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Infection and Immunity, April 2001, p. 2743-2747, Vol. 69, No. 4
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.4.2743-2747.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Evidence of Involvement of the Mannose Receptor in
Adhesion of Borrelia burgdorferi to
Monocyte/Macrophages
Marina
Cinco,1,*
Barbara
Cini,1
Rossella
Murgia,1
Gianni
Presani,2
Mario
Prodan,2 and
Sandra
Perticarari2
Dipartimento di Scienze Biomediche,
Università di Trieste,1 and
Laboratorio di Analisi Cliniche, IRCCS, "Burlo
Garofolo,"2 Trieste, Italy
Received 18 September 2000/Returned for modification 10 November
2000/Accepted 14 December 2000
 |
ABSTRACT |
The mannose receptor (MR) plays an important role in the
recognition of some pathogens in nonopsonic phagocytosis and in antigen presentation to T cells. We found that Borrelia
burgdorferi, the agent of Lyme borreliosis, adheres to
monocyte-derived macrophages and to rat MR-transfected cells
but not to untransfected cells. Antibodies to MR and sugars such as
mannose, mannan, fucose, and some lectins significantly lowered the
adhesion, confirming participation of the MR in the binding.
| |
TEXT |
The etiological agent of Lyme
disease, Borrelia burgdorferi, is able to disseminate widely
and avoid clearance by innate immunity and by the immune system,
thereby establishing chronic infection. Spirochetes undertake complex
interactions with a variety of mammalian cells, which contribute to the
establishment of infection in the host. Such interactions consist of
adhesion to cells and tissues: B. burgdorferi binds to
platelets via the integrins 
II
3 and to
endothelial cells through the integrins
V3 and 51
(7, 8) and to a variety of cells which express
glycosaminoglycans such as heparin, heparan sulfate, and dermatan
sulfate (19, 2). Lyme borreliosis Borrelia also
recognizes other substrates like fibronectin (17, 23) and
decorins (12), which explains the attachment of B. burgdorferi to the extracellular matrix of the skin and other
tissues. Binding to such receptors as integrins, which are true
cell-associated receptors, not only provides adhesion to cells,
allowing B. burgdorferi to attach itself firmly to the tissues, but also can induce effector mechanisms, normally triggered by
the integrin under appropriate stimuli. This is the case with integrin
M2, a dynamic molecule also known as CR3
or CD11b/CD18 receptor; this molecule was shown to bind borrelias
(4) and trigger phagocytosis by neutrophils in the absence
of specific opsonization; such binding activates the molecule to
up-regulation and increases adhesion to fibronectin (6).
The binding seems to involve not only the I domain of the molecule,
specific for the iC3b and the RGD motif, but also the lectin-like
domain, which is known to recognize lipopolysaccharide, mannose, and
other sugar residues (5).
Another cell receptor which is involved in microbe recognition and
phagocytosis in the absence of specific opsonization is the mannose
receptor (MR), which acts as a true lectin in the lectin phagocytosis
of microorganisms (22). It is a type I transmembrane glycoprotein of 165 kDa containing as many as eight adjoining carbohydrate recognition domains, a fibronectin type II domain, and a
cysteine-rich domain (2); it is expressed on tissue
macrophages, dendritic cells (mostly on Langerhans
cells), endothelium, and rat microglia. Besides acting as a scavenger
of mannose-containing glycoconjugates on the surface of a wide spectrum
of microorganisms, such as Escherichia coli, Klebsiella
pneumoniae, Mycobacterium tuberculosis, Pseudomonas aeruginosa, Candida
albicans, Leishmania, and Pneumocystis carinii
(21), it mediates their ingestion by macrophages.
