Salmonella enterica serovar Enteritidis has emerged during the last 20 years as the major causative agent of food-borne gastroenteritis in humans and as the major infectious agent on poultry farms, replacing Salmonella enterica serovar Typhimurium as the dominant pathogenic serovar. Because adhesion to gut tissues and colonization of the alimentary tract, mediated in large part by the FimH adhesins located on type 1 fimbriae, is an important stage in the pathogenesis of both serovars, the binding properties of the FimH adhesins from these two enteropathogens were compared. Salmonella Enteritidis FimH protein and the Salmonella Typhimurium low-adhesive variant of this adhesin were expressed in Escherichia coli and the recombinant proteins were analysed for their ability to bind glycoproteins carrying different oligomannosidic structures and different types of eukaryotic cells. In static binding assays (ELISA and Western blotting) both FimH proteins bound equally well to all three tested glycoproteins (RNase B, horseradish peroxidase and mannan-BSA). In addition, no differences were found in the binding specificity of the FimH proteins and intact cells of Salmonella Enteritidis and Salmonella Typhimurium to human colon carcinoma or bladder cancer cells. The presence of the same amino acid residues at positions 61 (glycine) and 118 (phenylalanine) and the similar binding properties of these two adhesins suggest that the newly described FimH protein of Salmonella Enteritidis represents the low-adhesive variant found in Salmonella Typhimurium. To study the binding specificity of Salmonella Enteritidis FimH protein further, direct kinetic analysis using surface plasmon resonance was performed. With this method it was found that Salmonella Enteritidis FimH adhesin bound with the highest Kd value to high-mannose type N-glycans carried by RNase B; about 100 times lower Kd values were obtained in the interactions with mannan-BSA and horseradish peroxidase.
AbrahamS. N.,
SunD.,
DaleJ. B.,
BeacheyE. H.
1988; Conservation of the d-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae. Nature 336:682–684[CrossRef]
Allen-VercoeE.,
WoodwardM. J.
1999; The role of flagella, but not fimbriae, in the adherence of Salmonella enterica serotype Enteritidis to chick gut explants. J Med Microbiol 48:771–780[CrossRef]
Allen-VercoeE.,
SayersA. R.,
WoodwardM. J.
1999; Virulence of Salmonella enterica serotype Enteritidis aflagellate and afimbriate mutants in a day-old chick model. Epidemiol Infect 122:395–402[CrossRef]
BarrowP. A.
1998; Virulence of Salmonella enterica serovar Enteritidis. In Salmonella Enterica Serovar Enteritidis in Humans and Animals: Epidemiology, Pathogenesis and Control pp 173–182 Edited by
SaeedA. M.,
GastR. K.,
PotterM.,
WallP. G.
Ames: Iowa State University Press;
BoddickerJ. D.,
LedeboerN. A.,
JagnowJ.,
JonesB. D.,
CleggS.
2002; Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol Microbiol 45:1255–1265[CrossRef]
ChristensenB.,
KielerJ.,
VilienM.,
DonP.,
WangC. Y.,
WolfH.
1984; A classification of human urothelial cells propagated in vitro. Anticancer Res 4:319–338
ClouthierS. C.,
DoranJ. L.,
CollinsonS. K.,
KayW. W,
MüllerK.-H.1993; Characterization of three fimbrial genes, sef ABC, of Salmonella enteritidis
. J Bacteriol 175:2523–2533
De BuckJ.,
Van ImmerseelF.,
MeulemansG.,
HaesebrouckF.,
DucatelleR.
2003; Adhesion of Salmonella enterica serotype Enteritidis isolates to chicken isthmal glandular secretions. Vet Microbiol 93:223–233[CrossRef]
Dibb-FullerM. P.,
WoodwardM. J.
2000; Contribution of fimbriae and flagella of Salmonella enteritidis to colonization and invasion of chicks. Avian Pathol 29:295–304[CrossRef]
Dibb-FullerM. P.,
Allen-VercoeE.,
ThornsC. J.,
WoodwardM. J.
1999; Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis
. Microbiology 145:1023–1031[CrossRef]
DukM.,
LisowskaE.,
WuJ. H.,
WuA. M.
1994; The biotin/avidin-mediated microtiter plate lectin assay with the use of chemically modified glycoprotein ligand. Anal Biochem 221:266–272[CrossRef]
EwenS. W.,
NaughtonP. J.,
GrantG.,
SojkaM.,
Allen-VercoeE.,
BardoczS.,
ThornsC. J.,
PusztaiA.
1997; Salmonella enterica var Typhimurium and Salmonella enterica var Enteritidis express type 1 fimbriae in the rat in vivo. FEMS Immunol Med Microbiol 18:185–192[CrossRef]
FironN.,
OfekI.,
SharonN.
