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Infection and Immunity, November 1998, p. 5388-5392, Vol. 66, No. 11
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
A Streptococcal Adhesion System for Salivary
Pellicle and Platelets
Ke
Gong,
T.
Ouyang, and
M. C.
Herzberg*
Department of Preventive Sciences, School of
Dentistry, University of Minnesota, Minneapolis, Minnesota 55455
Received 4 May 1998/Returned for modification 19 June 1998/Accepted 10 August 1998
 |
ABSTRACT |
A Streptococcus sanguis 133-79 adhesin identified by
the monoclonal antibody 1.1 (MAb 1.1) binds both saliva-coated
hydroxylapatite (sHA) and platelets. The complementary binding site(s)
for the adhesin was identified by the anti-idiotypical MAb 2.1. To
learn if this adhesion system, marked by the antiadhesin MAb 1.1 and anti-binding site MAb 2.1, is commonly used by strains within the
sanguis group and other viridans group streptococci, 42 strains from
seven species were tested. Strains that bind to both sHA and platelets
use the same adhesin and binding site epitopes. Strains that do not
adhere to platelets rely on other adhesin specificities to bind to sHA.
| |
INTRODUCTION |
Streptococcus sanguis
133-79, a prototype of many blood culture isolates from patients with
infective endocarditis (11, 13, 15, 29), adheres to human
platelets and induces them to aggregate in plasma (11-13,
28). Strain 133-79 also adheres to saliva-coated hydroxylapatite
(sHA), an in vitro model of the salivary enamel pellicle
(9). To characterize the adhesins of S. sanguis 133-79, monoclonal antibodies (MAbs) against whole bacterial cells were prepared. MAb 1.1 reacts with 87- and 150-kDa adhesins on strain 133-79 and, at maximal concentrations, partially inhibits adhesion to both platelets (10) and sHA
(9). To probe specific binding sites for S. sanguis 133-79 on platelets, MAb 1.1 was used to develop the
anti-idiotypical MAb 2.1. MAb 2.1 simulated the adhesin of strain
133-79 and identified 175- and 230-kDa platelet membrane proteins as
potential binding sites for this strain. On salivary pellicle, MAb 2.1 recognizes an 
-amylase-secretory immunoglobulin A (IgA) complex as a
presumptive receptor for strain 133-79 (10a). Hence, MAb 1.1 and MAb 2.1 appear to define a specific adhesion system.
The sanguis group is not readily discriminated from other viridans
streptococci based on their ability to adhere. For example, an
occasional strain of S. mutans or S. gordonii would cluster with the sanguis group based on their
reactions with platelets (11, 14). Within the sanguis group,
however, S. sanguis biovars 1 and 3 may preferentially
induce human platelets to aggregate (5). Given that there
may be similarities in the mechanisms of binding to platelets and sHA,
we sought to determine if oral streptococci commonly use the MAb
1.1-MAb 2.1 adhesion system. Since MAb 1.1 has been characterized as an
adhesin-reactive antibody (9), it was used to screen
streptococcal strains in an indirect enzyme-linked immunosorbent assay
(ELISA). From the screen, the prevalence of MAb 1.1-positive and
-negative strains was determined. For each strain, MAb 1.1 binding and
the ability to adhere to platelets and to sHA were then compared. To
demonstrate binding epitopes on platelets and sHA for MAb 1.1-positive
strains, MAb 2.1 was preincubated with platelets or sHA to inhibit
streptococcal adhesion. The results strongly suggest that most strains
of oral streptococci use the MAb 1.1-MAb 2.1 adhesion system in binding to platelets or sHA.
| |
MATERIALS AND METHODS |
Oral streptococcal strains and growth.