Moreover, it has been recently reported that dendritic cells expressing
the MR exhibit a 100-fold increase in antigen presentation to T cells
(10). Dendritic cells and Langerhans cells are the first
line of phagocytosis, serving as antigen-processing cells in the dermis
and epidermis which can internalize B. burgdorferi in the
tissues, in the absence of specific antibodies (11). It
has recently been demonstrated that the principal immunogens of
B. burgdorferi, the lipoproteins, are rapidly processed by human dendritic cells and presented to CD8+ T cells
(2). Since the MR is the main molecule involved in antigen
recognition and the binding process in antigen-presenting cells
(9, 10), this study was undertaken to establish whether B. burgdorferi recognizes and binds this receptor. We used
three cellular models; one was a culture of monocyte-derived
macrophages (MDMs), which naturally expresses the MR, while the
other two were cell line MRF-61 (a rat fibroblast line transfected with the human MR) and its wild-type, untransfected cell parent.
Microorganisms, cell cultures, and labeling.
The borreliae
used were Borrelia garinii strain BITS, isolated from
Ixodes ricinus, and the low-passage-number. B. garinii strain M3/5, isolated from a mouse. Culture conditions and
counting were as previously reported (3). When required,
borreliae were labeled with fluorescein isothiocyanate (FITC) as
previously described (3). C. albicans (ATCC
3153) was grown in Sabouraud medium and fluorescein labeled as for borreliae.
MDM monolayers were prepared from blood monocytes as described
elsewhere (25). In brief, buffy coats obtained from the
blood bank of the Ospedale Maggiore (Trieste, Italy) were diluted with an equal volume of Ca2+- and Mg2+-free
phosphate-buffered saline, pH 7.4 (PBS), containing 1 mM EDTA and 5 mM
glucose and then centrifuged at 250 × g for 10 min at
4°C to remove platelets. The pellet containing erythrocytes and
leukocytes was suspended in PBS-EDTA-glucose solution. Thirty-five milliliters of this suspension was layered over 15 ml of Lymphoprep and
centrifuged at 800 × g for 25 min at 4°C. The
band at the PBS-Lymphoprep interface containing the lymphocytes and
monocytes was collected, centrifuged at 250 × g
for 10 min at 4°C, and washed twice in PBS-EDTA-glucose
solution; the cells were resuspended in RPMI 1640 with 25 mM HEPES (pH
7.4) and counted electronically (Coulter Counter model ZBI; Coulter
Counter Electronics Ltd., Luton, United Kingdom). Differential
counts were then made on Diff-Quick-stained cytospin
preparations, and the cells were finally diluted to a
concentration of 1.5 × 106 monocytes/ml. Aliquots (3 ml) of the cell suspension were seeded in sterile 24-well plates
and incubated for 90 min at 37°C; adherent monocytes were cultured in
RPMI 1640 with 25 mM HEPES (pH 7.4) supplemented with penicillin (100 U/ml), streptomycin (100 µg/ml), 2 mM glutamine, and 10% human
serum. The cells were kept in culture for 3 to 9 days before
being used for the experiments; during this incubation, the
decrease in CD14 expression was checked as a marker of monocyte
differentiation into macrophages, by reaction with anti-CD14
My4 antibody (Coulter clone; Coulter, Zurich, Switzerland). The MDMs
were then tested for MR expression by reaction with the goat anti-MR
(G-anti-HuManRec, TNO-PG; Gaubius Laboratory) polyclonal antibody and
the isotype-matched control immunoglobulin G2a (Dako SpA Milano) by
immunofluorescence. Cells were resuspended in PBS-0.5% paraformaldehyde for cytometric reading. MRF-61 rat cells which had
been transfected with the human MR (27) were a generous gift from Philip Stahl (Department of Cell Biology and
Physiology, Washington University, St. Louis, Mo.); they were
cultured as monolayers in Dulbecco modified Eagle medium
(DMEM)-HEPES-25-mM medium and checked for MR expression as
described for macrophages. The untransfected parental rat
fibroblasts (clone Rat-6H) were used as the control and cultivated in
the same medium as MRF-61 cells.
Adhesion experiments.
