Non‐invasive <i>Salmonella typhimurium</i> mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer's patches

Penheiter, Kristi L.; Mathur, Nitin; Giles, Dobie L.; Fahlen, Thomas F.; Jones, Bradley D.

doi:10.1046/j.1365-2958.1997.3741745.x

Cited by 169 publications

(168 citation statements)

References 35 publications

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“…HA and HR serotypes may be permitted to give raise to a systemic infection provided they interact with a unique character of a specialized tissue of the host epithelium. This hypothesis is supported by the observation that, although the majority of salmonella epithelial cell interactions occur at the apical membrane of the enterocytes [147], early association and entry of salmonella appears to be via the M cells lining the small intestine PP [57,[170][171][172][173]. Cytokine secretion by M cells and activation of subepithelial phagocytic cells may regulate both intestinal inflammation and salmonella persistence in deeper tissues.…”

Section: Site Of In Asionmentioning

confidence: 97%

Host adapted serotypes of Salmonella enterica

et al. 2000

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Salmonella constitutes a genus of zoonotic bacteria of worldwide economic and health importance. The current view of salmonella taxonomy assigns the members of this genus to two species: S. enterica and S. bongori. S. enterica itself is divided into six subspecies, enterica, salamae, arizonae, diarizonae, indica, and houtenae, also known as subspecies I, II, IIIa, IIIb, IV, and VI, respectively [1]. Members of Salmonella enterica subspecies enterica are mainly associated with warm-blooded vertebrates and are usually transmitted by ingestion of food or water contaminated by infected faeces. The pathogenicity of most of the distinct serotypes remains undefined, and even within the most common serotypes, many questions remain to be answered regarding the interactions between the organism and the infected host.Salmonellosis manifests itself in three major forms: enteritis, septicaemia, and abortion, each of which may be present singly or in combination, depending on both the serotype and the host involved. Although currently over 2300 serovars of Salmonella are recognized, only about 50 serotypes are isolated in any significant numbers as human or animal pathogens [2, 3] and they all belong to subspecies enterica. Of these, most cause acute gastroenteritis characterized by a short incubation period and a severe systemic disease in man or animals, characterized by septicaemia, fever and/or abortion, and such serotypes are often associated with one or few host species [4–6].It is the intention of this review to present a summary of current knowledge of these host-adapted serotypes of S. enterica. The taxonomic relationships between the serotypes will be discussed together with a comparison of the pathology and pathogenesis of the disease that they cause in their natural host(s). Since much of our knowledge on salmonellosis is based on the results of work on Typhimurium, this serotype will often be used as the baseline in discussion. It is hoped that an appreciation of the differences that exist in the way these serotypes interact with the host will lead to a greater understanding of the complex host–parasite relationship that characterizes salmonella infections.

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Section: Site Of In Asionmentioning

confidence: 97%

Host adapted serotypes of Salmonella enterica

et al. 2000

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“…A serovar Typhimurium orgA::Tn5lacZY mutant is noninvasive and has reduced virulence for mice following oral infection. Other work has shown that this mutation prevents the invasion and destruction of M cells and has a general defect in secretion of invasion effector proteins (43). In addition, orgA is similar to the mxiK gene in Shigella (1), a putative component of the type III secretion system in that pathogen.…”

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confidence: 91%

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confidence: 99%

“…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, 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).…”

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confidence: 99%

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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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“…Salmonellae express a variety of virulence factors, including very polymorphic surface carbohydrates, multiple fimbrial adhesins, phase-variable flagella, and mechanisms for invasion and survival in host macrophages and other cells (see review in references 13 and 44). Because Salmonella is acquired mainly by oral ingestion of contaminated materials, a key step of infection is its passage across the intestinal epithelium by invasion of M cells in Peyer's patches (7,20,39) or of enterocytes (46). Many of the genes required for intestinal penetration and invasion of host cells are carried on the 40-kb region at centisome 63, which is called Salmonella pathogenicity island 1 (SPI1) (reviewed in reference 10).…”

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DNA-Binding Activities of the HilC and HilD Virulence Regulatory Proteins ofSalmonella entericaSerovar Typhimurium

2002

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The HilC and HilD proteins of Salmonella enterica serovar Typhimurium are members of the AraC/XylS family of transcription regulators. They are encoded on Salmonella pathogenicity island 1 (SPI1) and control expression of the hilA gene, which encodes the major transcriptional activator for many genes encoded on SPI1 and elsewhere that contribute to invasion of host cells. Gel electrophoretic shift and DNase footprinting assays revealed that purified HilC and HilD proteins can bind to multiple regions in the hilA and hilC promoters and to a single region in the hilD promoter. Although both HilC and -D proteins can bind to the same DNA regions, they showed different dependencies on the sequence and lengths of their DNA targets. To identify the binding-sequence specificity of HilC and HilD, a series of single base substitutions changing each position in a DNA fragment corresponding to positions ؊92 to ؊52 of the hilC promoter was tested for binding to HilC and HilD in a gel shift DNA-binding assay. This mutational analysis in combination with sequence alignments allowed deduction of consensus sequences for binding of both proteins. The consensus sequences overlap but differ so that HilC can bind to both types of sites but HilD only to one. The hilA and hilC promoters contain multiple binding sites of each type, whereas the hilD promoter contains a site that binds HilC but not HilD without additional binding elements. The HilC and HilD proteins had no major effect on transcription from the hilA or hilD promoters using purified proteins in vitro but changed the choice of promoter at hilC. These results are consistent with a model derived from analysis of lacZ fusions stating that HilC and HilD enhance hilA expression by counteracting a repressing activity.

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Non‐invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer's patches

Cited by 169 publications

References 35 publications

Host adapted serotypes of Salmonella enterica

Host adapted serotypes of Salmonella enterica

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

DNA-Binding Activities of the HilC and HilD Virulence Regulatory Proteins ofSalmonella entericaSerovar Typhimurium

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