A Salmonella fim homologue in Citrobacter freundii mediates invasion in vitro and crossing of the blood-brain barrier in the rat pup model

Petra Hess, Artur Altenhöfer, A. Salam Khan, Neda Daryab, Kwang Sik Kim, Jörg Hacker, Tobias A. Oelschlaeger

Research output: Contribution to journalArticle

Abstract

From the invasive Citrobacter freundii strain 3009, an invasion determinant was cloned, sequenced, and expressed. Sequence analysis of the determinant showed high homology with the fim determinant from Salmonella enterica serovar Typhimurium. The genes of the invasion determinant directed invasion of recombinant Escherichia coli K-12 strains into human epithelial cell lines of the bladder and gut as well as mannose-sensitive yeast agglutination and were termed fimCf genes. Expression of the FimCf proteins was shown by 35S labeling and/or Western blotting. In the infant rat model of experimental hematogenous meningitis, C. freundii strain 3009 and the in vitro invasive recombinant E. coli K-12 strain harboring the fim Cf, determinant reached the cerebrospinal fluid, in contrast to the case for the control strain. The fim determinant was also necessary for efficient in vitro invasion by C. freundii, because a deletion mutant was strongly reduced in its invasion efficiency. The mutation could be complemented in trans by the corresponding genes. Invasion by C. freundii could be blocked only by D-mannose, GlcNAc, and chitin hydrolysate and not by other carbohydrates tested. In contrast, yeast agglutination was not affected by GlcNAc or chitin hydrolysate. This finding indicated mannose residues to be essential for both yeast agglutination and invasion, whereas GlcNAc (oligomer) residues of host cells are involved exclusively in invasion. These results showed the fim determinant of C. freundii to be responsible for D-mannose- and GlcNAc-dependent in vitro invasion without being assembled into pili and for crossing of the blood-brain barrier in the infant rat model.

Original languageEnglish (US)
Pages (from-to)5298-5307
Number of pages10
JournalInfection and Immunity
Volume72
Issue number9
DOIs
StatePublished - Sep 2004

Fingerprint

Citrobacter freundii
Blood-Brain Barrier
Salmonella
Mannose
Agglutination
Chitin
Yeasts
Escherichia coli
Genes
Salmonella enterica
Meningitis
Sequence Analysis
Cerebrospinal Fluid
Urinary Bladder
Theoretical Models
Western Blotting
Epithelial Cells
Carbohydrates
In Vitro Techniques
Cell Line

ASJC Scopus subject areas

  • Immunology

Cite this

A Salmonella fim homologue in Citrobacter freundii mediates invasion in vitro and crossing of the blood-brain barrier in the rat pup model. / Hess, Petra; Altenhöfer, Artur; Khan, A. Salam; Daryab, Neda; Kim, Kwang Sik; Hacker, Jörg; Oelschlaeger, Tobias A.

In: Infection and Immunity, Vol. 72, No. 9, 09.2004, p. 5298-5307.

Research output: Contribution to journalArticle

Hess, Petra ; Altenhöfer, Artur ; Khan, A. Salam ; Daryab, Neda ; Kim, Kwang Sik ; Hacker, Jörg ; Oelschlaeger, Tobias A. / A Salmonella fim homologue in Citrobacter freundii mediates invasion in vitro and crossing of the blood-brain barrier in the rat pup model. In: Infection and Immunity. 2004 ; Vol. 72, No. 9. pp. 5298-5307.
@article{bcaf20dac399412498c2cdc23447b5ea,
title = "A Salmonella fim homologue in Citrobacter freundii mediates invasion in vitro and crossing of the blood-brain barrier in the rat pup model",
abstract = "From the invasive Citrobacter freundii strain 3009, an invasion determinant was cloned, sequenced, and expressed. Sequence analysis of the determinant showed high homology with the fim determinant from Salmonella enterica serovar Typhimurium. The genes of the invasion determinant directed invasion of recombinant Escherichia coli K-12 strains into human epithelial cell lines of the bladder and gut as well as mannose-sensitive yeast agglutination and were termed fimCf genes. Expression of the FimCf proteins was shown by 35S labeling and/or Western blotting. In the infant rat model of experimental hematogenous meningitis, C. freundii strain 3009 and the in vitro invasive recombinant E. coli K-12 strain harboring the fim Cf, determinant reached the cerebrospinal fluid, in contrast to the case for the control strain. The fim determinant was also necessary for efficient in vitro invasion by C. freundii, because a deletion mutant was strongly reduced in its invasion efficiency. The mutation could be complemented in trans by the corresponding genes. Invasion by C. freundii could be blocked only by D-mannose, GlcNAc, and chitin hydrolysate and not by other carbohydrates tested. In contrast, yeast agglutination was not affected by GlcNAc or chitin hydrolysate. This finding indicated mannose residues to be essential for both yeast agglutination and invasion, whereas GlcNAc (oligomer) residues of host cells are involved exclusively in invasion. These results showed the fim determinant of C. freundii to be responsible for D-mannose- and GlcNAc-dependent in vitro invasion without being assembled into pili and for crossing of the blood-brain barrier in the infant rat model.",
author = "Petra Hess and Artur Altenh{\"o}fer and Khan, {A. Salam} and Neda Daryab and Kim, {Kwang Sik} and J{\"o}rg Hacker and Oelschlaeger, {Tobias A.}",
year = "2004",
month = "9",
doi = "10.1128/IAI.72.9.5298-5307.2004",
language = "English (US)",
volume = "72",
pages = "5298--5307",
journal = "Infection and Immunity",
issn = "0019-9567",
publisher = "American Society for Microbiology",
number = "9",