S. sanguis
133-79 and 2017-78 were obtained from R. R. Facklam, Centers for
Disease Control and Prevention, Atlanta, Ga.; strains E1219 and S1219
were naturally occurring erythromycin- and streptomycin-resistant
variants derived from the parental strain, S. sanguis
133-79. DNA fingerprinting patterns were visually identical within the
parent-variant lineages (25). Strain 10556 was originally
obtained from the American Type Culture Collection (ATCC), and strains
12 and 12NA were obtained from B. McBride, University of British
Columbia, Vancouver, British Columbia, Canada. The following strains
were the kind gift of W. F. Liljemark, University of Minnesota,
Minneapolis: S. sanguis L74, L59, L14, L52, L22, 4124, L13, L31, and 4123; S. gordonii 10558, S7, and M5;
S. mutans GS-5 and BHT; and S. parasanguis FW 213. J. Rudney, University of Minnesota, kindly
provided S. sanguis 804 and HPC1; S. gordonii 12396, 33399, and Blackburn; S. parasanguis 15911, 15912, and MGH145; S. oralis
10557, 9811, and CR834; S. crista 51100 and 49999; and
S. mitis 903. S. gordonii V288 was from
L. Tao, University of Missouri, Kansas City; S. mutans
JBP was provided by N. Ganeshkumar, Forsyth Dental Center, Boston,
Mass.; and S. mutans 25175, 33402, 33535, and Ingbritt
were gifts from P. R. Erickson, University of Minnesota.
All strains were stored in skim milk at 
80°C. For ELISA and amylase
binding and adhesion assays, bacterial cells were transferred from
frozen stocks onto mitis salivarius plates and incubated for 48 h
at 37°C in 5% CO2. A single colony was picked,
inoculated into Todd-Hewitt broth (THB), and allowed to grow overnight
at 37°C in 5% CO2. The cells were washed three times in
0.01 M sodium phosphate buffer, pH 7.4, with 0.9% sodium chloride
(PBS). For assay of sialidase activity, the bacterial cells were grown
on Columbia agar supplemented with 5% sterile defibrinated sheep blood
(MicroPure, White Bear Lake, Minn.). All the broth and agar for
bacterial growth were obtained from Difco, Detroit, Mich.
Phenotypical analysis.
Our library of strains of the
viridans group streptococci including clinical isolates from human
dental plaque (L74, L59, L14, L52, L22, 4124, L13, L31, and 4123), had
been phenotyped according to the scheme of Facklam (7) as
described previously (14). To further characterize these
strains, each was assayed for amylase binding (3, 19) and
sialidase activity (1, 31).
To screen for amylase binding, 15-ml aliquots of THB cultures of
streptococci were harvested by centrifugation at 1,400 ×
g
for 15 min, washed twice in PBS, resuspended in 50 µl of clarified
saliva, and allowed to incubate at 37°C for 30 min. Streptococci
were
then removed by centrifugation and the saliva-containing
supernatant
(10 µl) was added into wells punched in starch agarose
(medium EEO;
Fisher, Fair Lawn, N.J.) plates and allowed to incubate
at 37°C for
3 h. The 1% (wt/vol) starch agarose was prepared in
PBS
containing 1% starch (Sigma, St. Louis, Mo.). After incubation,
plates
were stained by covering the surface with Lugol's iodine.
Amylase
activity remained in saliva after incubation with amylase
binding-negative strains, as indicated by clear or unstained rings
around each well. Strains that completely removed the amylase
activity
from saliva (amylase binding positive) showed no clear
or unstained
ring.
Sialidase activity was determined as described by Whiley et al.
(
31). The fluorogenic substrate
2'-(4-methylumbelliferyl)-
-
D-
N-acetylneuraminic
acid, dimethyl sulfoxide, and
N-trismethyl-2-aminoethanesulfonic
acid buffer (TES buffer,
pH 7.5) were purchased from Sigma. The
substrate was dissolved in a
minimum volume of dimethyl sulfoxide
and diluted in 50 mM TES buffer to
a final concentration of 100
µg/ml. Bacterial colonies were removed
with sterile swabs and
suspended in TES buffer. The suspension was
adjusted to an optical
density of 0.1 at 620 nm. Substrate solution (20 µl) was mixed
with 50 µl of bacterial suspension in wells of a
flat-bottomed,
clear microdilution plate and incubated at 37°C for
3 h. Degradation
of substrates (release of 4-methylumbelliferyl)
was visualized
by viewing the plates under a long-wave-length UV lamp;
sialidase-positive
strains produced blue fluorescence.
Preparation of MAbs.
MAbs were prepared as reported
previously (9, 10). Briefly, MAbs against S. sanguis adhesin (MAb 1.1) were raised by immunizing BALB/c mice
intraperitoneally with live cells of strain 133-79. MAb 1.1 was
screened against both adhesive and nonadhesive strains and tested for
the ability to inhibit adhesion of S. sanguis to both
platelets and sHA. To produce anti-idiotypic MAbs, the hybridoma
producing MAb 1.1 was injected intraperitoneally into BALB/c mice as
described previously (10). The enlarged spleens were
harvested and MAb 2.1 hybridomas were prepared. MAb 2.1 was screened in
indirect ELISA for reaction with rabbit polyclonal IgG antibodies
against the 87-kDa adhesin antigen and also tested for inhibition of
S. sanguis adhesion to platelets and sHA.
Indirect ELISA.