In adhesion experiments, MDMs were
detached from the plates with 5 mM EDTA-PBS, washed, and then
resuspended in minimal essential medium (MEM) plus 2 mM glutamine and
2% synthetic serum (Ultraser HY; Gibco BRL) at 106
cells/ml. The MRF-61 MR-expressing cells and Rat-H6 cells were washed
and suspended in 100 µl of MEM-0.1% bovine serum albumin at
106 cells/ml. The macrophages and cultured cells
were incubated with 20 µl of FITC-labeled B. burgdorferi
(5 × 108/ml) for 45 min at 37°C with shaking. The
final cell spirochete ratio was 1:100. When FITC-labeled C. albicans was used, the Candida /cell ratio was 2:1,
10:1, or 20:1. Adhesion experiments were performed in MEM solution
containing 0.1% bovine serum albumin for the purpose of reducing
nonspecific binding; PBS-0.5% paraformaldehyde was added to each
suspension to a final volume of 0.5 ml and analyzed by cytometry.
As potential inhibitors of MR-mediated adhesion, the following reagents
were added to the cells and incubated for 15 min at
37°C prior to
addition of the microorganisms: sugars such as mannan
(2 mg/ml) or
D-mannose,
L-fucose,
D-galactose,
and
N-acetyl-
D-glucosamine
(NAGD) (each at 100 mM), and the lectins asparagus pea, garden
pea, soybean,
and
Maackia (whose sugar specificity is reported
in
Table
1) at 100 µg/ml. The anti-MR
polyclonal antibody, at
a dilution of 1:200 (corresponding to 5 µg/ml), was preincubated
with the cells at 4°C for 15 min. Readings
of fluorescence were
performed with a FACSCalibur flow cytometer
(Becton Dickinson
Immunocytometry Systems, San Jose, Calif.) equipped
with an air-cooled
argon ion laser fitted at 488 nm and with a filter
setting for
FITC (530 nm). Events were acquired in list mode and
analyzed
with CellQuest software (Becton Dickinson). Acquisition of
10,000
events was dependent on a gating on MRF-61 or macrophage
cell
morphology (forward and side scatter) to exclude cells debris
or
abnormally large cells or aggregate from analysis. Detector
gain and
voltage adjustment and scatter gating had been set and
saved in
preliminary experiments with untreated cells, and the
same protocol was
used for all subsequent studies. Single green
fluorescence emission of
FITC-labeled borreliae bound to MRF-61
cells or MDMs was measured and
expressed as a percentage of positive
cells. To select the binding of
spirochetes to MDMs and cells,
the specific background fluorescence of
macrophages alone was
used as the threshold level, and a marker
was set. MDMs or MRF-61
cells, or Rat-H6 cells with a fluorescence
intensity higher than
the threshold level, were considered to represent
significant
adhesion. The expression of MR antigen on the cells was
quantified
as green fluorescence signal. For each experiment, unstained
cells
or cells stained with isotype-matched monoclonal antibodies were
used as negative controls to set the threshold for positivity.
Data
from repeated experiments were analyzed by the unpaired Student
t test, using GraphPad Prism (GraphPad Software, San Diego,
Calif.).
We first verified that the MR was expressed during the
differentiation
of human monocytes into macrophages and in the
MR-transfected
MRF-61 cell cultures. Detection of the receptor by the
anti-MR
antibody was evident by day 3 and increased thereafter to day
6 in about 80% of the MDMs; MR-associated fluorescence was detected
on
about 70% of the MRF-61 fibroblasts, and no fluorescence was
obtained
on non-MR-transfected Rat-H6 cells (data not shown).
Adhesion on MDMs.
Fluorescent B. burgdorferi was
added to MDM suspensions in the presence or absence of different
reagents, and binding of the spirochetes to phagocytes was quantified
by flow cytometry. Preliminary time course experiments were performed
to investigate the kinetics of adhesion to MDMs; as reported in Fig.
