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Infection and Immunity, May 1999, p. 2671-2676, Vol. 67, No. 5
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
The Cellular Form of Human Fibronectin as an
Adhesion Target for the S Fimbriae of Meningitis-Associated
Escherichia coli
Anne
Sarén,1
Ritva
Virkola,1,*
Jörg
Hacker,2 and
Timo K.
Korhonen1
Division of General Microbiology, Department
of Biosciences, FIN-00014 University of Helsinki,
Finland,1 and Institut für
Molekulare Infektionsbiologie, Universität Würzburg,
D-97070 Würzburg, Germany2
Received 5 October 1998/Returned for modification 25 November
1998/Accepted 10 February 1999
 |
ABSTRACT |
The adhesion of the S fimbriae of meningitis-associated
Escherichia coli O18ac:K1:H7 to the cellular and the plasma
forms of human fibronectin was studied. E. coli
HB101(pAZZ50) expressing the complete S-fimbria II gene cluster of
E. coli O18 adhered to cellular fibronectin (cFn) on glass
but not to plasma fibronectin (pFn). Adhesion to cFn was specifically
inhibited by neuraminidase treatment of cFn as well as by incubation of
the bacteria with sialyl-
2-3-lactose, a receptor analog of the S
fimbriae. No significant adhesion to cFn or pFn was detected with
E. coli HB101(pAZZ50-67) expressing S fimbriae lacking the
SfaS lectin subunit. Strain HB101(pAZZ50) also adhered to a human
fibroblast cell culture known to be rich in cFn, and the adhesion was
specifically inhibited in the presence of polyclonal antibodies to cFn.
The results show that the SfaS lectin of the S fimbriae mediates the
adherence of meningitis-associated E. coli to sialyl
oligosaccharide chains of cFn.
| |
TEXT |
The S fimbriae of Escherichia
coli recognize terminal sialyl-2-3-galactoside moieties of
glycoproteins (11) and are associated with serogroup
O18ac:K1:H7 E. coli as well as newborn meningitis (12). Genes encoding S-fimbrial adhesin (Sfa) complexes have been cloned and characterized from uropathogenic O6:K15:H31 E. coli 536 (the sfaI gene cluster) (4) and
meningitis-associated O18:K1:H7 E. coli IHE3034
(sfaII) (5). Nine chromosomal genes in the
sfa gene cluster are involved in the biogenesis and
structure of the S fimbriae. The major subunit, SfaA, forms the bulk of the fimbrial filament, with which three minor subunits (SfaG, SfaH, and
SfaS) are associated. SfaS is the sialic acid-binding adhesin and is
responsible for S-fimbrial binding to various human epithelial and
subepithelial tissue domains (33). In animal models of
newborn meningitis, it has been found that the S fimbriae are expressed
in vivo in blood and cerebrospinal fluid (21, 32) and that
they bind to epithelial cells lining the choroid plexuses and brain
ventricles and to subarachnoid endothelium (24). These
findings are in agreement with the observation that the choroid plexus
is the portal of entry into the cerebrospinal fluid by
meningitis-associated bacteria (16) and have suggested that
S fimbriae are involved in targeting E. coli O18:K1:H7 to the endothelium and epithelium in the mammalian choroid plexus (13).
Fibronectin is a high-molecular-mass (450- to 500-kDa) mammalian
glycoprotein found in a soluble form in plasma and other body fluids as
well as in an insoluble form in the interstitial connective tissues and
extracellular matrices (1, 19, 28, 31, 45). Fibronectin is a
dimer of two identical or very similar polypeptide chains that are
assembled into a series of continuous structural and functional domains
(28). Fibronectin is involved in many important functions of
cells and tissues, such as cell adhesion, spreading, and migration,
tissue development and differentiation, blood clot stabilization, and
wound healing (1, 31, 45). The functions of fibronectin
involve binding to a number of biological structures, e.g., eukaryotic
cell surface receptors (integrins), extracellular matrix components
(collagen and heparin), cytoskeletal components (actin), and plasma
proteins (fibrin) (31, 45).
