Salmonella Typhimurium SPI-1 genes promote intestinal but not tonsillar colonization in pigs

Boyen, Filip; Pasmans, Frank; Immerseel, Filip Van; Morgan, Elfed; Adriaensen, Connie; Hernálsteens, Jean-Pierre; Decostere, Annemie; Ducatelle, Richard; Haesebrouck, Freddy

doi:10.1016/j.micinf.2006.09.008

Cited by 54 publications

(52 citation statements)

References 33 publications

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“…Furthermore, both SPI-4 and SPI-1 genes are downregulated during infection of macrophages (30). However, whereas HilA is involved in the invasion of a broad range of hosts (e.g., chickens [9], cattle [83], and pigs [11]), SPI-4 was shown to be important for the colonization of cattle but not of chickens (61,62). Possibly additional regulatory effects control this host specificity.…”

Section: Discussionmentioning

confidence: 99%

Delineation of the Salmonella enterica Serovar Typhimurium HilA Regulon through Genome-Wide Location and Transcript Analysis

et al. 2007

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The Salmonella enterica serovar Typhimurium HilA protein is the key regulator for the invasion of epithelial cells. By a combination of genome-wide location and transcript analysis, the HilA-dependent regulon has been delineated. Under invasion-inducing conditions, HilA binds to most of the known target genes and a number of new target genes. The sopB, sopE, and sopA genes, encoding effector proteins secreted by the type III secretion system on Salmonella pathogenicity island 1 (SPI-1), were identified as being both bound by HilA and differentially regulated in an HilA mutant. This suggests a cooperative role for HilA and InvF in the regulation of SPI-1-secreted effectors. Also, siiA, the first gene of SPI-4, is both bound by HilA and differentially regulated in an HilA mutant, thus linking this pathogenicity island to the invasion key regulator. Finally, the interactions of HilA with the SPI-2 secretion system gene ssaH and the flagellar gene flhD imply a repressor function for HilA under invasion-inducing conditions. Salmonella enterica serovar Typhimurium causes a host-dependent range of diseases from self-limiting gastroenteritis to life-threatening systemic infections. The complex infection process is initiated by invasion of the intestinal epithelial monolayer (75) by means of a type III secretion system (TTSS), encoded on pathogenicity island 1 (SPI-1), through which effector proteins are translocated into the epithelial cells (17,53). By manipulating host cell functions via these effector proteins, S. enterica serovar Typhimurium alters the epithelial cell's cytoskeletal structure, leading to bacterial internalization (76).The key regulator for the composition and functioning of this invasion-enabling TTSS and associated effector proteins is HilA, an OmpR/ToxR family transcriptional regulator (5), which is also encoded within SPI-1. A complex interaction of environmental and genetic control elements (3,29,43) induces HilA to activate the inv/spa and prg operons, encoding components of the TTSS apparatus (51, 52), and the sic/sip operon, encoding a chaperone and secreted proteins (23). SPI-4, which is required for the enteric phase of pathogenesis (62), also has been related to HilA (2, 23, 61). Furthermore, HilA represses its own expression (23). In addition, HilA indirectly regulates expression of secreted proteins by activating the transcription of the SPI-1 invF gene, encoding an AraC family transcriptional regulator (19).In this work, data on in vivo HilA binding, obtained through genome-wide location analysis (GWLA) or chromatin immunoprecipitation microarray (CHIP-chip) experiments (12), have been combined with transcriptional profiling of an hilA mutant versus a wild-type strain and in silico motif detection to provide a delineation of the direct HilA regulon, i.e., all genes directly bound by HilA, on a genome-wide scale. Retrieval of most of the known direct HilA target genes validated this approach. Moreover, a number of new targets were identified. Based on these findings, an extension of the ...

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Section: Discussionmentioning

confidence: 99%

Delineation of the Salmonella enterica Serovar Typhimurium HilA Regulon through Genome-Wide Location and Transcript Analysis

et al. 2007

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“…SPI-1 regulatory gene hilA and sipB (SPI-1 effector gene) mutants have been shown to be attenuated in invasion relative to the wild-type strain in porcine intestinal epithelioid (IPI-21) cells. However, the use of polarized porcine intestinal epithelial cells (IPEC-J2) has revealed that, in addition to hilA and sipB mutant strains, a sipA (SPI-1 effector gene) mutant strain was also recovered at a significantly lower rate than the wild-type strain (4), suggesting that SPI-1 is important for efficient invasion. In another study, it was dem-onstrated that the S. Typhimurium SPI-1 effectors SipA, SopA, SopB, SopD, and SopE2 all contributed to invasion of polarized human colon carcinoma cells (T84).…”

