Formation of a Novel Surface Structure Encoded by Salmonella Pathogenicity Island 2

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2005 May 13

PMID 15889142

Citations 52

Authors

Dipshikha Chakravortty

Manfred Rohde

Lorenz Jager

Jorg Deiwick

Michael Hensel

Affiliations

Soon will be listed here.

Abstract

The type III secretion system (T3SS) encoded by Salmonella Pathogenicity Island 2 (SPI2) is essential for virulence and intracellular proliferation of Salmonella enterica. We have previously identified SPI2-encoded proteins that are secreted and function as a translocon for the injection of effector proteins. Here, we describe the formation of a novel SPI2-dependent appendage structure in vitro as well as on the surface of bacteria that reside inside a vacuole of infected host cells. In contrast to the T3SS of other pathogens, the translocon encoded by SPI2 is only present singly or in few copies at one pole of the bacterial cell. Under in vitro conditions, appendages are composed of a filamentous needle-like structure with a diameter of 10 nm that was sheathed with secreted protein. The formation of the appendage in vitro is dependent on acidic media conditions. We analyzed SPI2-encoded appendages in infected cells and observed that acidic vacuolar pH was not required for induction of SPI2 gene expression, but was essential for the assembly of these structures and their function as translocon for delivery of effector proteins.

Citing Articles

Morphogenetic penicillin-binding proteins control virulence-associated type III secretion systems in .

Castanheira S, Torronteras S, Cestero J, Garcia-Del Portillo F Infect Immun. 2025; 93(2):e0055524.

PMID: 39745378 PMC: 11834469. DOI: 10.1128/iai.00555-24.

Salmonella Typhimurium effector SseI regulates host peroxisomal dynamics to acquire lysosomal cholesterol.

Raj D, Nair A, Singh A, Basu S, Sarkar K, Sharma J EMBO Rep. 2024; 26(3):656-689.

PMID: 39695325 PMC: 11811301. DOI: 10.1038/s44319-024-00328-x.

Infection biology of .

Han J, Aljahdali N, Zhao S, Tang H, Harbottle H, Hoffmann M EcoSal Plus. 2024; 12(1):eesp00012023.

PMID: 38415623 PMC: 11636313. DOI: 10.1128/ecosalplus.esp-0001-2023.

Enteritidis activates inflammatory storm SPI-1 and SPI-2 to promote intracellular proliferation and bacterial virulence.

Xiong D, Song L, Chen Y, Jiao X, Pan Z Front Cell Infect Microbiol. 2023; 13:1158888.

PMID: 37325511 PMC: 10266283. DOI: 10.3389/fcimb.2023.1158888.

Bacterial effector kinases and strategies to identify their target host substrates.

St Louis B, Quagliato S, Lee P Front Microbiol. 2023; 14:1113021.

PMID: 36846793 PMC: 9950578. DOI: 10.3389/fmicb.2023.1113021.

References

Sekiya K, Ohishi M, Ogino T, Tamano K, Sasakawa C, Abe A . Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci U S A. 2001; 98(20):11638-43. PMC: 58782. DOI: 10.1073/pnas.191378598. View

Rappl C, Deiwick J, Hensel M . Acidic pH is required for the functional assembly of the type III secretion system encoded by Salmonella pathogenicity island 2. FEMS Microbiol Lett. 2003; 226(2):363-72. DOI: 10.1016/S0378-1097(03)00638-4. View

Wilson R, SHAW R, Daniell S, Knutton S, Frankel G . Role of EscF, a putative needle complex protein, in the type III protein translocation system of enteropathogenic Escherichia coli. Cell Microbiol. 2001; 3(11):753-62. DOI: 10.1046/j.1462-5822.2001.00159.x. View

Daniell S, Takahashi N, Wilson R, Friedberg D, Rosenshine I, Booy F . The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell Microbiol. 2001; 3(12):865-71. DOI: 10.1046/j.1462-5822.2001.00168.x. View

Jin Q, He S . Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science. 2001; 294(5551):2556-8. DOI: 10.1126/science.1066397. View

Miao E, Freeman J, Miller S . Transcription of the SsrAB regulon is repressed by alkaline pH and is independent of PhoPQ and magnesium concentration. J Bacteriol. 2002; 184(5):1493-7. PMC: 134869. DOI: 10.1128/JB.184.5.1493-1497.2002. View

Jantsch J, Cheminay C, Chakravortty D, Lindig T, Hein J, Hensel M . Intracellular activities of Salmonella enterica in murine dendritic cells. Cell Microbiol. 2003; 5(12):933-45. DOI: 10.1046/j.1462-5822.2003.00334.x. View

Rosqvist R, Magnusson K, Wolf-Watz H . Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 1994; 13(4):964-72. PMC: 394898. DOI: 10.1002/j.1460-2075.1994.tb06341.x. View

Tapper H, Sundler R . Bafilomycin A1 inhibits lysosomal, phagosomal, and plasma membrane H(+)-ATPase and induces lysosomal enzyme secretion in macrophages. J Cell Physiol. 1995; 163(1):137-44. DOI: 10.1002/jcp.1041630116. View

10.

Baumler A, Heffron F . Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium. J Bacteriol. 1995; 177(8):2087-97. PMC: 176853. DOI: 10.1128/jb.177.8.2087-2097.1995. View

11.

Shea J, Hensel M, Gleeson C, Holden D . Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci U S A. 1996; 93(6):2593-7. PMC: 39842. DOI: 10.1073/pnas.93.6.2593. View

12.

Rathman M, Sjaastad M, Falkow S . Acidification of phagosomes containing Salmonella typhimurium in murine macrophages. Infect Immun. 1996; 64(7):2765-73. PMC: 174137. DOI: 10.1128/iai.64.7.2765-2773.1996. View

13.

Knutton S, Rosenshine I, Pallen M, Nisan I, Neves B, Bain C . A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 1998; 17(8):2166-76. PMC: 1170561. DOI: 10.1093/emboj/17.8.2166. View

14.

Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, Sukhan A . Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science. 1998; 280(5363):602-5. DOI: 10.1126/science.280.5363.602. View

15.

Hueck C . Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 1998; 62(2):379-433. PMC: 98920. DOI: 10.1128/MMBR.62.2.379-433.1998. View

16.

Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y . Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct. 1998; 23(1):33-42. DOI: 10.1247/csf.23.33. View

17.

Hensel M, Shea J, Waterman S, MUNDY R, Nikolaus T, Banks G . Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol. 1998; 30(1):163-74. DOI: 10.1046/j.1365-2958.1998.01047.x. View

18.

Cirillo D, Valdivia R, Monack D, Falkow S . Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol. 1998; 30(1):175-88. DOI: 10.1046/j.1365-2958.1998.01048.x. View

19.

Medina E, Paglia P, Nikolaus T, Muller A, Hensel M, Guzman C . Pathogenicity island 2 mutants of Salmonella typhimurium are efficient carriers for heterologous antigens and enable modulation of immune responses. Infect Immun. 1999; 67(3):1093-9. PMC: 96434. DOI: 10.1128/IAI.67.3.1093-1099.1999. View

20.

Deiwick J, Nikolaus T, Erdogan S, Hensel M . Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol. 1999; 31(6):1759-73. DOI: 10.1046/j.1365-2958.1999.01312.x. View