Fibronectins can be divided into two major forms: plasma fibronectin
(pFn) and cellular fibronectin (cFn). pFn is produced by hepatocytes in
the liver and secreted in a soluble form into plasma (36).
cFn is produced locally in tissues by different cell types, such as
fibroblasts (6, 19) and endothelial cells (26).
cFn is mostly bound to the cell surface or deposited as an insoluble
multimer in the extracellular matrix (7, 19). Structural
differences between pFn and cFn in part result from different splicing
patterns of the fibronectin gene. cFn contains three extra domain
sequences: EDIIIA and EDIIIB, as well as a type III connecting strand
lacking pFn (28, 35). Fibronectins contain 4 to 9%
carbohydrate, mostly in N glycosidically linked complex oligosaccharide
chains (1, 28). cFn contains sialic acid linked to galactose
via an 2-3 linkage, whereas the 2-6 linkage is found in pFn
(1, 20, 28).
Various bacteria pathogenic for humans recognize pFn (reviewed in
references 25 and 43). Mutant
strains of Staphylococcus aureus and Streptococcus
sanguis with reduced fibronectin-binding activity have a decreased
ability to cause infective endocarditis in rats (15, 17),
suggesting that fibronectin binding is important for bacterial adhesion
and colonization at damaged heart valves. Selective binding of the
virulence-associated surface protein YadA of Yersinia
enterocolitica to cFn has been reported (34). YadA
exhibits multiple adhesive functions and promotes the invasiveness of
yersiniae for orally infected mice (30, 37), but the role of
cFn binding in bacterial spread has not been analyzed.
Several meningitis-associated bacteria have recently been found to bind
pFn; these bacteria include Haemophilus influenzae (40), Neisseria meningitidis (2), and
Streptococcus pneumoniae (38). The present study
was undertaken to determine whether meningitis-associated S-fimbriated
E. coli also expresses fibronectin binding.
Adhesion of S-fimbriated E. coli strains to immobilized
fibronectins.
We initially tested the adhesion of S-fimbriated
E. coli strains to human pFn and cFn. pFn was from normal
human plasma (Collaborative Biomedical Products, Bedford, Mass.), and
cFn was from human foreskin fibroblasts (Fibrinogenex, Chicago, Ill.).
Laminin, a major glycoprotein of basement membranes (18)
from Engelbreth-Holm-Swarm mouse tumors (Upstate Biotechnology Inc.,
Lake Placid, N.Y.) has been shown to be recognized by S fimbriae
(41) and was used as a positive control protein. Type IV
collagen from human placenta (Sigma Chemical Co., St. Louis, Mo.) and
bovine serum albumin (BSA; Sigma) were used as negative control
proteins (41). Matrix proteins were immobilized on glass
slides to obtain 2.5 pmol per well as described earlier
(44). Recombinant E. coli strains HB101(pAZZ50),
expressing the complete sfaII gene cluster from E. coli O18:K1:H7, and HB101(pAZZ50-67), expressing an
sfaS-deficient gene cluster (5), as well as the
nonfimbriated strain HB101(pBR322), with the vector plasmid alone, were
grown overnight at 37°C on Luria agar plates supplemented with
ampicillin. Before adhesion tests, the correct expression of the
fimbriae by the bacteria was confirmed by hemagglutination of human
blood group O erythrocytes, mannoside-sensitive yeast cell
agglutination (8), and bacterial agglutination in
S-fimbria-specific antiserum (41). Adhesion assays were
performed as detailed recently (40). The number of adherent
bacteria in 20 randomly chosen microscopic fields of 1.6 × 104 µm2 was determined by density slicing.
In accordance with our earlier findings (41), E. coli HB101(pAZZ50), with intact S-fimbrial filaments, strongly
adhered to laminin. The strain also adhered efficiently to cFn (Fig.
1), whereas adherence to pFn was poor and
equal to that seen with BSA. The difference in adhesiveness to cFn and
pFn was statistically significant (P, <0.001). No adhesion
to type IV collagen was detected. The sfaS mutant
strain HB101(pAZZ50-67) and the nonfimbriated strain
HB101(pBR322) exhibited only poor adhesiveness to the target proteins. These results suggested that the sialic acid-binding protein SfaS of the fimbrial filament is involved in adhesion.
