only one of three transposon insertions in ssaV results in a strain that is less invasive and in which SipC secretion is affected.…”

Section: Discussionmentioning

confidence: 99%

Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2

Hensel

Shea

Raupach

et al. 1997

Molecular Microbiology

163

186

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SummaryWe have investigated the structure and transcriptional organization of 13 genes of Salmonella Pathogenicity Island 2 (SPI2) that encode components of the second type III secretion apparatus of Salmonella typhimurium. ssaK, L, M, V, N, O, P, Q, R, S, T, U constitute one operon of 10 kb. ssaJ lies upstream of ssaK and is the terminal gene of another operon. The deduced products of ssaJ, ssaK, ssaV, ssaN, ssaO, ssaQ, ssaR, ssaS, ssaT, and ssaU show greatest similarity to the Yersinia spp. genes yscJ, yscL, lcrD, yscN, yscO, yscQ, yscR, yscS, yscT, and yscU, respectively. The products of the ssaL, ssaM and ssaP genes do not have significant similarity to products of other type III secretion systems, and might be important for the specific function of the SPI2 type III secretion system. Bacterial strains carrying different ssa mutations display minor alterations in terms of serum sensitivity when compared with the wild-type strain, but none are defective in replication within macrophage-like RAW 264.7 cells. However, some of the ssa mutant strains invade HEp2 cells less efficiently and are less cytotoxic to RAW 264.7 macrophages than the wild-type strain. We show that the invasion defect is correlated with a lack of SipC in culture supernatants of these mutant strains.SipC is a product of the SPI1 type III secretion system of S. typhimurium, and is important for epithelial cell invasion. Therefore, mutations in SPI2 can affect the SPI1 secretion system, which raises the possibility of an interaction between the two type III secretion systems.

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Section: Discussionmentioning

confidence: 99%

Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2

Hensel

Shea

Raupach

et al. 1997

Molecular Microbiology

163

186

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“…Genes required for Salmonella internalization into mammalian cells have been identified (4, 7, 14, 16, 17, 20, 22, 24, 27-29, 31, 39) and have been shown to reside on Salmonella pathogenicity island 1 (SPI-1) at centisome 63 (38) as well as two genes, sopE and sigD (sopB), that reside outside of SPI-1 (21,47,48). The invasion mechanism of Salmonella relies on a type III secretion system that secretes effector proteins into host cells targeted for invasion (6,7,20,22,28,29,33). Intracellular effector proteins transmit a signal to the cell which induces a rearrangement of the host cell cytoskeleton that results in bacterial uptake (12,13,16).…”

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confidence: 99%

Transcriptional Organization and Function of Invasion Genes within Salmonella enterica Serovar Typhimurium Pathogenicity Island 1, Including the prgH , prgI , prgJ , prgK , orgA , orgB , and orgC Genes

2000

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Salmonella enterica serovar Typhimurium initiates infection of a host by inducing its own uptake into specialized M cells which reside within the epithelium overlaying Peyer's patches. Entry of Salmonella into intestinal epithelial cells is dependent upon invasion genes that are clustered together in Salmonella pathogenicity island 1 (SPI-1). Upon contact between serovar Typhimurium and epithelial cells targeted for bacterial internalization, bacterial proteins are injected into the host cell through a type III secretion system that leads to internalization of the bacteria. Previous work has established that the prgH, -I, -J, and -K and orgA genes reside in SPI-1, and the products of these genes are predicted to be components of the invasion secretion apparatus. We report that an error in the published orgA DNA sequence has been identified so that this region encodes two small genes rather than a single large open reading frame. These genes have been designated orgA and orgB. Additionally, an opening reading frame downstream of orgB, which we have designated orgC, has been identified and partially characterized. Previously published work has indicated that the prgH, -I, -J, and -K genes are transcribed from a promoter distinct from that used by the gene immediately downstream, orgA. Here, we present experiments indicating that orgA expression is driven by the prgH promoter. In addition, using reverse transcriptase PCR analysis, we have found that this polycistronic message extends downstream of prgH to include a total of 10 genes. To more fully characterize this invasion operon, we demonstrate that the prgH, prgI, prgJ, prgK, orgA, and orgB genes are each required for invasion and secretion, while orgC is not essential for the invasive phenotype.Salmonella infections are an important health problem in both the developing and developed world (9,32,34). Pathogenic Salmonella species cause infections that range in severity from self-limiting gastroenteritis to life-threatening systemic dissemination (45). After entry into a host, the bacteria establish infection by attaching to and invading specialized M cells associated with Peyer's patches in the small intestine (5,23,26). Following M-cell invasion and destruction, host-restricted Salmonella species cause localized destruction of the intestinal epithelium (gastroenteritis). In contrast, passage of hostadapted Salmonella species through M cells allows rapid dissemination to the mesenteric lymph nodes and then to the liver and spleen, where unchecked growth causes death (25).A critical determinant in the development of Salmonella disease is the ability of the bacteria to invade cells. Salmonella enterica serovar Typhimurium mutants that are unable to invade tissue culture cells are defective in their ability to invade and destroy M cells (26,43). This defect severely limits the ability of the bacteria to initiate infection and reduces their virulence in mice (14,24,43). Genes required for Salmonella internalization into mammalian cells have been identified (4, 7, ...

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“…Time-lapse fluorescence microscopy using markers of the vacuolar membrane or using a FRET sensor to detect bacterial access to the cytosol, indicate that vacuolar lysis occurs in the continuation of the invasion process, within minutes following bacterial-cell contact (Ehsani et al 2012). Studies involving the complementation of mutants with orthologs from Salmonella typhimurium, an enteroinvasive bacterium that does not lyse, but replicates within an intracellular vacuole, point to a role for translocon components in vacuolar rupture (Hermant et al 1995), but the precise mech- …”

Section: Vacuolar Lysismentioning

confidence: 99%

The Inside Story of Shigella Invasion of Intestinal Epithelial Cells

Carayol

Nhieu

2013

Cold Spring Harbor Perspectives in Medicine

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Functional conservation of the Salmonella and Shigella effectors of entry into epithelial cells

Cited by 121 publications

References 38 publications

Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2

Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2

Transcriptional Organization and Function of Invasion Genes within Salmonella enterica Serovar Typhimurium Pathogenicity Island 1, Including the prgH , prgI , prgJ , prgK , orgA , orgB , and orgC Genes

The Inside Story of Shigella Invasion of Intestinal Epithelial Cells

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