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confidence: 99%

Salmonella enterica Serovar Enteritidis Pathogenicity Island 1 Is Not Essential for but Facilitates Rapid Systemic Spread in Chickens

et al. 2009

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Salmonella enterica subsp. enterica serovar Enteritidis is a leading cause of human food-borne illness that is mainly associated with the consumption of contaminated poultry meat and eggs. To cause infection, S. Enteritidis is known to use two type III secretion systems, which are encoded on two salmonella pathogenicity islands, SPI-1 and SPI-2, the first of which is thought to play a major role in invasion and bacterial uptake. In order to study the role of SPI-1 in the colonization of chicken, we constructed deletion mutants affecting the complete SPI-1 region (40 kb) and the invG gene. Both ⌬SPI-1 and ⌬invG mutant strains were impaired in the secretion of SipD, a SPI-1 effector protein. In vitro analysis using polarized human intestinal epithelial cells (Caco-2) revealed that both mutant strains were less invasive than the wild-type strain. A similar observation was made when chicken cecal and small intestinal explants were coinfected with the wild-type and ⌬SPI-1 mutant strains. Oral challenge of 1-week-old chicken with the wild-type or ⌬SPI-1 strains demonstrated that there was no difference in chicken cecal colonization. However, systemic infection of the liver and spleen was delayed in birds that were challenged with the ⌬SPI-1 strain. These data demonstrate that SPI-1 facilitates systemic infection but is not essential for invasion and systemic spread of the organism in chickens.

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“…The first steps of infection are adhesion on the surface, firm attachment, and penetration into intestinal epithelial cells. The invasion of intestinal epithelial cells is believed to be a very important step related to the virulence of Salmonella strains associated with infections (5).…”

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confidence: 99%

“…Following initial adhesion to phagocytes, special bacterial cell surface structures recognize receptors on the target cell surface (17,33). The virulence genes of S. enterica serovar Typhimurium located on SPI-1, which encode a type III protein export machinery, are necessary for invasion of either nonphagocytic (5) or phagocytic (28) cells. Salmonella is able to induce cell death in macrophages in two different ways (32).…”

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confidence: 99%

Interaction between Host Cells and Septicemic Salmonella enterica Serovar Typhimurium Isolates from Pigs

et al. 2009

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Salmonella enterica serovar Typhimurium is an important pathogen in swine and is also a frequently reported zoonotic agent. The objective of this study was to characterize isolates of S. enterica serovar Typhimurium associated with septicemia in swine and to compare them to isolates recovered from clinically healthy pigs. We were particularly interested in comparing the two groups of isolates for their ability to adhere to and invade host cells, to be phagocytized and survive in monocyte cells, to induce apoptosis, and to adhere to intestinal mucus. Their surface properties were also evaluated by interactions with solvents. The isolates recovered from diseased animals were shown to invade intestinal epithelial cell lines at a higher rate (P ‫؍‬ 0.003) than isolates from healthy pigs. Septicemic isolates were phagocytized by human monocytes at a higher rate than isolates from healthy pigs (P ‫؍‬ 0.009). The mean percentages of phagocytosis were significantly lower for human monocytes than for porcine monocytes (P ‫؍‬ 0.02 and P ‫؍‬ 0.008, respectively) for isolates from both diseased and healthy animals. Healthy animal isolates were phagocytized more by porcine monocytes at 15 min (P ‫؍‬ 0.02) than septicemic isolates. No difference between isolates from septicemic pigs and isolates from healthy pigs was detected for other tested parameters. These results suggest that septicemic isolates have a particular pattern of invasion.

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Salmonella Typhimurium SPI-1 genes promote intestinal but not tonsillar colonization in pigs

Cited by 54 publications

References 33 publications

Delineation of the Salmonella enterica Serovar Typhimurium HilA Regulon through Genome-Wide Location and Transcript Analysis

Delineation of the Salmonella enterica Serovar Typhimurium HilA Regulon through Genome-Wide Location and Transcript Analysis

Salmonella enterica Serovar Enteritidis Pathogenicity Island 1 Is Not Essential for but Facilitates Rapid Systemic Spread in Chickens

Interaction between Host Cells and Septicemic Salmonella enterica Serovar Typhimurium Isolates from Pigs

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