}

TY - JOUR

T1 - A Salmonella fim homologue in Citrobacter freundii mediates invasion in vitro and crossing of the blood-brain barrier in the rat pup model

AU - Hess, Petra

AU - Altenhöfer, Artur

AU - Khan, A. Salam

AU - Daryab, Neda

AU - Kim, Kwang Sik

AU - Hacker, Jörg

AU - Oelschlaeger, Tobias A.

PY - 2004/9

Y1 - 2004/9

N2 - From the invasive Citrobacter freundii strain 3009, an invasion determinant was cloned, sequenced, and expressed. Sequence analysis of the determinant showed high homology with the fim determinant from Salmonella enterica serovar Typhimurium. The genes of the invasion determinant directed invasion of recombinant Escherichia coli K-12 strains into human epithelial cell lines of the bladder and gut as well as mannose-sensitive yeast agglutination and were termed fimCf genes. Expression of the FimCf proteins was shown by 35S labeling and/or Western blotting. In the infant rat model of experimental hematogenous meningitis, C. freundii strain 3009 and the in vitro invasive recombinant E. coli K-12 strain harboring the fim Cf, determinant reached the cerebrospinal fluid, in contrast to the case for the control strain. The fim determinant was also necessary for efficient in vitro invasion by C. freundii, because a deletion mutant was strongly reduced in its invasion efficiency. The mutation could be complemented in trans by the corresponding genes. Invasion by C. freundii could be blocked only by D-mannose, GlcNAc, and chitin hydrolysate and not by other carbohydrates tested. In contrast, yeast agglutination was not affected by GlcNAc or chitin hydrolysate. This finding indicated mannose residues to be essential for both yeast agglutination and invasion, whereas GlcNAc (oligomer) residues of host cells are involved exclusively in invasion. These results showed the fim determinant of C. freundii to be responsible for D-mannose- and GlcNAc-dependent in vitro invasion without being assembled into pili and for crossing of the blood-brain barrier in the infant rat model.

AB - From the invasive Citrobacter freundii strain 3009, an invasion determinant was cloned, sequenced, and expressed. Sequence analysis of the determinant showed high homology with the fim determinant from Salmonella enterica serovar Typhimurium. The genes of the invasion determinant directed invasion of recombinant Escherichia coli K-12 strains into human epithelial cell lines of the bladder and gut as well as mannose-sensitive yeast agglutination and were termed fimCf genes. Expression of the FimCf proteins was shown by 35S labeling and/or Western blotting. In the infant rat model of experimental hematogenous meningitis, C. freundii strain 3009 and the in vitro invasive recombinant E. coli K-12 strain harboring the fim Cf, determinant reached the cerebrospinal fluid, in contrast to the case for the control strain. The fim determinant was also necessary for efficient in vitro invasion by C. freundii, because a deletion mutant was strongly reduced in its invasion efficiency. The mutation could be complemented in trans by the corresponding genes. Invasion by C. freundii could be blocked only by D-mannose, GlcNAc, and chitin hydrolysate and not by other carbohydrates tested. In contrast, yeast agglutination was not affected by GlcNAc or chitin hydrolysate. This finding indicated mannose residues to be essential for both yeast agglutination and invasion, whereas GlcNAc (oligomer) residues of host cells are involved exclusively in invasion. These results showed the fim determinant of C. freundii to be responsible for D-mannose- and GlcNAc-dependent in vitro invasion without being assembled into pili and for crossing of the blood-brain barrier in the infant rat model.

UR - http://www.scopus.com/inward/record.url?scp=4544341264&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=4544341264&partnerID=8YFLogxK

U2 - 10.1128/IAI.72.9.5298-5307.2004

DO - 10.1128/IAI.72.9.5298-5307.2004

M3 - Article

C2 - 15322026

AN - SCOPUS:4544341264

VL - 72

SP - 5298

EP - 5307

JO - Infection and Immunity

JF - Infection and Immunity

SN - 0019-9567

IS - 9

ER -