1A, the rate of adhesion of FITC-stained
borreliae to the cells increased with time during the 60 min of
incubation, involving up to 30% MDMs, and was expected to increase
more; we chose the 45-min time interval to perform the subsequent
adhesion experiments. MDMs preincubated for 15 min with the anti-MR
antibody (Fig. 1B) exhibited a 70% inhibition of adhesion which was
not detected with the isotype antibody. Although the use of whole
antibody G-anti-HuManRec can cause a potential cross-linking and
capping of the MR, this finding suggests that the MR is involved in the
binding. Further inhibition was observed after preincubation with
saccharides D-mannose (about 83%), D-galactose
(about 82%), L-fucose (56%), mannan (about 46%), and NADG (about 41% [not significant]). Increasing the
concentration of soluble ligand failed to further inhibit adhesion
(data not shown). Further evidence of probable involvement of the MR in MDM adhesion comes from the inhibition experiments with lectins (Fig.
1C): asparagus pea and garden pea, recognizing the
alpha-L-fucosyl and alpha-D-mannosyl residues,
respectively, strongly inhibited binding of the spirochetes; minor and
less significant inhibition was observed in the presence of lectins
Maackia and soybean, which are specific for sialic acids and
N-acetylgalactosamyl residues.
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FIG. 1.
Adhesion of FITC-labeled B. burgdorferi to
MDMs in different experimental conditions. (A) Time course of B. burgdorferi adhesion. (B) Inhibitory effect on adhesion by
pretreatment with sugars and with anti-MR serum. Isotype control serum
was used as control. (C) Inhibitory effect on adhesion by different
lectins. Adhesion was measured as the percentage of cells becoming
fluorescent after binding of FITC-labeled B. burgdorferi.
Bars express the means ± standard deviations of three independent
determinations. P  0.05.
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|
Adhesion on MR-transfected cells.
Adhesion assays were also
carried out on MRF-61 cells, a cell line used to avoid the
participation of CR3 or other unknown macrophage receptors
which might recognize B. burgdorferi in nonopsonic conditions; untransfected clone Rat-H6 cells were used as a control. Besides testing the level of MR expression, we also checked binding of
the MR in adhesion experiments with C. albicans, which is
known to be recognized by this receptor (18). As reported
in Fig. 2A, there was a clear
dose-dependent adhesion of Candida on MRF-61 cells and a
little adhesion on untransfected Rat-H6 fibroblasts. Involvement of the
MR in binding is indicated by a strong decrease of adhesion in the
presence of mannan, the classic antagonist of MR binding, and by the
anti-MR antibody; a nonsignificant level of inhibition was exerted by
L-fucose, as already reported (15) for
Candida. Taken together, these data confirm the expression of a functional MR on the cultured cells.
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FIG. 2.
Adhesion of FITC-labeled C. albicans on
MRF-61 cells. (A) Rate of adhesion on MRF-61 fibroblasts at different
concentrations of C. albicans. (B) Effect on adhesion by
pretreatment with mannan, L-fucose, and anti-MR serum.
Adhesion was measured as the percentage of cells becoming fluorescent
after binding of FITC-labeled C. albicans. Bars express the
means ± standard deviations of three independent determinations.
P 0.01.
|
|
Parallel experiments carried out with
B. burgdorferi (Fig.
3A) showed that the rates of adhesion of
the organism were in the
order of 22% on MR-transfected cells but only
6% on nontransfected
cells; this finding in itself seems to indicate
that the MR was
involved in the greater MRF-61 adhesion. When MRF-61
cells were
preincubated with potential antagonists of MR binding (Fig.
3B),
the anti-MR antibody decreased adhesion 20%; among the
saccharides,
significant inhibition was exerted by mannan (52%) and
D-mannose
(38.35%) but not by
L-fucose and
D-galactose. The pattern of inhibition
by saccharides
partly confirmed the results obtained with MDMs.