Streptococcal strains were screened by ELISA
for reaction with MAb 1.1 as described by Elder and Fives-Taylor
(6), with slight modifications (10). The bacteria
were washed in PBS, resuspended in sodium carbonate buffer (pH 9.6),
added to 96-well flat-bottom microtiter plates (Costar, Cambridge,
Mass.) at 5 × 106 cells/well, and allowed to incubate
overnight at 4°C. The plates were dried at room temperature (RT) and
stored at 4°C. Immediately before use in ELISA, the plates were
washed three times with PBS with 0.05% Tween 20 (PBST) and blocked
with 1% bovine serum albumin (Sigma) for 1 h at RT. Next, 100 µl of a 1:4 dilution of MAb 1.1 culture supernatant (containing about
1 µg of IgG1/ml) was added to each well and incubated for 3 h at
RT. After three additional washes with PBST, a 1:3,000 dilution of goat
anti-murine IgG conjugated with alkaline phosphatase (Bio-Rad,
Richmond, Calif.) was added at 100 µl/well. After 2 h of
incubation at RT, the wells were washed and the substrate was added at
150 µl/well. The plates were allowed to stand at RT for 1 h and
then read at 405 nm. Reaction of nonspecific mouse IgG (0.25 µg/ml,
100 µl/well) with each strain served as the negative control
(background).
Adhesion assays.
All procedures for the platelet-bacterium
adhesion assay were performed as described previously (11).
In brief, platelets from outdated platelet-rich plasma (PRP) (American
Red Cross Blood Center, St. Paul, Minn.) were washed with PBS.
Washed platelets and washed streptococcal cells were incubated together
or alone (controls) in microwells; the small clusters of adhering
platelets and bacteria were separated from noninteracting particles by
centrifugation. The sedimentation of adhering mixtures relative to
controls was quantitated by the following formula: percent
adhesion = 100 × {1 [mixture
A620/(bacterium A620 + washed-platelet A620)/2]}. Based on previous
studies of the variability of the method (14), only adhesion
scores of 
20% were considered positive.
Adhesion of streptococcal cells to sHA was assayed by a modification of
the method used by Liljemark and coworkers (
21,
22) and
Tellefson and Germaine (
30). The assay was performed
in
1.5-ml polypropylene microcentrifuge tubes with 0.01 M phosphate
buffer, pH 6.8 (PB), at RT in all experiments. Streptococci were
grown
overnight in THB with 10 µCi of
[
methyl-
3H]thymidine (Research Products
International Corp., Mount Prospect,
Ill.) per ml. Radiolabeled cells
were washed three times with
PB, sonicated three times for 3 s
each to break the bacterial
chains, and resuspended in the same buffer
at 10
9 cells/ml. The specific activity for labeled
streptococcal strains
varied from 752 ± 22 (mean ± standard
deviation) to 9,792 ± 152
bacteria per cpm. The data are
presented as a percentage of total
bacterial input (10
9
cells) adhering to 10 mg of sHA and were calculated as follows:
[(radioactivity associated with sHA × specific
activity)/10
9 cells] × 100. Given the sensitivity and
reproducibility of the
method, an adhesion score of
6.5% was
considered positive.
To learn if the strains adhere to the same binding site, platelets
(10
9/ml) or sHA (10 mg/ml) was preincubated for 30 min with
1% bovine
serum albumin and then incubated for 1 h at RT with MAb
2.1 (2
nmol of IgG/10
9 platelets/100 µl or 33.3 pmol of
IgG/10 mg of sHA). Nonbinding
MAb 2.1 was removed by washing, and
streptococcal adhesion to
platelets or sHA was tested. The percent
inhibition of streptococcal
adhesion was calculated as follows:
[(adhesion
PB adhesion
MAb)/adhesion
PB]
× 100, where
adhesion
PB occurs in the presence of buffer and
adhesion
MAb occurs in the presence of added antibody.
| |
RESULTS |
We confirmed the phenotypes of representative strains from our
panel (Table 1). Several strains were
previously classified as S. sanguis (14) but
based on additional criteria were considered for reassignment. Strain
L31 (inulin fermentation positive and arginine and esculin hydrolysis
positive) and E1219, an erythromycin-resistant variant of strain
133-79, were amylase binding positive. Based on its ability to bind
amylase, strain L31 was reclassified as S. gordonii.
