Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium

Ginocchio, Christine C.; Olmsted, Stephen B.; Wells, Carol L.; Galán, Jorge E.

doi:10.1016/0092-8674(94)90510-x

Cited by 249 publications

(218 citation statements)

References 39 publications

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“…Both Salmonella typhimurium and Shigella flexneri are enteroinvasive pathogens. S. typhimurium transiently produces filamentous surface appendages of 60 nm in diameter upon contact with epithelial cells during its invasion of host cells (52). The structural components of these appendages have not been identified.…”

Section: Discussionmentioning

confidence: 99%

Hrp pilus: An hrp -dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000

Roine

Wei

Yuan

et al. 1997

Proc. Natl. Acad. Sci. U.S.A.

323

279

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Hypersensitive response and pathogenicity (hrp) genes control the ability of major groups of plant pathogenic bacteria to elicit the hypersensitive response (HR) in resistant plants and to cause disease in susceptible plants. A number of Hrp proteins share significant similarities with components of the type III secretion apparatus and f lagellar assembly apparatus in animal pathogenic bacteria. Here we report that Pseudomonas syringae pv. tomato strain DC3000 (race 0) produces a filamentous surface appendage (Hrp pilus) of 6-8 nm in diameter in a solid minimal medium that induces hrp genes. Formation of the Hrp pilus is dependent on at least two hrp genes, hrpS and hrpH (recently renamed hrcC), which are involved in gene regulation and protein secretion, respectively. Our finding of the Hrp pilus, together with recent reports of Salmonella typhimurium surface appendages that are involved in bacterial invasion into the animal cell and of the Agrobacterium tumefaciens virB-dependent pilus that is involved in the transfer of T-DNA into plant cells, suggests that surface appendage formation is a common feature of animal and plant pathogenic bacteria in the infection of eukaryotic cells. Furthermore, we have identified HrpA as a major structural protein of the Hrp pilus. Finally, we show that a nonpolar hrpA mutant of P. syringae pv. tomato DC3000 is unable to form the Hrp pilus or to cause either an HR or disease in plants.Major groups of Gram-negative plant pathogenic bacteria belonging to genera Erwinia, Pseudomonas, Ralstonia, and Xanthomonas contain hypersensitive reaction and pathogenicity (hrp) genes. These genes control the ability of these bacteria to initiate interactions with plants, including elicitation of the hypersensitive reaction (HR), characterized by rapid localized death of plant cells at the pathogen infection site in resistant plants and causation of disease in susceptible plants (1, 2).hrp genes of Pseudomonas syringae are expressed in planta as a result of a regulatory cascade involving the gene products of hrpS and hrpR, positive transcriptional regulators, and of hrpL, an alternative sigma factor (3, 4). HrpL recognizes a consensus sequence motif (''harp box'') that has been identified in the upstream regions of many hrp and avr genes (4). The expression of hrp genes of many P. syringae pathovars can also be induced in vitro when bacteria are grown in defined minimal medium with low pH and containing certain sugars or sugar alcohols as carbon sources (5-7).The 25-kb hrp͞hrmA gene cluster of Pseudomonas syringae pv. syringae strain 61 is sufficient to enable nonpathogenic strains of Pseudomonas fluorescens and Escherichia coli to elicit the HR in nonhost plants (8). Sixteen of the 25 genes in this completely sequenced hrp͞hrmA gene cluster are either predicted or shown to be required for secretion of harpin Pss , a proteinaceous elicitor of the HR encoded by hrpZ (9, 10). Nine of these hrp genes, recently renamed hrc genes (11), are broadly conserved among P. syringae pathovars, Erwi...

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Section: Discussionmentioning

confidence: 99%

Hrp pilus: An hrp -dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000

Roine

Wei

Yuan

et al. 1997

Proc. Natl. Acad. Sci. U.S.A.

323

279

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“…Washed and fixed cells were treated with 2% OsO 4 for further fixation, and were processed for electron microscopy as described by Ginocchio et al (1994). Visualization of samples was carried out in a Hitachi S800 scanning electron microscope.…”

Section: Electron Microscopymentioning

confidence: 99%

Role of bundle-forming pilus of enteropathogenicEscherichia coliin host cell adherence and in microcolony development

Tobe¹,

Sasakawa

2001

Cellular Microbiology

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SummaryEnteropathogenic Escherichia coli (EPEC) adheres to epithelial cells and forms microcolonies in localized areas. Bundle-forming pili (BFP) are necessary for autoaggregation and the formation of microcolonies. In this study, we show that BFP, expressed by EPEC on epithelial cells, disappeared with the expansion of the microcolony. Bacterial dispersal and the release of BFP from the EPEC aggregates were induced by contact with host cellular membrane extract. In addition, BFP-expressing EPEC adhered directly to cell surfaces, in preference to attaching to pre-formed microcolonies on the cells. These results suggested that BFP mediate the initial attachment of EPEC through direct interaction with the host cell rather than through the recruitment of unattached bacteria to microcolonies on the cell.

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“…In Salmonella typhimurium and enteropathogenic Escherichia coli, filamentous surface appendages have been identified that might be involved in the translocation process (12,13). In E. coli, the surface structures containing the protein EspA are required for translocation of the protein EspB (13).…”

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confidence: 99%

Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells

Hoiczyk

Blobel

2001

Proc. Natl. Acad. Sci. U.S.A.

165

171

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A number of pathogenic, Gram-negative bacteria are able to secrete specific proteins across three membranes: the inner and outer bacterial membrane and the eukaryotic plasma membrane. In the pathogen Yersinia enterocolitica, the primary structure of the secreted proteins as well as of the components of the secretion machinery, both plasmid-encoded, is known. However, the mechanism of protein translocation is largely unknown. Here we show that Y. enterocolitica polymerizes a 6-kDa protein of the secretion machinery into needles that are able to puncture the eukaryotic plasma membrane. These needles form a conduit for the transport of specific proteins from the bacterial to the eukaryotic cytoplasm, where they exert their cytotoxic activity. In negatively stained electron micrographs, the isolated needles were 60 -80 nm long and 6 -7 nm wide and contained a hollow center of about 2 nm. Our data indicate that it is the polymerization of the 6-kDa protein into these needles that provides the force to perforate the eukaryotic plasma membrane.electron microscopy ͉ bacterial pathogenicity ͉ cell contact assays ͉ protein translocation

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Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium

Cited by 249 publications

References 39 publications

Hrp pilus: An hrp -dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000

Hrp pilus: An hrp -dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000

Role of bundle-forming pilus of enteropathogenicEscherichia coliin host cell adherence and in microcolony development

Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells

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