In fact, mannan and in
particular mannose behaved as strong antagonists
of binding in both
MDMs and MRF-61 cells;
L-fucose and
D-galactose
inhibited adhesion only on MDMs. The failure of
L-fucose to
inhibit
adhesion on MRF-61 cells had already been observed with
C. albicans (see above). The stronger antagonism of mannose
on MDM adhesion
and the antagonist effect of
D-galactose on
MDM binding may be
due to participation in the binding of integrin CR3
(recognized
by mannose) and of the 42-kDa lectin (
26)
which has recently
been found to specifically bind
D-galactose on macrophages. Both
of these receptors
act as lectins on MDMs and are absent on fibroblasts.
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FIG. 3.
Adhesion of FITC-labeled B. burgdorferi to
MRF-61 cells in different experimental conditions. (A) Adhesion on MR
transfected MRF-61 cells and untransfected Rat-6H cells P 0.01. (B) Effect of different saccharides and anti-MR antibody on
adhesion, determined as for Fig. 2. P 0.05.
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|
Taken together, these findings suggest that adhesion on MDMs is the
result of multiple binding of lectin-functioning receptors
such as CR3
and MR; also, we cannot exclude involvement of the
42-kDa
galactose-specific lectin and of the
-glucan receptor
(
26,
20). Further evidence of participation of the MR in binding
is provided by the higher adhesion of
B. burgdorferi on
MR-transfected
fibroblasts than on untransfected clone Rat-H6
fibroblasts; these
cells gave a low background adhesion, due to unknown
naive receptors
for
B. burgdorferi (
16).
Since the MR recognizes saccharides and glycosylated proteins, the
exact counter receptor present on the
B. burgdorferi outer
membrane is unclear; in fact, there is general agreement that
these
spirochetes mainly expose lipoproteins, although there are
interesting
reports on the presence of glycoconjugates on
B. burgdorferi (
13,
24) containing at least four sugars, mainly NADG and
mannose; these saccharides probably take part in adhesion to the
lectin-like domain of CR3 (
4,
5) and maybe to the MR CDR1
epitope.
However, the interaction with the MR is peculiar: it seems that binding
to the MR, which has multiple binding sites (
27),
involves
either multiple binding pathways or one single promiscuous
pathway, as
happens in the binding to different proteoglycans.
Thus, since it is
demonstrated that
B. burgdorferi avidly binds
to fibronectin
(
17,
23) and the MR exposes a fibronectin type
II repeat,
we can hypothesize that the adhesion is first mediated
by this domain,
followed by the participation and clustering of
the other
sugar-specific domains in a complex multiple
binding.
The consequence of MR-
B. burgdorferi recognition may
influence the host immune reactions at the beginning of the
Borrelia infection, when the spirochetes are inoculated into
the epidermis
and dermis and become phagocytosed and processed by
Langerhans
(
14) and dendritic (
11) cells. It
has been recently demonstrated
that dendritic cells play a crucial role
in the
Borrelia immune
response because they process and
present
B. burgdorferi antigens
associated with major
histocompatibility complex class I and class
II molecules, resulting in
the activation of both humoral and
cellular immunity. Given the
extensive literature (
9,
10)
on the role of the MR on
dendritic and Langerhans cells in processing
and presenting antigens,
following a pathway and subcellular fractionation
resembling that
observed in dendritic cells for
B. burgdorferi lipoproteins
(
1,
2), we are inclined to think that this
receptor plays
an important role in the development of macrophage
phagocytosis
and early immunity to
B. burgdorferi. Both of these
mechanisms affect the innate response of the
host.
| |
ACKNOWLEDGMENTS |
We thank Philip Stahl, Department of Cell Biology and Physiology,
Washington University, St. Louis, Mo., for sending the MRF-61 cells and
anti-MR antibody and for critical reading of the text.