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FIG. 1.
Adhesiveness of E. coli HB101(pAZZ50),
expressing the complete S-fimbria gene cluster, of HB101(pAZZ50-67),
with SfaS-defective fimbriae, and of HB101(pBR322), with the vector
plasmid alone, to target proteins immobilized on glass. The target
proteins were laminin, cFn, pFn, type IV collagen, and BSA. Means ± standard deviations of adherent bacteria in 20 microscopic fields of
1.6 × 104 µm2 are shown.
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Role of cFn carbohydrate in bacterial adhesion.
S fimbriae
recognize terminal sialyl-2-3-galactosides (11) present
in numerous mammalian glycoproteins (14). Human pFn and cFn
mainly carry biantennary oligosaccharide chains with terminal sialic
acids. cFn contains sialic acid linked to galactose via an 2-3
linkage, in contrast to the 2-6 linkage found in pFn (1).
To confirm the presence of terminal sialyl structures in the commercial
target proteins used in this study, we used a dot blot assay to assess
binding by digoxigenin-labeled Sambucus nigra agglutinin
(SNA) and Maackia amurensis agglutinin (MAA), included in a
glycan differentiation kit (Boehringer GmbH, Mannheim, Germany). SNA
recognizes terminal sialyl-2-6-galactosides, and MAA recognizes
sialyl-2-3-galactosides. Laminin, pFn, cFn, and type IV collagen
were immobilized on nitrocellulose membranes (Bio-Rad Laboratories,
Richmond, Calif.) at a concentration of 2 µg per dot. Lectin staining
was performed as described by Boehringer. SNA lectin reacted
strongly with pFn (Fig. 2A), whereas MAA
lectin bound to laminin and cFn (Fig. 2B), indicating the
presence of terminal sialyl-2-3-galactosides in these proteins.
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FIG. 2.
Reactivity of the sialyl-2-6-galactoside-binding SNA
lectin (A) and of the sialyl-2-3-galactoside-binding MAA lectin (B)
with laminin (Lam), pFn, cFn, and type IV collagen (CIV). The target
proteins were immobilized on a nitrocellulose membrane, and the binding
was visualized with digoxigenin-labeled lectins.
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|
To analyze the role of terminal sialyl-
2-3-galactosides in the
observed bacterial adhesion to cFn, we tested the effect of
neuraminidase treatment of cFn on bacterial adhesiveness. Immobilized
cFn and type IV collagen were incubated with neuraminidase (100
mU/ml
in Dulbecco's phosphate-buffered saline [PBS]; Boehringer)
at 37°C
for 3 h before bacteria (10
9 cells/ml) were added;
control wells were treated with buffer
alone. Neuraminidase treatment
significantly (
P, <0.001) decreased
bacterial adhesion to
cFn (Fig.
3A) but did not affect
low-level
adhesiveness to type IV collagen. We also tested the effect
of
sialyl-
2-3-lactose and lactose on the adhesiveness of
E. coli HB101(pAZZ50). Bacteria were incubated with 28.5 mM
sialyl-
2-3-lactose
(
10,
23) or lactose (Merck) for 30 min
over crushed ice and
then pipetted onto cFn- and type IV
collagen-coated glass slides.
Lactose had no significant
effect on adhesion to cFn, whereas
sialyl-
2-3-lactose
inhibited adhesion significantly (
P, <0.001)
to close to
the level seen with type IV collagen (Fig.
3B).
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FIG. 3.
Inhibition of the adherence of E. coli
HB101(pAZZ50) to cFn and type IV collagen (CIV) immobilized on glass.
(A) Bacterial adherence to neuraminidase-treated cFn and CIV; the
control bars show adherence to target proteins incubated in buffer
alone. (B) Effect of lactose and sialyl-2-3-lactose on adherence.
The carbohydrates were tested at a concentration of 28.5 mM. Means ± standard deviations of adherent bacteria in 20 microscopic fields of
1.6 × 104 µm2 are shown.
