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Infection and Immunity, April 1999, p. 2045-2049, Vol. 67, No. 4
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
1-Chain Integrins Are Not Essential
for Intimin-Mediated Host Cell Attachment and Enteropathogenic
Escherichia coli-Induced Actin Condensation
Hui
Liu,
Loranne
Magoun, and
John M.
Leong*
Department of Molecular Genetics and
Microbiology, University of Massachusetts Medical Center,
Worcester, Massachusetts 01655
Received 8 October 1998/Returned for modification 24 November
1998/Accepted 6 January 1999
 |
ABSTRACT |
Intimin is a bacterial outer membrane protein required for intimate
attachment of enterohemorrhagic and enteropathogenic Escherichia coli (EHEC and EPEC) to mammalian cells.
1-chain
integrins have been proposed as candidate receptors for intimin. We
found that binding of mammalian cells to immobilized intimin was not
detectable unless mammalian cells were preinfected with EPEC or EHEC.
1-chain integrin antagonists or inactivation of the gene
encoding the
1-chain did not affect binding of
preinfected mammalian cells to intimin or the actin condensation
associated with the attachment of EPEC. The results indicate that
1-chain integrins are not essential for intimin-mediated
cell attachment or EPEC-mediated actin polymerization.
 |
TEXT |
Several enteropathogenic bacteria,
such as enterohemorrhagic Escherichia coli (EHEC),
enteropathogenic E. coli (EPEC), and Citrobacter
rodentium, form a specific structure, termed an attaching and
effacing (A/E) lesion, on the surface of epithelial cells (6, 15,
18, 26). A/E lesions are thought to promote tight bacterial
adherence to intestinal epithelial cells, a critical step during
colonization (23, 24). Within these lesions, the actin
cytoskeleton is disrupted and the microvilli of the epithelial cell are
effaced. A highly organized cytoskeletal structure containing polymerized actin forms beneath the closely attached bacterium (reviewed in reference 4), which is raised on a
"pedestal" that may extend several microns above the plane of the
cell surface.
A multistep model of the formation of A/E lesions on host cells has
been proposed (4). Initial, nonintimate attachment of the
bacterium is followed by the injection of bacterial proteins into the
host cell (13, 17) via a specialized translocation apparatus, termed a type III secretion system (reviewed in reference 19). This results in cytoskeletal changes and the
effacement of microvilli. The last step requires a 94-kDa bacterial
outer membrane protein, termed intimin (14), and results in
close bacterium-host cell apposition on a pedestal. Intimin is encoded by the eae (E. coli attaching and effacing) gene
and is required for A/E lesion formation and for full virulence in
animal models and humans (5, 6, 22, 28).
A function for intimin in mammalian cell attachment was suggested by an
approximately 30% identity with invasin, a Yersinia pseudotuberculosis outer membrane protein that mediates entry into
mammalian cells by binding multiple
1-chain integrins
(11, 12, 29). Different candidate molecules, including
integrins, have been proposed to function as host cell receptors for
intimin. Integrins are a large family of heterodimeric receptors that
are involved in a wide variety of cell-cell and cell-extracellular matrix interactions (10). Frankel and coworkers showed that maltose binding protein (MBP) fusions containing the C-terminal 280 amino acids of EPEC intimin bound to the
1-chain
integrins
4
1 and
5
1, and antagonists of these integrins
inhibited binding of MBP-intimin to human CD4+ T cells
(8, 9). More recently, Kenny et al. (16)
presented evidence that a bacterial molecule, termed Tir (translocated
intimin receptor; also termed EspE [3]), is
translocated to the mammalian cell surface after secretion via the type
III secretion pathway and acts as a receptor for intimin. Soluble
MBP-intimin bound better to HeLa cell monolayers after preinfection
with EPEC (25). It has been postulated that perhaps both
integrins and Tir play roles in cell binding by intimin
(15). In this study, we tested whether
1-chain integrins are essential for intimin-mediated cell attachment and A/E lesion formation.
Efficient mammalian cell attachment to immobilized intimin requires
bacterial preinfection.
To develop an assay that could be used to
easily detect a role for integrins in intimin-mediated cell binding, we
tested whether preinfection of HEp-2 cells with EPEC or EHEC could
promote cell attachment to immobilized intimin. Given the clinical
significance of EHEC in the United States (23), we examined
cell binding to EHEC intimin, which is 83% identical to EPEC intimin
overall (29). The 3' 395 codons of the EHEC EDL933
eaeA gene were amplified and inserted into the 3' end of the
malE gene of pMAL-c2 (New England Biolabs, Beverly, Mass.),
and the resultant intimin fusion protein, MBP-Int395, was purified as
previously described (20). Because EPEC generates more
pronounced A/E lesions on cultured cells than EHEC (2), we
initially tested the effect on intimin binding of preincubation of
mammalian cells with EPEC strain JPN15.96/pMAR7, an eae
mutant of EPEC that retains a functional type III protein translocation
system (14). Bacteria grown overnight in Luria broth were
added to HEp-2 (epithelial) cells at a multiplicity of infection (MOI)
of approximately 200, centrifuged onto monolayers at 196 × g for 10 min, and incubated for 3 h at 37°C. Monolayers were washed three times in phosphate-buffered saline (PBS), incubated for 20 min in RHFM (RPMI 1640 supplemented with 20 mM HEPES [pH 7.0],
2% fetal bovine serum, and 0.5% D-mannose) containing 100 µg of gentamicin/ml to kill bacteria, and again washed three times with PBS. Cells were dispersed with EDTA as described previously (20) and were resuspended at 106/ml in RHFM.