Work in our laboratory was supported by the MURST 40% funding.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Dipartimento di
Scienze Biomediche, Università di Trieste, 34127 Trieste, Italy.
Phone: 39 40 676 7178. Fax: 39 40 351668. E-mail:
cinco{at}DSBMAIL.UNITS.it.
Editor:
D. L. Burns
| |
REFERENCES |
| 1.
|
Beerman, C.,
G. Lochnit,
R. Geyer,
P. Groscurth, and L. Filgueira.
2000.
The lipid component of lipoproteins from Borrelia burgdorferi: structural analysis, antigenicity and presentation via human dendritic cells.
Biochem. Biophys. Res. Commun.
267:897-905[CrossRef][Medline].
|
| 2.
|
Beermann, C.,
H. W. Allenspach,
P. Groscurth, and L. Filgueira.
2000.
Lipoproteins from Borrelia burgdorferi applied in liposomes and presented by dendritic cells induce CD8+ T-lymphocytes in vitro.
Cell. Immunol.
201:124-131[CrossRef][Medline].
|
| 3.
|
Cinco, M.,
R. Murgia,
G. Presani, and S. Perticarari.
1994.
Simultaneous measurement by flow cytometry of phagocytosis and metabolic burst induced in phagocytic cells in whole blood by Borrelia burgdorferi.
FEMS Microbiol. Lett.
122:187-194[CrossRef][Medline].
|
| 4.
|
Cinco, M.,
R. Murgia,
G. Presani, and S. Perticarari.
1997.
Integrin CR3 mediates the binding of nonspecifically osponized Borrelia burgdorferi to human phagocytes and mammalian cells.
Infect. Immun.
65:4784-4789[Abstract].
|
| 5.
|
Cinco, M.,
R. Murgia,
S. Perticarari, and G. Presani.
1998.
Surface receptors of neutrophils towards B. burgdorferi.
Middle Eur. J. Med.
110:866-869.
|
| 6.
|
Cinco, M.,
E. Panfili,
G. Presani, and S. Perticarari.
2000.
Interaction with Borrelia burgdorferi causes increased expression of the CR3 integrin and increased binding affinity to fibronectin via CR3.
J. Mol. Microbiol. Biotechnol.
2:575-579[CrossRef][Medline].
|
| 7.
|
Coburn, J.,
S. W. Barthold, and J. M. Leong.
1994.
Diverse Lyme disease spirochetes bind integrin II3 on human platelets.
Infect. Immun.
62:5559-5567[Abstract/Free Full Text].
|
| 8.
|
Coburn, J.,
L. Magoun,
S. C. Bodary, and J. Leong.
1998.
Integrin V3 and 51 mediate attachment of Lyme disease spirochetes to human cells.
Infect. Immun.
66:1946-1952[Abstract/Free Full Text].
|
| 9.
|
Condaminet, B.,
J. Peguet-Navarro,
P. D. Stahl,
C. Dalbiez-Gauthier,
D. Schmitt, and O. Berthier-Vergnes.
1998.
Human epidermal Langerhans cells express the mannose-fucose binding receptor.
Eur. J. Immunol.
28:3541-51[CrossRef][Medline].
|
| 10.
|
Engering, A. J.,
M. Cella, and D. Fluitsma.
1997.
The mannose receptor functions as high capacity and broad specificity antigen receptor in human dendritic cells.
Eur. J. Immunol.
27:2417-2425[Medline].
|
| 11.
|
Filgueira, L.,
F. Nestle,
M. Rittig,
H. I. Joller, and P. Groscurt.
1996.
Human dendritic cells phagocytose and process Borrelia burgdorferi.
J. Immunol.
157:2998-3005[Abstract].
|
| 12.
|
Guo, B. P.,
S. J. Norris,
L. C. Rosenberg, and M. Hook.
1995.
Adherence of Borrelia burgdorferi to the proteoglycan decorin.
Infect. Immun.