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Adhesion to human fibroblasts.
cFn is very efficiently
produced by human fibroblast cell lines in patches or long fibers along
cell surfaces and in intercellular spaces (7). We next
assessed whether S-fimbriated bacteria also recognize cFn present
on cell surfaces; this assessment was performed by double staining
(10) of the fibroblast culture with anti-cFn antibody and
bacterial cells. Human embryonic skin fibroblasts (6) were
grown to subconfluence on glass slides in MEM medium (Life Technologies
Gibco BRL, Paisley, Scotland) supplemented with 10% (wt/vol) fetal
calf serum (PAA Laboratories GmbH, Linz, Austria) and 2 mM
L-glutamine (Life Technologies Gibco BRL). E. coli clones HB101(pAZZ50) and HB101(pAZZ50-67) were labeled with fluorescein isothiocyanate (FITC; Sigma) as described
earlier (10). FITC-labeled bacteria (109
cells/ml in PBS) were pipetted onto glass slides and incubated at 4°C
for 2 h. After being washed, the cells were fixed with cold 3.5%
paraformaldehyde in PBS for 10 min and then were washed again with PBS.
For localization of cellular fibronectin, cells were stained with
monoclonal mouse anti-cFn antibodies specific for EDIIIA (diluted
1:100; Biohit, Helsinki, Finland) and tetramethyl rhodamine
isothiocyanate R (TRITC)-labeled secondary anti-mouse antibodies (diluted 1:50; Dako A/S, Glostrup, Denmark). The cells were
mounted with Nicethamid and examined in an Olympus standard fluorescence microscope (Olympus Optical Co., Hamburg, Germany).
FITC-labeled S-fimbriated HB101(pAZZ50) bacteria strongly adhered to
fibroblast cells (Fig.
4A to C), whereas
FITC-labeled
HB101(pAZZ50-67) bacteria, with
sfaS-deficient
type S fimbriae,
failed to adhere (Fig.
4D and E). HB101(pAZZ50) cells
were detected
at sites recognized by the anti-cFn monoclonal antibody
(Fig.
4A to C, arrows). However, bacterial cells were also detected
at
locations that were not stained by the anti-cFn antibody (Fig.
4A to C,
arrowheads). We estimated that 75% of the adherent HB101(pAZZ50)
cells colocalized with the anti-cFn antibody-binding sites on
fibroblasts. We also assessed the binding of purified S fimbriae
to
fibroblasts. Fimbriae from strain HB101(pAZZ50) were purified
by
use of deoxycholate and concentrated urea (
9). Fibroblasts
on glass slides were incubated with purified S fimbriae (950 µg/ml
in
28.5 mM lactose or in 28.5 mM sialyl-
2-3-lactose) at 4°C for
2 h. After being washed, the cells were fixed with 3.5%
paraformaldehyde
and then were washed again. To detect S-fimbrial
binding, cells
were incubated first with anti-S-fimbria antibodies
(diluted 1:50)
and then with FITC-labeled secondary antibodies (Dako
A/S) (diluted
1:50). S fimbriae bound to fibroblast cells, and the
binding was
specifically inhibited by sialyl-
2-3-lactose (Fig.
4F to
I).
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FIG. 4.
Binding of S-fimbriated E. coli and of S
fimbriae to human fibroblasts. (A) Adhesiveness of FITC-labeled
E. coli HB101(pAZZ50). (B) Same microscopic field as in
panel A double stained with the anti-cFn monoclonal antibody and
TRITC-labeled secondary antibodies. (C) Same field as in panel A
visualized by light microscopy. Arrows indicate bacterial adhesion to
cFn-containing sites, and arrowheads indicate adhesion to other cell
surface structures lacking cFn. (D) Adhesiveness of FITC-labeled
HB101(pAZZ50-67), devoid of the SfaS lectin. (E) Same field as in panel
D visualized by light microscopy. (F and H) Binding of purified S
fimbriae in the presence of 28.5 mM lactose (F) and in the presence of
28.5 mM sialyl-2-3-lactose (H). (G and I) Same fields as in panels F
and H, respectively, visualized by light microscopy. Bar, 10 µm.