Next, 0.1 ml of this suspension was added to microtiter wells coated
with 50 µl of 5-µg/ml MBP-Int395 or the equivalent MBP-invasin
fusion protein, MBP-Inv497, which contains the C-terminal 497 amino
acids of invasin (21). Bound cells were quantitated by
crystal violet staining (20). Mock-infected or E. coli K-12-infected cells did not bind MBP-Int395 above background
levels, but HEp-2 cells that had been preinfected with
JPN15.96/pMAR7 efficiently recognized MBP-Int395 (Fig.
1A). Preinfected cells did not
bind to a control MBP-
-galactosidase protein, and both
mock-infected and preinfected cells bound to MBP-Inv497. HEp-2 cells
preinfected with EHEC strain EDL933 prior to binding MBP-Int395 also
bound to intimin, albeit less efficiently than cells preinfected with EPEC strain JPN15.96/pMAR7 (Fig. 1B).

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FIG. 1.
Preinfection of HEp-2 cells with EPEC or EHEC stimulates
binding to immobilized MBP-intimin. HEp-2 cells were mock infected or
infected with E. coli K-12 JM109, EPEC strain JPN15.96/pMAR7
(eae mutant) (A), or EHEC strain EDL933 (B). Bacteria were
killed with gentamicin, and the HEp-2 cells were dispersed and added to
microtiter wells coated with a control MBP fusion protein ( -gal),
MBP-Int395 (Intimin) or MBP-Inv497 (Invasin). Bound cells were
quantitated as previously described (20). Shown are
representative results of two to six separate experiments. Binding to
invasin was performed in a separate experiment in which JM109
preinfection (Preinf.) was omitted. Error bars indicate the standard
deviations of quadruplicate samples. OD570, optical density
at 570 nm.
|
|
1-Chain integrins are not required for intimin
binding by mammalian cells.
Two integrin antagonists were tested
for the ability to block intimin binding to HEp-2 cells. Neither EDTA,
which chelates the divalent cations required for integrin function, nor
the anti-
1-chain monoclonal antibody (MAb) P4C10
(Gibco-BRL) inhibited intimin binding by EPEC-induced HEp-2 cells (Fig.
2, left). In contrast, both agents
blocked invasin binding by these cells (Fig. 2, right).

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FIG. 2.
Integrin antagonists do not inhibit mammalian cell
binding to intimin. HEp-2 cells were preinfected with EPEC strain
JPN15.96/pMAR7 as described in the text, and incubated in buffer alone
(No inhib.), 10 mM EDTA (EDTA), control mouse ascites diluted 1:300
(CMA), or ascites containing the anti- 1 MAb P4C10
(Gibco-BRL) diluted 1:300 (anti- 1 mAb) for 30 min. Cells
were then added to microtiter wells coated with MBP-Int395 (Intimin) or
MBP-Inv497 (Invasin). Bound cells were quantitated. Shown are the
means ± standard deviations of quadruplicate samples.
OD570, optical density at 570 nm.
|
|
Mammalian cells that are deficient for
1-chain integrin
expression were tested for the ability to bind intimin. F9 embryonal
carcinoma cells carry three copies of the gene encoding the
1 chain, and TKO (triple knockout) cells fail to express
1-chain
integrins due to insertions in each of the three
copies (
27).
DKO (double knockout) F9 cells retain one
intact copy of the
1 gene and thus retain expression of
1-integrins (
27). The expression
of
1-chain integrins in focal plaques of DKO but not TKO
cells
was confirmed by immunofluorescent staining with an anti-mouse
1-chain MAb (9EG7; Pharmingen, San Diego, Calif.) (data
not shown).
TKO and DKO cells were preinfected with EPEC JPN15.96/pMAR7
and
tested for the ability to bind MBP-Int395. Both cell lines bound
intimin after preinfection, and the minimal intimin coating
concentration
required for cell binding was identical for the two cell
lines
(Fig.
3A). Preinfection with
JPN15.96/pMAR7 was required for binding,
and EDTA had little effect on
intimin attachment by either cell
line (Fig.
3B). As expected, DKO but
not TKO cells bound to MBP-Inv497;
this binding was independent of
JPN15.96/pMAR7 preinfection and
was blocked by EDTA.

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FIG. 3.
1-Chain integrins are not required for
attachment to intimin. (A) TKO ( 1 ) or DKO
( 1+) cells were preinfected (Preinf.) with
EPEC strain JPN15.96/pMAR7 and then dispersed as described in the text.