Strain E1219, which was also amylase binding positive, was not
reassigned because the parent strain was confirmed to be S. sanguis. Strain L13 (inulin fermentation negative, raffinose positive, and arginine and esculin hydrolysis negative) showed sialidase activity and was reassigned as S. oralis.
Of 16 S. sanguis strains, 50% were adhesion positive
with both platelets (>20% adhesion) and sHA (>6.5% adhesion) (Table
2). Among the seven species surveyed, 13 of 42 strains (31%) adhered to platelets and 21 (50%) adhered to sHA.
All strains that bound to platelets also adhered to sHA and could be
identified as MAb 1.1 binding positive (Table
3). Strains that were MAb 1.1 binding negative did not adhere to platelets. Conversely, sHA
adhesion-positive, platelet adhesion-negative strains also did not
react with MAb 1.1.
Binding of MAb 1.1 by all strains was highly correlated with their
ability to adhere to platelets (r = 0.949) (Fig.
1). When strains that only adhered to sHA
were excluded from the analysis, the abilities of the remaining strains
to adhere to sHA and bind with MAb 1.1 were strongly related
(r = 0.897) (Fig. 2).
When all strains were included in the analysis, the correlation between the ability to adhere to sHA and binding with MAb 1.1 was lower (r = 0.481).
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FIG. 1.
Correlation between MAb 1.1 binding and platelet
adhesion. Each point represents the mean values for MAb 1.1 binding
(n = 4) and adhesion to platelets (n = 2) for a given strain of streptococcus.
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FIG. 2.
Relationship among strains in their ability to adhere to
sHA and bind with MAb 1.1. The broken line represents the relationship
when all 42 strains (open and solid circles) were included in the
analysis. For analysis excluding sHA adhesion-positive, platelet
adhesion-negative strains (open circles), the solid line represents the
relationship for all other strains (solid circles). Each point
represents the mean values for sHA binding (n = 3) and
MAb 1.1 binding (n = 4) for a given strain of
streptococcus.
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|
For all streptococcal strains that bound MAb 1.1, adhesion to sHA and
platelets could be inhibited by the anti-idiotypic MAb 2.1 (Table
4). Examples of MAb 1.1-positive strains
inhibited in adhesion activities by MAb 2.1 were noted in most taxa of
viridans group streptococci tested. Inhibition of streptococcal
adhesion to sHA and platelets by MAb 2.1 was highly correlated with the ability of strains to bind MAb 1.1 (r = 0.832 and
0.777, respectively) (Fig. 3).
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FIG. 3.
Correlation between MAb 1.1 binding and MAb 2.1 inhibition of streptococcal adhesion to sHA and platelets. MAb 2.1 was
preincubated with either sHA (solid circles) or platelets (open
circles) and then tested for inhibition of adhesion with strains of
viridans group streptococci. The relationship between MAb 2.1 inhibition of adhesion to sHA and the ability of strains to bind MAb
1.1 is shown by the solid line (solid circles). The relationship
between MAb 2.1 inhibition of adhesion to platelets and MAb 1.1 binding
is shown by the broken line (open circles). Each point represents the
mean of at least three determinations.
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| |
DISCUSSION |
Of the S. sanguis strains and viridans group
streptococci tested, every strain that bound to platelets also adhered
to sHA. Adhesion to sHA and platelets was shown previously to be
inhibited by MAb 1.1 in a dose-dependent manner (9, 10). MAb
1.1 reacts with a two-domain adhesin on S. sanguis
133-79 (9); this adhesin is required for interactions with
human platelets (10) and sHA (9). The
adhesin-specific MAb 1.1 reacts with strains that adhere to both
platelets and sHA (9, 10), suggesting that the same
functional adhesin epitope is expressed. MAb 1.1, therefore, served in
this study as a marker for this functional adhesin epitope. While
strains vary in the amount of MAb 1.1 required for saturation, the
current data show that the MAb 1.1-positive adhesin epitope is widely
expressed among the viridans group streptococci. MAb 1.1-positive
strains also adhere to these two disparate substrates. Other strains
are MAb 1.1-negative. As expected based on work with S. sanguis 133-79, these strains failed to bind to platelets (10). For those MAb 1.1-negative strains that adhered well
to sHA, an alternative adhesin specificity is implied to function.