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Terminal sialyl-
2-3-galactosides occur commonly in mammalian
glycoproteins (
14), and our observations above suggested
that
the fibroblast surface may express other receptor-active
glycoproteins
in addition to cFn. We analyzed the effect of antibodies
specific
for cFn on the adhesiveness of
E. coli
HB101(pAZZ50). Bacteria
(10
9 cells/ml) and antibodies,
polyclonal anti-collagen type IV immunoglobulin
G (IgG) (2 mg/ml) or
anti-cFn IgG, were pipetted onto fibroblast
cells and incubated as
described above. In the presence of polyclonal
anti-collagen type IV
IgG, bacterial adhesion was not significantly
decreased (Fig.
5, bars 1 and 2). In contrast, polyclonal
anti-cFn
IgG (Fig.
5, bars 1 and 3) decreased bacterial adhesion
significantly
(
P, <0.001) but did not completely abolish
it.
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FIG. 5.
Adherence of E. coli HB101(pAZZ50) to human
fibroblasts. Bar 1 shows bacterial adhesiveness (109
cells/ml) in PBS, bar 2 shows adhesiveness in the presence of
polyclonal IgG (2 mg/ml) against type IV collagen, and bar 3 shows
adhesiveness in the presence of polyclonal IgG (2 mg/ml) against cFn.
Bar 4 shows adherence of SfaS mutant HB101(pAZZ50-67). The adhesiveness
shown in bars 3 and 4 differed statistically significantly (P,
<0.001) from that shown in bar 1, whereas the adhesiveness shown
in bar 2 did not differ significantly from that shown in bar 1. Error
bars indicate standard deviations.
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|
Our results demonstrate that sialyl-
2-3-oligosaccharide chains of
cFn serve as adhesion targets for S-fimbriated
E. coli.
The
adhesion of S-fimbriated bacteria to cFn was inhibited by
sialyl-lactose as well as by the removal of terminal sialic acid
from
the cFn molecule. Furthermore, SfaS, the lectin protein of
the
S-fimbrial filament, was needed for cFn binding. On cultured
human
fibroblasts, which express cFn efficiently (
6), partial
overlap of the S-fimbria- and anti-cFn antibody-binding sites
was seen.
Furthermore, the anti-cFn antibody caused specific but
partial
inhibition of bacterial adhesion. The latter results are
compatible
with the common occurrence of sialyl-
2-3-oligosaccharides
in
mammalian glycoproteins and the hypothesis that the fibroblast
surface
expresses various glycoproteins recognized by S
fimbriae.
The common expression of fibronectin adhesiveness by
meningitis-associated or invasive bacterial species suggests that it
provides a pathogenic function for the bacteria. At present, we
can
only speculate on the role of cFn recognition in bacterial
meningitis.
In embryonic tissues, cFn is found in developing basement
membranes,
but in adult tissues, cFn is found mostly in vascular
endothelial cells
(
39). Both tissue types are strongly recognized
by S
fimbriae (
10,
13,
42). During tissue injury and repair,
the
distribution of fibronectin in the body changes. During vascular
injury, cFn is released and becomes widely distributed at inflamed
tissue sites. It accumulates at sites of injury and inflammation,
where
it appears to provide a provisional matrix for repair processes
(
27). cFn has been detected in tissues with local trauma,
such
as bacterial infection (
22,
29), tumor metastasis
(
39),
or wound healing and regeneration (
3).
Local production of
cFn may increase the colonization potential of
S-fimbriated
E. coli at sites of tissue trauma or
inflammation.
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ACKNOWLEDGMENTS |
This study was supported by the Academy of Finland (grants 29346 and 42103), the Sigrid Jusèlius Foundation, the University of
Helsinki, NorFA-Nordic Academy for Advanced Study, the Deutsche Forschungsgemeinschaft, and the Fonds der Chemischen Industrie.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Division of
General Microbiology, Department of Biosciences, P.O. Box 56, Viikinkaari 9, FIN-00014 University of Helsinki, Finland. Phone:
358-9-70859235. Fax: 358-9-70859262. E-mail:
ritva.virkola{at}helsinki.fi.
Editor:
P. E. Orndorff
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Infection and Immunity, May 1999, p. 2671-2676, Vol. 67, No. 5
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