Cells were added to microtiter wells coated with varying concentrations
of MBP-Int395. Cell binding was quantitated as described previously
(20), and the means of quadruplicate samples are shown. (B)
DKO ( 1+) or TKO
( 1 ) cells were mock-infected or infected
with EPEC strain JPN15.96/pMAR7 and then added to microtiter wells
coated with 5-µg/ml MBP-Int395 or 2-µg/ml MBP-Inv497. EDTA
indicates binding in the presence of 10 mM EDTA. Cell binding was
quantitated, and the means ± standard deviations of quadruplicate
samples are shown. OD570, optical density at 570 nm.
|
|
1-Chain integrins are not required for EPEC-mediated
actin condensation.
The results described above indicated that
integrins are not required for intimin binding after preinfection of
mammalian cells with EPEC. To determine whether integrins could be
required for some other step in the formation of A/E lesions, we
examined the ability of E. coli to induce actin condensation
on
1-chain integrin-deficient mammalian cells. Because
EPEC generates more pronounced A/E lesions in vitro than does EHEC
(2), TKO and DKO cells were infected with EPEC JPN15/pMAR7
(14). Filamentous actin (F-actin) was detected by using
fluorochrome-tagged phalloidin (18). A total of 50 microscopic fields containing over 400 bound bacteria were visually
scored for colocalization of bacteria and F-actin, and for both TKO and
DKO cells, every bound bacterium was associated with F-actin (Fig.
4; data not shown).

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FIG. 4.
1-Chain integrins are not required for
EPEC-mediated actin polymerization. DKO ( 1+)
(A and B) or TKO ( 1 ) (C and D) cells were
infected at an MOI of 20 with EPEC strain JPN15/pMAR7 expressing green
fluorescent protein (GFP) for 6 h at 37°C. Monolayers were
washed and permeabilized, and microscopic fields were then examined for
the presence of GFP-expressing bacteria (A and C) or were stained with
tetramethylrhodamine isothiocyanate(TRITC)-labeled phalloidin to
visualize F-actin (B and D). Arrows indicate examples of colocalized
bacteria and F-actin. Magnification, ×1,000.
|
|
The ability of EPEC to generate F-actin at sites of bacterial
attachment on cells that do not express
1-chain
integrins suggests
that
1-chain integrins do not play an
essential role at any step
in A/E lesion formation. Rather, the
requirement of preinfection
for cell attachment to immobilized
MBP-intimin is consistent with
the model that an intimin receptor is
injected during bacterium-host
cell contact (
16). The
MBP-intimin protein was derived from
EHEC strain EDL933, so if injected
Tir acts as a receptor for
intimin, EPEC Tir apparently can recognize
EHEC intimin. Consistent
with this, DeVinney and Finlay have recently
found that EPEC and
EHEC Tir recognize EHEC intimin indistinguishably
(
3a).
Frankel and coworkers showed that antagonists of
1-chain
integrins blocked binding of CD4
+ T cells to EPEC intimin
(
9). The most obvious methodological
difference between
these two studies is the preinfection of mammalian
cells by
E. coli competent for type III secretion. It is also
possible that
the apparent discrepancy may be due to differences
in the cell lines
used or to a fundamental functional difference
between EPEC and EHEC
intimins, which are only 49% identical in
the C-terminal putative
cell-binding domain (
29).
Other laboratories have also detected binding of soluble intimin to
uninduced cells (
1,
9a), and the experiments described
in
this study do not rule out the possibility that intimin also
contributes to binding of mammalian cells prior to signaling by
bacteria. The interaction of intimin with uninduced cells may
be too
weak to be detected in the assay described here or may
vary with the
particular recombinant intimin. A detailed description
of the
bacterium-host cell interactions critical for binding and
pedestal
formation will require further studies of the cell-binding
activity of
intimin.
 |
ACKNOWLEDGMENTS |
We thank Steve Luperchio, Trudy Morrison, Jon Goguen, and Jenifer
Coburn for valuable discussion and careful review of the manuscript;
Duane Jenness for assistance with microscopy; and Lisa Gansheroff,
Alison O'Brien, Rebekah DeVinney, and Brett Finlay for communication
of unpublished results. Ralph Isberg provided invaluable advice and
recombinant invasin protein, Mike Alrutz provided technical advice,
Gerald Keusch and David Acheson provided strains, and Caroline Damsky
provided the TKO and DKO cell lines used in this study. We especially
thank David Schauer for strains, encouragement, and invaluable advice.
This work was supported by a grant from the Small Grants Program of the
University of Massachusetts Medical Center.
 |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Molecular Genetics and Microbiology, University of Massachusetts
Medical Center, 55 Lake Ave. North, Worcester, MA 01655. Phone: (508) 856-4059. Fax: (508) 856-5920. E-mail:
john.leong{at}banyan.ummed.edu.
Editor:
P. J. Sansonetti
 |
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Infection and Immunity, April 1999, p. 2045-2049, Vol. 67, No. 4
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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