The anti-idiotypical MAb 2.1 was prepared by immunization of syngeneic
mice with MAb 1.1 (10). MAb 2.1 should mimic
immunochemically the adhesin epitope recognized by MAb 1.1. Hence, MAb
2.1 should bind the immunochemically complementary binding sites for
the S. sanguis adhesin marked by MAb 1.1 on adhesion
substrates such as platelets and sHA. Indeed, MAb 2.1 bound to sHA and
platelets to inhibit adhesion of MAb 1.1-positive strains. MAb 2.1 identifies, therefore, an immunochemically specific binding site
for adhesion of MAb 1.1-positive viridans group streptococci. These
platelet and sHA binding sites or receptors (identified by the
anti-idiotype MAb 2.1) for streptococcal cells are likely to
share essential structural features but to consist of very different
proteins. Alternative binding sites on sHA for viridans group
streptococci are also implied to function for MAb 1.1-negative strains.
The oral streptococci express a constellation of adhesins
(17), several of which may be MAb 1.1 reactive
(9). Among the better-characterized families of adhesins are
P1 (2, 16), CshA and -B (23), and FimA
(8, 20). In addition, S. gordonii expresses an amylase binding protein (27). While it is
clear that the sanguis group expresses many protein adhesins, this
report demonstrates a novel, epitope-specific, functional
conservation.
The data indicate that MAb 1.1 and the corresponding anti-idiotypic MAb
2.1 mark a specific adhesion system for viridans group streptococci.
The adhesion system is comprised of an adhesin epitope and its
structurally complementary binding site or receptor. Of the 42 strains
of viridans group streptococci tested, at least 13 employed this
adhesion system for platelets and sHA. The ability to use the MAb
1.1-MAb 2.1 adhesion system was independent of taxon. To consider
taxonomic restrictions on this trait, the classification of many of the
strains in the panel was reevaluated on the basis of amylase binding
(3, 4, 19) and sialidase activity (1). The
original taxonomy for the strains in the panel employed the strategy of
Kilian et al. (18). For several of the 16 strains for which
taxonomic identity was reevaluated, the classification could be
questioned. Strain L31, which produced acid from inulin, hydrolyzed
arginine and esculin, and bound -amylase, was reclassified from
S. sanguis to S. gordonii. S. sanguis-like strains that bind amylase are generally classified as
S. gordonii or other species (4, 19). In
contrast, strain L13, which was negative for inulin fermentation,
hydrolysis of arginine and esculin, and amylase binding, fermented
raffinose and expressed sialidase activity. Based on the
phenotypic characteristics, strain L13 was identified as
S. oralis (1, 31). Strain E1219 was an
erythromycin-resistant variant of S. sanguis
133-79 (14). It was not reclassified as S. gordonii, even though it binds amylase. The parent strain, 133-79, was confirmed to be S. sanguis by ribotyping
(24) and the variant, which was selected after growth in the
presence of erythromycin, was shown to be from the parental lineage by
DNA fingerprinting (25). Further study of strain E1219 will
be necessary to make a correct taxonomic assignment. Strain L4123 was
classified as S. sanguis, even though it did not
hydrolyze arginine. The assignment of this strain is clearly uncertain,
but the limited scope of phenotypic characteristics examined
precluded a decisively better assignment.
Hence, most of our S. sanguis strains remain assigned
to that taxon, except for strains L13 and L31. It is clear, however, that expression of the MAb 1.1-MAb 2.1 adhesion system, which confers
the ability of viridans group streptococci to adhere to both platelets
and sHA, is independent of taxon and is common among the viridans
group streptococci.
| |
ACKNOWLEDGMENTS |
This work was supported by NIH grants DE08590, P30DE09737, and
DE05501.
We are grateful to Joel Rudney for his advice about the statistical
analyses and streptococci taxonomy. We thank James Hodges for his
advice about the statistical analyses.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: 17-164 Moos
Tower, University of Minnesota, 515 Delaware St., S.E.,
Minneapolis, MN 55455-0348. Phone: (612) 625-8404. Fax: (612) 626-2651. E-mail: mcherzb{at}tc.umn.edu.
Editor:
V. A. Fischetti
| |
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Infection and Immunity, November 1998, p. 5388-5392, Vol. 66, No. 11
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