63:3467-3472[Abstract].
|
| 13.
|
Hulinska, D.,
P. Volf, and L. Grubhoffer.
1992.
Characterisation of Borrelia burgdorferi glycoconjugates and surface carbohydrates.
Zentbl. Bakteriol.
276:473-480.
|
| 14.
|
Hulinska, D.,
P. Bartak,
J. Hercogova,
J. Hancil,
J. Basta, and J. Schramlova.
1994.
Electron microscopy of Langerhans cells and Borrelia burgdorferi in Lyme disease patients.
Zentbl. Bakteriol.
280:348-359.
|
| 15.
|
Karbassi, A.,
M. J. Becker,
S. J. Foster, and R. N. Moore.
1987.
Enhanced killing of Candida albicans by murine macrophages treated with macrophage colony-stimulating factor: evidence for augmented expression of mannose receptors.
J. Immunol.
139:417-421[Abstract].
|
| 16.
|
Klempner, M. S.,
R. Noring, and R. A. Rogers.
1993.
Invasion of human skin fibroblasts by the Lyme disease spirochete, Borrelia burgdorferi.
J. Infect. Dis.
167:1074-1081[Medline].
|
| 17.
|
Kopp, P. A.,
M. Schmitt,
H. J. Wellensiek, and H. Blobel.
1995.
Isolation and characterization of fibronectin-binding sites of Borrelia garinii N34.
Infect. Immun.
63:3804-3808[Abstract].
|
| 18.
|
Lazlo, M.,
H. M. Korchak, and R. B. Johnston.
1991.
Mechanism of host defense against Candida species.
J. Immunol.
146:2783-2789[Abstract].
|
| 19.
|
Leong, J. M.,
P. E. Morissey,
E. Ortega-Barria,
M. E. Pereira, and J. Coburn.
1995.
Hemagglutination and proteoglycan binding by the Lyme disease spirochete, Borrelia burgdorferi.
Infect. Immun.
63:874-883[Abstract].
|
| 20.
|
Linehan, S. A.,
L. Martinez-Pomares, and S. Gordon.
2000.
Macrophage lectins in host defence.
Microb. Infect.
2:279-288[CrossRef][Medline].
|
| 21.
|
Mosser, D. M.
1994.
Receptors on phagocytic cells involved in microbial recognition.
Immunol. Ser.
60:99-114[Medline].
|
| 22.
|
Ofek, I.,
J. Goldhar, and Y. Keisari.
1992.
Nonopsonic phagocytosis of microorganisms.
Annu. Rev. Microbiol.
49:239-276[CrossRef][Medline].
|
| 23.
|
Probert, W. S., and B. J. Johnson.
1998.
Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31.
Mol. Microbiol.
30:1003-1015[CrossRef][Medline].
|
| 24.
|
Sambri, V.,
F. Massaria,
M. Ardizzoni,
C. Stefanelli, and R. Cevenini.
1993.
Glycoprotein patterns in Borrelia spp.
Zentbl. Bakteriol.
279:330-335.
|
| 25.
|
Spessotto, P.,
P. Dri,
R. Bulla,
G. Zabucchi, and P. Patriarca.
1995.
Human eosinophil peroxidase enhances tumor necrosis factor and hydrogen peroxide release by human monocyte-derived macrophages.
Eur. J. Immunol.
25:1366-1373[Medline].
|
| 26.
|
Stahl, P. D.
1992.
The mannose receptor and other macrophage lectins.
Curr. Opin. Immunol.
4:49-52[CrossRef][Medline].
|
| 27.
|
Taylor, M. E.,
J. T. Conary,
M. R. Lennartz,
P. D. Stahl, and K. Drickamer.
1990.
Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains.
Biol. Chem.
265:12156-12162[Abstract/Free Full Text].
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Infection and Immunity, April 2001, p. 2743-2747, Vol. 69, No. 4
0019-9567/01/$04.00+0 DOI: 10.1128/IAI.69.4.2743-2747.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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