1983; Carbohydrate specificity of the surface lectins of Escherichia coli , Klebsiella pneumoniae and Salmonella typhimurium
. Carbohydr Res 120:235–249[CrossRef]
FuD.,
ChenL.,
O'NeillR. A.
1994; A detailed structural characterization of ribonuclease B oligosaccharides by 1H NMR spectroscopy and mass spectrometry. Carbohydr Res 261:173–186[CrossRef]
HancoxL. S.,
Kuang-ShengY.,
CleggS.
1998; Construction and characterization of type 1 non-fimbriate and non-adhesive mutants of Salmonella typhimurium
. FEMS Immunol Med Microbiol 19:289–296
HumphriesA. D.,
RaffatelluM.,
WinterS.10 other authors2003; The use of flow cytometry to detect expression of subunits encoded by 11 Salmonella enterica serotype Typhimurium fimbrial operons. Mol Microbiol 48:1357–1376[CrossRef]
KimmichG. A.
1970; Preparation and properties of mucosal epithelial cells isolated from small intestine of the chicken. Biochemistry 9:3659–3668[CrossRef]
KisielaD.,
KiczakL.,
KuzminskaM.,
KuczkowskiM.,
FraniczekR.,
UgorskiM.
2005a; Analysis of the fimH gene coding type 1 fimbriae adhesin of Salmonella enterica serovar Enteritidis. Med Wet 61:1259–1262
KisielaD.,
SapetaA. M.,
KuczkowskiM.,
StefaniakT.,
WieliczkoA.,
UgorskiM.
2005b; Characterization of FimH adhesins expressed by Salmonella enterica serovar Gallinarum biovars Gallinarum and Pullorum: reconstitution of mannose-binding properties by single amino acid substitution. Infect Immun 73:6187–6190[CrossRef]
KrogfeltK. A.,
BergmansH.,
KlemmP.
1990; Direct evidence that the FimH protein is the adhesin of Escherichia coli type 1 fimbriae. Infect Immun 58:1995–1999
KurosakaA.,
YanoA.,
NobuyukiI.,
KurodaY.,
NakagawaT.,
KawasakiT.
1991; The structure of a neural specific carbohydrate epitope of horseradish peroxidase recognized by anti-horseradish peroxidase antiserum. J Biol Chem 266:4168–4172
OldD. C.
1972; Inhibition of interaction between fimbrial haemagglutinins and erythrocytes by d-mannose and other carbohydrates. J Gen Microbiol 71:149–157[CrossRef]
NaughtonP. J.,
GrantG.,
BardoczS.,
Allen-VercoeE.,
WoodwardM. J.,
PusztaiA.
2001; Expression of type 1 fimbriae (SEF 21) of Salmonella enterica serotype enteritidis in the early colonisation of the rat intestine. J Med Microbiol 50:191–197
RajashekaraG.,
MunirS.,
AlexeyevM. F.,
HalvorsonD. A.,
WellsC. L.,
NagarajaK. V.
2000; Pathogenic role of SEF14, SEF17, and SEF21 fimbriae in Salmonella enterica serovar Enteritidis infection of chickens. Appl Environ Microbiol 66:1759–1763[CrossRef]
RaschkeW. C.,
BallouC. E.
1972; Characterization of a yeast mannan containing N -acetyl-d-glucosamine as an immunochemical determinant. Biochemistry 11:3807–3816[CrossRef]
SohelI.,
PuenteJ. L.,
MurrayW. J.,
Vuopio-VarkilaJ.,
SchoolnikG. K.
1993; Cloning and characterization of the bundle-forming pilin gene of enteropathogenic Escherichia coli and its distribution in Salmonella serotypes. Mol Microbiol 7:563–575[CrossRef]
SokurenkoE. V.,
CourtneyH. S.,
OhmanD. E.,
KlemmP.,
HastyD. L.
1994; FimH family of type 1 fimbrial adhesins: functional heterogeneity due to minor sequence variations among fimH genes. J Bacteriol 176:748–755
SokurenkoE. V.,
CourtneyH. S.,
MaslowJ.,
SiitonenA.,
HastyD. L.
1995; Quantitative differences in adhesiveness of type 1 fimbriated Escherichia coli due to structural differences in fimH genes. J Bacteriol 177:3680–3686
WoodwardM. J.,
Allen-VercoeE.,
RedstoneJ. S.
1996; Distribution, gene sequence and expression in vivo of the plasmid encoded fimbrial antigen of Salmonella serotype Enteritidis. Epidemiol Infect 117:17–28[CrossRef]